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Nova Hedwigia 86 1mdash2 1mdash21 Stuttgart February 2008
DOI 1011270029-503520080086-0001 0029-5035080086-0001 $ 525copy 2008 J Cramer in der Gebruumlder Borntraeger
Verlagsbuchhandlung D-14129 Berlin middot D-70176 Stuttgart
A morpho-molecular classification of the mosses (Bryophyta)
by
Michael Stech1 and Wolfgang Frey2
1Nationaal Herbarium Nederland Universiteit Leiden branch PO Box 9514 2300 RA LeidenThe Netherlands E-mail stechnhnleidenunivnl
2Institut fuumlr Biologie - Systematische Botanik und Pflanzengeographie Freie Universitaumlt BerlinAltensteinstr 6 D-14195 Berlin Germany
With 1 figure and 2 tables
Stech M amp W Frey (2008) A morpho-molecular classification of the mosses (Bryophyta) NovaHedwigia 86 1-21
Abstract Molecular relationships within the Bryopsida are inferred from a new approach ie thecombined analysis of solely non-coding plastid markers (trnL
UAA intron atpB-rbcL spacer psbA-
trnH spacer) The current state of moss systematics is discussed with respect to the impact of thisapproach as well as other recently published molecular phylogenies and phylogenomic inferencesTaking into account the progress that has been made in the last few years by analysing molecular andnon-molecular data a new synopsis of the suprageneric classification of the Bryophyta is presentedTaxonomic changes comprise a re-evaluation of the taxonomy of Takakia (including Takakiophytinastat nov) Gigaspermidae subclass nov elevation of subfamilies of Dicranaceae to family level(Amphidiaceae stat nov Dicranellaceae stat nov Oncophoraceae stat nov) Hypodontiaceae famnov and Helicophyllales ord nov
Key words Bryophyta suprageneric classification molecular phylogeny trnLUAA
intron atpB-rbcLspacer psbA-trnH spacer
Introduction
Mosses form the second largest of the major land plant lineages They compriseapproximately 12800 species (Crosby et al 1999) and exhibit a high morphologicaland ecological diversity Traditionally the three groups of bryophytes (mossesliverworts and hornworts) were treated as classes of the division Bryophyta Moleculardata however revealed that bryophytes are paraphyletic with liverworts being sisterto all other extant land plants and mosses sister to a clade of hornworts and vascularplants (Qiu et al 2006) As the three bryophyte groups obviously represent independentlineages in land plant evolution it is now widely accepted to treat them as separatedivisions Bryophyta (mosses) Marchantiophyta (liverworts) and Anthocerotophyta
2
(hornworts) In contrast to the latter two groups mosses are scarcely characterisedin terms of morphological-anatomical synapomorphies At the molecular levelhowever all three bryophyte lineages are well circumscribed (eg Qiu et al 1998Stech et al 2003 Cox et al 2004 Shaw amp Renzaglia 2004 Groth-Malonek et al2005 Forrest et al 2006 Qiu et al 2006) A general overview of the present state ofbryophyte phylogeny was recently provided by Renzaglia et al (2007)
In the 19th and 20th century different and often contradictory classification systemsof mosses were published which either relied more on gametophytic or on sporophyticcharacters (summarised for example in Buck 2007) Nowadays the phylogeneticsignificance of morphological-anatomical characters can be evaluated based onmolecular phylogenies The most recent classifications of liverworts (Frey amp Stech2005 He-Nygreacuten et al 2006) hornworts (Stotler amp Crandall-Stotler 2005 Duff etal 2007) and mosses (Goffinet amp Buck 2004) already integrated molecular and non-molecular characters to provide a consensus of the current knowledge Howeverseveral suprageneric relationships within the mosses remained unresolved orambiguous at the time of the Goffinet amp Buck (2004) classification such as ordinalrelationships within the Bryidae and the closest relatives of pleurocarpous mossesA number of recent attempts shed more light on these problematic relationships(eg Tsubota et al 2004 Shaw et al 2005 Stech amp Quandt 2006 Bell et al 2007Goffinet et al 2007 contributions in Newton amp Tangney 2007 Quandt et al 2007this paper) Although some clades of the moss phylogeny are still partly contradictoryor do not receive significant statistical support these studies seem to converge on acommon hypothesis of moss relationship at suprageneric levels allowing us toestablish an updated and revised classification
In the present study a molecular phylogeny of the Bryopsida is presented based on anew approach ie the combined analysis of solely non-coding plastid markers (trnL
UAAintron atpB-rbcL spacer psbA-trnH spacer) The current state of moss systematicsis discussed with respect to the impact of this approach as well as recently publishedmolecular phylogenies and phylogenomic inferences Finally we propose a newsynopsis of the suprageneric classification of the Bryophyta which updates that ofGoffinet amp Buck (2004) A detailed description of the taxa down to genus level willbe provided by a forthcoming new edition of Englers Syllabus of Plant Familiesfor which additional taxonomic changes are made here
Material and methods
TAXON SAMPLING A molecular data set of 85 species of Bryopsida was assembled by compilingsequences from own previous analyses and by sequencing of herbarium material Voucher informationand GenBank accession numbers are summarised in Table 1 together with indications of the newlysequenced accessions From 21 species all three non-coding markers employed here were newlysequenced In few cases sequences available in GenBank were used to complete the data set Andreaearupestris Hedw (Andreaeopsida) and Pogonatum subulatum (Menzies ex Brid) Brid (Poly-trichopsida) were used as outgroup representatives
DNA EXTRACTION PCR AND SEQUENCING DNA was extracted using the mixer mill MM200 (Retsch)and following the method of Doyle amp Doyle (1990) PCR reactions for trnL intron and atpB-rbcLspacer followed the protocols given in Frey et al (1999) and Stech (2004) and were performed with
3
Tab
le 1
Vou
cher
info
rmat
ion
and
Gen
Ban
k ac
cess
ion
num
bers
of t
he s
peci
es u
sed
for t
he th
ree-
mar
ker a
naly
sis
of B
ryop
sida
s
eque
nces
take
n fr
omG
enB
ank
spec
ies
of w
hich
all
thre
e m
arke
rs w
ere
new
ly s
eque
nced
for
the
pres
ent s
tudy
Fam
ilyS
peci
esV
ouch
erH
erb
Acc
no
Acc
no
Acc
no
trnL
atpB
-rbc
Lps
bA-t
rnH
And
reae
acea
eA
ndre
aea
rupe
stri
s H
edw
S
tech
B97
0827
3L
AY
0502
78A
Y86
4297
EU
1635
06Po
lytr
icha
ceae
Pog
onat
um s
ubul
atum
(Men
zies
ex
Bri
d) B
rid
Pfe
iffe
r 98
-T20
7AC
HR
F
rey
AY
0502
77E
U12
4442
EU
1635
05D
iphy
scia
ceae
Dip
hysc
ium
fol
iosu
m (
Hed
w)
DM
ohr
Fre
y 1-
4982
(tr
nL)
Frey
EU
1865
37D
Q39
7161
AY
3128
99T
imm
iace
aeT
imm
ia m
egap
olit
ana
Hed
w
(Gen
Ban
k)-
AF
4783
20D
Q39
7137
AY
3129
23T
imm
ia a
ustr
iaca
Hed
w
S
tech
B97
0831
4L
EU
1865
43E
U18
6584
EU
1635
13E
ncal
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ceae
Enc
alyp
ta s
trep
toca
rpa
Hed
w
S
tech
B06
0412
2L
EU
1865
41E
U18
6582
EU
1635
11E
ncal
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vul
gari
s H
edw
S
tech
B95
0328
3L
EU
1280
00E
U12
4423
EU
1635
10Fu
nari
acea
eF
unar
ia h
ygro
met
rica
Hed
w
Ste
ch B
9811
301
LE
U18
6538
EU
1865
79E
U16
3507
Phy
scom
itre
lla
pate
ns (
Hed
w)
(ste
rile
cul
ture
)-
EU
1865
39E
U18
6580
EU
1635
08B
ruch
amp S
chim
pP
hysc
omit
rium
pyr
ifor
me
(Hed
w)
Ham
pe
Ste
ch B
0404
071
LE
U18
6540
EU
1865
81E
U16
3509
Cat
osco
piac
eae
Cat
osco
pium
nig
ritu
m (
Hed
w)
Bri
d
S
tech
B97
0828
13
LE
U18
6545
EU
1865
92E
U16
3524
Bry
oxip
hiac
eae
Bry
oxip
hium
nor
vegi
cum
(B
rid
) M
itt
Kop
onen
366
64B
AF
1351
01E
U18
6590
EU
1635
21G
rim
mia
ceae
Rac
omit
rium
mic
roca
rpum
(H
edw
) B
rid
Ste
ch B
9708
181
LA
F12
7186
EU
1865
89E
U16
3519
Schi
stid
ium
apo
carp
um (
Hed
w)
Ste
ch B
9702
262
LA
F12
7185
EU
1865
88E
U16
3518
Bru
ch amp
Sch
imp
Ptyc
hom
itria
ceae
Pty
chom
itri
um p
olyp
hyll
um (S
w)
Ste
ch e
t al
04-4
0L
EU
1865
42E
U18
6583
EU
1635
12B
ruch
amp S
chim
p
A
rchi
diac
eae
Arc
hidi
um a
ltern
ifoliu
m (D
icks
ex
Hed
w)
Mitt
F
rahm
sn
B
ON
NA
F13
5114
EU
1865
97E
U16
3529
Am
phid
iace
aeA
mph
idiu
m m
ouge
otii
(B
ruch
amp S
chim
p)
Fra
hm s
n
BO
NN
AF
1271
87A
Y15
9894
EU
1635
20S
chim
pD
icra
nace
aeD
icra
num
pol
yset
um S
w
Ste
ch B
9705
181
LA
F12
9587
AY
1598
95E
U16
3523
Dic
rane
llace
aeD
icra
nell
a ce
rvic
ulat
a (H
edw
) S
chim
pS
tech
B97
0824
1L
AF
1295
97E
U18
6591
EU
1635
22D
itric
hace
aeP
leur
idiu
m a
cum
inat
um L
indb
F
rey
1-49
91F
rey
EU
1865
46E
U18
6596
EU
1635
28Fi
ssid
enta
ceae
Fis
side
ns b
ryoi
des
Hed
w
Dar
mer
130
17B
SB
AF
1351
05E
U18
6586
EU
1635
15O
ctod
icer
as fo
ntan
um (
Bac
h P
yl)
Lin
db
Haa
pasa
ari s
n
LA
F13
5107
EU
1865
85E
U16
3514
Leu
cobr
yace
aeC
ampy
lopu
s fl
exuo
sus
(Hed
w)
Bri
dS
tech
B96
0905
2L
AF
1295
93A
Y15
9919
EU
1635
30L
euco
bryu
m ja
vens
e (B
rid
) M
itt
Men
zel e
t al
3841
Fre
yA
F44
2659
AY
1599
00E
U16
3531
Onc
opho
race
aeC
ynod
onti
um p
olyc
arpu
m (
Hed
w)
Sch
imp
Ste
ch B
930
721
2L
AF
1295
99E
U18
6595
EU
1635
27O
ncop
horu
s vi
rens
(H
edw
) B
rid
Ste
ch B
9608
011
LA
F12
9598
EU
1865
93E
U16
3525
Rha
bdow
eisi
a cr
enul
ata
(Mit
t) H
Jam
eson
Fra
hm s
n 1
810
97
BO
NN
AF
1271
81E
U18
6594
EU
1635
26
4
Potti
acea
eC
incl
idot
us n
igri
cans
(Brid
) W
ijk amp
Mar
gada
ntS
tech
B92
0517
4L
EU
1865
44E
U18
6587
EU
1635
17T
ortu
la m
ural
is H
edw
S
tech
B97
0226
3L
AF
1351
08A
Y15
9892
EU
1635
16Sp
lach
nace
aeSp
lach
num
lut
eum
Hed
w
S
tech
B97
0828
12
LE
U18
6555
EU
1866
13E
U16
3548
Tay
lori
a m
irab
ilis
(C
ardo
t) B
roth
Fre
y amp
Sch
aum
ann
F
Fre
yE
U18
6554
EU
1866
12E
U16
3547
01-3
6T
etra
plod
on m
nioi
des
(Sw
ex
Hed
w)
Ste
ch B
9106
154
LE
U18
6556
EU
1866
14E
U16
3549
Bru
ch amp
Sch
imp
Mee
siac
eae
Mee
sia
ulig
inos
a H
edw
Ste
ch B
9708
285
LE
U18
6552
EU
1866
10E
U16
3545
Pal
udel
la s
quar
rosa
(H
edw
) B
rid
Ste
ch B
9708
201
LE
U18
6553
EU
1866
11E
U16
3546
Pulc
hrin
odac
eae
Pul
chri
nodu
s in
flat
us (
Hoo
kf
amp W
ilso
n)P
feif
fer amp
Lin
dlar
CH
RA
F13
5065
EU
1866
03E
U16
3538
BH
All
en98
-Z21
5DL
epto
stom
atac
eae
Lep
tost
omum
men
zies
ii R
Br
Fre
y amp
Sch
aum
ann
F
Fre
yE
U18
6550
EU
1866
08E
U16
3543
01-3
88B
ryac
eae
Bry
um b
illa
rdie
rei
Sch
waumlg
rFr
ey amp
Pfe
iffer
98-
Mo1
7Fr
eyE
U18
6549
EU
1866
07E
U16
3542
Rho
dobr
yum
gig
ante
um (
Sch
waumlg
r)
Par
is(G
enB
ank)
-A
F02
3737
AF
5468
60A
Y31
2918
Mni
acea
eM
ielic
hhof
eria
mie
lichh
ofer
iana
(Fun
ck) L
oesk
eS
tech
B91
0615
3L
EU
1865
48E
U18
6605
EU
1635
40M
nium
hor
num
Hed
w
Fre
y 1-
4985
(tr
nL)
Frey
AF
3632
79A
F54
6857
AY
3129
08P
lagi
omni
um u
ndul
atum
(H
edw
) T
JK
op
Ste
ch e
t al
04-6
07L
DQ
1089
67E
U18
6604
EU
1635
39R
hizo
mni
um m
agni
foli
um (
Hor
ik)
TJ
Kop
S
tech
B97
0829
6L
DQ
1089
59E
U18
6606
EU
1635
41H
edw
igia
ceae
Hed
wig
ia c
ilia
ta (
Hed
w)
PB
eauv
(G
enB
ank)
-A
F47
8336
AJ2
4903
8A
Y31
2905
Rha
coca
rpac
eae
Rha
coca
rpus
pur
pura
scen
s (B
rid
) Pa
ris
(ste
rile
cul
ture
)-
AF
0237
24E
U18
6598
EU
1635
32H
elic
ophy
llace
aeH
elic
ophy
llum
torq
uatu
m (
Hoo
k)
Bri
dF
rahm
150
7F
rey
EU
1865
47E
U18
6602
EU
1635
37B
artr
amia
ceae
Ana
coli
a la
evis
phae
ra (
Tay
lor)
Flo
wer
sS
hevo
ck 1
7853
MO
EU
301
607
AF
4135
57E
U16
3533
Bar
tram
ia s
tric
ta B
rid
Muumll
ler
C15
52M
uumllle
rA
F02
3756
EU
1865
99E
U16
3534
Con
osto
mum
pen
tast
ichu
m (
Bri
d)
Lin
db
Fra
hm s
n
BO
NN
EU
301
606
EU
1866
00E
U16
3535
Phi
lono
tis
font
ana
(Hed
w)
Bri
dG
arto
n 20
748
BO
NN
EF
1075
40E
U18
6601
EU
1635
36O
rtho
tric
hace
aeO
rtho
tric
hum
ano
mal
um H
edw
S
tech
B97
0226
1L
AF
1303
14E
U18
6616
EU
1635
51O
rtho
tric
hum
str
amin
eum
Hor
nsch
(s
teri
le c
ultu
re)
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7183
EU
1866
18E
U16
3553
Ulo
ta c
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a (H
edw
) B
rid
Ste
ch B
0503
243
LE
U18
6557
EU
1866
17E
U16
3552
Zyg
odon
bau
mga
rtne
ri M
alta
Fra
hm s
n 4
51
985
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BA
F12
7184
EU
1866
15E
U16
3550
Aul
acom
niac
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Aul
acom
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pal
ustr
e (H
edw
) S
chw
aumlgr
Ste
ch B
0305
294
LE
U18
6551
EU
1866
09E
U16
3544
Aul
acom
nium
turg
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(W
ahle
nb)
Sch
waumlg
r(G
enB
ank)
-A
F02
3728
AF
4135
32A
Y31
2894
Hym
enod
onto
psis
mni
oide
s (H
ook
)F
rey
amp S
chau
man
nF
F
rey
EU
1865
63E
U18
6625
EU
1635
60N
EB
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AE
New
ton
amp D
Qua
ndt
01
-186
aO
rtho
dont
iace
aeH
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pil
ifer
Hoo
kf
amp W
ilso
nF
rahm
1-1
4F
rey
EU
1865
59E
U18
6620
EU
1635
55O
rtho
dont
ium
lin
eare
Sch
waumlg
r
S
tech
B95
0616
2L
EU
1865
58E
U18
6619
EU
1635
54L
epto
thec
a ga
udic
haud
ii S
chw
aumlgr
Fre
y amp
Sch
aum
ann
F
Fre
yA
F02
3750
EU
1866
24E
U16
3559
01-0
9
Tab
le 1
con
tinu
ed
5
Rhi
zogo
niac
eae
Cal
omni
on c
ompl
anat
umFr
ahm
20-
4Fr
eyE
U18
6560
EU
1866
21E
U16
3556
(Hoo
kf
amp W
ilso
n) L
indb
C
rypt
opod
ium
bar
tram
ioid
es (
Hoo
k)
Bri
d
Fr
ey amp
Sch
aum
ann
01-4
0F
F
rey
EU
1865
61E
U18
6622
EU
1635
57
Rhi
zogo
nium
dis
tich
um (
Sw
) B
rid
Fra
hm 2
-11
Fre
yE
U18
6562
EU
1866
23E
U16
3558
Hyp
node
ndra
ceae
Cyr
topu
s se
tosu
s (H
edw
) H
ook
fF
rahm
X16
-1F
rey
EU
1865
69E
U18
6631
EU
1635
66H
ypno
dend
ron
spin
iner
vium
(H
ook
)P
feif
fer
98-T
162
CH
R
Fre
yE
U18
6567
EU
1866
29E
U16
3564
AJ
aege
r amp
Sau
erb
Hyp
node
ndro
n vi
tien
se M
itt
Stre
iman
nB
EU
1865
68E
U18
6630
EU
1635
65Sc
iado
clad
us k
erri
i (M
itt)
AJ
aege
r ex
Bro
th
Pfe
iffe
r T
210
CH
R
Fre
yE
U18
6565
EU
1866
27E
U16
3562
Scia
docl
adus
men
zies
ii (
Hoo
k)
Fre
y amp
Pfe
iffe
rC
HR
F
rey
EU
1865
66E
U18
6628
EU
1635
63L
indb
ex
Bro
th
98-M
o5R
acop
ilace
aeR
acop
ilum
con
volu
tace
um (M
uumlllH
al)
Zan
k s
nF
rey
EU
1865
64E
U18
6626
EU
1635
61R
eich
ardt
Ptyc
hom
niac
eae
Pty
chom
nion
pty
choc
arpo
n (S
chw
aumlgr
)F
rey
amp S
chau
man
nF
F
rey
EU
1865
70E
U18
6632
EU
1635
67M
itt
01
-266
aH
ooke
riac
eae
Hoo
keri
a lu
cens
(H
edw
) S
m
Ste
ch B
8804
048
LA
F15
2380
EU
1866
35E
U16
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Lep
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Car
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l 04
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LE
U18
6571
EU
1866
33E
U16
3568
Tet
rast
ichi
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ntan
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Mit
t) C
ardo
t
Ste
ch e
t al
04-1
24L
EU
1865
72E
U18
6634
EU
1635
69H
ypop
tery
giac
eae
Arb
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lohy
popt
eryg
ium
arb
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la (
Bri
d)
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y 95
-17
CH
R
Fre
yA
F13
4637
EU
1866
37E
U16
3573
MS
tech
TP
feif
f amp
WF
rey
Cat
haro
mni
on c
ilia
tum
(H
edw
) W
ilso
nB
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r 97
-69
CH
R
Fre
yE
U18
6573
EU
1866
36E
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3572
Hyp
opte
rygi
um d
isco
lor
Mit
tS
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man
n 52
819
Fre
y ex
LA
F36
3282
AY
8642
93E
U16
3575
Hyp
opte
rygi
um t
amar
isci
(Sw
)Pf
eiff
er amp
Sip
man
BD
Q07
7169
AY
8642
94E
U16
3574
Bri
d e
x M
uumlllH
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99-6
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cinn
um (
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k)
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son
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y 95
-62
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8642
95E
U16
3571
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ca H
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ch e
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04-1
4L
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1865
74E
U18
6638
EU
1635
76A
mbl
yste
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Cra
tone
uron
fili
cinu
m (
Hed
w)
Spr
uce
Ste
ch B
9006
151
LA
F12
9586
EU
1866
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3583
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Dix
on
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04-2
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1865
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EU
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Ste
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04-4
54L
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1865
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EU
1635
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(E
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ex
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Kin
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ch B
9309
101
LA
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4046
EU
1866
39E
U16
3577
Cry
phae
acea
eC
ryph
aea
tasm
anic
a M
itt
Frah
m 3
1-1
Frey
EU
1865
76E
U18
6643
EU
1635
81L
euco
dont
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eA
ntitr
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a cu
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endu
la (T
imm
ex
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Brid
S
tech
B94
0717
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AY
0102
86E
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6641
EU
1635
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ecke
race
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ham
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(H
ook
f amp
Wil
son)
Fre
y amp
Fre
y 94
-117
Fre
yA
Y01
0297
EU
1866
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3580
IG
Sto
ne amp
GA
MS
cott
Plag
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ecia
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giot
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um u
ndul
atum
(H
edw
) S
chim
pS
tech
B88
1003
2L
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2640
45E
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6646
EU
1635
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onia
ceae
Cat
agon
ium
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ens
(Bri
d)
Car
dot
Fre
y amp
Sch
aum
ann
F
Fre
yE
U18
6575
EU
1866
40E
U16
3578
01-1
87a
Tab
le 1
con
tinu
ed
6
primers CM
DM
(slightly modified after Taberlet et al 1991 see Frey et al 1999) and atpB-1rbcL-1(Chiang et al 1998) respectively For amplification of the psbA-trnH spacer primers psbAF(5-GTT ATG CAT GAA CGT AAT GCT C-3 Sang et al 1997) and trnHR-2 (5-CGC GCA TGGTGG ATT CAC AAT CC-3 slightly modified after Sang et al 1997) were used with a PCRprotocol of 5 min 94degC 35 cycles (30 sec 94degC 1 min 48degC 1 min 40 sec 72degC) 7 min 72degC PCRproducts were purified using DNA purification kits (Qiagen Macherey-Nagel) Sequencing wasperformed as described in Stech (2004) using the amplification primers
ALIGNMENT AND PHYLOGENETIC ANALYSES DNA sequences were manually aligned in PhyDE v0992(Muumlller et al 2005) Following Quandt et al (2003) and Quandt amp Stech (2005) inversions inputative hairpin secondary structures were positionally separated in the alignment their presence orabsence was not coded for the phylogenetic analyses Phylogenetic reconstructions under the maximumparsimony criterion were performed using winPAUP 40b10 (Swofford 2002) in combination withPRAP (Muumlller 2004) as implemented in SeqState (Muumlller 2005) PRAP generates command filesfor PAUP that allow parsimony ratchet searches as designed by Nixon (1999) Heuristic searchesunder parsimony were performed with the following options all characters equally weighted andunordered TBR branch swapping collapse branches if maximum branch length is zero MulTreesoption in effect gaps treated as missing data Initially a heuristic search with 1000 addition sequencereplicates was performed For the parsimony ratchet ten random addition cycles of 200 ratchetiterations each were used with TBR branch swapping on a randomly re-weighted data set (25 ofthe positions) Heuristic bootstrap searches were performed with 1000 replicates with 10 additionsequence replicates per bootstrap replicate
Results
In the present data set of non-coding plastid markers sequence lengths ranged from243 to 368 nucleotides (nt) in the trnL intron and from 445 to 615 nt in the atpB-rbcL spacer The psbA-trnH spacer was considerably shorter than the other twomarkers and ranged from 103 to 186 nt The combined alignment of sequences from85 ingroup and two outgroup taxa comprised 2430 positions (trnL intron 668 atpB-rbcL spacer 1366 psbA-trnH spacer 396 positions) The most variable regions withambiguous alignment (781 positions) were excluded from phylogenetic analysis Ofthe 1649 included positions 628 (381) were variable and 455 of the variablepositions (725 or 276 of the total number of positions) were parsimony-informative The trnL intron comprised 124 the atpB-rbcL spacer 286 and the psbA-trnH spacer 45 of these included parsimony-informative positions
The shortest trees found in the heuristic maximum parsimony analysis of the combineddata set had a length of 2433 steps By applying the parsimony ratchet 129 treeswere retained that were one step shorter (length 2432 CI = 0419 RI = 0624) Thestrict consensus tree of the ratchet analysis is shown in Fig 1 The ingroup (Bryopsida)is supported with 100 bootstrap support (BS) Diphysciidae are sister to theremaining Bryopsida with 54 BS Encalyptidae Funariidae Timmiidae andDicranidae all receive gt 95 BS while Bryidae are slightly less supported (89BS) Relationships between these major lineages are resolved but unsupported Atordinal level within the Bryidae a lower resolution is observed SplachnalesOrthotrichales Aulacomniales Hypnodendrales Hookeriales and Hypnales areresolved as monophyletic with 67-100 BS whereas Hedwigiales BartramialesBryales Orthodontiales and Rhizogoniales are not A closer relationship ofOrthotrichales with the pleurocarpous mosses sl than with the more basal ordersHedwigiales Bartramiales Splachnales and Bryales is indicated
7
Discussion
Classification of mosses - recent progress and the current state
For a long time mosses were subdivided into three main lineages the subclassesSphagnidae Andreaeidae and Bryidae (eg Fleischer 1920 Vitt 1984 Frahm ampFrey 1987) the latter with a number of (super-)orders (eg Frey 1977) Howevermolecular data confirmed that mosses comprise a number of isolated basal lineagesrepresented by morphologically and ecologically distinct extant taxa such as TakakiaSphagnum Andreaea Andreaeobryum Oedipodium Tetraphis the Polytrichaceaeand Buxbaumia which probably have long independent phylogenetic histories (cfNewton et al 2007) As a result of molecular phylogenies and a re-evaluation ofmorphological-anatomical characters the classification of mosses has changedconsiderably in the last few years with the main lineages nowadays treated atsubdivision class and subclass levels within division Bryophyta (eg Doweld 2001Ochyra et al 2003 Goffinet amp Buck 2004 this study)
Takakia and Sphagnum are the earliest diverging moss taxa in molecular phylogenies(eg Newton et al 2000 Beckert et al 2001 Cox et al 2004 Qiu et al 2006Newton et al 2007) That Takakia is a moss and not a liverwort was confirmed byanalysis of DNA sequences and phylogenomic characters such as the distribution ofmitochondrial introns (eg Beckert et al 2001) Its taxonomic status however stillremains to be clarified On the one hand most molecular studies resolve Takakiaand Sphagnum as sister genera although only partly with high statistical supportThese molecular topologies do not support the recognition of division Takakiophytaas proposed by Crandall-Stotler (1986) One the other hand no morphologicalsynapomorphies unite Takakia with Sphagnum and significant molecular differencesseparating Takakia from all other mosses were also observed For example a regionin the plastid ITS3 is similar to that of other land plants but absent in mosses(Samigullin et al 2002) and a transition in the trnL
UAA gene changing the anticodon
to CAA was otherwise only found in leptosporangiate ferns and Ginkgo (Quandt etal 2004) Thus ldquoresolution of Sphagnum - Takakia clade may be an artifactrdquo (Shawamp Renzaglia 2004) Also Goffinet amp Buck (2004) did not unite Takakia and Sphagnumunder a formal taxonomic rank but placed them into different informal superclassesIn our opinion Takakia should be treated at the same level as Sphagnophytina andBryophytina (cf Doweld 2001) ie as a subdivision of Bryophyta However morefundamental nomenclatural changes are necessary as the family name Takakiaceaewas not validated in the original publication by Hattori amp Inoue (1958) (article411 of ICBN McNeill et al 2006) and consequently all higher taxa erected laterare invalid The corrected taxonomic treatment of Takakia is provided here withsporophytic characters included in the latin diagnosis of Takakiaceae (see taxonomy)
Within Bryophytina we recognise four morphologically and molecularly isolatedbasal lineages as separated from the arthrodontous mosses (Bryopsida) Andreaeopsida(with linear capsule dehiscence) the operculate but eperistomate Oedipodiopsida aswell as Polytrichopsida and Tetraphidopsida with nematodontous peristomes A fifthclass Andreaeobryopsida was erected by Buck amp Goffinet (2000) but re-includedin Andreaeopsida as a subclass by Ochyra et al (2003) The systematic status of
8
Andreaeobryum macrosporum Steere amp BMMurray and possible relationships withAndreaea and Takakia were discussed by Murray (1988) and summarised includingmolecular results by Shaw amp Renzaglia (2004)
On the next lower level a number of morphologically and molecularly divergentlineages are nowadays treated as subclasses of Bryopsida Buxbaumiidae andDiphysciidae are generally branching off first in molecular topologies (eg Beckertet al 2001 Magombo 2003 Cox et al 2004) followed by Timmiidae Encalyptidaeand Funariidae as well as Dicranidae (haplolepideous mosses) sister to Bryidae slThese subclasses (except Buxbaumiidae not included) are also well recognizable inthe present analysis of non-coding plastid sequences (Fig 1)
The morphologically very different Encalyptidae and Funariidae are revealed assister groups although mostly without high support in several molecular phylogenies(eg Goffinet et al 2001 Cox et al 2004 Hedderson et al 2004 Tsubota et al2003 2004) and also in the present study (Fig 1) Goffinet et al (2007) confirmedthis relationship by phylogenomic evidence namely a large (71 kb) inversion in thechloroplast genome of Funariaceae Disceliaceae and Encalyptaceae but not inGigaspermaceae Consequently the latter family was separated at ordinal level fromthe two remaining families of Funariales by Goffinet et al (2007) GigaspermalesFunariales and Encalyptales may share a common ancestor according to some butnot all molecular phylogenies (eg Goffinet et al 2001 2007 Hedderson et al2004 but not in Tsubota et al 2004) Although ontogenetic data from peristomedevelopment may support their common ancestry (Goffinet et al 2007) unambiguousmorphological synapomorphies are lacking We therefore propose to treatGigaspermaceae at subclass level within the Bryopsida (see taxonomy)
The haplolepideous mosses (Dicranidae) are clearly supported as a monophyleticlineage which obviously evolved from a diplolepideous ancestor according to theirposition in the molecular trees (eg Newton et al 2000 Tsubota et al 2003 Cox etal 2004 Goffinet amp Buck 2004) Molecular studies suitable for inferring ordinaland family level relationships within Dicranidae either focused on the haplolepideousmosses (eg Stech 1999ab 2004 LaFarge et al 2000 2002 Tsubota et al 2003Hedderson et al 2004) or included more than 15 haplolepideous taxa in analyses ofa broader range of mosses (eg Goffinet et al 2001 Tsubota et al 2004 this study)Major lineages supported by these analyses are for example Grimmiales(Grimmiaceae Ptychomitriaceae and Seligeriaceae) Leucobryaceae (incl formerDicranaceae-Campylopoideae and Paraleucobryoideae pp) Dicranaceae sstr(Dicranoideae plus former Dicnemonaceae and Paraleucobryoideae pp) Pottiaceae(incl Cinclidotaceae and Splachnobryum) and Calymperaceae (probably exclOctoblepharum) Furthermore several genera and families belong to Dicranidaewhose systematic positions have been controversial (eg Stech et al 1999b LaFarge et al 2002 Hedderson et al 2004 OBrien 2007 Quandt et al 2007 thisstudy) Amphidium Archidium Catoscopium Drummondia EphemeraceaeErpodiaceae Mittenia (cf OBrien 2007 sequences in some earlier analyses werebased on misdentified specimens) Rhachitheciaceae Schistostega Splachnobryumand Wardia On the contrary several problems remain such as the circumscriptionof Ditrichaceae and relationships of the major haplolepideous lineages in general
9
Fig 1 Strict consensus tree of 129 most parsimonious trees inferred from combined trnLUAA
intronatpB-rbcL spacer and psbA-trnH spacer sequences of 85 taxa of Bryopsida as well as Andreaearupestris (Andreaeopsida) and Pogonatum subulatum (Polytrichopsida) as outgroup representativesBootstrap support values gt50 are depicted above the branches
10
Consequently resolving the phylogeny of Dicranidae with confidence is one of themajor future challenges in moss systematics
As mentioned above Dicranaceae are monophyletic in a narrow circumscriptionaccording to molecular data In contrast to former Campylopoideae andParaleucobryoideae the status of Rhabdoweisioideae (= Oncophoroideae Ochyra2002) and Dicranelloideae needs further consideration Stech (1999ab) suggestedto recognise RhabdoweisioideaeRhabdoweisiaceae in a broad sense includingDicranoweisia Amphidium and Aongstroemia Subsequent molecular analysesconfirmed a close relationship of the genera Arctoa Cynodontium DicranoweisiaKiaeria Oncophorus Oreoweisia Oreas Rhabdoweisia and Symblepharis althoughwithout significant support (La Farge et al 2002 Tsubota et al 2003 Hedderson etal 2004) With respect to the molecular evidence available so far we propose toelevate Oncophoroideae to family level to accomodate these genera and perhapsGlyphomitrium (cf Tsubota et al 2003) whereas we consider AongstroemiaDichodontium and Diobelonella to belong to Aongstroemiaceae (cf Stech 1999a)Amphidium is neither closely related to Dicranaceae sstr nor to Oncophoroideae(La Farge et al 2002 Tsubota et al 2003 Hedderson et al 2004 Stech 2004 thisstudy) and should be treated at family level rather than placed in Dicranaceae assubfam Amphidioideae (Ochyra et al 2003) The circumscription of Dicranelloideaeis more difficult to evaluate as few representatives have been included in molecularanalyses However Dicranella heteromalla (Hedw) Schimp as well as the generaCampylopodium and Microcampylopus are clearly separated from Dicranaceae sstr(Stech 1999a 2004 La Farge et al 2002 Tsubota et al 2003 Hedderson et al2004) and consequently the subfamily deserves family status as well Finallymolecular data showed that the genus Hypodontium does not belong to Pottiaceae(Hedderson et al 2004 Tsubota et al 2004) Taxonomic conclusions have not beendrawn from these results which is made up here (see taxonomy)
All mosses with diplolepideous-alternate peristomes together with Splachnales witha diplolepideous-opposite (Funaria-type) peristome form a monophyletic group inmolecular analyses (eg Newton et al 2000 Beckert et al 2001 Goffinet et al2001 Cox et al 2004 Tsubota et al 2004 references in Table 2) Differentclassifications of this by far most species-rich group of mosses were proposed (egVitt et al 1998 Ochyra et al 2003 Goffinet amp Buck 2004) However at least someof the recognised subclasses and superorders are paraphyletic according to themolecular topologies and assigning formal ranks to all evolutionarily significantmonophyletic entities is problematic if the main taxonomic framework of Bryophytaand Bryopsida should be maintained (cf discussion in Bell et al 2007) Thereforein the present synopsis only one subclass Bryidae is recognised for all diplolepideous-alternate mosses and Splachnales This broadly defined Bryidae is subdivided into13 orders most of them resolved as monophyletic in the majority of the phylogeneticanalyses summarised in Table 2 although with different levels of statistical supportin maximum parsimony analyses To define monophyletic lineages at supraordinallevel informal node-based names may be chosen according to Bell et al (2007) Forexample the pleurocarpous mosses (pleurocarpy sensu Bell amp Newton 2007) andtheir closest acrocarpous relatives (Orthodontiales to Hypnales) were already
11
Table 2 Taxon sampling and bootstrap support (BS) for Dicranidae Bryidae and orders within theBryidae in recent phylogenetic analyses (MP only) based on combined molecular markers Markersare given in square brackets (non-coding regions in bold) numbers of included taxa in brackets ++respective clade present with ge 80 BS + clade present with lt 80 BS - clade not present no oronly one representative included
Bell amp Newton OBrien Quandt et al Bell et al this study(2004) (2007) (2007) (2007)
[rbcL rps4 [atpB atpB- [rbcL rps4 [rbcL rps4 [atpB-rbcLnad5] rbcL rbcL trnL-F nad5] trnL-F nad5] psbA-trnH
rps4 trnL-F] trnL]
Dicranidae + (2) + (4) ++ (3) (1) ++ (19)Bryidae ++ (57) + (53) ++ (52) ++ (98) ++ (58)Hedwigiales ++ (2) (1) ++ (2) ++ (2) - (3)Bartramiales ++ (2) ++ (4) ++ (4) ++ (3) - (4)Splachnales (0) ++ (2) ++ (3) ++ (2) ++ (5)Bryales - (4) - (5) ++ (18) + (17) - (8)Orthotrichales (1) ++ (3) ++ (3) ++ (2) ++ (4)Orthodontiales + (4) + (4) + (3) + (6) - (3)Aulacomniales + (6) + (7) ++ (2) + (7) + (3)Rhizogoniales ++ (13) + (8) ++ (5) ++ (14) - (3)Hypnodendrales ++ (13) + (7) ++ (4) ++ (29) ++ (6)Ptychomniales ++ (3) ++ (3) (1) ++ (4) (1)Hookeriales - (4) + (2) (1) + (2) + (8)Hypnales - (5) - (7) ++ (5) ++ (10) + (10)
summarised under the informal node based name pleurcarpids (Bell et al 2007)and can be distinguished from a basal grade of acrocarpous or cladocarpous lineages(Hedwigiales to Orthotrichales) Within the latter monophyly of BartramialesSplachnales and Orthotrichales is well-supported in all analyses including two ormore taxa except Bartramiales in the present data set (cf Fig 1) In contrast Bryalesreceive significant support less frequently (but see Bell et al 2007 Quandt et al2007) Hedwigiales are well supported if only Hedwigia (Hedwigiaceae) andRhacocarpus (Rhacocarpaceae) are included whereas the monospecific Helicophyllum(Helicophyllaceae) is not closely related to these taxa but shows affinities withBartramiales (Goffinet et al 2001 this study) With respect to the differentmorphologies of Helicophyllaceae and Bartramiaceae however the former shouldbe separated at ordinal level (see taxonomy)
Clarifying relationships of the Orthotrichales is still a difficult issue Analyses ofsingle chloroplast markers or parsimony analyses of combined markers from differentgenomes mostly indicated a close relationship either with Splachnales (eg Cox etal 2000 Newton et al 2000 Tsubota et al 2004 Quandt et al 2007) or with thepleurocarpids (Goffinet et al 2001 this study) Although none of these alternativesis well-supported the latter seems more likely with regard to the moderately tomaximally supported Orthotrichales - pleurocarpid sister group relationship in allanalyses of mitochondrial data and in likelihood analyses of combined plastidmitochondrial markers (Beckert et al 2001 Quandt et al 2007)
12
The molecular polyphyly of Rhizogoniaceae (eg Bell amp Newton 2004) was solvedby the transfer of rhizogonioid genera into broadly defined Aulacomniaceae andOrthodontiaceae (Bell et al 2007) which now include both acrocarpous andpleurocarpous taxa These systematic changes are also comprehensible by non-molecular characters such as morphological traits shared by Mesochaete andAulacomnium heterostichum (Hedw) Bruch amp Schimp or the variously reducedperistomes of Orthodontiaceae pp in contrast to the generally fully developed Bryum-type peristomes of rhizogonioid and hypnodendroid mosses (Bell et al 2007) Theposition of the solely pleurocarpous Hypnodendrales sister to the former Hypnidaeled to the recognition of the informal group core pleurocarps (Bell et al 2007)The former Hypnidae (Ptychomniales Hookeriales and Hypnales summarised ashomocostate pleurocarps) are monophyletic in most molecular analyses (eg Goffinetet al 2001 Tsubota et al 2004 Bell et al 2007) with Ptychomniales being well-supported (Pedersen amp Newton 2007 Table 2) Clarifying relationships betweenHookeriales and Hypnales and within the latter is still a challenge but recent molecularstudies seem to support a sister group relationship of both orders (Bell et al 2007present study)
Phylogenetic utility of non-coding plastid markers
Non-coding plastid markers that comprise both variable and conserved regionssuch as the trnL
UAA intron have repeatedly been shown to possess potential for
resolving relationships at high taxonomic levels (eg Borsch et al 2003 Quandtet al 2004) Both the trnL intron and atpB-rbcL spacer were characterised indetail in mosses with respect to their structure and molecular evolution (Quandt ampStech 2005 Stech amp Quandt 2006) They include conservative regions that can beunambiguosly aligned and even parts of the more variable regions can be used ifrepeats hairpin loops etc are correctly identified and adequately treated in thephylogenetic analyses (eg Quandt et al 2003 Quandt amp Stech 2005) Using theatpB-rbcL spacer alone (Stech amp Quandt 2006) relationships of the major mosslineages were largely consistent with the ldquototal evidencerdquo molecular tree of Goffinetamp Buck (2004) However in addition to general limitations that result from singlemarker analyses the use of non-coding markers may pose further problems suchas a high amount of homoplasy resulting in low resolution or low statistical supportfor many clades Therefore several recent molecular studies of relationships withinBryidae have employed both coding and non-coding markers (Table 2)Nevertheless the usefulness of analyses of combined non-coding plastid markerscannot be ruled out In fact Fig 1 and Table 2 indicate a phylogenetic signal inthe present data set as many clades are recovered that are usually also resolvedin analyses of coding or combined coding and non-coding markers Especiallywith regard to statistical support however the present analysis is inferior tothose of other recent data sets especially Bell et al (2007) and Quandt et al(2007) In addition the non-coding markers used here are of different suitabilityand even the two intergenic spacers differ considerably from each other ThepsbA-trnH spacer contributes much less to the trees resolution than the atpB-rbcL spacer first because it is much shorter and second because relatively largeparts are attributed to hairpin loops or otherwise hypervariable regions These
13
results indicate that future studies should evaluate the molecular evolution andphylogenetic potential of new markers both coding and con-coding and choosethe most suitable ones in a combined analysis to resolve the remaining uncertaintiesin moss phylogeny
Taxonomy
Takakiaceae Stech amp WFrey stat nov
Plantae virides nusquam rhizophorae sine protonemate e caudicis rhizomatis erectae Caudicesrhizomati et axes geotropi radiformes frequenter intercalariter ramificantes sine phyllidiis cumpapillis mucilaginis rostratis Caules phyllidiiferi saepe furcati Phyllidia sine lamina et costadistincta profunde 2-4(-5)-lobata pluristratosa tristicha sed torsione spiraliter disposita Filumcentralium in ambabus generationibus (axibus gametophyti et setis) adest Plantae dioicae Antheridiaet archegonia nuda Sporophytum terminale solitarium Seta persistens Capsula tortilis admaturitatem schizocarpa secus unam rimam spiralem longitudinalem dehiscens Stomata etoperculum absunt peristomium nullum Calyptra mitriformis
TYPUS Takakia SHatt amp Inoue J Hattori Bot Lab 19 137 1958
Takakiaceae SHatt amp Inoue J Hattori Bot Lab 19 137 1958 nom inval (Art 411)
Takakiales Stech amp WFrey stat nov
Based on Takakiaceae Stech amp WFrey Nova Hedwigia 86 13 2008
TYPUS Takakia SHatt amp Inoue J Hattori Bot Lab 19 137 1958
Takakiales SHatt amp Inoue J Hattori Bot Lab 19 137 1958 nom inval
Takakiales SHatt amp Inoue ex RMSchust J Hattori Bot Lab 26 224 1963 nom inval (cumdescr latin)
Takakiopsida Stech amp WFrey statnov
Based on Takakiaceae Stech amp WFrey Nova Hedwigia 86 13 2008
TYPUS Takakia SHatt amp Inoue J Hattori Bot Lab 19 137 1958
Takakiopsida Goffinet amp WRBuck Monogr Syst Bot Missouri Bot Gard 98 232 2004 nominval
Takakiopsida Jia et al Acta Phytotax Sin 41 350 351 2003 nom nud
Takakiopsida Wang amp Wu Fl Bryophyt Sin 8 447 2004 nom inval (cum descr latin)
Takakiophytina Stech amp WFrey stat nov
Based on Takakiaceae Stech amp WFrey Nova Hedwigia 86 13 2008
TYPUS Takakia SHatt amp Inoue JHattori Bot Lab 19 137 1958
Gigaspermidae Stech amp WFrey subclass nov
Plantae acrocarpae terrestres stoloniferae ramis brevibus erectis Folia unicostata cellulis laxislaevibus Capsula plerumque valde rugosa gymnostomatica vel cleistocarpa stomata cum duabuscellulis sociis Ab Funariidis et Encalyptidis charactere phylogenomico (71-kb inversio abest)separatae
14
TYPUS Gigaspermum Lindb Oumlfversigt af Foumlrhandlingar Kongl Svenska Vetenskaps-Akademien21 599 1865
Amphidiaceae Stech stat nov
Based on Dicranaceae subfam Amphidioideae Ochyra in Ochyra Zarnowiec amp Bednarek-OchyraCens Cat Polish Mosses 110 2003
TYPUS Amphidium Schimp Coroll Bryol Eur 39 1856
Amphidiaceae AJESm Moss Fl Britain Ireland 2nd ed 657 2004 nom inval descr angl
Dicranellaceae Stech stat nov
Based on Dicranaceae subfam Dicranelloideae Lindb Utkast Eur Bladmoss 33 1878[lsquoUnderfamilje Dicranelleaersquo]
TYPUS Dicranella (MuumlllHal) Schimp Coroll Bryol Eur 13 1856
Oncophoraceae Stech stat nov
Based on Dicranaceae subfam Oncophoroideae Lindb Utkast Eur Bladmoss 34 1878[lsquoUnderfamilje Oncophoreaersquo]
TYPUS Oncophorus (Brid) Brid Bryol Univ 1 389 1826
Hypodontiaceae Stech fam nov
Plantae robustae characteribus morphologicis Pottiaceis et Calymperaceis similes sedcharacteribus molecularicis separatae Bracteae perichaetiales internae e basi vaginantes subulataevel aristatae Capsula aspectu succulenta cellulae exothecii incrassatae annulus magnopereabsens Peristomii dentes breves triangulati incurvati aurantiaci leves vel infirme verrucosiCalyptra cucullata
TYPUS Hypodontium MuumlllHal Hedwigia 38 96 1899
Helicophyllales Stech amp WFrey ord nov
Plantae acrocarpae prostratae tomentosae Folia dimorpha in duas series laterales et unam seriemventralem divisa Costa percurrens Cellulae hexagonae ad subquadratae papillosae Capsula immersacupulata ad oblonga infra orificium abrupte incurvata stomata destituta Peristomium nullum Sporaeisomorphae heteropolares granulatae
TYPUS Helicophyllum Brid Bryol Univ 2 771 1827
Synopsis of the suprageneric classification of BryophytaAuthor citations are in accordance with Art 492 of the Vienna Code (McNeill et al 2006)
Subdivision Takakiophytina Stech amp WFreyClass Takakiopsida Stech amp WFrey
Order Takakiales Stech amp WFreyTakakiaceae Stech amp WFrey
Subdivision Sphagnophytina DoweldClass Sphagnopsida Schimp
Order Sphagnales Limpr
15
Sphagnaceae DumortOrder Ambuchananiales Seppelt amp HACrum
Ambuchananiaceae Seppelt amp HACrumSubdivision Bryophytina Engler
Class Andreaeopsida JHSchaffnSubclass Andreaeidae Engl
Order Andreaeales LimprAndreaeaceae Dumort
Subclass Andreaeobryidae OchyraOrder Andreaeobryales BMMurray
Andreaeobryaceae Steere amp BMMurrayClass Oedipodiopsida Goffinet amp WRBuck
Order Oedipodiales Goffinet amp WRBuckOedipodiaceae Schimp
Class Tetraphidopsida Goffinet amp WRBuckOrder Tetraphidales MFleisch
Tetraphidaceae SchimpClass Polytrichopsida Doweld
Order Polytrichales MFleischPolytrichaceae Schwaumlgr
Class Bryopsida PaxSubclass Buxbaumiidae Doweld
Order Buxbaumiales MFleischBuxbaumiaceae Schimp
Subclass Diphysciidae OchyraOrder Diphysciales MFleisch
Diphysciaceae MFleischSubclass Timmiidae Ochyra
Order Timmiales OchyraTimmiaceae Schimp
Subclass Encalyptidae Ochyra Żarnowiec amp Bednarek-OchyraOrder Encalyptales Dixon
Encalyptaceae SchimpSubclass Funariidae Ochyra
Order Funariales MFleischFunariaceae Schwaumlgr Disceliaceae Schimp
Subclass Gigaspermidae Stech amp WFreyOrder Gigaspermales Goffinet Wickett OWerner Ros AJShaw amp CJCox
Gigaspermaceae LindbSubclass Dicranidae Doweld
Order Catoscopiales Ignatov amp IgnatovaCatoscopiaceae Broth
Order Scouleriales Goffinet amp WRBuckDrummondiaceae Goffinet Scouleriaceae SPChurchill
Order Bryoxiphiales HACrum amp LEAndersonBryoxiphiaceae Besch
16
Order Grimmiales MFleischGrimmiaceae Arn Ptychomitriaceae Schimp Seligeriaceae Schimp
Order Archidiales LimprArchidiaceae Schimp
Order Mitteniales ShawMitteniaceae Broth
Order Dicranales HPhilib ex MFleischAmphidiaceae Stech Aongstroemiaceae De Not BruchiaceaeSchimp Calymperaceae Kindb Dicranaceae Schimp Dicranel-laceae Stech Ditrichaceae Limpr Erpodiaceae Broth EustichiaceaeBroth Fissidentaceae Schimp Leucobryaceae Schimp Onco-phoraceae Stech Rhachitheciaceae HRob Schistostegaceae SchimpViridivelleraceae IGStone Wardiaceae Welch
Order Pottiales MFleischEphemeraceae Schimp Hypodontiaceae Stech PleurophascaceaeBroth Pottiaceae Schimp Serpotortellaceae WDReese amp RHZander
Subclass Bryidae EnglOrder Hedwigiales Ochyra
Hedwigiaceae Schimp Rhacocarpaceae KindbOrder Helicophyllales Stech amp WFrey
Helicophyllaceae BrothOrder Bartramiales DQuandt NEBell amp Stech
Bartramiaceae SchwaumlgrOrder Splachnales Ochyra
Meesiaceae Schimp Splachnaceae Grev amp ArnOrder Bryales Limpr
Bryaceae Schwaumlgr Leptostomataceae Schwaumlgr Mniaceae SchwaumlgrPhyllodrepaniaceae Crosby Pseudoditrichaceae Steere amp ZIwatsPulchrinodaceae DQuandt NEBell amp Stech
Order Orthotrichales DixonOrthotrichaceae Arn
Order Orthodontiales NEBell AENewton amp DQuandtOrthodontiaceae Goffinet
Order Aulacomniales NEBell AENewton amp DQuandtAulacomniaceae Schimp
Order Rhizogoniales Goffinet amp WRBuckRhizogoniaceae Broth
Order Hypnodendrales NEBell AENewton amp DQuandtBraithwaiteaceae NEBell AENewton amp DQuandt Hypnodendra-ceae Broth Pterobryellaceae WRBuck amp Vitt Racopilaceae Kindb
Order Ptychomniales WRBuck CJCox AJShaw amp GoffinetPtychomniaceae MFleisch
Order Hookeriales MFleischDaltoniaceae Schimp Hookeriaceae Schimp HypopterygiaceaeMitt Leucomiaceae Broth Pilotrichaceae Kindb SaulomataceaeWRBuck CJCox AJShaw amp Goffinet Schimperobryaceae WR
17
Buck CJCox AJShaw amp GoffinetOrder Hypnales WRBuck amp Vitt
Amblystegiaceae GRoth Anomodontaceae Kindb BrachytheciaceaeSchimp Calliergonaceae Vanderpoorten Hedenaumls CJCox amp AJShaw Catagoniaceae WRBuck amp Ireland Climaciaceae KindbCryphaeaceae Schimp Echinodiaceae Broth Entodontaceae KindbFabroniaceae Schimp Fontinalaceae Schimp Helodiaceae OchyraHeterocladiaceae Ignatov amp Ignatova Hylocomiaceae MFleischHypnaceae Schimp Lembophyllaceae Broth LeptodontaceaeSchimp Lepyrodontaceae Broth Leskeaceae Schimp Leucodon-taceae Schimp Meteoriaceae Kindb Microtheciellaceae HAMillamp AJHarr Myriniaceae Schimp Myuriaceae MFleisch NeckeraceaeSchimp Orthorrhynchiaceae SHLin Phyllogoniaceae KindbPlagiotheciaceae MFleisch Pleuroziopsidaceae Ireland Prionodon-taceae Broth Pseudoleskeaceae Schimp PseudoleskeellaceaeIgnatov amp Ignatova Pterigynandraceae Schimp PterobryaceaeKindb Pylaisiaceae Schimp Pylaisiadelphaceae Goffinet amp WRBuck Regmatodontaceae Broth Rhytidiaceae Broth RigodiaceaeHACrum Rutenbergiaceae MFleisch Scorpidiaceae Ignatov ampIgnatova Sematophyllaceae Broth Sorapillaceae MFleisch Ste-reophyllaceae WRBuck amp Ireland Symphyodontaceae MFleischTheliaceae MFleisch Thuidiaceae Schimp TrachylomataceaeWRBuck amp Vitt
Acknowledgements
Sincere thanks are due to JLReveal (Ithaca) as well as WFPrudhomme van Reine and JFVeldkamp(Leiden) for comments and discussions about suprafamilial taxonomy to DQuandt (Dresden) for providingDNA from Rhacocarpus and Bartramiaceae species and to BGiesicke (Berlin) for technical assistance
References
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BELL NE amp AE NEWTON (2004) Systematic studies of non-hypnanaean pleurocarps establishinga phylogenetic framework for investigating the origins of pleurocarpy - In GOFFINET BV HOLLOWELL amp R MAGILL (eds) Molecular systematics of bryophytes Monogr Syst BotMissouri Bot Gard 98 290-319
BELL NE amp AE NEWTON (2007) Pleurocarpy in the Rhizogoniaceous grade - In NEWTONAE amp RS TANGNEY (eds) Pleurocarpous mosses systematics and evolution SystematicsAssociation Special Volume Series 71 41-64
BELL NE D QUANDT TJ OBRIEN amp AE NEWTON (2007) Taxonomy and phylogeny inthe earliest diverging pleurocarps square holes and bifurcating pegs - Bryologist 110 533-560
BORSCH T KW HILU D QUANDT V WILDE C NEINHUIS amp W BARTHLOTT(2003) Non-coding plastid trnT-trnF sequences reveal a well resolved phylogeny of basal angiosperms- J Evol Biol 16 558-576
18
BUCK WR (2007) The history of pleurocarp classification two steps forward one step back - InNEWTON AE amp RS TANGNEY (eds) Pleurocarpous mosses systematics and evolutionSystematics Association Special Volume Series 71 1-18
BUCK WR amp B GOFFINET (2000) Morphology and classification of mosses - In SHAWAJ amp B GOFFINET (eds) Bryophyte Biology pp 71-123 Cambridge University PressCambridge
CHIANG TY BA SCHAAL amp CI PENG (1998) Universal primers for amplification andsequencing a noncoding spacer between atpB and rbcL genes of chloroplast DNA - Bot Bull AcadSin 39 245-250
COX CJ B GOFFINET AE NEWTON AJ SHAW amp TAJ HEDDERSON (2000)Phylogenetic relationships among the diplolepideous-alternate mosses (Bryidae) inferred from nuclearand chloroplast DNA sequences - Bryologist 103 224-241
COX CJ B GOFFINET AJ SHAW amp SB BOLES (2004) Phylogenetic relationships amongthe mosses based on heterogeneous Bayesian analysis of multiple genes from multiple genomiccompartments - Syst Bot 29 234-250
CRANDALL-STOTLER B (1986) Morphogenesis developmental anatomy and bryophytephylogenetics contra-indications of monophyly - J Bryol 14 1-23
CROSBY MR RE MAGILL B ALLEN amp S HE (1999) A checklist of the mosses - MissouriBotanical Garden St Louis Missouri
DOWELD A (2001) Prosyllabus Tracheophytorum - GEOS Moscow i-lxxx + 110 pp
DOYLE JJ amp JL DOYLE (1990) Isolation of plant DNA from fresh tissue - Focus 12 13-15
DUFF RJ JC VILLAREAL DC CARGILL amp KS RENZAGLIA (2007) Progress andchallenges towards developing a phylogeny and classification of the hornworts - Bryologist 110214-243
FLEISCHER M (1920) Natuumlrliches System der Laubmoose - Hedwigia 61 390-400
FORREST LL EC DAVIS DG LONG BJ CRANDALL-STOTLER A CLARK ampML HOLLINGSWORTH (2006) Unraveling the evolutionary history of the liverworts (Marchantio-phyta) multiple taxa genomes and analyses - Bryologist 109 303-334
FRAHM J-P amp W FREY (1987) Moosflora 2 Aufl - UTB 1250 Stuttgart
FREY W (1977) Neue Vorstellungen uumlber die Verwandtschaftsgruppen und die Stammesgeschichteder Laubmoose - In FREY W H HURKA amp F OBERWINKLER (Hrsg) Beitraumlge zur Biologieder Pflanzen pp 117-139 Stuttgart
FREY W amp M STECH (2005) A morpho-molecular classification of the liverworts (Hepa-ticophytina Bryophyta) - Nova Hedwigia 81 55-78
FREY W M STECH amp K MEIszligNER (1999) Chloroplast DNA-relationship in palaeoaustralLopidium concinnum (Hypopterygiaceae Musci) An example of steno-evolution in mosses Studiesin austral temperate rain forest bryophytes 2 - Plant Syst Evol 218 67-75
GOFFINET B amp WR BUCK (2004) Systematics of Bryophyta (mosses) from molecules to arevised classification - In GOFFINET B V HOLLOWELL amp R MAGILL (eds) Molecularsystematics of bryophytes Monogr Syst Bot Missouri Bot Gard 98 205-239
GOFFINET B CJ COX AJ SHAW amp TAJ HEDDERSON (2001) The Bryophyta (mosses)Systematic and evolutionary inferences from an rps4 gene (cpDNA) phylogeny - Ann Bot 87191-208
GOFFINET B NJ WICKETT O WERNER RM ROS AJ SHAW amp CJ COX (2007)Distribution and phylogenetic significance of the 71-kb inversion in the plastid genome in Funariidae(Bryophyta) - Ann Bot 99 747-753
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GROTH-MALONEK M D PRUCHNER F GREWE amp V KNOOP (2005) Ancestors oftrans-splicing mitochondrial introns support serial sister group relationships of hornworts and mosseswith vascular plants - Mol Biol Evol 22 117-125
HATTORI S amp H INOUE (1958) Preliminary report on Takakia lepidozioides - J Hattori BotLab 19 133-137
HE-NYGREacuteN X A JUSLEacuteN I AHONEN D GLENNY amp S PIIPPO (2006) Illuminating theevolutionary history of liverworts (Marchantiophyta) - towards a natural classification - Cladistics22 1-31
HEDDERSON TAJ DJ MURRAY CJ COX amp TL NOWELL (2004) Phylogeneticrelationships of haplolepideous mosses (Dicranidae) inferred from rps4 gene sequences - Syst Bot29 29-41
LA FARGE C BD MISHER JA WHEELER DP WALL K JOHANNES S SCHAFFERamp AJ SHAW (2000) Phylogenetic relationships within the haplolepideous mosses - Bryologist103 257-276
LA FARGE C AJ SHAW amp DH VITT (2002) The circumscription of the Dicranaceae(Bryopsida) based on the chloroplast regions trnL-trnF and rps4 - Syst Bot 27 435-452
MAGOMBO ZLK (2003) The phylogeny of basal peristomate mosses evidence from cpDNAand implications for peristome evolution - Syst Bot 28 24-38
MCNEILL J FR BARRIE HM BURDET V DEMOULIN DL HAWKSWORTHK MARHOLD DH NICOLSON J PRADO PC SILVA JE SKOG JH WIERSEMA ampNJ TURLAND (2006) International Code of Botanical Nomenclature (Vienna Code) - RegnumVegetabile 146 1-568
MUumlLLER K (2004) PRAP - computation of Bremer support for large data sets - Mol PhylogenetEvol 31 780-782
MUumlLLER K (2005) SeqState - primer design and sequence statistics for phylogenetic DNA datasets - Appl Bioinformatics 4 65-69
MUumlLLER K D QUANDT J MUumlLLER amp C NEINHUIS (2005) PhyDE v0992 PhylogeneticData Editor - httpwwwphydede
MURRAY BM (1988) Systematics of the Andreaeopsida (Bryophyta) two orders with links toTakakia - Nova Hedwigia Beih 90 289-336
NEWTON AE amp RS TANGNEY (eds) (2007) Pleurocarpous mosses systematics and evolutionSystematics Association Special Volume Series 71 CRC Press Boca Raton 434 pp
NEWTON AE CJ COX JG DUCKETT JA WHEELER B GOFFINET TAJ HEDDER-SON amp BD MISHLER (2000) Evolution of the major moss lineages Phylogenetic analyses basedon multiple gene sequences and morphology - Bryologist 103 187-211
NEWTON AE N WIKSTROumlM NE BELL LL FORREST amp MS IGNATOV (2007)Dating the diversification of the pleurocarpous mosses - In NEWTON AE amp RS TANGNEY(eds) Pleurocarpous mosses systematics and evolution Systematics Association Special VolumeSeries 71 337-366
NIXON KC (1999) The parsimony ratchet a new method for rapid parsimony analysis - Cladistics15 407-411
OBRIEN TJ (2007) The phylogenetic distribution of pleurocarpous mosses evidence fromcpDNA sequences - In NEWTON AE amp RS TANGNEY (eds) Pleurocarpous mossessystematics and evolution Systematics Association Special Volume Series 71 19-41
OCHYRA R (2002) Nomenclatural changes in subfamilies of the Dicranaceae - CryptogamieBryol 23 345-349
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OCHYRA R J ŻARNOWIEC amp H BEDNAREK-OCHYRA (2003) Census catalogue ofPolish mosses - Biodiv Poland 3 1-372
PEDERSEN N amp AE NEWTON (2007) Phylogenetic and morphological studies within thePtychomniales with emphasis on the evolution of dwarf males - In NEWTON AE amp RSTANGNEY (eds) Pleurocarpous mosses systematics and evolution Systematics AssociationSpecial Volume Series 71 367-392
QUANDT D amp M STECH (2005) Molecular evolution and secondary structure of the chloroplasttrnL intron in bryophytes - Mol Phylogenet Evol 36 429-443
QUANDT D K MUumlLLER amp S HUTTUNEN (2003) Characterisation of the chloroplast DNApsbT-H region and the influence of dyad symmetrical elements on phylogenetic reconstructions -Plant Biol 5 400-410
QUANDT D K MUumlLLER M STECH W FREY KW HILU amp T BORSCH (2004) Molecularevolution of the chloroplast trnL-F-region in land plants - In GOFFINET B V HOLLOWELL ampR MAGILL (eds) Molecular systematics of bryophytes Monogr Syst Bot Missouri Bot Gard98 13-37
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QIU Y-L Y CHO JC COX amp JD PALMER (1998) The gain of three mitochondrial intronsidentifies liverworts as the earliest land plants - Nature 394 671-674
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RENZAGLIA KS S SCHUETTE RJ DUFF R LIGRONE AJ SHAW BD MISHLER ampJG DUCKETT (2007) Bryophyte phylogeny Advancing the molecular and morphological frontiers- Bryologist 110 179-213
SAMIGULLIN TH SP YACENTYUK GV DEGTYARYEVA KM VALIEJO-ROMANVK BOBROVA I CAPESIUS WF MARTIN AV TROITSKY VR FILIN amp ASANTONOV (2002) Paraphyly of bryophytes and close relationships of hornworts and vascularplants inferred from analysis of chloroplast rDNA ITS (cpITS) sequences - Arctoa 11 31-43
SANG T DJ CRAWFORD amp TF STUESSY (1997) Chloroplast DNA phylogeny reticulateevolution and biogeography of Paeonia (Paeoniaceae) - Amer J Bot 84 1120-1136
SHAW AJ amp KS RENZAGLIA (2004) Phylogeny and diversification of bryophytes - AmerJ Bot 91 1557-1581
SHAW AJ CJ COX amp B GOFFINET (2005) Global patterns of moss diversity taxonomic andmolecular inferences - Taxon 54 337-352
STECH M (1999a) A reclassification of Dicranaceae (Bryopsida) based on non-coding cpDNAsequence data - J Hattori Bot Lab 86 137-159
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STECH M (2004) Supraspecific circumscription and classification of Campylopus Brid(Dicranaceae Bryopsida) based on molecular data - Syst Bot 29 817-824
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21
STECH M D QUANDT amp W FREY (2003) Molecular circumscription of the hornworts(Antho-cerotophyta) based on the chloroplast DNA trnL-trnF region - J Plant Res 116 389-398
STOTLER RE amp B CRANDALL-STOTLER (2005) A revised classification of theAnthocerotophyta and a checklist of the hornworts of North America north of Mexico - Bryologist108 16-26
SWOFFORD DL (2002) PAUP Phylogenetic analysis using parsimony (and other methods)version 40b10 - Sunderland MA
TABERLET P L GIELLY G PAUTOU amp J BOUVET (1991) Universal primers for amplificationof three non-coding regions of chloroplast DNA - Plant Mol Biol 17 1105-1109
TSUBOTA H Y AGENO B ESTEacuteBANEZ T YAMAGUCHI amp H DEGUCHI (2003)Molecular phylogeny of the Grimmiales (Musci) based on chloroplast rbcL sequences - Hikobia 1455-70
TSUBOTA H E DE LUNA D GONZAacuteLEZ MS IGNATOV amp H DEGUCHI (2004) Molecularphylogenetics and ordinal relationships based on analyses of a large-scale data set of 600 rbcLsequences of mosses - Hikobia 14 149-170
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VITT DH B GOFFINET amp T HEDDERSON (1998) 8 The ordinal classification of the mossesquestions and answers for the 1990s - In BATES JW NW ASHTON amp JG DUCKETT (eds)Bryology for the twenty-first century British Bryol Soc pp 113-123
Received 3 September 2007 accepted in revised form 30 October 2007
2
(hornworts) In contrast to the latter two groups mosses are scarcely characterisedin terms of morphological-anatomical synapomorphies At the molecular levelhowever all three bryophyte lineages are well circumscribed (eg Qiu et al 1998Stech et al 2003 Cox et al 2004 Shaw amp Renzaglia 2004 Groth-Malonek et al2005 Forrest et al 2006 Qiu et al 2006) A general overview of the present state ofbryophyte phylogeny was recently provided by Renzaglia et al (2007)
In the 19th and 20th century different and often contradictory classification systemsof mosses were published which either relied more on gametophytic or on sporophyticcharacters (summarised for example in Buck 2007) Nowadays the phylogeneticsignificance of morphological-anatomical characters can be evaluated based onmolecular phylogenies The most recent classifications of liverworts (Frey amp Stech2005 He-Nygreacuten et al 2006) hornworts (Stotler amp Crandall-Stotler 2005 Duff etal 2007) and mosses (Goffinet amp Buck 2004) already integrated molecular and non-molecular characters to provide a consensus of the current knowledge Howeverseveral suprageneric relationships within the mosses remained unresolved orambiguous at the time of the Goffinet amp Buck (2004) classification such as ordinalrelationships within the Bryidae and the closest relatives of pleurocarpous mossesA number of recent attempts shed more light on these problematic relationships(eg Tsubota et al 2004 Shaw et al 2005 Stech amp Quandt 2006 Bell et al 2007Goffinet et al 2007 contributions in Newton amp Tangney 2007 Quandt et al 2007this paper) Although some clades of the moss phylogeny are still partly contradictoryor do not receive significant statistical support these studies seem to converge on acommon hypothesis of moss relationship at suprageneric levels allowing us toestablish an updated and revised classification
In the present study a molecular phylogeny of the Bryopsida is presented based on anew approach ie the combined analysis of solely non-coding plastid markers (trnL
UAAintron atpB-rbcL spacer psbA-trnH spacer) The current state of moss systematicsis discussed with respect to the impact of this approach as well as recently publishedmolecular phylogenies and phylogenomic inferences Finally we propose a newsynopsis of the suprageneric classification of the Bryophyta which updates that ofGoffinet amp Buck (2004) A detailed description of the taxa down to genus level willbe provided by a forthcoming new edition of Englers Syllabus of Plant Familiesfor which additional taxonomic changes are made here
Material and methods
TAXON SAMPLING A molecular data set of 85 species of Bryopsida was assembled by compilingsequences from own previous analyses and by sequencing of herbarium material Voucher informationand GenBank accession numbers are summarised in Table 1 together with indications of the newlysequenced accessions From 21 species all three non-coding markers employed here were newlysequenced In few cases sequences available in GenBank were used to complete the data set Andreaearupestris Hedw (Andreaeopsida) and Pogonatum subulatum (Menzies ex Brid) Brid (Poly-trichopsida) were used as outgroup representatives
DNA EXTRACTION PCR AND SEQUENCING DNA was extracted using the mixer mill MM200 (Retsch)and following the method of Doyle amp Doyle (1990) PCR reactions for trnL intron and atpB-rbcLspacer followed the protocols given in Frey et al (1999) and Stech (2004) and were performed with
3
Tab
le 1
Vou
cher
info
rmat
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and
Gen
Ban
k ac
cess
ion
num
bers
of t
he s
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sed
for t
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B97
0827
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0502
78A
Y86
4297
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1635
06Po
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Pog
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(Men
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rid
Pfe
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r 98
-T20
7AC
HR
F
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AY
0502
77E
U12
4442
EU
1635
05D
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Dip
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fol
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m (
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DM
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4982
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1865
37D
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7161
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3128
99T
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301
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1865
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1271
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9705
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6625
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1866
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3559
01-0
9
Tab
le 1
con
tinu
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5
Rhi
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ahm
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1865
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6622
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1635
57
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1865
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3583
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0102
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6641
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1635
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y 94
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Fre
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0297
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1866
42E
U16
3580
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cott
Plag
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chim
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1003
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U18
6646
EU
1635
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ann
F
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yE
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6575
EU
1866
40E
U16
3578
01-1
87a
Tab
le 1
con
tinu
ed
6
primers CM
DM
(slightly modified after Taberlet et al 1991 see Frey et al 1999) and atpB-1rbcL-1(Chiang et al 1998) respectively For amplification of the psbA-trnH spacer primers psbAF(5-GTT ATG CAT GAA CGT AAT GCT C-3 Sang et al 1997) and trnHR-2 (5-CGC GCA TGGTGG ATT CAC AAT CC-3 slightly modified after Sang et al 1997) were used with a PCRprotocol of 5 min 94degC 35 cycles (30 sec 94degC 1 min 48degC 1 min 40 sec 72degC) 7 min 72degC PCRproducts were purified using DNA purification kits (Qiagen Macherey-Nagel) Sequencing wasperformed as described in Stech (2004) using the amplification primers
ALIGNMENT AND PHYLOGENETIC ANALYSES DNA sequences were manually aligned in PhyDE v0992(Muumlller et al 2005) Following Quandt et al (2003) and Quandt amp Stech (2005) inversions inputative hairpin secondary structures were positionally separated in the alignment their presence orabsence was not coded for the phylogenetic analyses Phylogenetic reconstructions under the maximumparsimony criterion were performed using winPAUP 40b10 (Swofford 2002) in combination withPRAP (Muumlller 2004) as implemented in SeqState (Muumlller 2005) PRAP generates command filesfor PAUP that allow parsimony ratchet searches as designed by Nixon (1999) Heuristic searchesunder parsimony were performed with the following options all characters equally weighted andunordered TBR branch swapping collapse branches if maximum branch length is zero MulTreesoption in effect gaps treated as missing data Initially a heuristic search with 1000 addition sequencereplicates was performed For the parsimony ratchet ten random addition cycles of 200 ratchetiterations each were used with TBR branch swapping on a randomly re-weighted data set (25 ofthe positions) Heuristic bootstrap searches were performed with 1000 replicates with 10 additionsequence replicates per bootstrap replicate
Results
In the present data set of non-coding plastid markers sequence lengths ranged from243 to 368 nucleotides (nt) in the trnL intron and from 445 to 615 nt in the atpB-rbcL spacer The psbA-trnH spacer was considerably shorter than the other twomarkers and ranged from 103 to 186 nt The combined alignment of sequences from85 ingroup and two outgroup taxa comprised 2430 positions (trnL intron 668 atpB-rbcL spacer 1366 psbA-trnH spacer 396 positions) The most variable regions withambiguous alignment (781 positions) were excluded from phylogenetic analysis Ofthe 1649 included positions 628 (381) were variable and 455 of the variablepositions (725 or 276 of the total number of positions) were parsimony-informative The trnL intron comprised 124 the atpB-rbcL spacer 286 and the psbA-trnH spacer 45 of these included parsimony-informative positions
The shortest trees found in the heuristic maximum parsimony analysis of the combineddata set had a length of 2433 steps By applying the parsimony ratchet 129 treeswere retained that were one step shorter (length 2432 CI = 0419 RI = 0624) Thestrict consensus tree of the ratchet analysis is shown in Fig 1 The ingroup (Bryopsida)is supported with 100 bootstrap support (BS) Diphysciidae are sister to theremaining Bryopsida with 54 BS Encalyptidae Funariidae Timmiidae andDicranidae all receive gt 95 BS while Bryidae are slightly less supported (89BS) Relationships between these major lineages are resolved but unsupported Atordinal level within the Bryidae a lower resolution is observed SplachnalesOrthotrichales Aulacomniales Hypnodendrales Hookeriales and Hypnales areresolved as monophyletic with 67-100 BS whereas Hedwigiales BartramialesBryales Orthodontiales and Rhizogoniales are not A closer relationship ofOrthotrichales with the pleurocarpous mosses sl than with the more basal ordersHedwigiales Bartramiales Splachnales and Bryales is indicated
7
Discussion
Classification of mosses - recent progress and the current state
For a long time mosses were subdivided into three main lineages the subclassesSphagnidae Andreaeidae and Bryidae (eg Fleischer 1920 Vitt 1984 Frahm ampFrey 1987) the latter with a number of (super-)orders (eg Frey 1977) Howevermolecular data confirmed that mosses comprise a number of isolated basal lineagesrepresented by morphologically and ecologically distinct extant taxa such as TakakiaSphagnum Andreaea Andreaeobryum Oedipodium Tetraphis the Polytrichaceaeand Buxbaumia which probably have long independent phylogenetic histories (cfNewton et al 2007) As a result of molecular phylogenies and a re-evaluation ofmorphological-anatomical characters the classification of mosses has changedconsiderably in the last few years with the main lineages nowadays treated atsubdivision class and subclass levels within division Bryophyta (eg Doweld 2001Ochyra et al 2003 Goffinet amp Buck 2004 this study)
Takakia and Sphagnum are the earliest diverging moss taxa in molecular phylogenies(eg Newton et al 2000 Beckert et al 2001 Cox et al 2004 Qiu et al 2006Newton et al 2007) That Takakia is a moss and not a liverwort was confirmed byanalysis of DNA sequences and phylogenomic characters such as the distribution ofmitochondrial introns (eg Beckert et al 2001) Its taxonomic status however stillremains to be clarified On the one hand most molecular studies resolve Takakiaand Sphagnum as sister genera although only partly with high statistical supportThese molecular topologies do not support the recognition of division Takakiophytaas proposed by Crandall-Stotler (1986) One the other hand no morphologicalsynapomorphies unite Takakia with Sphagnum and significant molecular differencesseparating Takakia from all other mosses were also observed For example a regionin the plastid ITS3 is similar to that of other land plants but absent in mosses(Samigullin et al 2002) and a transition in the trnL
UAA gene changing the anticodon
to CAA was otherwise only found in leptosporangiate ferns and Ginkgo (Quandt etal 2004) Thus ldquoresolution of Sphagnum - Takakia clade may be an artifactrdquo (Shawamp Renzaglia 2004) Also Goffinet amp Buck (2004) did not unite Takakia and Sphagnumunder a formal taxonomic rank but placed them into different informal superclassesIn our opinion Takakia should be treated at the same level as Sphagnophytina andBryophytina (cf Doweld 2001) ie as a subdivision of Bryophyta However morefundamental nomenclatural changes are necessary as the family name Takakiaceaewas not validated in the original publication by Hattori amp Inoue (1958) (article411 of ICBN McNeill et al 2006) and consequently all higher taxa erected laterare invalid The corrected taxonomic treatment of Takakia is provided here withsporophytic characters included in the latin diagnosis of Takakiaceae (see taxonomy)
Within Bryophytina we recognise four morphologically and molecularly isolatedbasal lineages as separated from the arthrodontous mosses (Bryopsida) Andreaeopsida(with linear capsule dehiscence) the operculate but eperistomate Oedipodiopsida aswell as Polytrichopsida and Tetraphidopsida with nematodontous peristomes A fifthclass Andreaeobryopsida was erected by Buck amp Goffinet (2000) but re-includedin Andreaeopsida as a subclass by Ochyra et al (2003) The systematic status of
8
Andreaeobryum macrosporum Steere amp BMMurray and possible relationships withAndreaea and Takakia were discussed by Murray (1988) and summarised includingmolecular results by Shaw amp Renzaglia (2004)
On the next lower level a number of morphologically and molecularly divergentlineages are nowadays treated as subclasses of Bryopsida Buxbaumiidae andDiphysciidae are generally branching off first in molecular topologies (eg Beckertet al 2001 Magombo 2003 Cox et al 2004) followed by Timmiidae Encalyptidaeand Funariidae as well as Dicranidae (haplolepideous mosses) sister to Bryidae slThese subclasses (except Buxbaumiidae not included) are also well recognizable inthe present analysis of non-coding plastid sequences (Fig 1)
The morphologically very different Encalyptidae and Funariidae are revealed assister groups although mostly without high support in several molecular phylogenies(eg Goffinet et al 2001 Cox et al 2004 Hedderson et al 2004 Tsubota et al2003 2004) and also in the present study (Fig 1) Goffinet et al (2007) confirmedthis relationship by phylogenomic evidence namely a large (71 kb) inversion in thechloroplast genome of Funariaceae Disceliaceae and Encalyptaceae but not inGigaspermaceae Consequently the latter family was separated at ordinal level fromthe two remaining families of Funariales by Goffinet et al (2007) GigaspermalesFunariales and Encalyptales may share a common ancestor according to some butnot all molecular phylogenies (eg Goffinet et al 2001 2007 Hedderson et al2004 but not in Tsubota et al 2004) Although ontogenetic data from peristomedevelopment may support their common ancestry (Goffinet et al 2007) unambiguousmorphological synapomorphies are lacking We therefore propose to treatGigaspermaceae at subclass level within the Bryopsida (see taxonomy)
The haplolepideous mosses (Dicranidae) are clearly supported as a monophyleticlineage which obviously evolved from a diplolepideous ancestor according to theirposition in the molecular trees (eg Newton et al 2000 Tsubota et al 2003 Cox etal 2004 Goffinet amp Buck 2004) Molecular studies suitable for inferring ordinaland family level relationships within Dicranidae either focused on the haplolepideousmosses (eg Stech 1999ab 2004 LaFarge et al 2000 2002 Tsubota et al 2003Hedderson et al 2004) or included more than 15 haplolepideous taxa in analyses ofa broader range of mosses (eg Goffinet et al 2001 Tsubota et al 2004 this study)Major lineages supported by these analyses are for example Grimmiales(Grimmiaceae Ptychomitriaceae and Seligeriaceae) Leucobryaceae (incl formerDicranaceae-Campylopoideae and Paraleucobryoideae pp) Dicranaceae sstr(Dicranoideae plus former Dicnemonaceae and Paraleucobryoideae pp) Pottiaceae(incl Cinclidotaceae and Splachnobryum) and Calymperaceae (probably exclOctoblepharum) Furthermore several genera and families belong to Dicranidaewhose systematic positions have been controversial (eg Stech et al 1999b LaFarge et al 2002 Hedderson et al 2004 OBrien 2007 Quandt et al 2007 thisstudy) Amphidium Archidium Catoscopium Drummondia EphemeraceaeErpodiaceae Mittenia (cf OBrien 2007 sequences in some earlier analyses werebased on misdentified specimens) Rhachitheciaceae Schistostega Splachnobryumand Wardia On the contrary several problems remain such as the circumscriptionof Ditrichaceae and relationships of the major haplolepideous lineages in general
9
Fig 1 Strict consensus tree of 129 most parsimonious trees inferred from combined trnLUAA
intronatpB-rbcL spacer and psbA-trnH spacer sequences of 85 taxa of Bryopsida as well as Andreaearupestris (Andreaeopsida) and Pogonatum subulatum (Polytrichopsida) as outgroup representativesBootstrap support values gt50 are depicted above the branches
10
Consequently resolving the phylogeny of Dicranidae with confidence is one of themajor future challenges in moss systematics
As mentioned above Dicranaceae are monophyletic in a narrow circumscriptionaccording to molecular data In contrast to former Campylopoideae andParaleucobryoideae the status of Rhabdoweisioideae (= Oncophoroideae Ochyra2002) and Dicranelloideae needs further consideration Stech (1999ab) suggestedto recognise RhabdoweisioideaeRhabdoweisiaceae in a broad sense includingDicranoweisia Amphidium and Aongstroemia Subsequent molecular analysesconfirmed a close relationship of the genera Arctoa Cynodontium DicranoweisiaKiaeria Oncophorus Oreoweisia Oreas Rhabdoweisia and Symblepharis althoughwithout significant support (La Farge et al 2002 Tsubota et al 2003 Hedderson etal 2004) With respect to the molecular evidence available so far we propose toelevate Oncophoroideae to family level to accomodate these genera and perhapsGlyphomitrium (cf Tsubota et al 2003) whereas we consider AongstroemiaDichodontium and Diobelonella to belong to Aongstroemiaceae (cf Stech 1999a)Amphidium is neither closely related to Dicranaceae sstr nor to Oncophoroideae(La Farge et al 2002 Tsubota et al 2003 Hedderson et al 2004 Stech 2004 thisstudy) and should be treated at family level rather than placed in Dicranaceae assubfam Amphidioideae (Ochyra et al 2003) The circumscription of Dicranelloideaeis more difficult to evaluate as few representatives have been included in molecularanalyses However Dicranella heteromalla (Hedw) Schimp as well as the generaCampylopodium and Microcampylopus are clearly separated from Dicranaceae sstr(Stech 1999a 2004 La Farge et al 2002 Tsubota et al 2003 Hedderson et al2004) and consequently the subfamily deserves family status as well Finallymolecular data showed that the genus Hypodontium does not belong to Pottiaceae(Hedderson et al 2004 Tsubota et al 2004) Taxonomic conclusions have not beendrawn from these results which is made up here (see taxonomy)
All mosses with diplolepideous-alternate peristomes together with Splachnales witha diplolepideous-opposite (Funaria-type) peristome form a monophyletic group inmolecular analyses (eg Newton et al 2000 Beckert et al 2001 Goffinet et al2001 Cox et al 2004 Tsubota et al 2004 references in Table 2) Differentclassifications of this by far most species-rich group of mosses were proposed (egVitt et al 1998 Ochyra et al 2003 Goffinet amp Buck 2004) However at least someof the recognised subclasses and superorders are paraphyletic according to themolecular topologies and assigning formal ranks to all evolutionarily significantmonophyletic entities is problematic if the main taxonomic framework of Bryophytaand Bryopsida should be maintained (cf discussion in Bell et al 2007) Thereforein the present synopsis only one subclass Bryidae is recognised for all diplolepideous-alternate mosses and Splachnales This broadly defined Bryidae is subdivided into13 orders most of them resolved as monophyletic in the majority of the phylogeneticanalyses summarised in Table 2 although with different levels of statistical supportin maximum parsimony analyses To define monophyletic lineages at supraordinallevel informal node-based names may be chosen according to Bell et al (2007) Forexample the pleurocarpous mosses (pleurocarpy sensu Bell amp Newton 2007) andtheir closest acrocarpous relatives (Orthodontiales to Hypnales) were already
11
Table 2 Taxon sampling and bootstrap support (BS) for Dicranidae Bryidae and orders within theBryidae in recent phylogenetic analyses (MP only) based on combined molecular markers Markersare given in square brackets (non-coding regions in bold) numbers of included taxa in brackets ++respective clade present with ge 80 BS + clade present with lt 80 BS - clade not present no oronly one representative included
Bell amp Newton OBrien Quandt et al Bell et al this study(2004) (2007) (2007) (2007)
[rbcL rps4 [atpB atpB- [rbcL rps4 [rbcL rps4 [atpB-rbcLnad5] rbcL rbcL trnL-F nad5] trnL-F nad5] psbA-trnH
rps4 trnL-F] trnL]
Dicranidae + (2) + (4) ++ (3) (1) ++ (19)Bryidae ++ (57) + (53) ++ (52) ++ (98) ++ (58)Hedwigiales ++ (2) (1) ++ (2) ++ (2) - (3)Bartramiales ++ (2) ++ (4) ++ (4) ++ (3) - (4)Splachnales (0) ++ (2) ++ (3) ++ (2) ++ (5)Bryales - (4) - (5) ++ (18) + (17) - (8)Orthotrichales (1) ++ (3) ++ (3) ++ (2) ++ (4)Orthodontiales + (4) + (4) + (3) + (6) - (3)Aulacomniales + (6) + (7) ++ (2) + (7) + (3)Rhizogoniales ++ (13) + (8) ++ (5) ++ (14) - (3)Hypnodendrales ++ (13) + (7) ++ (4) ++ (29) ++ (6)Ptychomniales ++ (3) ++ (3) (1) ++ (4) (1)Hookeriales - (4) + (2) (1) + (2) + (8)Hypnales - (5) - (7) ++ (5) ++ (10) + (10)
summarised under the informal node based name pleurcarpids (Bell et al 2007)and can be distinguished from a basal grade of acrocarpous or cladocarpous lineages(Hedwigiales to Orthotrichales) Within the latter monophyly of BartramialesSplachnales and Orthotrichales is well-supported in all analyses including two ormore taxa except Bartramiales in the present data set (cf Fig 1) In contrast Bryalesreceive significant support less frequently (but see Bell et al 2007 Quandt et al2007) Hedwigiales are well supported if only Hedwigia (Hedwigiaceae) andRhacocarpus (Rhacocarpaceae) are included whereas the monospecific Helicophyllum(Helicophyllaceae) is not closely related to these taxa but shows affinities withBartramiales (Goffinet et al 2001 this study) With respect to the differentmorphologies of Helicophyllaceae and Bartramiaceae however the former shouldbe separated at ordinal level (see taxonomy)
Clarifying relationships of the Orthotrichales is still a difficult issue Analyses ofsingle chloroplast markers or parsimony analyses of combined markers from differentgenomes mostly indicated a close relationship either with Splachnales (eg Cox etal 2000 Newton et al 2000 Tsubota et al 2004 Quandt et al 2007) or with thepleurocarpids (Goffinet et al 2001 this study) Although none of these alternativesis well-supported the latter seems more likely with regard to the moderately tomaximally supported Orthotrichales - pleurocarpid sister group relationship in allanalyses of mitochondrial data and in likelihood analyses of combined plastidmitochondrial markers (Beckert et al 2001 Quandt et al 2007)
12
The molecular polyphyly of Rhizogoniaceae (eg Bell amp Newton 2004) was solvedby the transfer of rhizogonioid genera into broadly defined Aulacomniaceae andOrthodontiaceae (Bell et al 2007) which now include both acrocarpous andpleurocarpous taxa These systematic changes are also comprehensible by non-molecular characters such as morphological traits shared by Mesochaete andAulacomnium heterostichum (Hedw) Bruch amp Schimp or the variously reducedperistomes of Orthodontiaceae pp in contrast to the generally fully developed Bryum-type peristomes of rhizogonioid and hypnodendroid mosses (Bell et al 2007) Theposition of the solely pleurocarpous Hypnodendrales sister to the former Hypnidaeled to the recognition of the informal group core pleurocarps (Bell et al 2007)The former Hypnidae (Ptychomniales Hookeriales and Hypnales summarised ashomocostate pleurocarps) are monophyletic in most molecular analyses (eg Goffinetet al 2001 Tsubota et al 2004 Bell et al 2007) with Ptychomniales being well-supported (Pedersen amp Newton 2007 Table 2) Clarifying relationships betweenHookeriales and Hypnales and within the latter is still a challenge but recent molecularstudies seem to support a sister group relationship of both orders (Bell et al 2007present study)
Phylogenetic utility of non-coding plastid markers
Non-coding plastid markers that comprise both variable and conserved regionssuch as the trnL
UAA intron have repeatedly been shown to possess potential for
resolving relationships at high taxonomic levels (eg Borsch et al 2003 Quandtet al 2004) Both the trnL intron and atpB-rbcL spacer were characterised indetail in mosses with respect to their structure and molecular evolution (Quandt ampStech 2005 Stech amp Quandt 2006) They include conservative regions that can beunambiguosly aligned and even parts of the more variable regions can be used ifrepeats hairpin loops etc are correctly identified and adequately treated in thephylogenetic analyses (eg Quandt et al 2003 Quandt amp Stech 2005) Using theatpB-rbcL spacer alone (Stech amp Quandt 2006) relationships of the major mosslineages were largely consistent with the ldquototal evidencerdquo molecular tree of Goffinetamp Buck (2004) However in addition to general limitations that result from singlemarker analyses the use of non-coding markers may pose further problems suchas a high amount of homoplasy resulting in low resolution or low statistical supportfor many clades Therefore several recent molecular studies of relationships withinBryidae have employed both coding and non-coding markers (Table 2)Nevertheless the usefulness of analyses of combined non-coding plastid markerscannot be ruled out In fact Fig 1 and Table 2 indicate a phylogenetic signal inthe present data set as many clades are recovered that are usually also resolvedin analyses of coding or combined coding and non-coding markers Especiallywith regard to statistical support however the present analysis is inferior tothose of other recent data sets especially Bell et al (2007) and Quandt et al(2007) In addition the non-coding markers used here are of different suitabilityand even the two intergenic spacers differ considerably from each other ThepsbA-trnH spacer contributes much less to the trees resolution than the atpB-rbcL spacer first because it is much shorter and second because relatively largeparts are attributed to hairpin loops or otherwise hypervariable regions These
13
results indicate that future studies should evaluate the molecular evolution andphylogenetic potential of new markers both coding and con-coding and choosethe most suitable ones in a combined analysis to resolve the remaining uncertaintiesin moss phylogeny
Taxonomy
Takakiaceae Stech amp WFrey stat nov
Plantae virides nusquam rhizophorae sine protonemate e caudicis rhizomatis erectae Caudicesrhizomati et axes geotropi radiformes frequenter intercalariter ramificantes sine phyllidiis cumpapillis mucilaginis rostratis Caules phyllidiiferi saepe furcati Phyllidia sine lamina et costadistincta profunde 2-4(-5)-lobata pluristratosa tristicha sed torsione spiraliter disposita Filumcentralium in ambabus generationibus (axibus gametophyti et setis) adest Plantae dioicae Antheridiaet archegonia nuda Sporophytum terminale solitarium Seta persistens Capsula tortilis admaturitatem schizocarpa secus unam rimam spiralem longitudinalem dehiscens Stomata etoperculum absunt peristomium nullum Calyptra mitriformis
TYPUS Takakia SHatt amp Inoue J Hattori Bot Lab 19 137 1958
Takakiaceae SHatt amp Inoue J Hattori Bot Lab 19 137 1958 nom inval (Art 411)
Takakiales Stech amp WFrey stat nov
Based on Takakiaceae Stech amp WFrey Nova Hedwigia 86 13 2008
TYPUS Takakia SHatt amp Inoue J Hattori Bot Lab 19 137 1958
Takakiales SHatt amp Inoue J Hattori Bot Lab 19 137 1958 nom inval
Takakiales SHatt amp Inoue ex RMSchust J Hattori Bot Lab 26 224 1963 nom inval (cumdescr latin)
Takakiopsida Stech amp WFrey statnov
Based on Takakiaceae Stech amp WFrey Nova Hedwigia 86 13 2008
TYPUS Takakia SHatt amp Inoue J Hattori Bot Lab 19 137 1958
Takakiopsida Goffinet amp WRBuck Monogr Syst Bot Missouri Bot Gard 98 232 2004 nominval
Takakiopsida Jia et al Acta Phytotax Sin 41 350 351 2003 nom nud
Takakiopsida Wang amp Wu Fl Bryophyt Sin 8 447 2004 nom inval (cum descr latin)
Takakiophytina Stech amp WFrey stat nov
Based on Takakiaceae Stech amp WFrey Nova Hedwigia 86 13 2008
TYPUS Takakia SHatt amp Inoue JHattori Bot Lab 19 137 1958
Gigaspermidae Stech amp WFrey subclass nov
Plantae acrocarpae terrestres stoloniferae ramis brevibus erectis Folia unicostata cellulis laxislaevibus Capsula plerumque valde rugosa gymnostomatica vel cleistocarpa stomata cum duabuscellulis sociis Ab Funariidis et Encalyptidis charactere phylogenomico (71-kb inversio abest)separatae
14
TYPUS Gigaspermum Lindb Oumlfversigt af Foumlrhandlingar Kongl Svenska Vetenskaps-Akademien21 599 1865
Amphidiaceae Stech stat nov
Based on Dicranaceae subfam Amphidioideae Ochyra in Ochyra Zarnowiec amp Bednarek-OchyraCens Cat Polish Mosses 110 2003
TYPUS Amphidium Schimp Coroll Bryol Eur 39 1856
Amphidiaceae AJESm Moss Fl Britain Ireland 2nd ed 657 2004 nom inval descr angl
Dicranellaceae Stech stat nov
Based on Dicranaceae subfam Dicranelloideae Lindb Utkast Eur Bladmoss 33 1878[lsquoUnderfamilje Dicranelleaersquo]
TYPUS Dicranella (MuumlllHal) Schimp Coroll Bryol Eur 13 1856
Oncophoraceae Stech stat nov
Based on Dicranaceae subfam Oncophoroideae Lindb Utkast Eur Bladmoss 34 1878[lsquoUnderfamilje Oncophoreaersquo]
TYPUS Oncophorus (Brid) Brid Bryol Univ 1 389 1826
Hypodontiaceae Stech fam nov
Plantae robustae characteribus morphologicis Pottiaceis et Calymperaceis similes sedcharacteribus molecularicis separatae Bracteae perichaetiales internae e basi vaginantes subulataevel aristatae Capsula aspectu succulenta cellulae exothecii incrassatae annulus magnopereabsens Peristomii dentes breves triangulati incurvati aurantiaci leves vel infirme verrucosiCalyptra cucullata
TYPUS Hypodontium MuumlllHal Hedwigia 38 96 1899
Helicophyllales Stech amp WFrey ord nov
Plantae acrocarpae prostratae tomentosae Folia dimorpha in duas series laterales et unam seriemventralem divisa Costa percurrens Cellulae hexagonae ad subquadratae papillosae Capsula immersacupulata ad oblonga infra orificium abrupte incurvata stomata destituta Peristomium nullum Sporaeisomorphae heteropolares granulatae
TYPUS Helicophyllum Brid Bryol Univ 2 771 1827
Synopsis of the suprageneric classification of BryophytaAuthor citations are in accordance with Art 492 of the Vienna Code (McNeill et al 2006)
Subdivision Takakiophytina Stech amp WFreyClass Takakiopsida Stech amp WFrey
Order Takakiales Stech amp WFreyTakakiaceae Stech amp WFrey
Subdivision Sphagnophytina DoweldClass Sphagnopsida Schimp
Order Sphagnales Limpr
15
Sphagnaceae DumortOrder Ambuchananiales Seppelt amp HACrum
Ambuchananiaceae Seppelt amp HACrumSubdivision Bryophytina Engler
Class Andreaeopsida JHSchaffnSubclass Andreaeidae Engl
Order Andreaeales LimprAndreaeaceae Dumort
Subclass Andreaeobryidae OchyraOrder Andreaeobryales BMMurray
Andreaeobryaceae Steere amp BMMurrayClass Oedipodiopsida Goffinet amp WRBuck
Order Oedipodiales Goffinet amp WRBuckOedipodiaceae Schimp
Class Tetraphidopsida Goffinet amp WRBuckOrder Tetraphidales MFleisch
Tetraphidaceae SchimpClass Polytrichopsida Doweld
Order Polytrichales MFleischPolytrichaceae Schwaumlgr
Class Bryopsida PaxSubclass Buxbaumiidae Doweld
Order Buxbaumiales MFleischBuxbaumiaceae Schimp
Subclass Diphysciidae OchyraOrder Diphysciales MFleisch
Diphysciaceae MFleischSubclass Timmiidae Ochyra
Order Timmiales OchyraTimmiaceae Schimp
Subclass Encalyptidae Ochyra Żarnowiec amp Bednarek-OchyraOrder Encalyptales Dixon
Encalyptaceae SchimpSubclass Funariidae Ochyra
Order Funariales MFleischFunariaceae Schwaumlgr Disceliaceae Schimp
Subclass Gigaspermidae Stech amp WFreyOrder Gigaspermales Goffinet Wickett OWerner Ros AJShaw amp CJCox
Gigaspermaceae LindbSubclass Dicranidae Doweld
Order Catoscopiales Ignatov amp IgnatovaCatoscopiaceae Broth
Order Scouleriales Goffinet amp WRBuckDrummondiaceae Goffinet Scouleriaceae SPChurchill
Order Bryoxiphiales HACrum amp LEAndersonBryoxiphiaceae Besch
16
Order Grimmiales MFleischGrimmiaceae Arn Ptychomitriaceae Schimp Seligeriaceae Schimp
Order Archidiales LimprArchidiaceae Schimp
Order Mitteniales ShawMitteniaceae Broth
Order Dicranales HPhilib ex MFleischAmphidiaceae Stech Aongstroemiaceae De Not BruchiaceaeSchimp Calymperaceae Kindb Dicranaceae Schimp Dicranel-laceae Stech Ditrichaceae Limpr Erpodiaceae Broth EustichiaceaeBroth Fissidentaceae Schimp Leucobryaceae Schimp Onco-phoraceae Stech Rhachitheciaceae HRob Schistostegaceae SchimpViridivelleraceae IGStone Wardiaceae Welch
Order Pottiales MFleischEphemeraceae Schimp Hypodontiaceae Stech PleurophascaceaeBroth Pottiaceae Schimp Serpotortellaceae WDReese amp RHZander
Subclass Bryidae EnglOrder Hedwigiales Ochyra
Hedwigiaceae Schimp Rhacocarpaceae KindbOrder Helicophyllales Stech amp WFrey
Helicophyllaceae BrothOrder Bartramiales DQuandt NEBell amp Stech
Bartramiaceae SchwaumlgrOrder Splachnales Ochyra
Meesiaceae Schimp Splachnaceae Grev amp ArnOrder Bryales Limpr
Bryaceae Schwaumlgr Leptostomataceae Schwaumlgr Mniaceae SchwaumlgrPhyllodrepaniaceae Crosby Pseudoditrichaceae Steere amp ZIwatsPulchrinodaceae DQuandt NEBell amp Stech
Order Orthotrichales DixonOrthotrichaceae Arn
Order Orthodontiales NEBell AENewton amp DQuandtOrthodontiaceae Goffinet
Order Aulacomniales NEBell AENewton amp DQuandtAulacomniaceae Schimp
Order Rhizogoniales Goffinet amp WRBuckRhizogoniaceae Broth
Order Hypnodendrales NEBell AENewton amp DQuandtBraithwaiteaceae NEBell AENewton amp DQuandt Hypnodendra-ceae Broth Pterobryellaceae WRBuck amp Vitt Racopilaceae Kindb
Order Ptychomniales WRBuck CJCox AJShaw amp GoffinetPtychomniaceae MFleisch
Order Hookeriales MFleischDaltoniaceae Schimp Hookeriaceae Schimp HypopterygiaceaeMitt Leucomiaceae Broth Pilotrichaceae Kindb SaulomataceaeWRBuck CJCox AJShaw amp Goffinet Schimperobryaceae WR
17
Buck CJCox AJShaw amp GoffinetOrder Hypnales WRBuck amp Vitt
Amblystegiaceae GRoth Anomodontaceae Kindb BrachytheciaceaeSchimp Calliergonaceae Vanderpoorten Hedenaumls CJCox amp AJShaw Catagoniaceae WRBuck amp Ireland Climaciaceae KindbCryphaeaceae Schimp Echinodiaceae Broth Entodontaceae KindbFabroniaceae Schimp Fontinalaceae Schimp Helodiaceae OchyraHeterocladiaceae Ignatov amp Ignatova Hylocomiaceae MFleischHypnaceae Schimp Lembophyllaceae Broth LeptodontaceaeSchimp Lepyrodontaceae Broth Leskeaceae Schimp Leucodon-taceae Schimp Meteoriaceae Kindb Microtheciellaceae HAMillamp AJHarr Myriniaceae Schimp Myuriaceae MFleisch NeckeraceaeSchimp Orthorrhynchiaceae SHLin Phyllogoniaceae KindbPlagiotheciaceae MFleisch Pleuroziopsidaceae Ireland Prionodon-taceae Broth Pseudoleskeaceae Schimp PseudoleskeellaceaeIgnatov amp Ignatova Pterigynandraceae Schimp PterobryaceaeKindb Pylaisiaceae Schimp Pylaisiadelphaceae Goffinet amp WRBuck Regmatodontaceae Broth Rhytidiaceae Broth RigodiaceaeHACrum Rutenbergiaceae MFleisch Scorpidiaceae Ignatov ampIgnatova Sematophyllaceae Broth Sorapillaceae MFleisch Ste-reophyllaceae WRBuck amp Ireland Symphyodontaceae MFleischTheliaceae MFleisch Thuidiaceae Schimp TrachylomataceaeWRBuck amp Vitt
Acknowledgements
Sincere thanks are due to JLReveal (Ithaca) as well as WFPrudhomme van Reine and JFVeldkamp(Leiden) for comments and discussions about suprafamilial taxonomy to DQuandt (Dresden) for providingDNA from Rhacocarpus and Bartramiaceae species and to BGiesicke (Berlin) for technical assistance
References
BECKERT S H MUHLE D PRUCHNER amp V KNOOP (2001) The mitochondrial nad2 geneas a novel marker locus for phylogenetic analysis of early land plants a comparative analysis inmosses - Mol Phylogenet Evol 18 117-126
BELL NE amp AE NEWTON (2004) Systematic studies of non-hypnanaean pleurocarps establishinga phylogenetic framework for investigating the origins of pleurocarpy - In GOFFINET BV HOLLOWELL amp R MAGILL (eds) Molecular systematics of bryophytes Monogr Syst BotMissouri Bot Gard 98 290-319
BELL NE amp AE NEWTON (2007) Pleurocarpy in the Rhizogoniaceous grade - In NEWTONAE amp RS TANGNEY (eds) Pleurocarpous mosses systematics and evolution SystematicsAssociation Special Volume Series 71 41-64
BELL NE D QUANDT TJ OBRIEN amp AE NEWTON (2007) Taxonomy and phylogeny inthe earliest diverging pleurocarps square holes and bifurcating pegs - Bryologist 110 533-560
BORSCH T KW HILU D QUANDT V WILDE C NEINHUIS amp W BARTHLOTT(2003) Non-coding plastid trnT-trnF sequences reveal a well resolved phylogeny of basal angiosperms- J Evol Biol 16 558-576
18
BUCK WR (2007) The history of pleurocarp classification two steps forward one step back - InNEWTON AE amp RS TANGNEY (eds) Pleurocarpous mosses systematics and evolutionSystematics Association Special Volume Series 71 1-18
BUCK WR amp B GOFFINET (2000) Morphology and classification of mosses - In SHAWAJ amp B GOFFINET (eds) Bryophyte Biology pp 71-123 Cambridge University PressCambridge
CHIANG TY BA SCHAAL amp CI PENG (1998) Universal primers for amplification andsequencing a noncoding spacer between atpB and rbcL genes of chloroplast DNA - Bot Bull AcadSin 39 245-250
COX CJ B GOFFINET AE NEWTON AJ SHAW amp TAJ HEDDERSON (2000)Phylogenetic relationships among the diplolepideous-alternate mosses (Bryidae) inferred from nuclearand chloroplast DNA sequences - Bryologist 103 224-241
COX CJ B GOFFINET AJ SHAW amp SB BOLES (2004) Phylogenetic relationships amongthe mosses based on heterogeneous Bayesian analysis of multiple genes from multiple genomiccompartments - Syst Bot 29 234-250
CRANDALL-STOTLER B (1986) Morphogenesis developmental anatomy and bryophytephylogenetics contra-indications of monophyly - J Bryol 14 1-23
CROSBY MR RE MAGILL B ALLEN amp S HE (1999) A checklist of the mosses - MissouriBotanical Garden St Louis Missouri
DOWELD A (2001) Prosyllabus Tracheophytorum - GEOS Moscow i-lxxx + 110 pp
DOYLE JJ amp JL DOYLE (1990) Isolation of plant DNA from fresh tissue - Focus 12 13-15
DUFF RJ JC VILLAREAL DC CARGILL amp KS RENZAGLIA (2007) Progress andchallenges towards developing a phylogeny and classification of the hornworts - Bryologist 110214-243
FLEISCHER M (1920) Natuumlrliches System der Laubmoose - Hedwigia 61 390-400
FORREST LL EC DAVIS DG LONG BJ CRANDALL-STOTLER A CLARK ampML HOLLINGSWORTH (2006) Unraveling the evolutionary history of the liverworts (Marchantio-phyta) multiple taxa genomes and analyses - Bryologist 109 303-334
FRAHM J-P amp W FREY (1987) Moosflora 2 Aufl - UTB 1250 Stuttgart
FREY W (1977) Neue Vorstellungen uumlber die Verwandtschaftsgruppen und die Stammesgeschichteder Laubmoose - In FREY W H HURKA amp F OBERWINKLER (Hrsg) Beitraumlge zur Biologieder Pflanzen pp 117-139 Stuttgart
FREY W amp M STECH (2005) A morpho-molecular classification of the liverworts (Hepa-ticophytina Bryophyta) - Nova Hedwigia 81 55-78
FREY W M STECH amp K MEIszligNER (1999) Chloroplast DNA-relationship in palaeoaustralLopidium concinnum (Hypopterygiaceae Musci) An example of steno-evolution in mosses Studiesin austral temperate rain forest bryophytes 2 - Plant Syst Evol 218 67-75
GOFFINET B amp WR BUCK (2004) Systematics of Bryophyta (mosses) from molecules to arevised classification - In GOFFINET B V HOLLOWELL amp R MAGILL (eds) Molecularsystematics of bryophytes Monogr Syst Bot Missouri Bot Gard 98 205-239
GOFFINET B CJ COX AJ SHAW amp TAJ HEDDERSON (2001) The Bryophyta (mosses)Systematic and evolutionary inferences from an rps4 gene (cpDNA) phylogeny - Ann Bot 87191-208
GOFFINET B NJ WICKETT O WERNER RM ROS AJ SHAW amp CJ COX (2007)Distribution and phylogenetic significance of the 71-kb inversion in the plastid genome in Funariidae(Bryophyta) - Ann Bot 99 747-753
19
GROTH-MALONEK M D PRUCHNER F GREWE amp V KNOOP (2005) Ancestors oftrans-splicing mitochondrial introns support serial sister group relationships of hornworts and mosseswith vascular plants - Mol Biol Evol 22 117-125
HATTORI S amp H INOUE (1958) Preliminary report on Takakia lepidozioides - J Hattori BotLab 19 133-137
HE-NYGREacuteN X A JUSLEacuteN I AHONEN D GLENNY amp S PIIPPO (2006) Illuminating theevolutionary history of liverworts (Marchantiophyta) - towards a natural classification - Cladistics22 1-31
HEDDERSON TAJ DJ MURRAY CJ COX amp TL NOWELL (2004) Phylogeneticrelationships of haplolepideous mosses (Dicranidae) inferred from rps4 gene sequences - Syst Bot29 29-41
LA FARGE C BD MISHER JA WHEELER DP WALL K JOHANNES S SCHAFFERamp AJ SHAW (2000) Phylogenetic relationships within the haplolepideous mosses - Bryologist103 257-276
LA FARGE C AJ SHAW amp DH VITT (2002) The circumscription of the Dicranaceae(Bryopsida) based on the chloroplast regions trnL-trnF and rps4 - Syst Bot 27 435-452
MAGOMBO ZLK (2003) The phylogeny of basal peristomate mosses evidence from cpDNAand implications for peristome evolution - Syst Bot 28 24-38
MCNEILL J FR BARRIE HM BURDET V DEMOULIN DL HAWKSWORTHK MARHOLD DH NICOLSON J PRADO PC SILVA JE SKOG JH WIERSEMA ampNJ TURLAND (2006) International Code of Botanical Nomenclature (Vienna Code) - RegnumVegetabile 146 1-568
MUumlLLER K (2004) PRAP - computation of Bremer support for large data sets - Mol PhylogenetEvol 31 780-782
MUumlLLER K (2005) SeqState - primer design and sequence statistics for phylogenetic DNA datasets - Appl Bioinformatics 4 65-69
MUumlLLER K D QUANDT J MUumlLLER amp C NEINHUIS (2005) PhyDE v0992 PhylogeneticData Editor - httpwwwphydede
MURRAY BM (1988) Systematics of the Andreaeopsida (Bryophyta) two orders with links toTakakia - Nova Hedwigia Beih 90 289-336
NEWTON AE amp RS TANGNEY (eds) (2007) Pleurocarpous mosses systematics and evolutionSystematics Association Special Volume Series 71 CRC Press Boca Raton 434 pp
NEWTON AE CJ COX JG DUCKETT JA WHEELER B GOFFINET TAJ HEDDER-SON amp BD MISHLER (2000) Evolution of the major moss lineages Phylogenetic analyses basedon multiple gene sequences and morphology - Bryologist 103 187-211
NEWTON AE N WIKSTROumlM NE BELL LL FORREST amp MS IGNATOV (2007)Dating the diversification of the pleurocarpous mosses - In NEWTON AE amp RS TANGNEY(eds) Pleurocarpous mosses systematics and evolution Systematics Association Special VolumeSeries 71 337-366
NIXON KC (1999) The parsimony ratchet a new method for rapid parsimony analysis - Cladistics15 407-411
OBRIEN TJ (2007) The phylogenetic distribution of pleurocarpous mosses evidence fromcpDNA sequences - In NEWTON AE amp RS TANGNEY (eds) Pleurocarpous mossessystematics and evolution Systematics Association Special Volume Series 71 19-41
OCHYRA R (2002) Nomenclatural changes in subfamilies of the Dicranaceae - CryptogamieBryol 23 345-349
20
OCHYRA R J ŻARNOWIEC amp H BEDNAREK-OCHYRA (2003) Census catalogue ofPolish mosses - Biodiv Poland 3 1-372
PEDERSEN N amp AE NEWTON (2007) Phylogenetic and morphological studies within thePtychomniales with emphasis on the evolution of dwarf males - In NEWTON AE amp RSTANGNEY (eds) Pleurocarpous mosses systematics and evolution Systematics AssociationSpecial Volume Series 71 367-392
QUANDT D amp M STECH (2005) Molecular evolution and secondary structure of the chloroplasttrnL intron in bryophytes - Mol Phylogenet Evol 36 429-443
QUANDT D K MUumlLLER amp S HUTTUNEN (2003) Characterisation of the chloroplast DNApsbT-H region and the influence of dyad symmetrical elements on phylogenetic reconstructions -Plant Biol 5 400-410
QUANDT D K MUumlLLER M STECH W FREY KW HILU amp T BORSCH (2004) Molecularevolution of the chloroplast trnL-F-region in land plants - In GOFFINET B V HOLLOWELL ampR MAGILL (eds) Molecular systematics of bryophytes Monogr Syst Bot Missouri Bot Gard98 13-37
QUANDT D NE BELL amp M STECH (2007) Unravelling the knot the Pulchrinodaceae famnov (Bryales) - In KUumlRSCHNER H T PFEIFFER amp M STECH (eds) A Festschrift to Wolf-gang Frey - a scientists life between deserts and rain forests Nova Hedwigia Beih 131 21-39
QIU Y-L Y CHO JC COX amp JD PALMER (1998) The gain of three mitochondrial intronsidentifies liverworts as the earliest land plants - Nature 394 671-674
QIU Y-L L LI B WANG Z CHEN V KNOOP M GROTH-MALONEK O DOM-BROVSKA J LEE L KENT J REST GF ESTABROOK TA HENDRY DW TAYLORCM TESTA M AMBROS B CRANDALL-STOTLER J DUFF M STECH W FREYD QUANDT amp CC DAVIS (2006) The deepest divergences in land plants inferred fromphylogenomic evidence - Proc Natl Acad Sci USA 103 15511-15516
RENZAGLIA KS S SCHUETTE RJ DUFF R LIGRONE AJ SHAW BD MISHLER ampJG DUCKETT (2007) Bryophyte phylogeny Advancing the molecular and morphological frontiers- Bryologist 110 179-213
SAMIGULLIN TH SP YACENTYUK GV DEGTYARYEVA KM VALIEJO-ROMANVK BOBROVA I CAPESIUS WF MARTIN AV TROITSKY VR FILIN amp ASANTONOV (2002) Paraphyly of bryophytes and close relationships of hornworts and vascularplants inferred from analysis of chloroplast rDNA ITS (cpITS) sequences - Arctoa 11 31-43
SANG T DJ CRAWFORD amp TF STUESSY (1997) Chloroplast DNA phylogeny reticulateevolution and biogeography of Paeonia (Paeoniaceae) - Amer J Bot 84 1120-1136
SHAW AJ amp KS RENZAGLIA (2004) Phylogeny and diversification of bryophytes - AmerJ Bot 91 1557-1581
SHAW AJ CJ COX amp B GOFFINET (2005) Global patterns of moss diversity taxonomic andmolecular inferences - Taxon 54 337-352
STECH M (1999a) A reclassification of Dicranaceae (Bryopsida) based on non-coding cpDNAsequence data - J Hattori Bot Lab 86 137-159
STECH M (1999b) A molecular systematic contribution to the position of Amphidium Schimp(Rhabdoweisiaceae Bryopsida) - Nova Hedwigia 68 291-300
STECH M (2004) Supraspecific circumscription and classification of Campylopus Brid(Dicranaceae Bryopsida) based on molecular data - Syst Bot 29 817-824
STECH M amp D QUANDT (2006) Molecular evolution of the chloroplast atpB-rbcL spacer inbryophytes - In SHARMA AK amp A SHARMA (eds) Plant Genome Biodiversity and EvolutionVol 2 Part B pp 409-431 Science Publishers Enfield New Hampshire
21
STECH M D QUANDT amp W FREY (2003) Molecular circumscription of the hornworts(Antho-cerotophyta) based on the chloroplast DNA trnL-trnF region - J Plant Res 116 389-398
STOTLER RE amp B CRANDALL-STOTLER (2005) A revised classification of theAnthocerotophyta and a checklist of the hornworts of North America north of Mexico - Bryologist108 16-26
SWOFFORD DL (2002) PAUP Phylogenetic analysis using parsimony (and other methods)version 40b10 - Sunderland MA
TABERLET P L GIELLY G PAUTOU amp J BOUVET (1991) Universal primers for amplificationof three non-coding regions of chloroplast DNA - Plant Mol Biol 17 1105-1109
TSUBOTA H Y AGENO B ESTEacuteBANEZ T YAMAGUCHI amp H DEGUCHI (2003)Molecular phylogeny of the Grimmiales (Musci) based on chloroplast rbcL sequences - Hikobia 1455-70
TSUBOTA H E DE LUNA D GONZAacuteLEZ MS IGNATOV amp H DEGUCHI (2004) Molecularphylogenetics and ordinal relationships based on analyses of a large-scale data set of 600 rbcLsequences of mosses - Hikobia 14 149-170
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Received 3 September 2007 accepted in revised form 30 October 2007
3
Tab
le 1
Vou
cher
info
rmat
ion
and
Gen
Ban
k ac
cess
ion
num
bers
of t
he s
peci
es u
sed
for t
he th
ree-
mar
ker a
naly
sis
of B
ryop
sida
s
eque
nces
take
n fr
omG
enB
ank
spec
ies
of w
hich
all
thre
e m
arke
rs w
ere
new
ly s
eque
nced
for
the
pres
ent s
tudy
Fam
ilyS
peci
esV
ouch
erH
erb
Acc
no
Acc
no
Acc
no
trnL
atpB
-rbc
Lps
bA-t
rnH
And
reae
acea
eA
ndre
aea
rupe
stri
s H
edw
S
tech
B97
0827
3L
AY
0502
78A
Y86
4297
EU
1635
06Po
lytr
icha
ceae
Pog
onat
um s
ubul
atum
(Men
zies
ex
Bri
d) B
rid
Pfe
iffe
r 98
-T20
7AC
HR
F
rey
AY
0502
77E
U12
4442
EU
1635
05D
iphy
scia
ceae
Dip
hysc
ium
fol
iosu
m (
Hed
w)
DM
ohr
Fre
y 1-
4982
(tr
nL)
Frey
EU
1865
37D
Q39
7161
AY
3128
99T
imm
iace
aeT
imm
ia m
egap
olit
ana
Hed
w
(Gen
Ban
k)-
AF
4783
20D
Q39
7137
AY
3129
23T
imm
ia a
ustr
iaca
Hed
w
S
tech
B97
0831
4L
EU
1865
43E
U18
6584
EU
1635
13E
ncal
ypta
ceae
Enc
alyp
ta s
trep
toca
rpa
Hed
w
S
tech
B06
0412
2L
EU
1865
41E
U18
6582
EU
1635
11E
ncal
ypta
vul
gari
s H
edw
S
tech
B95
0328
3L
EU
1280
00E
U12
4423
EU
1635
10Fu
nari
acea
eF
unar
ia h
ygro
met
rica
Hed
w
Ste
ch B
9811
301
LE
U18
6538
EU
1865
79E
U16
3507
Phy
scom
itre
lla
pate
ns (
Hed
w)
(ste
rile
cul
ture
)-
EU
1865
39E
U18
6580
EU
1635
08B
ruch
amp S
chim
pP
hysc
omit
rium
pyr
ifor
me
(Hed
w)
Ham
pe
Ste
ch B
0404
071
LE
U18
6540
EU
1865
81E
U16
3509
Cat
osco
piac
eae
Cat
osco
pium
nig
ritu
m (
Hed
w)
Bri
d
S
tech
B97
0828
13
LE
U18
6545
EU
1865
92E
U16
3524
Bry
oxip
hiac
eae
Bry
oxip
hium
nor
vegi
cum
(B
rid
) M
itt
Kop
onen
366
64B
AF
1351
01E
U18
6590
EU
1635
21G
rim
mia
ceae
Rac
omit
rium
mic
roca
rpum
(H
edw
) B
rid
Ste
ch B
9708
181
LA
F12
7186
EU
1865
89E
U16
3519
Schi
stid
ium
apo
carp
um (
Hed
w)
Ste
ch B
9702
262
LA
F12
7185
EU
1865
88E
U16
3518
Bru
ch amp
Sch
imp
Ptyc
hom
itria
ceae
Pty
chom
itri
um p
olyp
hyll
um (S
w)
Ste
ch e
t al
04-4
0L
EU
1865
42E
U18
6583
EU
1635
12B
ruch
amp S
chim
p
A
rchi
diac
eae
Arc
hidi
um a
ltern
ifoliu
m (D
icks
ex
Hed
w)
Mitt
F
rahm
sn
B
ON
NA
F13
5114
EU
1865
97E
U16
3529
Am
phid
iace
aeA
mph
idiu
m m
ouge
otii
(B
ruch
amp S
chim
p)
Fra
hm s
n
BO
NN
AF
1271
87A
Y15
9894
EU
1635
20S
chim
pD
icra
nace
aeD
icra
num
pol
yset
um S
w
Ste
ch B
9705
181
LA
F12
9587
AY
1598
95E
U16
3523
Dic
rane
llace
aeD
icra
nell
a ce
rvic
ulat
a (H
edw
) S
chim
pS
tech
B97
0824
1L
AF
1295
97E
U18
6591
EU
1635
22D
itric
hace
aeP
leur
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m a
cum
inat
um L
indb
F
rey
1-49
91F
rey
EU
1865
46E
U18
6596
EU
1635
28Fi
ssid
enta
ceae
Fis
side
ns b
ryoi
des
Hed
w
Dar
mer
130
17B
SB
AF
1351
05E
U18
6586
EU
1635
15O
ctod
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ntan
um (
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h P
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db
Haa
pasa
ari s
n
LA
F13
5107
EU
1865
85E
U16
3514
Leu
cobr
yace
aeC
ampy
lopu
s fl
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sus
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w)
Bri
dS
tech
B96
0905
2L
AF
1295
93A
Y15
9919
EU
1635
30L
euco
bryu
m ja
vens
e (B
rid
) M
itt
Men
zel e
t al
3841
Fre
yA
F44
2659
AY
1599
00E
U16
3531
Onc
opho
race
aeC
ynod
onti
um p
olyc
arpu
m (
Hed
w)
Sch
imp
Ste
ch B
930
721
2L
AF
1295
99E
U18
6595
EU
1635
27O
ncop
horu
s vi
rens
(H
edw
) B
rid
Ste
ch B
9608
011
LA
F12
9598
EU
1865
93E
U16
3525
Rha
bdow
eisi
a cr
enul
ata
(Mit
t) H
Jam
eson
Fra
hm s
n 1
810
97
BO
NN
AF
1271
81E
U18
6594
EU
1635
26
4
Potti
acea
eC
incl
idot
us n
igri
cans
(Brid
) W
ijk amp
Mar
gada
ntS
tech
B92
0517
4L
EU
1865
44E
U18
6587
EU
1635
17T
ortu
la m
ural
is H
edw
S
tech
B97
0226
3L
AF
1351
08A
Y15
9892
EU
1635
16Sp
lach
nace
aeSp
lach
num
lut
eum
Hed
w
S
tech
B97
0828
12
LE
U18
6555
EU
1866
13E
U16
3548
Tay
lori
a m
irab
ilis
(C
ardo
t) B
roth
Fre
y amp
Sch
aum
ann
F
Fre
yE
U18
6554
EU
1866
12E
U16
3547
01-3
6T
etra
plod
on m
nioi
des
(Sw
ex
Hed
w)
Ste
ch B
9106
154
LE
U18
6556
EU
1866
14E
U16
3549
Bru
ch amp
Sch
imp
Mee
siac
eae
Mee
sia
ulig
inos
a H
edw
Ste
ch B
9708
285
LE
U18
6552
EU
1866
10E
U16
3545
Pal
udel
la s
quar
rosa
(H
edw
) B
rid
Ste
ch B
9708
201
LE
U18
6553
EU
1866
11E
U16
3546
Pulc
hrin
odac
eae
Pul
chri
nodu
s in
flat
us (
Hoo
kf
amp W
ilso
n)P
feif
fer amp
Lin
dlar
CH
RA
F13
5065
EU
1866
03E
U16
3538
BH
All
en98
-Z21
5DL
epto
stom
atac
eae
Lep
tost
omum
men
zies
ii R
Br
Fre
y amp
Sch
aum
ann
F
Fre
yE
U18
6550
EU
1866
08E
U16
3543
01-3
88B
ryac
eae
Bry
um b
illa
rdie
rei
Sch
waumlg
rFr
ey amp
Pfe
iffer
98-
Mo1
7Fr
eyE
U18
6549
EU
1866
07E
U16
3542
Rho
dobr
yum
gig
ante
um (
Sch
waumlg
r)
Par
is(G
enB
ank)
-A
F02
3737
AF
5468
60A
Y31
2918
Mni
acea
eM
ielic
hhof
eria
mie
lichh
ofer
iana
(Fun
ck) L
oesk
eS
tech
B91
0615
3L
EU
1865
48E
U18
6605
EU
1635
40M
nium
hor
num
Hed
w
Fre
y 1-
4985
(tr
nL)
Frey
AF
3632
79A
F54
6857
AY
3129
08P
lagi
omni
um u
ndul
atum
(H
edw
) T
JK
op
Ste
ch e
t al
04-6
07L
DQ
1089
67E
U18
6604
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1635
39R
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mni
um m
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foli
um (
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ik)
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Kop
S
tech
B97
0829
6L
DQ
1089
59E
U18
6606
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1635
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ia c
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ta (
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w)
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ank)
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8336
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8A
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2905
Rha
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coca
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s (B
rid
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cul
ture
)-
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0237
24E
U18
6598
EU
1635
32H
elic
ophy
llace
aeH
elic
ophy
llum
torq
uatu
m (
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k)
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dF
rahm
150
7F
rey
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1865
47E
U18
6602
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1635
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artr
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Ana
coli
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301
607
AF
4135
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U16
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Bar
tram
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Con
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301
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3535
Phi
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w)
Bri
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NN
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1075
40E
U18
6601
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1635
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tech
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0226
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1303
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1635
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Ulo
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LE
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6557
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1866
17E
U16
3552
Zyg
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alta
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985
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Aul
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6551
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1866
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amp S
chau
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1865
63E
U18
6625
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1635
60N
EB
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New
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amp W
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4F
rey
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1865
59E
U18
6620
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1635
55O
rtho
dont
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Sch
waumlg
r
S
tech
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0616
2L
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1865
58E
U18
6619
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1635
54L
epto
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udic
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ii S
chw
aumlgr
Fre
y amp
Sch
aum
ann
F
Fre
yA
F02
3750
EU
1866
24E
U16
3559
01-0
9
Tab
le 1
con
tinu
ed
5
Rhi
zogo
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6560
EU
1866
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U16
3556
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Hoo
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Bri
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Sch
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01-4
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EU
1865
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U18
6622
EU
1635
57
Rhi
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dis
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Sw
) B
rid
Fra
hm 2
-11
Fre
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6562
EU
1866
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3558
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6631
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1635
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EU
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amp S
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1865
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6632
EU
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01
-266
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2380
EU
1866
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U16
3570
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-109
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U18
6571
EU
1866
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U16
3568
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04-1
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EU
1865
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6634
EU
1635
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y 95
-17
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F13
4637
EU
1866
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U16
3573
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) W
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3572
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man
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819
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3575
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)Pf
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7169
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3574
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1865
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6638
EU
1635
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Cra
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3583
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1865
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6647
EU
1635
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3577
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1865
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EU
1635
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6641
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1635
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f amp
Wil
son)
Fre
y amp
Fre
y 94
-117
Fre
yA
Y01
0297
EU
1866
42E
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3580
IG
Sto
ne amp
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Plag
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ecia
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um u
ndul
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(H
edw
) S
chim
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2640
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6646
EU
1635
84C
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Cat
agon
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ens
(Bri
d)
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dot
Fre
y amp
Sch
aum
ann
F
Fre
yE
U18
6575
EU
1866
40E
U16
3578
01-1
87a
Tab
le 1
con
tinu
ed
6
primers CM
DM
(slightly modified after Taberlet et al 1991 see Frey et al 1999) and atpB-1rbcL-1(Chiang et al 1998) respectively For amplification of the psbA-trnH spacer primers psbAF(5-GTT ATG CAT GAA CGT AAT GCT C-3 Sang et al 1997) and trnHR-2 (5-CGC GCA TGGTGG ATT CAC AAT CC-3 slightly modified after Sang et al 1997) were used with a PCRprotocol of 5 min 94degC 35 cycles (30 sec 94degC 1 min 48degC 1 min 40 sec 72degC) 7 min 72degC PCRproducts were purified using DNA purification kits (Qiagen Macherey-Nagel) Sequencing wasperformed as described in Stech (2004) using the amplification primers
ALIGNMENT AND PHYLOGENETIC ANALYSES DNA sequences were manually aligned in PhyDE v0992(Muumlller et al 2005) Following Quandt et al (2003) and Quandt amp Stech (2005) inversions inputative hairpin secondary structures were positionally separated in the alignment their presence orabsence was not coded for the phylogenetic analyses Phylogenetic reconstructions under the maximumparsimony criterion were performed using winPAUP 40b10 (Swofford 2002) in combination withPRAP (Muumlller 2004) as implemented in SeqState (Muumlller 2005) PRAP generates command filesfor PAUP that allow parsimony ratchet searches as designed by Nixon (1999) Heuristic searchesunder parsimony were performed with the following options all characters equally weighted andunordered TBR branch swapping collapse branches if maximum branch length is zero MulTreesoption in effect gaps treated as missing data Initially a heuristic search with 1000 addition sequencereplicates was performed For the parsimony ratchet ten random addition cycles of 200 ratchetiterations each were used with TBR branch swapping on a randomly re-weighted data set (25 ofthe positions) Heuristic bootstrap searches were performed with 1000 replicates with 10 additionsequence replicates per bootstrap replicate
Results
In the present data set of non-coding plastid markers sequence lengths ranged from243 to 368 nucleotides (nt) in the trnL intron and from 445 to 615 nt in the atpB-rbcL spacer The psbA-trnH spacer was considerably shorter than the other twomarkers and ranged from 103 to 186 nt The combined alignment of sequences from85 ingroup and two outgroup taxa comprised 2430 positions (trnL intron 668 atpB-rbcL spacer 1366 psbA-trnH spacer 396 positions) The most variable regions withambiguous alignment (781 positions) were excluded from phylogenetic analysis Ofthe 1649 included positions 628 (381) were variable and 455 of the variablepositions (725 or 276 of the total number of positions) were parsimony-informative The trnL intron comprised 124 the atpB-rbcL spacer 286 and the psbA-trnH spacer 45 of these included parsimony-informative positions
The shortest trees found in the heuristic maximum parsimony analysis of the combineddata set had a length of 2433 steps By applying the parsimony ratchet 129 treeswere retained that were one step shorter (length 2432 CI = 0419 RI = 0624) Thestrict consensus tree of the ratchet analysis is shown in Fig 1 The ingroup (Bryopsida)is supported with 100 bootstrap support (BS) Diphysciidae are sister to theremaining Bryopsida with 54 BS Encalyptidae Funariidae Timmiidae andDicranidae all receive gt 95 BS while Bryidae are slightly less supported (89BS) Relationships between these major lineages are resolved but unsupported Atordinal level within the Bryidae a lower resolution is observed SplachnalesOrthotrichales Aulacomniales Hypnodendrales Hookeriales and Hypnales areresolved as monophyletic with 67-100 BS whereas Hedwigiales BartramialesBryales Orthodontiales and Rhizogoniales are not A closer relationship ofOrthotrichales with the pleurocarpous mosses sl than with the more basal ordersHedwigiales Bartramiales Splachnales and Bryales is indicated
7
Discussion
Classification of mosses - recent progress and the current state
For a long time mosses were subdivided into three main lineages the subclassesSphagnidae Andreaeidae and Bryidae (eg Fleischer 1920 Vitt 1984 Frahm ampFrey 1987) the latter with a number of (super-)orders (eg Frey 1977) Howevermolecular data confirmed that mosses comprise a number of isolated basal lineagesrepresented by morphologically and ecologically distinct extant taxa such as TakakiaSphagnum Andreaea Andreaeobryum Oedipodium Tetraphis the Polytrichaceaeand Buxbaumia which probably have long independent phylogenetic histories (cfNewton et al 2007) As a result of molecular phylogenies and a re-evaluation ofmorphological-anatomical characters the classification of mosses has changedconsiderably in the last few years with the main lineages nowadays treated atsubdivision class and subclass levels within division Bryophyta (eg Doweld 2001Ochyra et al 2003 Goffinet amp Buck 2004 this study)
Takakia and Sphagnum are the earliest diverging moss taxa in molecular phylogenies(eg Newton et al 2000 Beckert et al 2001 Cox et al 2004 Qiu et al 2006Newton et al 2007) That Takakia is a moss and not a liverwort was confirmed byanalysis of DNA sequences and phylogenomic characters such as the distribution ofmitochondrial introns (eg Beckert et al 2001) Its taxonomic status however stillremains to be clarified On the one hand most molecular studies resolve Takakiaand Sphagnum as sister genera although only partly with high statistical supportThese molecular topologies do not support the recognition of division Takakiophytaas proposed by Crandall-Stotler (1986) One the other hand no morphologicalsynapomorphies unite Takakia with Sphagnum and significant molecular differencesseparating Takakia from all other mosses were also observed For example a regionin the plastid ITS3 is similar to that of other land plants but absent in mosses(Samigullin et al 2002) and a transition in the trnL
UAA gene changing the anticodon
to CAA was otherwise only found in leptosporangiate ferns and Ginkgo (Quandt etal 2004) Thus ldquoresolution of Sphagnum - Takakia clade may be an artifactrdquo (Shawamp Renzaglia 2004) Also Goffinet amp Buck (2004) did not unite Takakia and Sphagnumunder a formal taxonomic rank but placed them into different informal superclassesIn our opinion Takakia should be treated at the same level as Sphagnophytina andBryophytina (cf Doweld 2001) ie as a subdivision of Bryophyta However morefundamental nomenclatural changes are necessary as the family name Takakiaceaewas not validated in the original publication by Hattori amp Inoue (1958) (article411 of ICBN McNeill et al 2006) and consequently all higher taxa erected laterare invalid The corrected taxonomic treatment of Takakia is provided here withsporophytic characters included in the latin diagnosis of Takakiaceae (see taxonomy)
Within Bryophytina we recognise four morphologically and molecularly isolatedbasal lineages as separated from the arthrodontous mosses (Bryopsida) Andreaeopsida(with linear capsule dehiscence) the operculate but eperistomate Oedipodiopsida aswell as Polytrichopsida and Tetraphidopsida with nematodontous peristomes A fifthclass Andreaeobryopsida was erected by Buck amp Goffinet (2000) but re-includedin Andreaeopsida as a subclass by Ochyra et al (2003) The systematic status of
8
Andreaeobryum macrosporum Steere amp BMMurray and possible relationships withAndreaea and Takakia were discussed by Murray (1988) and summarised includingmolecular results by Shaw amp Renzaglia (2004)
On the next lower level a number of morphologically and molecularly divergentlineages are nowadays treated as subclasses of Bryopsida Buxbaumiidae andDiphysciidae are generally branching off first in molecular topologies (eg Beckertet al 2001 Magombo 2003 Cox et al 2004) followed by Timmiidae Encalyptidaeand Funariidae as well as Dicranidae (haplolepideous mosses) sister to Bryidae slThese subclasses (except Buxbaumiidae not included) are also well recognizable inthe present analysis of non-coding plastid sequences (Fig 1)
The morphologically very different Encalyptidae and Funariidae are revealed assister groups although mostly without high support in several molecular phylogenies(eg Goffinet et al 2001 Cox et al 2004 Hedderson et al 2004 Tsubota et al2003 2004) and also in the present study (Fig 1) Goffinet et al (2007) confirmedthis relationship by phylogenomic evidence namely a large (71 kb) inversion in thechloroplast genome of Funariaceae Disceliaceae and Encalyptaceae but not inGigaspermaceae Consequently the latter family was separated at ordinal level fromthe two remaining families of Funariales by Goffinet et al (2007) GigaspermalesFunariales and Encalyptales may share a common ancestor according to some butnot all molecular phylogenies (eg Goffinet et al 2001 2007 Hedderson et al2004 but not in Tsubota et al 2004) Although ontogenetic data from peristomedevelopment may support their common ancestry (Goffinet et al 2007) unambiguousmorphological synapomorphies are lacking We therefore propose to treatGigaspermaceae at subclass level within the Bryopsida (see taxonomy)
The haplolepideous mosses (Dicranidae) are clearly supported as a monophyleticlineage which obviously evolved from a diplolepideous ancestor according to theirposition in the molecular trees (eg Newton et al 2000 Tsubota et al 2003 Cox etal 2004 Goffinet amp Buck 2004) Molecular studies suitable for inferring ordinaland family level relationships within Dicranidae either focused on the haplolepideousmosses (eg Stech 1999ab 2004 LaFarge et al 2000 2002 Tsubota et al 2003Hedderson et al 2004) or included more than 15 haplolepideous taxa in analyses ofa broader range of mosses (eg Goffinet et al 2001 Tsubota et al 2004 this study)Major lineages supported by these analyses are for example Grimmiales(Grimmiaceae Ptychomitriaceae and Seligeriaceae) Leucobryaceae (incl formerDicranaceae-Campylopoideae and Paraleucobryoideae pp) Dicranaceae sstr(Dicranoideae plus former Dicnemonaceae and Paraleucobryoideae pp) Pottiaceae(incl Cinclidotaceae and Splachnobryum) and Calymperaceae (probably exclOctoblepharum) Furthermore several genera and families belong to Dicranidaewhose systematic positions have been controversial (eg Stech et al 1999b LaFarge et al 2002 Hedderson et al 2004 OBrien 2007 Quandt et al 2007 thisstudy) Amphidium Archidium Catoscopium Drummondia EphemeraceaeErpodiaceae Mittenia (cf OBrien 2007 sequences in some earlier analyses werebased on misdentified specimens) Rhachitheciaceae Schistostega Splachnobryumand Wardia On the contrary several problems remain such as the circumscriptionof Ditrichaceae and relationships of the major haplolepideous lineages in general
9
Fig 1 Strict consensus tree of 129 most parsimonious trees inferred from combined trnLUAA
intronatpB-rbcL spacer and psbA-trnH spacer sequences of 85 taxa of Bryopsida as well as Andreaearupestris (Andreaeopsida) and Pogonatum subulatum (Polytrichopsida) as outgroup representativesBootstrap support values gt50 are depicted above the branches
10
Consequently resolving the phylogeny of Dicranidae with confidence is one of themajor future challenges in moss systematics
As mentioned above Dicranaceae are monophyletic in a narrow circumscriptionaccording to molecular data In contrast to former Campylopoideae andParaleucobryoideae the status of Rhabdoweisioideae (= Oncophoroideae Ochyra2002) and Dicranelloideae needs further consideration Stech (1999ab) suggestedto recognise RhabdoweisioideaeRhabdoweisiaceae in a broad sense includingDicranoweisia Amphidium and Aongstroemia Subsequent molecular analysesconfirmed a close relationship of the genera Arctoa Cynodontium DicranoweisiaKiaeria Oncophorus Oreoweisia Oreas Rhabdoweisia and Symblepharis althoughwithout significant support (La Farge et al 2002 Tsubota et al 2003 Hedderson etal 2004) With respect to the molecular evidence available so far we propose toelevate Oncophoroideae to family level to accomodate these genera and perhapsGlyphomitrium (cf Tsubota et al 2003) whereas we consider AongstroemiaDichodontium and Diobelonella to belong to Aongstroemiaceae (cf Stech 1999a)Amphidium is neither closely related to Dicranaceae sstr nor to Oncophoroideae(La Farge et al 2002 Tsubota et al 2003 Hedderson et al 2004 Stech 2004 thisstudy) and should be treated at family level rather than placed in Dicranaceae assubfam Amphidioideae (Ochyra et al 2003) The circumscription of Dicranelloideaeis more difficult to evaluate as few representatives have been included in molecularanalyses However Dicranella heteromalla (Hedw) Schimp as well as the generaCampylopodium and Microcampylopus are clearly separated from Dicranaceae sstr(Stech 1999a 2004 La Farge et al 2002 Tsubota et al 2003 Hedderson et al2004) and consequently the subfamily deserves family status as well Finallymolecular data showed that the genus Hypodontium does not belong to Pottiaceae(Hedderson et al 2004 Tsubota et al 2004) Taxonomic conclusions have not beendrawn from these results which is made up here (see taxonomy)
All mosses with diplolepideous-alternate peristomes together with Splachnales witha diplolepideous-opposite (Funaria-type) peristome form a monophyletic group inmolecular analyses (eg Newton et al 2000 Beckert et al 2001 Goffinet et al2001 Cox et al 2004 Tsubota et al 2004 references in Table 2) Differentclassifications of this by far most species-rich group of mosses were proposed (egVitt et al 1998 Ochyra et al 2003 Goffinet amp Buck 2004) However at least someof the recognised subclasses and superorders are paraphyletic according to themolecular topologies and assigning formal ranks to all evolutionarily significantmonophyletic entities is problematic if the main taxonomic framework of Bryophytaand Bryopsida should be maintained (cf discussion in Bell et al 2007) Thereforein the present synopsis only one subclass Bryidae is recognised for all diplolepideous-alternate mosses and Splachnales This broadly defined Bryidae is subdivided into13 orders most of them resolved as monophyletic in the majority of the phylogeneticanalyses summarised in Table 2 although with different levels of statistical supportin maximum parsimony analyses To define monophyletic lineages at supraordinallevel informal node-based names may be chosen according to Bell et al (2007) Forexample the pleurocarpous mosses (pleurocarpy sensu Bell amp Newton 2007) andtheir closest acrocarpous relatives (Orthodontiales to Hypnales) were already
11
Table 2 Taxon sampling and bootstrap support (BS) for Dicranidae Bryidae and orders within theBryidae in recent phylogenetic analyses (MP only) based on combined molecular markers Markersare given in square brackets (non-coding regions in bold) numbers of included taxa in brackets ++respective clade present with ge 80 BS + clade present with lt 80 BS - clade not present no oronly one representative included
Bell amp Newton OBrien Quandt et al Bell et al this study(2004) (2007) (2007) (2007)
[rbcL rps4 [atpB atpB- [rbcL rps4 [rbcL rps4 [atpB-rbcLnad5] rbcL rbcL trnL-F nad5] trnL-F nad5] psbA-trnH
rps4 trnL-F] trnL]
Dicranidae + (2) + (4) ++ (3) (1) ++ (19)Bryidae ++ (57) + (53) ++ (52) ++ (98) ++ (58)Hedwigiales ++ (2) (1) ++ (2) ++ (2) - (3)Bartramiales ++ (2) ++ (4) ++ (4) ++ (3) - (4)Splachnales (0) ++ (2) ++ (3) ++ (2) ++ (5)Bryales - (4) - (5) ++ (18) + (17) - (8)Orthotrichales (1) ++ (3) ++ (3) ++ (2) ++ (4)Orthodontiales + (4) + (4) + (3) + (6) - (3)Aulacomniales + (6) + (7) ++ (2) + (7) + (3)Rhizogoniales ++ (13) + (8) ++ (5) ++ (14) - (3)Hypnodendrales ++ (13) + (7) ++ (4) ++ (29) ++ (6)Ptychomniales ++ (3) ++ (3) (1) ++ (4) (1)Hookeriales - (4) + (2) (1) + (2) + (8)Hypnales - (5) - (7) ++ (5) ++ (10) + (10)
summarised under the informal node based name pleurcarpids (Bell et al 2007)and can be distinguished from a basal grade of acrocarpous or cladocarpous lineages(Hedwigiales to Orthotrichales) Within the latter monophyly of BartramialesSplachnales and Orthotrichales is well-supported in all analyses including two ormore taxa except Bartramiales in the present data set (cf Fig 1) In contrast Bryalesreceive significant support less frequently (but see Bell et al 2007 Quandt et al2007) Hedwigiales are well supported if only Hedwigia (Hedwigiaceae) andRhacocarpus (Rhacocarpaceae) are included whereas the monospecific Helicophyllum(Helicophyllaceae) is not closely related to these taxa but shows affinities withBartramiales (Goffinet et al 2001 this study) With respect to the differentmorphologies of Helicophyllaceae and Bartramiaceae however the former shouldbe separated at ordinal level (see taxonomy)
Clarifying relationships of the Orthotrichales is still a difficult issue Analyses ofsingle chloroplast markers or parsimony analyses of combined markers from differentgenomes mostly indicated a close relationship either with Splachnales (eg Cox etal 2000 Newton et al 2000 Tsubota et al 2004 Quandt et al 2007) or with thepleurocarpids (Goffinet et al 2001 this study) Although none of these alternativesis well-supported the latter seems more likely with regard to the moderately tomaximally supported Orthotrichales - pleurocarpid sister group relationship in allanalyses of mitochondrial data and in likelihood analyses of combined plastidmitochondrial markers (Beckert et al 2001 Quandt et al 2007)
12
The molecular polyphyly of Rhizogoniaceae (eg Bell amp Newton 2004) was solvedby the transfer of rhizogonioid genera into broadly defined Aulacomniaceae andOrthodontiaceae (Bell et al 2007) which now include both acrocarpous andpleurocarpous taxa These systematic changes are also comprehensible by non-molecular characters such as morphological traits shared by Mesochaete andAulacomnium heterostichum (Hedw) Bruch amp Schimp or the variously reducedperistomes of Orthodontiaceae pp in contrast to the generally fully developed Bryum-type peristomes of rhizogonioid and hypnodendroid mosses (Bell et al 2007) Theposition of the solely pleurocarpous Hypnodendrales sister to the former Hypnidaeled to the recognition of the informal group core pleurocarps (Bell et al 2007)The former Hypnidae (Ptychomniales Hookeriales and Hypnales summarised ashomocostate pleurocarps) are monophyletic in most molecular analyses (eg Goffinetet al 2001 Tsubota et al 2004 Bell et al 2007) with Ptychomniales being well-supported (Pedersen amp Newton 2007 Table 2) Clarifying relationships betweenHookeriales and Hypnales and within the latter is still a challenge but recent molecularstudies seem to support a sister group relationship of both orders (Bell et al 2007present study)
Phylogenetic utility of non-coding plastid markers
Non-coding plastid markers that comprise both variable and conserved regionssuch as the trnL
UAA intron have repeatedly been shown to possess potential for
resolving relationships at high taxonomic levels (eg Borsch et al 2003 Quandtet al 2004) Both the trnL intron and atpB-rbcL spacer were characterised indetail in mosses with respect to their structure and molecular evolution (Quandt ampStech 2005 Stech amp Quandt 2006) They include conservative regions that can beunambiguosly aligned and even parts of the more variable regions can be used ifrepeats hairpin loops etc are correctly identified and adequately treated in thephylogenetic analyses (eg Quandt et al 2003 Quandt amp Stech 2005) Using theatpB-rbcL spacer alone (Stech amp Quandt 2006) relationships of the major mosslineages were largely consistent with the ldquototal evidencerdquo molecular tree of Goffinetamp Buck (2004) However in addition to general limitations that result from singlemarker analyses the use of non-coding markers may pose further problems suchas a high amount of homoplasy resulting in low resolution or low statistical supportfor many clades Therefore several recent molecular studies of relationships withinBryidae have employed both coding and non-coding markers (Table 2)Nevertheless the usefulness of analyses of combined non-coding plastid markerscannot be ruled out In fact Fig 1 and Table 2 indicate a phylogenetic signal inthe present data set as many clades are recovered that are usually also resolvedin analyses of coding or combined coding and non-coding markers Especiallywith regard to statistical support however the present analysis is inferior tothose of other recent data sets especially Bell et al (2007) and Quandt et al(2007) In addition the non-coding markers used here are of different suitabilityand even the two intergenic spacers differ considerably from each other ThepsbA-trnH spacer contributes much less to the trees resolution than the atpB-rbcL spacer first because it is much shorter and second because relatively largeparts are attributed to hairpin loops or otherwise hypervariable regions These
13
results indicate that future studies should evaluate the molecular evolution andphylogenetic potential of new markers both coding and con-coding and choosethe most suitable ones in a combined analysis to resolve the remaining uncertaintiesin moss phylogeny
Taxonomy
Takakiaceae Stech amp WFrey stat nov
Plantae virides nusquam rhizophorae sine protonemate e caudicis rhizomatis erectae Caudicesrhizomati et axes geotropi radiformes frequenter intercalariter ramificantes sine phyllidiis cumpapillis mucilaginis rostratis Caules phyllidiiferi saepe furcati Phyllidia sine lamina et costadistincta profunde 2-4(-5)-lobata pluristratosa tristicha sed torsione spiraliter disposita Filumcentralium in ambabus generationibus (axibus gametophyti et setis) adest Plantae dioicae Antheridiaet archegonia nuda Sporophytum terminale solitarium Seta persistens Capsula tortilis admaturitatem schizocarpa secus unam rimam spiralem longitudinalem dehiscens Stomata etoperculum absunt peristomium nullum Calyptra mitriformis
TYPUS Takakia SHatt amp Inoue J Hattori Bot Lab 19 137 1958
Takakiaceae SHatt amp Inoue J Hattori Bot Lab 19 137 1958 nom inval (Art 411)
Takakiales Stech amp WFrey stat nov
Based on Takakiaceae Stech amp WFrey Nova Hedwigia 86 13 2008
TYPUS Takakia SHatt amp Inoue J Hattori Bot Lab 19 137 1958
Takakiales SHatt amp Inoue J Hattori Bot Lab 19 137 1958 nom inval
Takakiales SHatt amp Inoue ex RMSchust J Hattori Bot Lab 26 224 1963 nom inval (cumdescr latin)
Takakiopsida Stech amp WFrey statnov
Based on Takakiaceae Stech amp WFrey Nova Hedwigia 86 13 2008
TYPUS Takakia SHatt amp Inoue J Hattori Bot Lab 19 137 1958
Takakiopsida Goffinet amp WRBuck Monogr Syst Bot Missouri Bot Gard 98 232 2004 nominval
Takakiopsida Jia et al Acta Phytotax Sin 41 350 351 2003 nom nud
Takakiopsida Wang amp Wu Fl Bryophyt Sin 8 447 2004 nom inval (cum descr latin)
Takakiophytina Stech amp WFrey stat nov
Based on Takakiaceae Stech amp WFrey Nova Hedwigia 86 13 2008
TYPUS Takakia SHatt amp Inoue JHattori Bot Lab 19 137 1958
Gigaspermidae Stech amp WFrey subclass nov
Plantae acrocarpae terrestres stoloniferae ramis brevibus erectis Folia unicostata cellulis laxislaevibus Capsula plerumque valde rugosa gymnostomatica vel cleistocarpa stomata cum duabuscellulis sociis Ab Funariidis et Encalyptidis charactere phylogenomico (71-kb inversio abest)separatae
14
TYPUS Gigaspermum Lindb Oumlfversigt af Foumlrhandlingar Kongl Svenska Vetenskaps-Akademien21 599 1865
Amphidiaceae Stech stat nov
Based on Dicranaceae subfam Amphidioideae Ochyra in Ochyra Zarnowiec amp Bednarek-OchyraCens Cat Polish Mosses 110 2003
TYPUS Amphidium Schimp Coroll Bryol Eur 39 1856
Amphidiaceae AJESm Moss Fl Britain Ireland 2nd ed 657 2004 nom inval descr angl
Dicranellaceae Stech stat nov
Based on Dicranaceae subfam Dicranelloideae Lindb Utkast Eur Bladmoss 33 1878[lsquoUnderfamilje Dicranelleaersquo]
TYPUS Dicranella (MuumlllHal) Schimp Coroll Bryol Eur 13 1856
Oncophoraceae Stech stat nov
Based on Dicranaceae subfam Oncophoroideae Lindb Utkast Eur Bladmoss 34 1878[lsquoUnderfamilje Oncophoreaersquo]
TYPUS Oncophorus (Brid) Brid Bryol Univ 1 389 1826
Hypodontiaceae Stech fam nov
Plantae robustae characteribus morphologicis Pottiaceis et Calymperaceis similes sedcharacteribus molecularicis separatae Bracteae perichaetiales internae e basi vaginantes subulataevel aristatae Capsula aspectu succulenta cellulae exothecii incrassatae annulus magnopereabsens Peristomii dentes breves triangulati incurvati aurantiaci leves vel infirme verrucosiCalyptra cucullata
TYPUS Hypodontium MuumlllHal Hedwigia 38 96 1899
Helicophyllales Stech amp WFrey ord nov
Plantae acrocarpae prostratae tomentosae Folia dimorpha in duas series laterales et unam seriemventralem divisa Costa percurrens Cellulae hexagonae ad subquadratae papillosae Capsula immersacupulata ad oblonga infra orificium abrupte incurvata stomata destituta Peristomium nullum Sporaeisomorphae heteropolares granulatae
TYPUS Helicophyllum Brid Bryol Univ 2 771 1827
Synopsis of the suprageneric classification of BryophytaAuthor citations are in accordance with Art 492 of the Vienna Code (McNeill et al 2006)
Subdivision Takakiophytina Stech amp WFreyClass Takakiopsida Stech amp WFrey
Order Takakiales Stech amp WFreyTakakiaceae Stech amp WFrey
Subdivision Sphagnophytina DoweldClass Sphagnopsida Schimp
Order Sphagnales Limpr
15
Sphagnaceae DumortOrder Ambuchananiales Seppelt amp HACrum
Ambuchananiaceae Seppelt amp HACrumSubdivision Bryophytina Engler
Class Andreaeopsida JHSchaffnSubclass Andreaeidae Engl
Order Andreaeales LimprAndreaeaceae Dumort
Subclass Andreaeobryidae OchyraOrder Andreaeobryales BMMurray
Andreaeobryaceae Steere amp BMMurrayClass Oedipodiopsida Goffinet amp WRBuck
Order Oedipodiales Goffinet amp WRBuckOedipodiaceae Schimp
Class Tetraphidopsida Goffinet amp WRBuckOrder Tetraphidales MFleisch
Tetraphidaceae SchimpClass Polytrichopsida Doweld
Order Polytrichales MFleischPolytrichaceae Schwaumlgr
Class Bryopsida PaxSubclass Buxbaumiidae Doweld
Order Buxbaumiales MFleischBuxbaumiaceae Schimp
Subclass Diphysciidae OchyraOrder Diphysciales MFleisch
Diphysciaceae MFleischSubclass Timmiidae Ochyra
Order Timmiales OchyraTimmiaceae Schimp
Subclass Encalyptidae Ochyra Żarnowiec amp Bednarek-OchyraOrder Encalyptales Dixon
Encalyptaceae SchimpSubclass Funariidae Ochyra
Order Funariales MFleischFunariaceae Schwaumlgr Disceliaceae Schimp
Subclass Gigaspermidae Stech amp WFreyOrder Gigaspermales Goffinet Wickett OWerner Ros AJShaw amp CJCox
Gigaspermaceae LindbSubclass Dicranidae Doweld
Order Catoscopiales Ignatov amp IgnatovaCatoscopiaceae Broth
Order Scouleriales Goffinet amp WRBuckDrummondiaceae Goffinet Scouleriaceae SPChurchill
Order Bryoxiphiales HACrum amp LEAndersonBryoxiphiaceae Besch
16
Order Grimmiales MFleischGrimmiaceae Arn Ptychomitriaceae Schimp Seligeriaceae Schimp
Order Archidiales LimprArchidiaceae Schimp
Order Mitteniales ShawMitteniaceae Broth
Order Dicranales HPhilib ex MFleischAmphidiaceae Stech Aongstroemiaceae De Not BruchiaceaeSchimp Calymperaceae Kindb Dicranaceae Schimp Dicranel-laceae Stech Ditrichaceae Limpr Erpodiaceae Broth EustichiaceaeBroth Fissidentaceae Schimp Leucobryaceae Schimp Onco-phoraceae Stech Rhachitheciaceae HRob Schistostegaceae SchimpViridivelleraceae IGStone Wardiaceae Welch
Order Pottiales MFleischEphemeraceae Schimp Hypodontiaceae Stech PleurophascaceaeBroth Pottiaceae Schimp Serpotortellaceae WDReese amp RHZander
Subclass Bryidae EnglOrder Hedwigiales Ochyra
Hedwigiaceae Schimp Rhacocarpaceae KindbOrder Helicophyllales Stech amp WFrey
Helicophyllaceae BrothOrder Bartramiales DQuandt NEBell amp Stech
Bartramiaceae SchwaumlgrOrder Splachnales Ochyra
Meesiaceae Schimp Splachnaceae Grev amp ArnOrder Bryales Limpr
Bryaceae Schwaumlgr Leptostomataceae Schwaumlgr Mniaceae SchwaumlgrPhyllodrepaniaceae Crosby Pseudoditrichaceae Steere amp ZIwatsPulchrinodaceae DQuandt NEBell amp Stech
Order Orthotrichales DixonOrthotrichaceae Arn
Order Orthodontiales NEBell AENewton amp DQuandtOrthodontiaceae Goffinet
Order Aulacomniales NEBell AENewton amp DQuandtAulacomniaceae Schimp
Order Rhizogoniales Goffinet amp WRBuckRhizogoniaceae Broth
Order Hypnodendrales NEBell AENewton amp DQuandtBraithwaiteaceae NEBell AENewton amp DQuandt Hypnodendra-ceae Broth Pterobryellaceae WRBuck amp Vitt Racopilaceae Kindb
Order Ptychomniales WRBuck CJCox AJShaw amp GoffinetPtychomniaceae MFleisch
Order Hookeriales MFleischDaltoniaceae Schimp Hookeriaceae Schimp HypopterygiaceaeMitt Leucomiaceae Broth Pilotrichaceae Kindb SaulomataceaeWRBuck CJCox AJShaw amp Goffinet Schimperobryaceae WR
17
Buck CJCox AJShaw amp GoffinetOrder Hypnales WRBuck amp Vitt
Amblystegiaceae GRoth Anomodontaceae Kindb BrachytheciaceaeSchimp Calliergonaceae Vanderpoorten Hedenaumls CJCox amp AJShaw Catagoniaceae WRBuck amp Ireland Climaciaceae KindbCryphaeaceae Schimp Echinodiaceae Broth Entodontaceae KindbFabroniaceae Schimp Fontinalaceae Schimp Helodiaceae OchyraHeterocladiaceae Ignatov amp Ignatova Hylocomiaceae MFleischHypnaceae Schimp Lembophyllaceae Broth LeptodontaceaeSchimp Lepyrodontaceae Broth Leskeaceae Schimp Leucodon-taceae Schimp Meteoriaceae Kindb Microtheciellaceae HAMillamp AJHarr Myriniaceae Schimp Myuriaceae MFleisch NeckeraceaeSchimp Orthorrhynchiaceae SHLin Phyllogoniaceae KindbPlagiotheciaceae MFleisch Pleuroziopsidaceae Ireland Prionodon-taceae Broth Pseudoleskeaceae Schimp PseudoleskeellaceaeIgnatov amp Ignatova Pterigynandraceae Schimp PterobryaceaeKindb Pylaisiaceae Schimp Pylaisiadelphaceae Goffinet amp WRBuck Regmatodontaceae Broth Rhytidiaceae Broth RigodiaceaeHACrum Rutenbergiaceae MFleisch Scorpidiaceae Ignatov ampIgnatova Sematophyllaceae Broth Sorapillaceae MFleisch Ste-reophyllaceae WRBuck amp Ireland Symphyodontaceae MFleischTheliaceae MFleisch Thuidiaceae Schimp TrachylomataceaeWRBuck amp Vitt
Acknowledgements
Sincere thanks are due to JLReveal (Ithaca) as well as WFPrudhomme van Reine and JFVeldkamp(Leiden) for comments and discussions about suprafamilial taxonomy to DQuandt (Dresden) for providingDNA from Rhacocarpus and Bartramiaceae species and to BGiesicke (Berlin) for technical assistance
References
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18
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Received 3 September 2007 accepted in revised form 30 October 2007
4
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scen
s (B
rid
) Pa
ris
(ste
rile
cul
ture
)-
AF
0237
24E
U18
6598
EU
1635
32H
elic
ophy
llace
aeH
elic
ophy
llum
torq
uatu
m (
Hoo
k)
Bri
dF
rahm
150
7F
rey
EU
1865
47E
U18
6602
EU
1635
37B
artr
amia
ceae
Ana
coli
a la
evis
phae
ra (
Tay
lor)
Flo
wer
sS
hevo
ck 1
7853
MO
EU
301
607
AF
4135
57E
U16
3533
Bar
tram
ia s
tric
ta B
rid
Muumll
ler
C15
52M
uumllle
rA
F02
3756
EU
1865
99E
U16
3534
Con
osto
mum
pen
tast
ichu
m (
Bri
d)
Lin
db
Fra
hm s
n
BO
NN
EU
301
606
EU
1866
00E
U16
3535
Phi
lono
tis
font
ana
(Hed
w)
Bri
dG
arto
n 20
748
BO
NN
EF
1075
40E
U18
6601
EU
1635
36O
rtho
tric
hace
aeO
rtho
tric
hum
ano
mal
um H
edw
S
tech
B97
0226
1L
AF
1303
14E
U18
6616
EU
1635
51O
rtho
tric
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str
amin
eum
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nsch
(s
teri
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-A
F12
7183
EU
1866
18E
U16
3553
Ulo
ta c
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a (H
edw
) B
rid
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ch B
0503
243
LE
U18
6557
EU
1866
17E
U16
3552
Zyg
odon
bau
mga
rtne
ri M
alta
Fra
hm s
n 4
51
985
BS
BA
F12
7184
EU
1866
15E
U16
3550
Aul
acom
niac
eae
Aul
acom
nium
pal
ustr
e (H
edw
) S
chw
aumlgr
Ste
ch B
0305
294
LE
U18
6551
EU
1866
09E
U16
3544
Aul
acom
nium
turg
idum
(W
ahle
nb)
Sch
waumlg
r(G
enB
ank)
-A
F02
3728
AF
4135
32A
Y31
2894
Hym
enod
onto
psis
mni
oide
s (H
ook
)F
rey
amp S
chau
man
nF
F
rey
EU
1865
63E
U18
6625
EU
1635
60N
EB
ell
AE
New
ton
amp D
Qua
ndt
01
-186
aO
rtho
dont
iace
aeH
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odon
pil
ifer
Hoo
kf
amp W
ilso
nF
rahm
1-1
4F
rey
EU
1865
59E
U18
6620
EU
1635
55O
rtho
dont
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lin
eare
Sch
waumlg
r
S
tech
B95
0616
2L
EU
1865
58E
U18
6619
EU
1635
54L
epto
thec
a ga
udic
haud
ii S
chw
aumlgr
Fre
y amp
Sch
aum
ann
F
Fre
yA
F02
3750
EU
1866
24E
U16
3559
01-0
9
Tab
le 1
con
tinu
ed
5
Rhi
zogo
niac
eae
Cal
omni
on c
ompl
anat
umFr
ahm
20-
4Fr
eyE
U18
6560
EU
1866
21E
U16
3556
(Hoo
kf
amp W
ilso
n) L
indb
C
rypt
opod
ium
bar
tram
ioid
es (
Hoo
k)
Bri
d
Fr
ey amp
Sch
aum
ann
01-4
0F
F
rey
EU
1865
61E
U18
6622
EU
1635
57
Rhi
zogo
nium
dis
tich
um (
Sw
) B
rid
Fra
hm 2
-11
Fre
yE
U18
6562
EU
1866
23E
U16
3558
Hyp
node
ndra
ceae
Cyr
topu
s se
tosu
s (H
edw
) H
ook
fF
rahm
X16
-1F
rey
EU
1865
69E
U18
6631
EU
1635
66H
ypno
dend
ron
spin
iner
vium
(H
ook
)P
feif
fer
98-T
162
CH
R
Fre
yE
U18
6567
EU
1866
29E
U16
3564
AJ
aege
r amp
Sau
erb
Hyp
node
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n vi
tien
se M
itt
Stre
iman
nB
EU
1865
68E
U18
6630
EU
1635
65Sc
iado
clad
us k
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itt)
AJ
aege
r ex
Bro
th
Pfe
iffe
r T
210
CH
R
Fre
yE
U18
6565
EU
1866
27E
U16
3562
Scia
docl
adus
men
zies
ii (
Hoo
k)
Fre
y amp
Pfe
iffe
rC
HR
F
rey
EU
1865
66E
U18
6628
EU
1635
63L
indb
ex
Bro
th
98-M
o5R
acop
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aeR
acop
ilum
con
volu
tace
um (M
uumlllH
al)
Zan
k s
nF
rey
EU
1865
64E
U18
6626
EU
1635
61R
eich
ardt
Ptyc
hom
niac
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Pty
chom
nion
pty
choc
arpo
n (S
chw
aumlgr
)F
rey
amp S
chau
man
nF
F
rey
EU
1865
70E
U18
6632
EU
1635
67M
itt
01
-266
aH
ooke
riac
eae
Hoo
keri
a lu
cens
(H
edw
) S
m
Ste
ch B
8804
048
LA
F15
2380
EU
1866
35E
U16
3570
Lep
idop
ilum
vir
ens
Car
dot
S
tech
et a
l 04
-109
LE
U18
6571
EU
1866
33E
U16
3568
Tet
rast
ichi
um fo
ntan
um (
Mit
t) C
ardo
t
Ste
ch e
t al
04-1
24L
EU
1865
72E
U18
6634
EU
1635
69H
ypop
tery
giac
eae
Arb
uscu
lohy
popt
eryg
ium
arb
uscu
la (
Bri
d)
Fre
y 95
-17
CH
R
Fre
yA
F13
4637
EU
1866
37E
U16
3573
MS
tech
TP
feif
f amp
WF
rey
Cat
haro
mni
on c
ilia
tum
(H
edw
) W
ilso
nB
eeve
r 97
-69
CH
R
Fre
yE
U18
6573
EU
1866
36E
U16
3572
Hyp
opte
rygi
um d
isco
lor
Mit
tS
trei
man
n 52
819
Fre
y ex
LA
F36
3282
AY
8642
93E
U16
3575
Hyp
opte
rygi
um t
amar
isci
(Sw
)Pf
eiff
er amp
Sip
man
BD
Q07
7169
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8642
94E
U16
3574
Bri
d e
x M
uumlllH
al
99-6
9L
opid
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con
cinn
um (
Hoo
k)
Wil
son
Fre
y 95
-62
Fre
yA
F03
3231
AY
8642
95E
U16
3571
Font
inal
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nali
s an
tipy
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ca H
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Ste
ch e
t al
04-1
4L
EU
1865
74E
U18
6638
EU
1635
76A
mbl
yste
giac
eae
Cra
tone
uron
fili
cinu
m (
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w)
Spr
uce
Ste
ch B
9006
151
LA
F12
9586
EU
1866
45E
U16
3583
Bra
chyt
heci
acea
eP
laty
hypn
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m r
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es (
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w)
Dix
on
Ste
ch e
t al
04-2
37L
EU
1865
77E
U18
6644
EU
1635
82H
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ceae
Hyp
num
and
oi A
JE
Sm
Ste
ch e
t al
04-4
54L
EU
1865
78E
U18
6647
EU
1635
85R
hytid
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aeR
hyti
dium
rug
osum
(E
hrh
ex
Hed
w)
Kin
db
Ste
ch B
9309
101
LA
F26
4046
EU
1866
39E
U16
3577
Cry
phae
acea
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ryph
aea
tasm
anic
a M
itt
Frah
m 3
1-1
Frey
EU
1865
76E
U18
6643
EU
1635
81L
euco
dont
acea
eA
ntitr
ichi
a cu
rtip
endu
la (T
imm
ex
Hed
w)
Brid
S
tech
B94
0717
3L
AY
0102
86E
U18
6641
EU
1635
79N
ecke
race
aeT
ham
nobr
yum
pan
dum
(H
ook
f amp
Wil
son)
Fre
y amp
Fre
y 94
-117
Fre
yA
Y01
0297
EU
1866
42E
U16
3580
IG
Sto
ne amp
GA
MS
cott
Plag
ioth
ecia
ceae
Pla
giot
heci
um u
ndul
atum
(H
edw
) S
chim
pS
tech
B88
1003
2L
AF
2640
45E
U18
6646
EU
1635
84C
atag
onia
ceae
Cat
agon
ium
nit
ens
(Bri
d)
Car
dot
Fre
y amp
Sch
aum
ann
F
Fre
yE
U18
6575
EU
1866
40E
U16
3578
01-1
87a
Tab
le 1
con
tinu
ed
6
primers CM
DM
(slightly modified after Taberlet et al 1991 see Frey et al 1999) and atpB-1rbcL-1(Chiang et al 1998) respectively For amplification of the psbA-trnH spacer primers psbAF(5-GTT ATG CAT GAA CGT AAT GCT C-3 Sang et al 1997) and trnHR-2 (5-CGC GCA TGGTGG ATT CAC AAT CC-3 slightly modified after Sang et al 1997) were used with a PCRprotocol of 5 min 94degC 35 cycles (30 sec 94degC 1 min 48degC 1 min 40 sec 72degC) 7 min 72degC PCRproducts were purified using DNA purification kits (Qiagen Macherey-Nagel) Sequencing wasperformed as described in Stech (2004) using the amplification primers
ALIGNMENT AND PHYLOGENETIC ANALYSES DNA sequences were manually aligned in PhyDE v0992(Muumlller et al 2005) Following Quandt et al (2003) and Quandt amp Stech (2005) inversions inputative hairpin secondary structures were positionally separated in the alignment their presence orabsence was not coded for the phylogenetic analyses Phylogenetic reconstructions under the maximumparsimony criterion were performed using winPAUP 40b10 (Swofford 2002) in combination withPRAP (Muumlller 2004) as implemented in SeqState (Muumlller 2005) PRAP generates command filesfor PAUP that allow parsimony ratchet searches as designed by Nixon (1999) Heuristic searchesunder parsimony were performed with the following options all characters equally weighted andunordered TBR branch swapping collapse branches if maximum branch length is zero MulTreesoption in effect gaps treated as missing data Initially a heuristic search with 1000 addition sequencereplicates was performed For the parsimony ratchet ten random addition cycles of 200 ratchetiterations each were used with TBR branch swapping on a randomly re-weighted data set (25 ofthe positions) Heuristic bootstrap searches were performed with 1000 replicates with 10 additionsequence replicates per bootstrap replicate
Results
In the present data set of non-coding plastid markers sequence lengths ranged from243 to 368 nucleotides (nt) in the trnL intron and from 445 to 615 nt in the atpB-rbcL spacer The psbA-trnH spacer was considerably shorter than the other twomarkers and ranged from 103 to 186 nt The combined alignment of sequences from85 ingroup and two outgroup taxa comprised 2430 positions (trnL intron 668 atpB-rbcL spacer 1366 psbA-trnH spacer 396 positions) The most variable regions withambiguous alignment (781 positions) were excluded from phylogenetic analysis Ofthe 1649 included positions 628 (381) were variable and 455 of the variablepositions (725 or 276 of the total number of positions) were parsimony-informative The trnL intron comprised 124 the atpB-rbcL spacer 286 and the psbA-trnH spacer 45 of these included parsimony-informative positions
The shortest trees found in the heuristic maximum parsimony analysis of the combineddata set had a length of 2433 steps By applying the parsimony ratchet 129 treeswere retained that were one step shorter (length 2432 CI = 0419 RI = 0624) Thestrict consensus tree of the ratchet analysis is shown in Fig 1 The ingroup (Bryopsida)is supported with 100 bootstrap support (BS) Diphysciidae are sister to theremaining Bryopsida with 54 BS Encalyptidae Funariidae Timmiidae andDicranidae all receive gt 95 BS while Bryidae are slightly less supported (89BS) Relationships between these major lineages are resolved but unsupported Atordinal level within the Bryidae a lower resolution is observed SplachnalesOrthotrichales Aulacomniales Hypnodendrales Hookeriales and Hypnales areresolved as monophyletic with 67-100 BS whereas Hedwigiales BartramialesBryales Orthodontiales and Rhizogoniales are not A closer relationship ofOrthotrichales with the pleurocarpous mosses sl than with the more basal ordersHedwigiales Bartramiales Splachnales and Bryales is indicated
7
Discussion
Classification of mosses - recent progress and the current state
For a long time mosses were subdivided into three main lineages the subclassesSphagnidae Andreaeidae and Bryidae (eg Fleischer 1920 Vitt 1984 Frahm ampFrey 1987) the latter with a number of (super-)orders (eg Frey 1977) Howevermolecular data confirmed that mosses comprise a number of isolated basal lineagesrepresented by morphologically and ecologically distinct extant taxa such as TakakiaSphagnum Andreaea Andreaeobryum Oedipodium Tetraphis the Polytrichaceaeand Buxbaumia which probably have long independent phylogenetic histories (cfNewton et al 2007) As a result of molecular phylogenies and a re-evaluation ofmorphological-anatomical characters the classification of mosses has changedconsiderably in the last few years with the main lineages nowadays treated atsubdivision class and subclass levels within division Bryophyta (eg Doweld 2001Ochyra et al 2003 Goffinet amp Buck 2004 this study)
Takakia and Sphagnum are the earliest diverging moss taxa in molecular phylogenies(eg Newton et al 2000 Beckert et al 2001 Cox et al 2004 Qiu et al 2006Newton et al 2007) That Takakia is a moss and not a liverwort was confirmed byanalysis of DNA sequences and phylogenomic characters such as the distribution ofmitochondrial introns (eg Beckert et al 2001) Its taxonomic status however stillremains to be clarified On the one hand most molecular studies resolve Takakiaand Sphagnum as sister genera although only partly with high statistical supportThese molecular topologies do not support the recognition of division Takakiophytaas proposed by Crandall-Stotler (1986) One the other hand no morphologicalsynapomorphies unite Takakia with Sphagnum and significant molecular differencesseparating Takakia from all other mosses were also observed For example a regionin the plastid ITS3 is similar to that of other land plants but absent in mosses(Samigullin et al 2002) and a transition in the trnL
UAA gene changing the anticodon
to CAA was otherwise only found in leptosporangiate ferns and Ginkgo (Quandt etal 2004) Thus ldquoresolution of Sphagnum - Takakia clade may be an artifactrdquo (Shawamp Renzaglia 2004) Also Goffinet amp Buck (2004) did not unite Takakia and Sphagnumunder a formal taxonomic rank but placed them into different informal superclassesIn our opinion Takakia should be treated at the same level as Sphagnophytina andBryophytina (cf Doweld 2001) ie as a subdivision of Bryophyta However morefundamental nomenclatural changes are necessary as the family name Takakiaceaewas not validated in the original publication by Hattori amp Inoue (1958) (article411 of ICBN McNeill et al 2006) and consequently all higher taxa erected laterare invalid The corrected taxonomic treatment of Takakia is provided here withsporophytic characters included in the latin diagnosis of Takakiaceae (see taxonomy)
Within Bryophytina we recognise four morphologically and molecularly isolatedbasal lineages as separated from the arthrodontous mosses (Bryopsida) Andreaeopsida(with linear capsule dehiscence) the operculate but eperistomate Oedipodiopsida aswell as Polytrichopsida and Tetraphidopsida with nematodontous peristomes A fifthclass Andreaeobryopsida was erected by Buck amp Goffinet (2000) but re-includedin Andreaeopsida as a subclass by Ochyra et al (2003) The systematic status of
8
Andreaeobryum macrosporum Steere amp BMMurray and possible relationships withAndreaea and Takakia were discussed by Murray (1988) and summarised includingmolecular results by Shaw amp Renzaglia (2004)
On the next lower level a number of morphologically and molecularly divergentlineages are nowadays treated as subclasses of Bryopsida Buxbaumiidae andDiphysciidae are generally branching off first in molecular topologies (eg Beckertet al 2001 Magombo 2003 Cox et al 2004) followed by Timmiidae Encalyptidaeand Funariidae as well as Dicranidae (haplolepideous mosses) sister to Bryidae slThese subclasses (except Buxbaumiidae not included) are also well recognizable inthe present analysis of non-coding plastid sequences (Fig 1)
The morphologically very different Encalyptidae and Funariidae are revealed assister groups although mostly without high support in several molecular phylogenies(eg Goffinet et al 2001 Cox et al 2004 Hedderson et al 2004 Tsubota et al2003 2004) and also in the present study (Fig 1) Goffinet et al (2007) confirmedthis relationship by phylogenomic evidence namely a large (71 kb) inversion in thechloroplast genome of Funariaceae Disceliaceae and Encalyptaceae but not inGigaspermaceae Consequently the latter family was separated at ordinal level fromthe two remaining families of Funariales by Goffinet et al (2007) GigaspermalesFunariales and Encalyptales may share a common ancestor according to some butnot all molecular phylogenies (eg Goffinet et al 2001 2007 Hedderson et al2004 but not in Tsubota et al 2004) Although ontogenetic data from peristomedevelopment may support their common ancestry (Goffinet et al 2007) unambiguousmorphological synapomorphies are lacking We therefore propose to treatGigaspermaceae at subclass level within the Bryopsida (see taxonomy)
The haplolepideous mosses (Dicranidae) are clearly supported as a monophyleticlineage which obviously evolved from a diplolepideous ancestor according to theirposition in the molecular trees (eg Newton et al 2000 Tsubota et al 2003 Cox etal 2004 Goffinet amp Buck 2004) Molecular studies suitable for inferring ordinaland family level relationships within Dicranidae either focused on the haplolepideousmosses (eg Stech 1999ab 2004 LaFarge et al 2000 2002 Tsubota et al 2003Hedderson et al 2004) or included more than 15 haplolepideous taxa in analyses ofa broader range of mosses (eg Goffinet et al 2001 Tsubota et al 2004 this study)Major lineages supported by these analyses are for example Grimmiales(Grimmiaceae Ptychomitriaceae and Seligeriaceae) Leucobryaceae (incl formerDicranaceae-Campylopoideae and Paraleucobryoideae pp) Dicranaceae sstr(Dicranoideae plus former Dicnemonaceae and Paraleucobryoideae pp) Pottiaceae(incl Cinclidotaceae and Splachnobryum) and Calymperaceae (probably exclOctoblepharum) Furthermore several genera and families belong to Dicranidaewhose systematic positions have been controversial (eg Stech et al 1999b LaFarge et al 2002 Hedderson et al 2004 OBrien 2007 Quandt et al 2007 thisstudy) Amphidium Archidium Catoscopium Drummondia EphemeraceaeErpodiaceae Mittenia (cf OBrien 2007 sequences in some earlier analyses werebased on misdentified specimens) Rhachitheciaceae Schistostega Splachnobryumand Wardia On the contrary several problems remain such as the circumscriptionof Ditrichaceae and relationships of the major haplolepideous lineages in general
9
Fig 1 Strict consensus tree of 129 most parsimonious trees inferred from combined trnLUAA
intronatpB-rbcL spacer and psbA-trnH spacer sequences of 85 taxa of Bryopsida as well as Andreaearupestris (Andreaeopsida) and Pogonatum subulatum (Polytrichopsida) as outgroup representativesBootstrap support values gt50 are depicted above the branches
10
Consequently resolving the phylogeny of Dicranidae with confidence is one of themajor future challenges in moss systematics
As mentioned above Dicranaceae are monophyletic in a narrow circumscriptionaccording to molecular data In contrast to former Campylopoideae andParaleucobryoideae the status of Rhabdoweisioideae (= Oncophoroideae Ochyra2002) and Dicranelloideae needs further consideration Stech (1999ab) suggestedto recognise RhabdoweisioideaeRhabdoweisiaceae in a broad sense includingDicranoweisia Amphidium and Aongstroemia Subsequent molecular analysesconfirmed a close relationship of the genera Arctoa Cynodontium DicranoweisiaKiaeria Oncophorus Oreoweisia Oreas Rhabdoweisia and Symblepharis althoughwithout significant support (La Farge et al 2002 Tsubota et al 2003 Hedderson etal 2004) With respect to the molecular evidence available so far we propose toelevate Oncophoroideae to family level to accomodate these genera and perhapsGlyphomitrium (cf Tsubota et al 2003) whereas we consider AongstroemiaDichodontium and Diobelonella to belong to Aongstroemiaceae (cf Stech 1999a)Amphidium is neither closely related to Dicranaceae sstr nor to Oncophoroideae(La Farge et al 2002 Tsubota et al 2003 Hedderson et al 2004 Stech 2004 thisstudy) and should be treated at family level rather than placed in Dicranaceae assubfam Amphidioideae (Ochyra et al 2003) The circumscription of Dicranelloideaeis more difficult to evaluate as few representatives have been included in molecularanalyses However Dicranella heteromalla (Hedw) Schimp as well as the generaCampylopodium and Microcampylopus are clearly separated from Dicranaceae sstr(Stech 1999a 2004 La Farge et al 2002 Tsubota et al 2003 Hedderson et al2004) and consequently the subfamily deserves family status as well Finallymolecular data showed that the genus Hypodontium does not belong to Pottiaceae(Hedderson et al 2004 Tsubota et al 2004) Taxonomic conclusions have not beendrawn from these results which is made up here (see taxonomy)
All mosses with diplolepideous-alternate peristomes together with Splachnales witha diplolepideous-opposite (Funaria-type) peristome form a monophyletic group inmolecular analyses (eg Newton et al 2000 Beckert et al 2001 Goffinet et al2001 Cox et al 2004 Tsubota et al 2004 references in Table 2) Differentclassifications of this by far most species-rich group of mosses were proposed (egVitt et al 1998 Ochyra et al 2003 Goffinet amp Buck 2004) However at least someof the recognised subclasses and superorders are paraphyletic according to themolecular topologies and assigning formal ranks to all evolutionarily significantmonophyletic entities is problematic if the main taxonomic framework of Bryophytaand Bryopsida should be maintained (cf discussion in Bell et al 2007) Thereforein the present synopsis only one subclass Bryidae is recognised for all diplolepideous-alternate mosses and Splachnales This broadly defined Bryidae is subdivided into13 orders most of them resolved as monophyletic in the majority of the phylogeneticanalyses summarised in Table 2 although with different levels of statistical supportin maximum parsimony analyses To define monophyletic lineages at supraordinallevel informal node-based names may be chosen according to Bell et al (2007) Forexample the pleurocarpous mosses (pleurocarpy sensu Bell amp Newton 2007) andtheir closest acrocarpous relatives (Orthodontiales to Hypnales) were already
11
Table 2 Taxon sampling and bootstrap support (BS) for Dicranidae Bryidae and orders within theBryidae in recent phylogenetic analyses (MP only) based on combined molecular markers Markersare given in square brackets (non-coding regions in bold) numbers of included taxa in brackets ++respective clade present with ge 80 BS + clade present with lt 80 BS - clade not present no oronly one representative included
Bell amp Newton OBrien Quandt et al Bell et al this study(2004) (2007) (2007) (2007)
[rbcL rps4 [atpB atpB- [rbcL rps4 [rbcL rps4 [atpB-rbcLnad5] rbcL rbcL trnL-F nad5] trnL-F nad5] psbA-trnH
rps4 trnL-F] trnL]
Dicranidae + (2) + (4) ++ (3) (1) ++ (19)Bryidae ++ (57) + (53) ++ (52) ++ (98) ++ (58)Hedwigiales ++ (2) (1) ++ (2) ++ (2) - (3)Bartramiales ++ (2) ++ (4) ++ (4) ++ (3) - (4)Splachnales (0) ++ (2) ++ (3) ++ (2) ++ (5)Bryales - (4) - (5) ++ (18) + (17) - (8)Orthotrichales (1) ++ (3) ++ (3) ++ (2) ++ (4)Orthodontiales + (4) + (4) + (3) + (6) - (3)Aulacomniales + (6) + (7) ++ (2) + (7) + (3)Rhizogoniales ++ (13) + (8) ++ (5) ++ (14) - (3)Hypnodendrales ++ (13) + (7) ++ (4) ++ (29) ++ (6)Ptychomniales ++ (3) ++ (3) (1) ++ (4) (1)Hookeriales - (4) + (2) (1) + (2) + (8)Hypnales - (5) - (7) ++ (5) ++ (10) + (10)
summarised under the informal node based name pleurcarpids (Bell et al 2007)and can be distinguished from a basal grade of acrocarpous or cladocarpous lineages(Hedwigiales to Orthotrichales) Within the latter monophyly of BartramialesSplachnales and Orthotrichales is well-supported in all analyses including two ormore taxa except Bartramiales in the present data set (cf Fig 1) In contrast Bryalesreceive significant support less frequently (but see Bell et al 2007 Quandt et al2007) Hedwigiales are well supported if only Hedwigia (Hedwigiaceae) andRhacocarpus (Rhacocarpaceae) are included whereas the monospecific Helicophyllum(Helicophyllaceae) is not closely related to these taxa but shows affinities withBartramiales (Goffinet et al 2001 this study) With respect to the differentmorphologies of Helicophyllaceae and Bartramiaceae however the former shouldbe separated at ordinal level (see taxonomy)
Clarifying relationships of the Orthotrichales is still a difficult issue Analyses ofsingle chloroplast markers or parsimony analyses of combined markers from differentgenomes mostly indicated a close relationship either with Splachnales (eg Cox etal 2000 Newton et al 2000 Tsubota et al 2004 Quandt et al 2007) or with thepleurocarpids (Goffinet et al 2001 this study) Although none of these alternativesis well-supported the latter seems more likely with regard to the moderately tomaximally supported Orthotrichales - pleurocarpid sister group relationship in allanalyses of mitochondrial data and in likelihood analyses of combined plastidmitochondrial markers (Beckert et al 2001 Quandt et al 2007)
12
The molecular polyphyly of Rhizogoniaceae (eg Bell amp Newton 2004) was solvedby the transfer of rhizogonioid genera into broadly defined Aulacomniaceae andOrthodontiaceae (Bell et al 2007) which now include both acrocarpous andpleurocarpous taxa These systematic changes are also comprehensible by non-molecular characters such as morphological traits shared by Mesochaete andAulacomnium heterostichum (Hedw) Bruch amp Schimp or the variously reducedperistomes of Orthodontiaceae pp in contrast to the generally fully developed Bryum-type peristomes of rhizogonioid and hypnodendroid mosses (Bell et al 2007) Theposition of the solely pleurocarpous Hypnodendrales sister to the former Hypnidaeled to the recognition of the informal group core pleurocarps (Bell et al 2007)The former Hypnidae (Ptychomniales Hookeriales and Hypnales summarised ashomocostate pleurocarps) are monophyletic in most molecular analyses (eg Goffinetet al 2001 Tsubota et al 2004 Bell et al 2007) with Ptychomniales being well-supported (Pedersen amp Newton 2007 Table 2) Clarifying relationships betweenHookeriales and Hypnales and within the latter is still a challenge but recent molecularstudies seem to support a sister group relationship of both orders (Bell et al 2007present study)
Phylogenetic utility of non-coding plastid markers
Non-coding plastid markers that comprise both variable and conserved regionssuch as the trnL
UAA intron have repeatedly been shown to possess potential for
resolving relationships at high taxonomic levels (eg Borsch et al 2003 Quandtet al 2004) Both the trnL intron and atpB-rbcL spacer were characterised indetail in mosses with respect to their structure and molecular evolution (Quandt ampStech 2005 Stech amp Quandt 2006) They include conservative regions that can beunambiguosly aligned and even parts of the more variable regions can be used ifrepeats hairpin loops etc are correctly identified and adequately treated in thephylogenetic analyses (eg Quandt et al 2003 Quandt amp Stech 2005) Using theatpB-rbcL spacer alone (Stech amp Quandt 2006) relationships of the major mosslineages were largely consistent with the ldquototal evidencerdquo molecular tree of Goffinetamp Buck (2004) However in addition to general limitations that result from singlemarker analyses the use of non-coding markers may pose further problems suchas a high amount of homoplasy resulting in low resolution or low statistical supportfor many clades Therefore several recent molecular studies of relationships withinBryidae have employed both coding and non-coding markers (Table 2)Nevertheless the usefulness of analyses of combined non-coding plastid markerscannot be ruled out In fact Fig 1 and Table 2 indicate a phylogenetic signal inthe present data set as many clades are recovered that are usually also resolvedin analyses of coding or combined coding and non-coding markers Especiallywith regard to statistical support however the present analysis is inferior tothose of other recent data sets especially Bell et al (2007) and Quandt et al(2007) In addition the non-coding markers used here are of different suitabilityand even the two intergenic spacers differ considerably from each other ThepsbA-trnH spacer contributes much less to the trees resolution than the atpB-rbcL spacer first because it is much shorter and second because relatively largeparts are attributed to hairpin loops or otherwise hypervariable regions These
13
results indicate that future studies should evaluate the molecular evolution andphylogenetic potential of new markers both coding and con-coding and choosethe most suitable ones in a combined analysis to resolve the remaining uncertaintiesin moss phylogeny
Taxonomy
Takakiaceae Stech amp WFrey stat nov
Plantae virides nusquam rhizophorae sine protonemate e caudicis rhizomatis erectae Caudicesrhizomati et axes geotropi radiformes frequenter intercalariter ramificantes sine phyllidiis cumpapillis mucilaginis rostratis Caules phyllidiiferi saepe furcati Phyllidia sine lamina et costadistincta profunde 2-4(-5)-lobata pluristratosa tristicha sed torsione spiraliter disposita Filumcentralium in ambabus generationibus (axibus gametophyti et setis) adest Plantae dioicae Antheridiaet archegonia nuda Sporophytum terminale solitarium Seta persistens Capsula tortilis admaturitatem schizocarpa secus unam rimam spiralem longitudinalem dehiscens Stomata etoperculum absunt peristomium nullum Calyptra mitriformis
TYPUS Takakia SHatt amp Inoue J Hattori Bot Lab 19 137 1958
Takakiaceae SHatt amp Inoue J Hattori Bot Lab 19 137 1958 nom inval (Art 411)
Takakiales Stech amp WFrey stat nov
Based on Takakiaceae Stech amp WFrey Nova Hedwigia 86 13 2008
TYPUS Takakia SHatt amp Inoue J Hattori Bot Lab 19 137 1958
Takakiales SHatt amp Inoue J Hattori Bot Lab 19 137 1958 nom inval
Takakiales SHatt amp Inoue ex RMSchust J Hattori Bot Lab 26 224 1963 nom inval (cumdescr latin)
Takakiopsida Stech amp WFrey statnov
Based on Takakiaceae Stech amp WFrey Nova Hedwigia 86 13 2008
TYPUS Takakia SHatt amp Inoue J Hattori Bot Lab 19 137 1958
Takakiopsida Goffinet amp WRBuck Monogr Syst Bot Missouri Bot Gard 98 232 2004 nominval
Takakiopsida Jia et al Acta Phytotax Sin 41 350 351 2003 nom nud
Takakiopsida Wang amp Wu Fl Bryophyt Sin 8 447 2004 nom inval (cum descr latin)
Takakiophytina Stech amp WFrey stat nov
Based on Takakiaceae Stech amp WFrey Nova Hedwigia 86 13 2008
TYPUS Takakia SHatt amp Inoue JHattori Bot Lab 19 137 1958
Gigaspermidae Stech amp WFrey subclass nov
Plantae acrocarpae terrestres stoloniferae ramis brevibus erectis Folia unicostata cellulis laxislaevibus Capsula plerumque valde rugosa gymnostomatica vel cleistocarpa stomata cum duabuscellulis sociis Ab Funariidis et Encalyptidis charactere phylogenomico (71-kb inversio abest)separatae
14
TYPUS Gigaspermum Lindb Oumlfversigt af Foumlrhandlingar Kongl Svenska Vetenskaps-Akademien21 599 1865
Amphidiaceae Stech stat nov
Based on Dicranaceae subfam Amphidioideae Ochyra in Ochyra Zarnowiec amp Bednarek-OchyraCens Cat Polish Mosses 110 2003
TYPUS Amphidium Schimp Coroll Bryol Eur 39 1856
Amphidiaceae AJESm Moss Fl Britain Ireland 2nd ed 657 2004 nom inval descr angl
Dicranellaceae Stech stat nov
Based on Dicranaceae subfam Dicranelloideae Lindb Utkast Eur Bladmoss 33 1878[lsquoUnderfamilje Dicranelleaersquo]
TYPUS Dicranella (MuumlllHal) Schimp Coroll Bryol Eur 13 1856
Oncophoraceae Stech stat nov
Based on Dicranaceae subfam Oncophoroideae Lindb Utkast Eur Bladmoss 34 1878[lsquoUnderfamilje Oncophoreaersquo]
TYPUS Oncophorus (Brid) Brid Bryol Univ 1 389 1826
Hypodontiaceae Stech fam nov
Plantae robustae characteribus morphologicis Pottiaceis et Calymperaceis similes sedcharacteribus molecularicis separatae Bracteae perichaetiales internae e basi vaginantes subulataevel aristatae Capsula aspectu succulenta cellulae exothecii incrassatae annulus magnopereabsens Peristomii dentes breves triangulati incurvati aurantiaci leves vel infirme verrucosiCalyptra cucullata
TYPUS Hypodontium MuumlllHal Hedwigia 38 96 1899
Helicophyllales Stech amp WFrey ord nov
Plantae acrocarpae prostratae tomentosae Folia dimorpha in duas series laterales et unam seriemventralem divisa Costa percurrens Cellulae hexagonae ad subquadratae papillosae Capsula immersacupulata ad oblonga infra orificium abrupte incurvata stomata destituta Peristomium nullum Sporaeisomorphae heteropolares granulatae
TYPUS Helicophyllum Brid Bryol Univ 2 771 1827
Synopsis of the suprageneric classification of BryophytaAuthor citations are in accordance with Art 492 of the Vienna Code (McNeill et al 2006)
Subdivision Takakiophytina Stech amp WFreyClass Takakiopsida Stech amp WFrey
Order Takakiales Stech amp WFreyTakakiaceae Stech amp WFrey
Subdivision Sphagnophytina DoweldClass Sphagnopsida Schimp
Order Sphagnales Limpr
15
Sphagnaceae DumortOrder Ambuchananiales Seppelt amp HACrum
Ambuchananiaceae Seppelt amp HACrumSubdivision Bryophytina Engler
Class Andreaeopsida JHSchaffnSubclass Andreaeidae Engl
Order Andreaeales LimprAndreaeaceae Dumort
Subclass Andreaeobryidae OchyraOrder Andreaeobryales BMMurray
Andreaeobryaceae Steere amp BMMurrayClass Oedipodiopsida Goffinet amp WRBuck
Order Oedipodiales Goffinet amp WRBuckOedipodiaceae Schimp
Class Tetraphidopsida Goffinet amp WRBuckOrder Tetraphidales MFleisch
Tetraphidaceae SchimpClass Polytrichopsida Doweld
Order Polytrichales MFleischPolytrichaceae Schwaumlgr
Class Bryopsida PaxSubclass Buxbaumiidae Doweld
Order Buxbaumiales MFleischBuxbaumiaceae Schimp
Subclass Diphysciidae OchyraOrder Diphysciales MFleisch
Diphysciaceae MFleischSubclass Timmiidae Ochyra
Order Timmiales OchyraTimmiaceae Schimp
Subclass Encalyptidae Ochyra Żarnowiec amp Bednarek-OchyraOrder Encalyptales Dixon
Encalyptaceae SchimpSubclass Funariidae Ochyra
Order Funariales MFleischFunariaceae Schwaumlgr Disceliaceae Schimp
Subclass Gigaspermidae Stech amp WFreyOrder Gigaspermales Goffinet Wickett OWerner Ros AJShaw amp CJCox
Gigaspermaceae LindbSubclass Dicranidae Doweld
Order Catoscopiales Ignatov amp IgnatovaCatoscopiaceae Broth
Order Scouleriales Goffinet amp WRBuckDrummondiaceae Goffinet Scouleriaceae SPChurchill
Order Bryoxiphiales HACrum amp LEAndersonBryoxiphiaceae Besch
16
Order Grimmiales MFleischGrimmiaceae Arn Ptychomitriaceae Schimp Seligeriaceae Schimp
Order Archidiales LimprArchidiaceae Schimp
Order Mitteniales ShawMitteniaceae Broth
Order Dicranales HPhilib ex MFleischAmphidiaceae Stech Aongstroemiaceae De Not BruchiaceaeSchimp Calymperaceae Kindb Dicranaceae Schimp Dicranel-laceae Stech Ditrichaceae Limpr Erpodiaceae Broth EustichiaceaeBroth Fissidentaceae Schimp Leucobryaceae Schimp Onco-phoraceae Stech Rhachitheciaceae HRob Schistostegaceae SchimpViridivelleraceae IGStone Wardiaceae Welch
Order Pottiales MFleischEphemeraceae Schimp Hypodontiaceae Stech PleurophascaceaeBroth Pottiaceae Schimp Serpotortellaceae WDReese amp RHZander
Subclass Bryidae EnglOrder Hedwigiales Ochyra
Hedwigiaceae Schimp Rhacocarpaceae KindbOrder Helicophyllales Stech amp WFrey
Helicophyllaceae BrothOrder Bartramiales DQuandt NEBell amp Stech
Bartramiaceae SchwaumlgrOrder Splachnales Ochyra
Meesiaceae Schimp Splachnaceae Grev amp ArnOrder Bryales Limpr
Bryaceae Schwaumlgr Leptostomataceae Schwaumlgr Mniaceae SchwaumlgrPhyllodrepaniaceae Crosby Pseudoditrichaceae Steere amp ZIwatsPulchrinodaceae DQuandt NEBell amp Stech
Order Orthotrichales DixonOrthotrichaceae Arn
Order Orthodontiales NEBell AENewton amp DQuandtOrthodontiaceae Goffinet
Order Aulacomniales NEBell AENewton amp DQuandtAulacomniaceae Schimp
Order Rhizogoniales Goffinet amp WRBuckRhizogoniaceae Broth
Order Hypnodendrales NEBell AENewton amp DQuandtBraithwaiteaceae NEBell AENewton amp DQuandt Hypnodendra-ceae Broth Pterobryellaceae WRBuck amp Vitt Racopilaceae Kindb
Order Ptychomniales WRBuck CJCox AJShaw amp GoffinetPtychomniaceae MFleisch
Order Hookeriales MFleischDaltoniaceae Schimp Hookeriaceae Schimp HypopterygiaceaeMitt Leucomiaceae Broth Pilotrichaceae Kindb SaulomataceaeWRBuck CJCox AJShaw amp Goffinet Schimperobryaceae WR
17
Buck CJCox AJShaw amp GoffinetOrder Hypnales WRBuck amp Vitt
Amblystegiaceae GRoth Anomodontaceae Kindb BrachytheciaceaeSchimp Calliergonaceae Vanderpoorten Hedenaumls CJCox amp AJShaw Catagoniaceae WRBuck amp Ireland Climaciaceae KindbCryphaeaceae Schimp Echinodiaceae Broth Entodontaceae KindbFabroniaceae Schimp Fontinalaceae Schimp Helodiaceae OchyraHeterocladiaceae Ignatov amp Ignatova Hylocomiaceae MFleischHypnaceae Schimp Lembophyllaceae Broth LeptodontaceaeSchimp Lepyrodontaceae Broth Leskeaceae Schimp Leucodon-taceae Schimp Meteoriaceae Kindb Microtheciellaceae HAMillamp AJHarr Myriniaceae Schimp Myuriaceae MFleisch NeckeraceaeSchimp Orthorrhynchiaceae SHLin Phyllogoniaceae KindbPlagiotheciaceae MFleisch Pleuroziopsidaceae Ireland Prionodon-taceae Broth Pseudoleskeaceae Schimp PseudoleskeellaceaeIgnatov amp Ignatova Pterigynandraceae Schimp PterobryaceaeKindb Pylaisiaceae Schimp Pylaisiadelphaceae Goffinet amp WRBuck Regmatodontaceae Broth Rhytidiaceae Broth RigodiaceaeHACrum Rutenbergiaceae MFleisch Scorpidiaceae Ignatov ampIgnatova Sematophyllaceae Broth Sorapillaceae MFleisch Ste-reophyllaceae WRBuck amp Ireland Symphyodontaceae MFleischTheliaceae MFleisch Thuidiaceae Schimp TrachylomataceaeWRBuck amp Vitt
Acknowledgements
Sincere thanks are due to JLReveal (Ithaca) as well as WFPrudhomme van Reine and JFVeldkamp(Leiden) for comments and discussions about suprafamilial taxonomy to DQuandt (Dresden) for providingDNA from Rhacocarpus and Bartramiaceae species and to BGiesicke (Berlin) for technical assistance
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18
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TABERLET P L GIELLY G PAUTOU amp J BOUVET (1991) Universal primers for amplificationof three non-coding regions of chloroplast DNA - Plant Mol Biol 17 1105-1109
TSUBOTA H Y AGENO B ESTEacuteBANEZ T YAMAGUCHI amp H DEGUCHI (2003)Molecular phylogeny of the Grimmiales (Musci) based on chloroplast rbcL sequences - Hikobia 1455-70
TSUBOTA H E DE LUNA D GONZAacuteLEZ MS IGNATOV amp H DEGUCHI (2004) Molecularphylogenetics and ordinal relationships based on analyses of a large-scale data set of 600 rbcLsequences of mosses - Hikobia 14 149-170
VITT DH (1984) Classification of the Bryopsida - In SCHUSTER RM (ed) New Manual ofBryology 2 696-759 Hattori Botanical Laboratory Nichinan Japan
VITT DH B GOFFINET amp T HEDDERSON (1998) 8 The ordinal classification of the mossesquestions and answers for the 1990s - In BATES JW NW ASHTON amp JG DUCKETT (eds)Bryology for the twenty-first century British Bryol Soc pp 113-123
Received 3 September 2007 accepted in revised form 30 October 2007
5
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Tab
le 1
con
tinu
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6
primers CM
DM
(slightly modified after Taberlet et al 1991 see Frey et al 1999) and atpB-1rbcL-1(Chiang et al 1998) respectively For amplification of the psbA-trnH spacer primers psbAF(5-GTT ATG CAT GAA CGT AAT GCT C-3 Sang et al 1997) and trnHR-2 (5-CGC GCA TGGTGG ATT CAC AAT CC-3 slightly modified after Sang et al 1997) were used with a PCRprotocol of 5 min 94degC 35 cycles (30 sec 94degC 1 min 48degC 1 min 40 sec 72degC) 7 min 72degC PCRproducts were purified using DNA purification kits (Qiagen Macherey-Nagel) Sequencing wasperformed as described in Stech (2004) using the amplification primers
ALIGNMENT AND PHYLOGENETIC ANALYSES DNA sequences were manually aligned in PhyDE v0992(Muumlller et al 2005) Following Quandt et al (2003) and Quandt amp Stech (2005) inversions inputative hairpin secondary structures were positionally separated in the alignment their presence orabsence was not coded for the phylogenetic analyses Phylogenetic reconstructions under the maximumparsimony criterion were performed using winPAUP 40b10 (Swofford 2002) in combination withPRAP (Muumlller 2004) as implemented in SeqState (Muumlller 2005) PRAP generates command filesfor PAUP that allow parsimony ratchet searches as designed by Nixon (1999) Heuristic searchesunder parsimony were performed with the following options all characters equally weighted andunordered TBR branch swapping collapse branches if maximum branch length is zero MulTreesoption in effect gaps treated as missing data Initially a heuristic search with 1000 addition sequencereplicates was performed For the parsimony ratchet ten random addition cycles of 200 ratchetiterations each were used with TBR branch swapping on a randomly re-weighted data set (25 ofthe positions) Heuristic bootstrap searches were performed with 1000 replicates with 10 additionsequence replicates per bootstrap replicate
Results
In the present data set of non-coding plastid markers sequence lengths ranged from243 to 368 nucleotides (nt) in the trnL intron and from 445 to 615 nt in the atpB-rbcL spacer The psbA-trnH spacer was considerably shorter than the other twomarkers and ranged from 103 to 186 nt The combined alignment of sequences from85 ingroup and two outgroup taxa comprised 2430 positions (trnL intron 668 atpB-rbcL spacer 1366 psbA-trnH spacer 396 positions) The most variable regions withambiguous alignment (781 positions) were excluded from phylogenetic analysis Ofthe 1649 included positions 628 (381) were variable and 455 of the variablepositions (725 or 276 of the total number of positions) were parsimony-informative The trnL intron comprised 124 the atpB-rbcL spacer 286 and the psbA-trnH spacer 45 of these included parsimony-informative positions
The shortest trees found in the heuristic maximum parsimony analysis of the combineddata set had a length of 2433 steps By applying the parsimony ratchet 129 treeswere retained that were one step shorter (length 2432 CI = 0419 RI = 0624) Thestrict consensus tree of the ratchet analysis is shown in Fig 1 The ingroup (Bryopsida)is supported with 100 bootstrap support (BS) Diphysciidae are sister to theremaining Bryopsida with 54 BS Encalyptidae Funariidae Timmiidae andDicranidae all receive gt 95 BS while Bryidae are slightly less supported (89BS) Relationships between these major lineages are resolved but unsupported Atordinal level within the Bryidae a lower resolution is observed SplachnalesOrthotrichales Aulacomniales Hypnodendrales Hookeriales and Hypnales areresolved as monophyletic with 67-100 BS whereas Hedwigiales BartramialesBryales Orthodontiales and Rhizogoniales are not A closer relationship ofOrthotrichales with the pleurocarpous mosses sl than with the more basal ordersHedwigiales Bartramiales Splachnales and Bryales is indicated
7
Discussion
Classification of mosses - recent progress and the current state
For a long time mosses were subdivided into three main lineages the subclassesSphagnidae Andreaeidae and Bryidae (eg Fleischer 1920 Vitt 1984 Frahm ampFrey 1987) the latter with a number of (super-)orders (eg Frey 1977) Howevermolecular data confirmed that mosses comprise a number of isolated basal lineagesrepresented by morphologically and ecologically distinct extant taxa such as TakakiaSphagnum Andreaea Andreaeobryum Oedipodium Tetraphis the Polytrichaceaeand Buxbaumia which probably have long independent phylogenetic histories (cfNewton et al 2007) As a result of molecular phylogenies and a re-evaluation ofmorphological-anatomical characters the classification of mosses has changedconsiderably in the last few years with the main lineages nowadays treated atsubdivision class and subclass levels within division Bryophyta (eg Doweld 2001Ochyra et al 2003 Goffinet amp Buck 2004 this study)
Takakia and Sphagnum are the earliest diverging moss taxa in molecular phylogenies(eg Newton et al 2000 Beckert et al 2001 Cox et al 2004 Qiu et al 2006Newton et al 2007) That Takakia is a moss and not a liverwort was confirmed byanalysis of DNA sequences and phylogenomic characters such as the distribution ofmitochondrial introns (eg Beckert et al 2001) Its taxonomic status however stillremains to be clarified On the one hand most molecular studies resolve Takakiaand Sphagnum as sister genera although only partly with high statistical supportThese molecular topologies do not support the recognition of division Takakiophytaas proposed by Crandall-Stotler (1986) One the other hand no morphologicalsynapomorphies unite Takakia with Sphagnum and significant molecular differencesseparating Takakia from all other mosses were also observed For example a regionin the plastid ITS3 is similar to that of other land plants but absent in mosses(Samigullin et al 2002) and a transition in the trnL
UAA gene changing the anticodon
to CAA was otherwise only found in leptosporangiate ferns and Ginkgo (Quandt etal 2004) Thus ldquoresolution of Sphagnum - Takakia clade may be an artifactrdquo (Shawamp Renzaglia 2004) Also Goffinet amp Buck (2004) did not unite Takakia and Sphagnumunder a formal taxonomic rank but placed them into different informal superclassesIn our opinion Takakia should be treated at the same level as Sphagnophytina andBryophytina (cf Doweld 2001) ie as a subdivision of Bryophyta However morefundamental nomenclatural changes are necessary as the family name Takakiaceaewas not validated in the original publication by Hattori amp Inoue (1958) (article411 of ICBN McNeill et al 2006) and consequently all higher taxa erected laterare invalid The corrected taxonomic treatment of Takakia is provided here withsporophytic characters included in the latin diagnosis of Takakiaceae (see taxonomy)
Within Bryophytina we recognise four morphologically and molecularly isolatedbasal lineages as separated from the arthrodontous mosses (Bryopsida) Andreaeopsida(with linear capsule dehiscence) the operculate but eperistomate Oedipodiopsida aswell as Polytrichopsida and Tetraphidopsida with nematodontous peristomes A fifthclass Andreaeobryopsida was erected by Buck amp Goffinet (2000) but re-includedin Andreaeopsida as a subclass by Ochyra et al (2003) The systematic status of
8
Andreaeobryum macrosporum Steere amp BMMurray and possible relationships withAndreaea and Takakia were discussed by Murray (1988) and summarised includingmolecular results by Shaw amp Renzaglia (2004)
On the next lower level a number of morphologically and molecularly divergentlineages are nowadays treated as subclasses of Bryopsida Buxbaumiidae andDiphysciidae are generally branching off first in molecular topologies (eg Beckertet al 2001 Magombo 2003 Cox et al 2004) followed by Timmiidae Encalyptidaeand Funariidae as well as Dicranidae (haplolepideous mosses) sister to Bryidae slThese subclasses (except Buxbaumiidae not included) are also well recognizable inthe present analysis of non-coding plastid sequences (Fig 1)
The morphologically very different Encalyptidae and Funariidae are revealed assister groups although mostly without high support in several molecular phylogenies(eg Goffinet et al 2001 Cox et al 2004 Hedderson et al 2004 Tsubota et al2003 2004) and also in the present study (Fig 1) Goffinet et al (2007) confirmedthis relationship by phylogenomic evidence namely a large (71 kb) inversion in thechloroplast genome of Funariaceae Disceliaceae and Encalyptaceae but not inGigaspermaceae Consequently the latter family was separated at ordinal level fromthe two remaining families of Funariales by Goffinet et al (2007) GigaspermalesFunariales and Encalyptales may share a common ancestor according to some butnot all molecular phylogenies (eg Goffinet et al 2001 2007 Hedderson et al2004 but not in Tsubota et al 2004) Although ontogenetic data from peristomedevelopment may support their common ancestry (Goffinet et al 2007) unambiguousmorphological synapomorphies are lacking We therefore propose to treatGigaspermaceae at subclass level within the Bryopsida (see taxonomy)
The haplolepideous mosses (Dicranidae) are clearly supported as a monophyleticlineage which obviously evolved from a diplolepideous ancestor according to theirposition in the molecular trees (eg Newton et al 2000 Tsubota et al 2003 Cox etal 2004 Goffinet amp Buck 2004) Molecular studies suitable for inferring ordinaland family level relationships within Dicranidae either focused on the haplolepideousmosses (eg Stech 1999ab 2004 LaFarge et al 2000 2002 Tsubota et al 2003Hedderson et al 2004) or included more than 15 haplolepideous taxa in analyses ofa broader range of mosses (eg Goffinet et al 2001 Tsubota et al 2004 this study)Major lineages supported by these analyses are for example Grimmiales(Grimmiaceae Ptychomitriaceae and Seligeriaceae) Leucobryaceae (incl formerDicranaceae-Campylopoideae and Paraleucobryoideae pp) Dicranaceae sstr(Dicranoideae plus former Dicnemonaceae and Paraleucobryoideae pp) Pottiaceae(incl Cinclidotaceae and Splachnobryum) and Calymperaceae (probably exclOctoblepharum) Furthermore several genera and families belong to Dicranidaewhose systematic positions have been controversial (eg Stech et al 1999b LaFarge et al 2002 Hedderson et al 2004 OBrien 2007 Quandt et al 2007 thisstudy) Amphidium Archidium Catoscopium Drummondia EphemeraceaeErpodiaceae Mittenia (cf OBrien 2007 sequences in some earlier analyses werebased on misdentified specimens) Rhachitheciaceae Schistostega Splachnobryumand Wardia On the contrary several problems remain such as the circumscriptionof Ditrichaceae and relationships of the major haplolepideous lineages in general
9
Fig 1 Strict consensus tree of 129 most parsimonious trees inferred from combined trnLUAA
intronatpB-rbcL spacer and psbA-trnH spacer sequences of 85 taxa of Bryopsida as well as Andreaearupestris (Andreaeopsida) and Pogonatum subulatum (Polytrichopsida) as outgroup representativesBootstrap support values gt50 are depicted above the branches
10
Consequently resolving the phylogeny of Dicranidae with confidence is one of themajor future challenges in moss systematics
As mentioned above Dicranaceae are monophyletic in a narrow circumscriptionaccording to molecular data In contrast to former Campylopoideae andParaleucobryoideae the status of Rhabdoweisioideae (= Oncophoroideae Ochyra2002) and Dicranelloideae needs further consideration Stech (1999ab) suggestedto recognise RhabdoweisioideaeRhabdoweisiaceae in a broad sense includingDicranoweisia Amphidium and Aongstroemia Subsequent molecular analysesconfirmed a close relationship of the genera Arctoa Cynodontium DicranoweisiaKiaeria Oncophorus Oreoweisia Oreas Rhabdoweisia and Symblepharis althoughwithout significant support (La Farge et al 2002 Tsubota et al 2003 Hedderson etal 2004) With respect to the molecular evidence available so far we propose toelevate Oncophoroideae to family level to accomodate these genera and perhapsGlyphomitrium (cf Tsubota et al 2003) whereas we consider AongstroemiaDichodontium and Diobelonella to belong to Aongstroemiaceae (cf Stech 1999a)Amphidium is neither closely related to Dicranaceae sstr nor to Oncophoroideae(La Farge et al 2002 Tsubota et al 2003 Hedderson et al 2004 Stech 2004 thisstudy) and should be treated at family level rather than placed in Dicranaceae assubfam Amphidioideae (Ochyra et al 2003) The circumscription of Dicranelloideaeis more difficult to evaluate as few representatives have been included in molecularanalyses However Dicranella heteromalla (Hedw) Schimp as well as the generaCampylopodium and Microcampylopus are clearly separated from Dicranaceae sstr(Stech 1999a 2004 La Farge et al 2002 Tsubota et al 2003 Hedderson et al2004) and consequently the subfamily deserves family status as well Finallymolecular data showed that the genus Hypodontium does not belong to Pottiaceae(Hedderson et al 2004 Tsubota et al 2004) Taxonomic conclusions have not beendrawn from these results which is made up here (see taxonomy)
All mosses with diplolepideous-alternate peristomes together with Splachnales witha diplolepideous-opposite (Funaria-type) peristome form a monophyletic group inmolecular analyses (eg Newton et al 2000 Beckert et al 2001 Goffinet et al2001 Cox et al 2004 Tsubota et al 2004 references in Table 2) Differentclassifications of this by far most species-rich group of mosses were proposed (egVitt et al 1998 Ochyra et al 2003 Goffinet amp Buck 2004) However at least someof the recognised subclasses and superorders are paraphyletic according to themolecular topologies and assigning formal ranks to all evolutionarily significantmonophyletic entities is problematic if the main taxonomic framework of Bryophytaand Bryopsida should be maintained (cf discussion in Bell et al 2007) Thereforein the present synopsis only one subclass Bryidae is recognised for all diplolepideous-alternate mosses and Splachnales This broadly defined Bryidae is subdivided into13 orders most of them resolved as monophyletic in the majority of the phylogeneticanalyses summarised in Table 2 although with different levels of statistical supportin maximum parsimony analyses To define monophyletic lineages at supraordinallevel informal node-based names may be chosen according to Bell et al (2007) Forexample the pleurocarpous mosses (pleurocarpy sensu Bell amp Newton 2007) andtheir closest acrocarpous relatives (Orthodontiales to Hypnales) were already
11
Table 2 Taxon sampling and bootstrap support (BS) for Dicranidae Bryidae and orders within theBryidae in recent phylogenetic analyses (MP only) based on combined molecular markers Markersare given in square brackets (non-coding regions in bold) numbers of included taxa in brackets ++respective clade present with ge 80 BS + clade present with lt 80 BS - clade not present no oronly one representative included
Bell amp Newton OBrien Quandt et al Bell et al this study(2004) (2007) (2007) (2007)
[rbcL rps4 [atpB atpB- [rbcL rps4 [rbcL rps4 [atpB-rbcLnad5] rbcL rbcL trnL-F nad5] trnL-F nad5] psbA-trnH
rps4 trnL-F] trnL]
Dicranidae + (2) + (4) ++ (3) (1) ++ (19)Bryidae ++ (57) + (53) ++ (52) ++ (98) ++ (58)Hedwigiales ++ (2) (1) ++ (2) ++ (2) - (3)Bartramiales ++ (2) ++ (4) ++ (4) ++ (3) - (4)Splachnales (0) ++ (2) ++ (3) ++ (2) ++ (5)Bryales - (4) - (5) ++ (18) + (17) - (8)Orthotrichales (1) ++ (3) ++ (3) ++ (2) ++ (4)Orthodontiales + (4) + (4) + (3) + (6) - (3)Aulacomniales + (6) + (7) ++ (2) + (7) + (3)Rhizogoniales ++ (13) + (8) ++ (5) ++ (14) - (3)Hypnodendrales ++ (13) + (7) ++ (4) ++ (29) ++ (6)Ptychomniales ++ (3) ++ (3) (1) ++ (4) (1)Hookeriales - (4) + (2) (1) + (2) + (8)Hypnales - (5) - (7) ++ (5) ++ (10) + (10)
summarised under the informal node based name pleurcarpids (Bell et al 2007)and can be distinguished from a basal grade of acrocarpous or cladocarpous lineages(Hedwigiales to Orthotrichales) Within the latter monophyly of BartramialesSplachnales and Orthotrichales is well-supported in all analyses including two ormore taxa except Bartramiales in the present data set (cf Fig 1) In contrast Bryalesreceive significant support less frequently (but see Bell et al 2007 Quandt et al2007) Hedwigiales are well supported if only Hedwigia (Hedwigiaceae) andRhacocarpus (Rhacocarpaceae) are included whereas the monospecific Helicophyllum(Helicophyllaceae) is not closely related to these taxa but shows affinities withBartramiales (Goffinet et al 2001 this study) With respect to the differentmorphologies of Helicophyllaceae and Bartramiaceae however the former shouldbe separated at ordinal level (see taxonomy)
Clarifying relationships of the Orthotrichales is still a difficult issue Analyses ofsingle chloroplast markers or parsimony analyses of combined markers from differentgenomes mostly indicated a close relationship either with Splachnales (eg Cox etal 2000 Newton et al 2000 Tsubota et al 2004 Quandt et al 2007) or with thepleurocarpids (Goffinet et al 2001 this study) Although none of these alternativesis well-supported the latter seems more likely with regard to the moderately tomaximally supported Orthotrichales - pleurocarpid sister group relationship in allanalyses of mitochondrial data and in likelihood analyses of combined plastidmitochondrial markers (Beckert et al 2001 Quandt et al 2007)
12
The molecular polyphyly of Rhizogoniaceae (eg Bell amp Newton 2004) was solvedby the transfer of rhizogonioid genera into broadly defined Aulacomniaceae andOrthodontiaceae (Bell et al 2007) which now include both acrocarpous andpleurocarpous taxa These systematic changes are also comprehensible by non-molecular characters such as morphological traits shared by Mesochaete andAulacomnium heterostichum (Hedw) Bruch amp Schimp or the variously reducedperistomes of Orthodontiaceae pp in contrast to the generally fully developed Bryum-type peristomes of rhizogonioid and hypnodendroid mosses (Bell et al 2007) Theposition of the solely pleurocarpous Hypnodendrales sister to the former Hypnidaeled to the recognition of the informal group core pleurocarps (Bell et al 2007)The former Hypnidae (Ptychomniales Hookeriales and Hypnales summarised ashomocostate pleurocarps) are monophyletic in most molecular analyses (eg Goffinetet al 2001 Tsubota et al 2004 Bell et al 2007) with Ptychomniales being well-supported (Pedersen amp Newton 2007 Table 2) Clarifying relationships betweenHookeriales and Hypnales and within the latter is still a challenge but recent molecularstudies seem to support a sister group relationship of both orders (Bell et al 2007present study)
Phylogenetic utility of non-coding plastid markers
Non-coding plastid markers that comprise both variable and conserved regionssuch as the trnL
UAA intron have repeatedly been shown to possess potential for
resolving relationships at high taxonomic levels (eg Borsch et al 2003 Quandtet al 2004) Both the trnL intron and atpB-rbcL spacer were characterised indetail in mosses with respect to their structure and molecular evolution (Quandt ampStech 2005 Stech amp Quandt 2006) They include conservative regions that can beunambiguosly aligned and even parts of the more variable regions can be used ifrepeats hairpin loops etc are correctly identified and adequately treated in thephylogenetic analyses (eg Quandt et al 2003 Quandt amp Stech 2005) Using theatpB-rbcL spacer alone (Stech amp Quandt 2006) relationships of the major mosslineages were largely consistent with the ldquototal evidencerdquo molecular tree of Goffinetamp Buck (2004) However in addition to general limitations that result from singlemarker analyses the use of non-coding markers may pose further problems suchas a high amount of homoplasy resulting in low resolution or low statistical supportfor many clades Therefore several recent molecular studies of relationships withinBryidae have employed both coding and non-coding markers (Table 2)Nevertheless the usefulness of analyses of combined non-coding plastid markerscannot be ruled out In fact Fig 1 and Table 2 indicate a phylogenetic signal inthe present data set as many clades are recovered that are usually also resolvedin analyses of coding or combined coding and non-coding markers Especiallywith regard to statistical support however the present analysis is inferior tothose of other recent data sets especially Bell et al (2007) and Quandt et al(2007) In addition the non-coding markers used here are of different suitabilityand even the two intergenic spacers differ considerably from each other ThepsbA-trnH spacer contributes much less to the trees resolution than the atpB-rbcL spacer first because it is much shorter and second because relatively largeparts are attributed to hairpin loops or otherwise hypervariable regions These
13
results indicate that future studies should evaluate the molecular evolution andphylogenetic potential of new markers both coding and con-coding and choosethe most suitable ones in a combined analysis to resolve the remaining uncertaintiesin moss phylogeny
Taxonomy
Takakiaceae Stech amp WFrey stat nov
Plantae virides nusquam rhizophorae sine protonemate e caudicis rhizomatis erectae Caudicesrhizomati et axes geotropi radiformes frequenter intercalariter ramificantes sine phyllidiis cumpapillis mucilaginis rostratis Caules phyllidiiferi saepe furcati Phyllidia sine lamina et costadistincta profunde 2-4(-5)-lobata pluristratosa tristicha sed torsione spiraliter disposita Filumcentralium in ambabus generationibus (axibus gametophyti et setis) adest Plantae dioicae Antheridiaet archegonia nuda Sporophytum terminale solitarium Seta persistens Capsula tortilis admaturitatem schizocarpa secus unam rimam spiralem longitudinalem dehiscens Stomata etoperculum absunt peristomium nullum Calyptra mitriformis
TYPUS Takakia SHatt amp Inoue J Hattori Bot Lab 19 137 1958
Takakiaceae SHatt amp Inoue J Hattori Bot Lab 19 137 1958 nom inval (Art 411)
Takakiales Stech amp WFrey stat nov
Based on Takakiaceae Stech amp WFrey Nova Hedwigia 86 13 2008
TYPUS Takakia SHatt amp Inoue J Hattori Bot Lab 19 137 1958
Takakiales SHatt amp Inoue J Hattori Bot Lab 19 137 1958 nom inval
Takakiales SHatt amp Inoue ex RMSchust J Hattori Bot Lab 26 224 1963 nom inval (cumdescr latin)
Takakiopsida Stech amp WFrey statnov
Based on Takakiaceae Stech amp WFrey Nova Hedwigia 86 13 2008
TYPUS Takakia SHatt amp Inoue J Hattori Bot Lab 19 137 1958
Takakiopsida Goffinet amp WRBuck Monogr Syst Bot Missouri Bot Gard 98 232 2004 nominval
Takakiopsida Jia et al Acta Phytotax Sin 41 350 351 2003 nom nud
Takakiopsida Wang amp Wu Fl Bryophyt Sin 8 447 2004 nom inval (cum descr latin)
Takakiophytina Stech amp WFrey stat nov
Based on Takakiaceae Stech amp WFrey Nova Hedwigia 86 13 2008
TYPUS Takakia SHatt amp Inoue JHattori Bot Lab 19 137 1958
Gigaspermidae Stech amp WFrey subclass nov
Plantae acrocarpae terrestres stoloniferae ramis brevibus erectis Folia unicostata cellulis laxislaevibus Capsula plerumque valde rugosa gymnostomatica vel cleistocarpa stomata cum duabuscellulis sociis Ab Funariidis et Encalyptidis charactere phylogenomico (71-kb inversio abest)separatae
14
TYPUS Gigaspermum Lindb Oumlfversigt af Foumlrhandlingar Kongl Svenska Vetenskaps-Akademien21 599 1865
Amphidiaceae Stech stat nov
Based on Dicranaceae subfam Amphidioideae Ochyra in Ochyra Zarnowiec amp Bednarek-OchyraCens Cat Polish Mosses 110 2003
TYPUS Amphidium Schimp Coroll Bryol Eur 39 1856
Amphidiaceae AJESm Moss Fl Britain Ireland 2nd ed 657 2004 nom inval descr angl
Dicranellaceae Stech stat nov
Based on Dicranaceae subfam Dicranelloideae Lindb Utkast Eur Bladmoss 33 1878[lsquoUnderfamilje Dicranelleaersquo]
TYPUS Dicranella (MuumlllHal) Schimp Coroll Bryol Eur 13 1856
Oncophoraceae Stech stat nov
Based on Dicranaceae subfam Oncophoroideae Lindb Utkast Eur Bladmoss 34 1878[lsquoUnderfamilje Oncophoreaersquo]
TYPUS Oncophorus (Brid) Brid Bryol Univ 1 389 1826
Hypodontiaceae Stech fam nov
Plantae robustae characteribus morphologicis Pottiaceis et Calymperaceis similes sedcharacteribus molecularicis separatae Bracteae perichaetiales internae e basi vaginantes subulataevel aristatae Capsula aspectu succulenta cellulae exothecii incrassatae annulus magnopereabsens Peristomii dentes breves triangulati incurvati aurantiaci leves vel infirme verrucosiCalyptra cucullata
TYPUS Hypodontium MuumlllHal Hedwigia 38 96 1899
Helicophyllales Stech amp WFrey ord nov
Plantae acrocarpae prostratae tomentosae Folia dimorpha in duas series laterales et unam seriemventralem divisa Costa percurrens Cellulae hexagonae ad subquadratae papillosae Capsula immersacupulata ad oblonga infra orificium abrupte incurvata stomata destituta Peristomium nullum Sporaeisomorphae heteropolares granulatae
TYPUS Helicophyllum Brid Bryol Univ 2 771 1827
Synopsis of the suprageneric classification of BryophytaAuthor citations are in accordance with Art 492 of the Vienna Code (McNeill et al 2006)
Subdivision Takakiophytina Stech amp WFreyClass Takakiopsida Stech amp WFrey
Order Takakiales Stech amp WFreyTakakiaceae Stech amp WFrey
Subdivision Sphagnophytina DoweldClass Sphagnopsida Schimp
Order Sphagnales Limpr
15
Sphagnaceae DumortOrder Ambuchananiales Seppelt amp HACrum
Ambuchananiaceae Seppelt amp HACrumSubdivision Bryophytina Engler
Class Andreaeopsida JHSchaffnSubclass Andreaeidae Engl
Order Andreaeales LimprAndreaeaceae Dumort
Subclass Andreaeobryidae OchyraOrder Andreaeobryales BMMurray
Andreaeobryaceae Steere amp BMMurrayClass Oedipodiopsida Goffinet amp WRBuck
Order Oedipodiales Goffinet amp WRBuckOedipodiaceae Schimp
Class Tetraphidopsida Goffinet amp WRBuckOrder Tetraphidales MFleisch
Tetraphidaceae SchimpClass Polytrichopsida Doweld
Order Polytrichales MFleischPolytrichaceae Schwaumlgr
Class Bryopsida PaxSubclass Buxbaumiidae Doweld
Order Buxbaumiales MFleischBuxbaumiaceae Schimp
Subclass Diphysciidae OchyraOrder Diphysciales MFleisch
Diphysciaceae MFleischSubclass Timmiidae Ochyra
Order Timmiales OchyraTimmiaceae Schimp
Subclass Encalyptidae Ochyra Żarnowiec amp Bednarek-OchyraOrder Encalyptales Dixon
Encalyptaceae SchimpSubclass Funariidae Ochyra
Order Funariales MFleischFunariaceae Schwaumlgr Disceliaceae Schimp
Subclass Gigaspermidae Stech amp WFreyOrder Gigaspermales Goffinet Wickett OWerner Ros AJShaw amp CJCox
Gigaspermaceae LindbSubclass Dicranidae Doweld
Order Catoscopiales Ignatov amp IgnatovaCatoscopiaceae Broth
Order Scouleriales Goffinet amp WRBuckDrummondiaceae Goffinet Scouleriaceae SPChurchill
Order Bryoxiphiales HACrum amp LEAndersonBryoxiphiaceae Besch
16
Order Grimmiales MFleischGrimmiaceae Arn Ptychomitriaceae Schimp Seligeriaceae Schimp
Order Archidiales LimprArchidiaceae Schimp
Order Mitteniales ShawMitteniaceae Broth
Order Dicranales HPhilib ex MFleischAmphidiaceae Stech Aongstroemiaceae De Not BruchiaceaeSchimp Calymperaceae Kindb Dicranaceae Schimp Dicranel-laceae Stech Ditrichaceae Limpr Erpodiaceae Broth EustichiaceaeBroth Fissidentaceae Schimp Leucobryaceae Schimp Onco-phoraceae Stech Rhachitheciaceae HRob Schistostegaceae SchimpViridivelleraceae IGStone Wardiaceae Welch
Order Pottiales MFleischEphemeraceae Schimp Hypodontiaceae Stech PleurophascaceaeBroth Pottiaceae Schimp Serpotortellaceae WDReese amp RHZander
Subclass Bryidae EnglOrder Hedwigiales Ochyra
Hedwigiaceae Schimp Rhacocarpaceae KindbOrder Helicophyllales Stech amp WFrey
Helicophyllaceae BrothOrder Bartramiales DQuandt NEBell amp Stech
Bartramiaceae SchwaumlgrOrder Splachnales Ochyra
Meesiaceae Schimp Splachnaceae Grev amp ArnOrder Bryales Limpr
Bryaceae Schwaumlgr Leptostomataceae Schwaumlgr Mniaceae SchwaumlgrPhyllodrepaniaceae Crosby Pseudoditrichaceae Steere amp ZIwatsPulchrinodaceae DQuandt NEBell amp Stech
Order Orthotrichales DixonOrthotrichaceae Arn
Order Orthodontiales NEBell AENewton amp DQuandtOrthodontiaceae Goffinet
Order Aulacomniales NEBell AENewton amp DQuandtAulacomniaceae Schimp
Order Rhizogoniales Goffinet amp WRBuckRhizogoniaceae Broth
Order Hypnodendrales NEBell AENewton amp DQuandtBraithwaiteaceae NEBell AENewton amp DQuandt Hypnodendra-ceae Broth Pterobryellaceae WRBuck amp Vitt Racopilaceae Kindb
Order Ptychomniales WRBuck CJCox AJShaw amp GoffinetPtychomniaceae MFleisch
Order Hookeriales MFleischDaltoniaceae Schimp Hookeriaceae Schimp HypopterygiaceaeMitt Leucomiaceae Broth Pilotrichaceae Kindb SaulomataceaeWRBuck CJCox AJShaw amp Goffinet Schimperobryaceae WR
17
Buck CJCox AJShaw amp GoffinetOrder Hypnales WRBuck amp Vitt
Amblystegiaceae GRoth Anomodontaceae Kindb BrachytheciaceaeSchimp Calliergonaceae Vanderpoorten Hedenaumls CJCox amp AJShaw Catagoniaceae WRBuck amp Ireland Climaciaceae KindbCryphaeaceae Schimp Echinodiaceae Broth Entodontaceae KindbFabroniaceae Schimp Fontinalaceae Schimp Helodiaceae OchyraHeterocladiaceae Ignatov amp Ignatova Hylocomiaceae MFleischHypnaceae Schimp Lembophyllaceae Broth LeptodontaceaeSchimp Lepyrodontaceae Broth Leskeaceae Schimp Leucodon-taceae Schimp Meteoriaceae Kindb Microtheciellaceae HAMillamp AJHarr Myriniaceae Schimp Myuriaceae MFleisch NeckeraceaeSchimp Orthorrhynchiaceae SHLin Phyllogoniaceae KindbPlagiotheciaceae MFleisch Pleuroziopsidaceae Ireland Prionodon-taceae Broth Pseudoleskeaceae Schimp PseudoleskeellaceaeIgnatov amp Ignatova Pterigynandraceae Schimp PterobryaceaeKindb Pylaisiaceae Schimp Pylaisiadelphaceae Goffinet amp WRBuck Regmatodontaceae Broth Rhytidiaceae Broth RigodiaceaeHACrum Rutenbergiaceae MFleisch Scorpidiaceae Ignatov ampIgnatova Sematophyllaceae Broth Sorapillaceae MFleisch Ste-reophyllaceae WRBuck amp Ireland Symphyodontaceae MFleischTheliaceae MFleisch Thuidiaceae Schimp TrachylomataceaeWRBuck amp Vitt
Acknowledgements
Sincere thanks are due to JLReveal (Ithaca) as well as WFPrudhomme van Reine and JFVeldkamp(Leiden) for comments and discussions about suprafamilial taxonomy to DQuandt (Dresden) for providingDNA from Rhacocarpus and Bartramiaceae species and to BGiesicke (Berlin) for technical assistance
References
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BELL NE amp AE NEWTON (2004) Systematic studies of non-hypnanaean pleurocarps establishinga phylogenetic framework for investigating the origins of pleurocarpy - In GOFFINET BV HOLLOWELL amp R MAGILL (eds) Molecular systematics of bryophytes Monogr Syst BotMissouri Bot Gard 98 290-319
BELL NE amp AE NEWTON (2007) Pleurocarpy in the Rhizogoniaceous grade - In NEWTONAE amp RS TANGNEY (eds) Pleurocarpous mosses systematics and evolution SystematicsAssociation Special Volume Series 71 41-64
BELL NE D QUANDT TJ OBRIEN amp AE NEWTON (2007) Taxonomy and phylogeny inthe earliest diverging pleurocarps square holes and bifurcating pegs - Bryologist 110 533-560
BORSCH T KW HILU D QUANDT V WILDE C NEINHUIS amp W BARTHLOTT(2003) Non-coding plastid trnT-trnF sequences reveal a well resolved phylogeny of basal angiosperms- J Evol Biol 16 558-576
18
BUCK WR (2007) The history of pleurocarp classification two steps forward one step back - InNEWTON AE amp RS TANGNEY (eds) Pleurocarpous mosses systematics and evolutionSystematics Association Special Volume Series 71 1-18
BUCK WR amp B GOFFINET (2000) Morphology and classification of mosses - In SHAWAJ amp B GOFFINET (eds) Bryophyte Biology pp 71-123 Cambridge University PressCambridge
CHIANG TY BA SCHAAL amp CI PENG (1998) Universal primers for amplification andsequencing a noncoding spacer between atpB and rbcL genes of chloroplast DNA - Bot Bull AcadSin 39 245-250
COX CJ B GOFFINET AE NEWTON AJ SHAW amp TAJ HEDDERSON (2000)Phylogenetic relationships among the diplolepideous-alternate mosses (Bryidae) inferred from nuclearand chloroplast DNA sequences - Bryologist 103 224-241
COX CJ B GOFFINET AJ SHAW amp SB BOLES (2004) Phylogenetic relationships amongthe mosses based on heterogeneous Bayesian analysis of multiple genes from multiple genomiccompartments - Syst Bot 29 234-250
CRANDALL-STOTLER B (1986) Morphogenesis developmental anatomy and bryophytephylogenetics contra-indications of monophyly - J Bryol 14 1-23
CROSBY MR RE MAGILL B ALLEN amp S HE (1999) A checklist of the mosses - MissouriBotanical Garden St Louis Missouri
DOWELD A (2001) Prosyllabus Tracheophytorum - GEOS Moscow i-lxxx + 110 pp
DOYLE JJ amp JL DOYLE (1990) Isolation of plant DNA from fresh tissue - Focus 12 13-15
DUFF RJ JC VILLAREAL DC CARGILL amp KS RENZAGLIA (2007) Progress andchallenges towards developing a phylogeny and classification of the hornworts - Bryologist 110214-243
FLEISCHER M (1920) Natuumlrliches System der Laubmoose - Hedwigia 61 390-400
FORREST LL EC DAVIS DG LONG BJ CRANDALL-STOTLER A CLARK ampML HOLLINGSWORTH (2006) Unraveling the evolutionary history of the liverworts (Marchantio-phyta) multiple taxa genomes and analyses - Bryologist 109 303-334
FRAHM J-P amp W FREY (1987) Moosflora 2 Aufl - UTB 1250 Stuttgart
FREY W (1977) Neue Vorstellungen uumlber die Verwandtschaftsgruppen und die Stammesgeschichteder Laubmoose - In FREY W H HURKA amp F OBERWINKLER (Hrsg) Beitraumlge zur Biologieder Pflanzen pp 117-139 Stuttgart
FREY W amp M STECH (2005) A morpho-molecular classification of the liverworts (Hepa-ticophytina Bryophyta) - Nova Hedwigia 81 55-78
FREY W M STECH amp K MEIszligNER (1999) Chloroplast DNA-relationship in palaeoaustralLopidium concinnum (Hypopterygiaceae Musci) An example of steno-evolution in mosses Studiesin austral temperate rain forest bryophytes 2 - Plant Syst Evol 218 67-75
GOFFINET B amp WR BUCK (2004) Systematics of Bryophyta (mosses) from molecules to arevised classification - In GOFFINET B V HOLLOWELL amp R MAGILL (eds) Molecularsystematics of bryophytes Monogr Syst Bot Missouri Bot Gard 98 205-239
GOFFINET B CJ COX AJ SHAW amp TAJ HEDDERSON (2001) The Bryophyta (mosses)Systematic and evolutionary inferences from an rps4 gene (cpDNA) phylogeny - Ann Bot 87191-208
GOFFINET B NJ WICKETT O WERNER RM ROS AJ SHAW amp CJ COX (2007)Distribution and phylogenetic significance of the 71-kb inversion in the plastid genome in Funariidae(Bryophyta) - Ann Bot 99 747-753
19
GROTH-MALONEK M D PRUCHNER F GREWE amp V KNOOP (2005) Ancestors oftrans-splicing mitochondrial introns support serial sister group relationships of hornworts and mosseswith vascular plants - Mol Biol Evol 22 117-125
HATTORI S amp H INOUE (1958) Preliminary report on Takakia lepidozioides - J Hattori BotLab 19 133-137
HE-NYGREacuteN X A JUSLEacuteN I AHONEN D GLENNY amp S PIIPPO (2006) Illuminating theevolutionary history of liverworts (Marchantiophyta) - towards a natural classification - Cladistics22 1-31
HEDDERSON TAJ DJ MURRAY CJ COX amp TL NOWELL (2004) Phylogeneticrelationships of haplolepideous mosses (Dicranidae) inferred from rps4 gene sequences - Syst Bot29 29-41
LA FARGE C BD MISHER JA WHEELER DP WALL K JOHANNES S SCHAFFERamp AJ SHAW (2000) Phylogenetic relationships within the haplolepideous mosses - Bryologist103 257-276
LA FARGE C AJ SHAW amp DH VITT (2002) The circumscription of the Dicranaceae(Bryopsida) based on the chloroplast regions trnL-trnF and rps4 - Syst Bot 27 435-452
MAGOMBO ZLK (2003) The phylogeny of basal peristomate mosses evidence from cpDNAand implications for peristome evolution - Syst Bot 28 24-38
MCNEILL J FR BARRIE HM BURDET V DEMOULIN DL HAWKSWORTHK MARHOLD DH NICOLSON J PRADO PC SILVA JE SKOG JH WIERSEMA ampNJ TURLAND (2006) International Code of Botanical Nomenclature (Vienna Code) - RegnumVegetabile 146 1-568
MUumlLLER K (2004) PRAP - computation of Bremer support for large data sets - Mol PhylogenetEvol 31 780-782
MUumlLLER K (2005) SeqState - primer design and sequence statistics for phylogenetic DNA datasets - Appl Bioinformatics 4 65-69
MUumlLLER K D QUANDT J MUumlLLER amp C NEINHUIS (2005) PhyDE v0992 PhylogeneticData Editor - httpwwwphydede
MURRAY BM (1988) Systematics of the Andreaeopsida (Bryophyta) two orders with links toTakakia - Nova Hedwigia Beih 90 289-336
NEWTON AE amp RS TANGNEY (eds) (2007) Pleurocarpous mosses systematics and evolutionSystematics Association Special Volume Series 71 CRC Press Boca Raton 434 pp
NEWTON AE CJ COX JG DUCKETT JA WHEELER B GOFFINET TAJ HEDDER-SON amp BD MISHLER (2000) Evolution of the major moss lineages Phylogenetic analyses basedon multiple gene sequences and morphology - Bryologist 103 187-211
NEWTON AE N WIKSTROumlM NE BELL LL FORREST amp MS IGNATOV (2007)Dating the diversification of the pleurocarpous mosses - In NEWTON AE amp RS TANGNEY(eds) Pleurocarpous mosses systematics and evolution Systematics Association Special VolumeSeries 71 337-366
NIXON KC (1999) The parsimony ratchet a new method for rapid parsimony analysis - Cladistics15 407-411
OBRIEN TJ (2007) The phylogenetic distribution of pleurocarpous mosses evidence fromcpDNA sequences - In NEWTON AE amp RS TANGNEY (eds) Pleurocarpous mossessystematics and evolution Systematics Association Special Volume Series 71 19-41
OCHYRA R (2002) Nomenclatural changes in subfamilies of the Dicranaceae - CryptogamieBryol 23 345-349
20
OCHYRA R J ŻARNOWIEC amp H BEDNAREK-OCHYRA (2003) Census catalogue ofPolish mosses - Biodiv Poland 3 1-372
PEDERSEN N amp AE NEWTON (2007) Phylogenetic and morphological studies within thePtychomniales with emphasis on the evolution of dwarf males - In NEWTON AE amp RSTANGNEY (eds) Pleurocarpous mosses systematics and evolution Systematics AssociationSpecial Volume Series 71 367-392
QUANDT D amp M STECH (2005) Molecular evolution and secondary structure of the chloroplasttrnL intron in bryophytes - Mol Phylogenet Evol 36 429-443
QUANDT D K MUumlLLER amp S HUTTUNEN (2003) Characterisation of the chloroplast DNApsbT-H region and the influence of dyad symmetrical elements on phylogenetic reconstructions -Plant Biol 5 400-410
QUANDT D K MUumlLLER M STECH W FREY KW HILU amp T BORSCH (2004) Molecularevolution of the chloroplast trnL-F-region in land plants - In GOFFINET B V HOLLOWELL ampR MAGILL (eds) Molecular systematics of bryophytes Monogr Syst Bot Missouri Bot Gard98 13-37
QUANDT D NE BELL amp M STECH (2007) Unravelling the knot the Pulchrinodaceae famnov (Bryales) - In KUumlRSCHNER H T PFEIFFER amp M STECH (eds) A Festschrift to Wolf-gang Frey - a scientists life between deserts and rain forests Nova Hedwigia Beih 131 21-39
QIU Y-L Y CHO JC COX amp JD PALMER (1998) The gain of three mitochondrial intronsidentifies liverworts as the earliest land plants - Nature 394 671-674
QIU Y-L L LI B WANG Z CHEN V KNOOP M GROTH-MALONEK O DOM-BROVSKA J LEE L KENT J REST GF ESTABROOK TA HENDRY DW TAYLORCM TESTA M AMBROS B CRANDALL-STOTLER J DUFF M STECH W FREYD QUANDT amp CC DAVIS (2006) The deepest divergences in land plants inferred fromphylogenomic evidence - Proc Natl Acad Sci USA 103 15511-15516
RENZAGLIA KS S SCHUETTE RJ DUFF R LIGRONE AJ SHAW BD MISHLER ampJG DUCKETT (2007) Bryophyte phylogeny Advancing the molecular and morphological frontiers- Bryologist 110 179-213
SAMIGULLIN TH SP YACENTYUK GV DEGTYARYEVA KM VALIEJO-ROMANVK BOBROVA I CAPESIUS WF MARTIN AV TROITSKY VR FILIN amp ASANTONOV (2002) Paraphyly of bryophytes and close relationships of hornworts and vascularplants inferred from analysis of chloroplast rDNA ITS (cpITS) sequences - Arctoa 11 31-43
SANG T DJ CRAWFORD amp TF STUESSY (1997) Chloroplast DNA phylogeny reticulateevolution and biogeography of Paeonia (Paeoniaceae) - Amer J Bot 84 1120-1136
SHAW AJ amp KS RENZAGLIA (2004) Phylogeny and diversification of bryophytes - AmerJ Bot 91 1557-1581
SHAW AJ CJ COX amp B GOFFINET (2005) Global patterns of moss diversity taxonomic andmolecular inferences - Taxon 54 337-352
STECH M (1999a) A reclassification of Dicranaceae (Bryopsida) based on non-coding cpDNAsequence data - J Hattori Bot Lab 86 137-159
STECH M (1999b) A molecular systematic contribution to the position of Amphidium Schimp(Rhabdoweisiaceae Bryopsida) - Nova Hedwigia 68 291-300
STECH M (2004) Supraspecific circumscription and classification of Campylopus Brid(Dicranaceae Bryopsida) based on molecular data - Syst Bot 29 817-824
STECH M amp D QUANDT (2006) Molecular evolution of the chloroplast atpB-rbcL spacer inbryophytes - In SHARMA AK amp A SHARMA (eds) Plant Genome Biodiversity and EvolutionVol 2 Part B pp 409-431 Science Publishers Enfield New Hampshire
21
STECH M D QUANDT amp W FREY (2003) Molecular circumscription of the hornworts(Antho-cerotophyta) based on the chloroplast DNA trnL-trnF region - J Plant Res 116 389-398
STOTLER RE amp B CRANDALL-STOTLER (2005) A revised classification of theAnthocerotophyta and a checklist of the hornworts of North America north of Mexico - Bryologist108 16-26
SWOFFORD DL (2002) PAUP Phylogenetic analysis using parsimony (and other methods)version 40b10 - Sunderland MA
TABERLET P L GIELLY G PAUTOU amp J BOUVET (1991) Universal primers for amplificationof three non-coding regions of chloroplast DNA - Plant Mol Biol 17 1105-1109
TSUBOTA H Y AGENO B ESTEacuteBANEZ T YAMAGUCHI amp H DEGUCHI (2003)Molecular phylogeny of the Grimmiales (Musci) based on chloroplast rbcL sequences - Hikobia 1455-70
TSUBOTA H E DE LUNA D GONZAacuteLEZ MS IGNATOV amp H DEGUCHI (2004) Molecularphylogenetics and ordinal relationships based on analyses of a large-scale data set of 600 rbcLsequences of mosses - Hikobia 14 149-170
VITT DH (1984) Classification of the Bryopsida - In SCHUSTER RM (ed) New Manual ofBryology 2 696-759 Hattori Botanical Laboratory Nichinan Japan
VITT DH B GOFFINET amp T HEDDERSON (1998) 8 The ordinal classification of the mossesquestions and answers for the 1990s - In BATES JW NW ASHTON amp JG DUCKETT (eds)Bryology for the twenty-first century British Bryol Soc pp 113-123
Received 3 September 2007 accepted in revised form 30 October 2007
6
primers CM
DM
(slightly modified after Taberlet et al 1991 see Frey et al 1999) and atpB-1rbcL-1(Chiang et al 1998) respectively For amplification of the psbA-trnH spacer primers psbAF(5-GTT ATG CAT GAA CGT AAT GCT C-3 Sang et al 1997) and trnHR-2 (5-CGC GCA TGGTGG ATT CAC AAT CC-3 slightly modified after Sang et al 1997) were used with a PCRprotocol of 5 min 94degC 35 cycles (30 sec 94degC 1 min 48degC 1 min 40 sec 72degC) 7 min 72degC PCRproducts were purified using DNA purification kits (Qiagen Macherey-Nagel) Sequencing wasperformed as described in Stech (2004) using the amplification primers
ALIGNMENT AND PHYLOGENETIC ANALYSES DNA sequences were manually aligned in PhyDE v0992(Muumlller et al 2005) Following Quandt et al (2003) and Quandt amp Stech (2005) inversions inputative hairpin secondary structures were positionally separated in the alignment their presence orabsence was not coded for the phylogenetic analyses Phylogenetic reconstructions under the maximumparsimony criterion were performed using winPAUP 40b10 (Swofford 2002) in combination withPRAP (Muumlller 2004) as implemented in SeqState (Muumlller 2005) PRAP generates command filesfor PAUP that allow parsimony ratchet searches as designed by Nixon (1999) Heuristic searchesunder parsimony were performed with the following options all characters equally weighted andunordered TBR branch swapping collapse branches if maximum branch length is zero MulTreesoption in effect gaps treated as missing data Initially a heuristic search with 1000 addition sequencereplicates was performed For the parsimony ratchet ten random addition cycles of 200 ratchetiterations each were used with TBR branch swapping on a randomly re-weighted data set (25 ofthe positions) Heuristic bootstrap searches were performed with 1000 replicates with 10 additionsequence replicates per bootstrap replicate
Results
In the present data set of non-coding plastid markers sequence lengths ranged from243 to 368 nucleotides (nt) in the trnL intron and from 445 to 615 nt in the atpB-rbcL spacer The psbA-trnH spacer was considerably shorter than the other twomarkers and ranged from 103 to 186 nt The combined alignment of sequences from85 ingroup and two outgroup taxa comprised 2430 positions (trnL intron 668 atpB-rbcL spacer 1366 psbA-trnH spacer 396 positions) The most variable regions withambiguous alignment (781 positions) were excluded from phylogenetic analysis Ofthe 1649 included positions 628 (381) were variable and 455 of the variablepositions (725 or 276 of the total number of positions) were parsimony-informative The trnL intron comprised 124 the atpB-rbcL spacer 286 and the psbA-trnH spacer 45 of these included parsimony-informative positions
The shortest trees found in the heuristic maximum parsimony analysis of the combineddata set had a length of 2433 steps By applying the parsimony ratchet 129 treeswere retained that were one step shorter (length 2432 CI = 0419 RI = 0624) Thestrict consensus tree of the ratchet analysis is shown in Fig 1 The ingroup (Bryopsida)is supported with 100 bootstrap support (BS) Diphysciidae are sister to theremaining Bryopsida with 54 BS Encalyptidae Funariidae Timmiidae andDicranidae all receive gt 95 BS while Bryidae are slightly less supported (89BS) Relationships between these major lineages are resolved but unsupported Atordinal level within the Bryidae a lower resolution is observed SplachnalesOrthotrichales Aulacomniales Hypnodendrales Hookeriales and Hypnales areresolved as monophyletic with 67-100 BS whereas Hedwigiales BartramialesBryales Orthodontiales and Rhizogoniales are not A closer relationship ofOrthotrichales with the pleurocarpous mosses sl than with the more basal ordersHedwigiales Bartramiales Splachnales and Bryales is indicated
7
Discussion
Classification of mosses - recent progress and the current state
For a long time mosses were subdivided into three main lineages the subclassesSphagnidae Andreaeidae and Bryidae (eg Fleischer 1920 Vitt 1984 Frahm ampFrey 1987) the latter with a number of (super-)orders (eg Frey 1977) Howevermolecular data confirmed that mosses comprise a number of isolated basal lineagesrepresented by morphologically and ecologically distinct extant taxa such as TakakiaSphagnum Andreaea Andreaeobryum Oedipodium Tetraphis the Polytrichaceaeand Buxbaumia which probably have long independent phylogenetic histories (cfNewton et al 2007) As a result of molecular phylogenies and a re-evaluation ofmorphological-anatomical characters the classification of mosses has changedconsiderably in the last few years with the main lineages nowadays treated atsubdivision class and subclass levels within division Bryophyta (eg Doweld 2001Ochyra et al 2003 Goffinet amp Buck 2004 this study)
Takakia and Sphagnum are the earliest diverging moss taxa in molecular phylogenies(eg Newton et al 2000 Beckert et al 2001 Cox et al 2004 Qiu et al 2006Newton et al 2007) That Takakia is a moss and not a liverwort was confirmed byanalysis of DNA sequences and phylogenomic characters such as the distribution ofmitochondrial introns (eg Beckert et al 2001) Its taxonomic status however stillremains to be clarified On the one hand most molecular studies resolve Takakiaand Sphagnum as sister genera although only partly with high statistical supportThese molecular topologies do not support the recognition of division Takakiophytaas proposed by Crandall-Stotler (1986) One the other hand no morphologicalsynapomorphies unite Takakia with Sphagnum and significant molecular differencesseparating Takakia from all other mosses were also observed For example a regionin the plastid ITS3 is similar to that of other land plants but absent in mosses(Samigullin et al 2002) and a transition in the trnL
UAA gene changing the anticodon
to CAA was otherwise only found in leptosporangiate ferns and Ginkgo (Quandt etal 2004) Thus ldquoresolution of Sphagnum - Takakia clade may be an artifactrdquo (Shawamp Renzaglia 2004) Also Goffinet amp Buck (2004) did not unite Takakia and Sphagnumunder a formal taxonomic rank but placed them into different informal superclassesIn our opinion Takakia should be treated at the same level as Sphagnophytina andBryophytina (cf Doweld 2001) ie as a subdivision of Bryophyta However morefundamental nomenclatural changes are necessary as the family name Takakiaceaewas not validated in the original publication by Hattori amp Inoue (1958) (article411 of ICBN McNeill et al 2006) and consequently all higher taxa erected laterare invalid The corrected taxonomic treatment of Takakia is provided here withsporophytic characters included in the latin diagnosis of Takakiaceae (see taxonomy)
Within Bryophytina we recognise four morphologically and molecularly isolatedbasal lineages as separated from the arthrodontous mosses (Bryopsida) Andreaeopsida(with linear capsule dehiscence) the operculate but eperistomate Oedipodiopsida aswell as Polytrichopsida and Tetraphidopsida with nematodontous peristomes A fifthclass Andreaeobryopsida was erected by Buck amp Goffinet (2000) but re-includedin Andreaeopsida as a subclass by Ochyra et al (2003) The systematic status of
8
Andreaeobryum macrosporum Steere amp BMMurray and possible relationships withAndreaea and Takakia were discussed by Murray (1988) and summarised includingmolecular results by Shaw amp Renzaglia (2004)
On the next lower level a number of morphologically and molecularly divergentlineages are nowadays treated as subclasses of Bryopsida Buxbaumiidae andDiphysciidae are generally branching off first in molecular topologies (eg Beckertet al 2001 Magombo 2003 Cox et al 2004) followed by Timmiidae Encalyptidaeand Funariidae as well as Dicranidae (haplolepideous mosses) sister to Bryidae slThese subclasses (except Buxbaumiidae not included) are also well recognizable inthe present analysis of non-coding plastid sequences (Fig 1)
The morphologically very different Encalyptidae and Funariidae are revealed assister groups although mostly without high support in several molecular phylogenies(eg Goffinet et al 2001 Cox et al 2004 Hedderson et al 2004 Tsubota et al2003 2004) and also in the present study (Fig 1) Goffinet et al (2007) confirmedthis relationship by phylogenomic evidence namely a large (71 kb) inversion in thechloroplast genome of Funariaceae Disceliaceae and Encalyptaceae but not inGigaspermaceae Consequently the latter family was separated at ordinal level fromthe two remaining families of Funariales by Goffinet et al (2007) GigaspermalesFunariales and Encalyptales may share a common ancestor according to some butnot all molecular phylogenies (eg Goffinet et al 2001 2007 Hedderson et al2004 but not in Tsubota et al 2004) Although ontogenetic data from peristomedevelopment may support their common ancestry (Goffinet et al 2007) unambiguousmorphological synapomorphies are lacking We therefore propose to treatGigaspermaceae at subclass level within the Bryopsida (see taxonomy)
The haplolepideous mosses (Dicranidae) are clearly supported as a monophyleticlineage which obviously evolved from a diplolepideous ancestor according to theirposition in the molecular trees (eg Newton et al 2000 Tsubota et al 2003 Cox etal 2004 Goffinet amp Buck 2004) Molecular studies suitable for inferring ordinaland family level relationships within Dicranidae either focused on the haplolepideousmosses (eg Stech 1999ab 2004 LaFarge et al 2000 2002 Tsubota et al 2003Hedderson et al 2004) or included more than 15 haplolepideous taxa in analyses ofa broader range of mosses (eg Goffinet et al 2001 Tsubota et al 2004 this study)Major lineages supported by these analyses are for example Grimmiales(Grimmiaceae Ptychomitriaceae and Seligeriaceae) Leucobryaceae (incl formerDicranaceae-Campylopoideae and Paraleucobryoideae pp) Dicranaceae sstr(Dicranoideae plus former Dicnemonaceae and Paraleucobryoideae pp) Pottiaceae(incl Cinclidotaceae and Splachnobryum) and Calymperaceae (probably exclOctoblepharum) Furthermore several genera and families belong to Dicranidaewhose systematic positions have been controversial (eg Stech et al 1999b LaFarge et al 2002 Hedderson et al 2004 OBrien 2007 Quandt et al 2007 thisstudy) Amphidium Archidium Catoscopium Drummondia EphemeraceaeErpodiaceae Mittenia (cf OBrien 2007 sequences in some earlier analyses werebased on misdentified specimens) Rhachitheciaceae Schistostega Splachnobryumand Wardia On the contrary several problems remain such as the circumscriptionof Ditrichaceae and relationships of the major haplolepideous lineages in general
9
Fig 1 Strict consensus tree of 129 most parsimonious trees inferred from combined trnLUAA
intronatpB-rbcL spacer and psbA-trnH spacer sequences of 85 taxa of Bryopsida as well as Andreaearupestris (Andreaeopsida) and Pogonatum subulatum (Polytrichopsida) as outgroup representativesBootstrap support values gt50 are depicted above the branches
10
Consequently resolving the phylogeny of Dicranidae with confidence is one of themajor future challenges in moss systematics
As mentioned above Dicranaceae are monophyletic in a narrow circumscriptionaccording to molecular data In contrast to former Campylopoideae andParaleucobryoideae the status of Rhabdoweisioideae (= Oncophoroideae Ochyra2002) and Dicranelloideae needs further consideration Stech (1999ab) suggestedto recognise RhabdoweisioideaeRhabdoweisiaceae in a broad sense includingDicranoweisia Amphidium and Aongstroemia Subsequent molecular analysesconfirmed a close relationship of the genera Arctoa Cynodontium DicranoweisiaKiaeria Oncophorus Oreoweisia Oreas Rhabdoweisia and Symblepharis althoughwithout significant support (La Farge et al 2002 Tsubota et al 2003 Hedderson etal 2004) With respect to the molecular evidence available so far we propose toelevate Oncophoroideae to family level to accomodate these genera and perhapsGlyphomitrium (cf Tsubota et al 2003) whereas we consider AongstroemiaDichodontium and Diobelonella to belong to Aongstroemiaceae (cf Stech 1999a)Amphidium is neither closely related to Dicranaceae sstr nor to Oncophoroideae(La Farge et al 2002 Tsubota et al 2003 Hedderson et al 2004 Stech 2004 thisstudy) and should be treated at family level rather than placed in Dicranaceae assubfam Amphidioideae (Ochyra et al 2003) The circumscription of Dicranelloideaeis more difficult to evaluate as few representatives have been included in molecularanalyses However Dicranella heteromalla (Hedw) Schimp as well as the generaCampylopodium and Microcampylopus are clearly separated from Dicranaceae sstr(Stech 1999a 2004 La Farge et al 2002 Tsubota et al 2003 Hedderson et al2004) and consequently the subfamily deserves family status as well Finallymolecular data showed that the genus Hypodontium does not belong to Pottiaceae(Hedderson et al 2004 Tsubota et al 2004) Taxonomic conclusions have not beendrawn from these results which is made up here (see taxonomy)
All mosses with diplolepideous-alternate peristomes together with Splachnales witha diplolepideous-opposite (Funaria-type) peristome form a monophyletic group inmolecular analyses (eg Newton et al 2000 Beckert et al 2001 Goffinet et al2001 Cox et al 2004 Tsubota et al 2004 references in Table 2) Differentclassifications of this by far most species-rich group of mosses were proposed (egVitt et al 1998 Ochyra et al 2003 Goffinet amp Buck 2004) However at least someof the recognised subclasses and superorders are paraphyletic according to themolecular topologies and assigning formal ranks to all evolutionarily significantmonophyletic entities is problematic if the main taxonomic framework of Bryophytaand Bryopsida should be maintained (cf discussion in Bell et al 2007) Thereforein the present synopsis only one subclass Bryidae is recognised for all diplolepideous-alternate mosses and Splachnales This broadly defined Bryidae is subdivided into13 orders most of them resolved as monophyletic in the majority of the phylogeneticanalyses summarised in Table 2 although with different levels of statistical supportin maximum parsimony analyses To define monophyletic lineages at supraordinallevel informal node-based names may be chosen according to Bell et al (2007) Forexample the pleurocarpous mosses (pleurocarpy sensu Bell amp Newton 2007) andtheir closest acrocarpous relatives (Orthodontiales to Hypnales) were already
11
Table 2 Taxon sampling and bootstrap support (BS) for Dicranidae Bryidae and orders within theBryidae in recent phylogenetic analyses (MP only) based on combined molecular markers Markersare given in square brackets (non-coding regions in bold) numbers of included taxa in brackets ++respective clade present with ge 80 BS + clade present with lt 80 BS - clade not present no oronly one representative included
Bell amp Newton OBrien Quandt et al Bell et al this study(2004) (2007) (2007) (2007)
[rbcL rps4 [atpB atpB- [rbcL rps4 [rbcL rps4 [atpB-rbcLnad5] rbcL rbcL trnL-F nad5] trnL-F nad5] psbA-trnH
rps4 trnL-F] trnL]
Dicranidae + (2) + (4) ++ (3) (1) ++ (19)Bryidae ++ (57) + (53) ++ (52) ++ (98) ++ (58)Hedwigiales ++ (2) (1) ++ (2) ++ (2) - (3)Bartramiales ++ (2) ++ (4) ++ (4) ++ (3) - (4)Splachnales (0) ++ (2) ++ (3) ++ (2) ++ (5)Bryales - (4) - (5) ++ (18) + (17) - (8)Orthotrichales (1) ++ (3) ++ (3) ++ (2) ++ (4)Orthodontiales + (4) + (4) + (3) + (6) - (3)Aulacomniales + (6) + (7) ++ (2) + (7) + (3)Rhizogoniales ++ (13) + (8) ++ (5) ++ (14) - (3)Hypnodendrales ++ (13) + (7) ++ (4) ++ (29) ++ (6)Ptychomniales ++ (3) ++ (3) (1) ++ (4) (1)Hookeriales - (4) + (2) (1) + (2) + (8)Hypnales - (5) - (7) ++ (5) ++ (10) + (10)
summarised under the informal node based name pleurcarpids (Bell et al 2007)and can be distinguished from a basal grade of acrocarpous or cladocarpous lineages(Hedwigiales to Orthotrichales) Within the latter monophyly of BartramialesSplachnales and Orthotrichales is well-supported in all analyses including two ormore taxa except Bartramiales in the present data set (cf Fig 1) In contrast Bryalesreceive significant support less frequently (but see Bell et al 2007 Quandt et al2007) Hedwigiales are well supported if only Hedwigia (Hedwigiaceae) andRhacocarpus (Rhacocarpaceae) are included whereas the monospecific Helicophyllum(Helicophyllaceae) is not closely related to these taxa but shows affinities withBartramiales (Goffinet et al 2001 this study) With respect to the differentmorphologies of Helicophyllaceae and Bartramiaceae however the former shouldbe separated at ordinal level (see taxonomy)
Clarifying relationships of the Orthotrichales is still a difficult issue Analyses ofsingle chloroplast markers or parsimony analyses of combined markers from differentgenomes mostly indicated a close relationship either with Splachnales (eg Cox etal 2000 Newton et al 2000 Tsubota et al 2004 Quandt et al 2007) or with thepleurocarpids (Goffinet et al 2001 this study) Although none of these alternativesis well-supported the latter seems more likely with regard to the moderately tomaximally supported Orthotrichales - pleurocarpid sister group relationship in allanalyses of mitochondrial data and in likelihood analyses of combined plastidmitochondrial markers (Beckert et al 2001 Quandt et al 2007)
12
The molecular polyphyly of Rhizogoniaceae (eg Bell amp Newton 2004) was solvedby the transfer of rhizogonioid genera into broadly defined Aulacomniaceae andOrthodontiaceae (Bell et al 2007) which now include both acrocarpous andpleurocarpous taxa These systematic changes are also comprehensible by non-molecular characters such as morphological traits shared by Mesochaete andAulacomnium heterostichum (Hedw) Bruch amp Schimp or the variously reducedperistomes of Orthodontiaceae pp in contrast to the generally fully developed Bryum-type peristomes of rhizogonioid and hypnodendroid mosses (Bell et al 2007) Theposition of the solely pleurocarpous Hypnodendrales sister to the former Hypnidaeled to the recognition of the informal group core pleurocarps (Bell et al 2007)The former Hypnidae (Ptychomniales Hookeriales and Hypnales summarised ashomocostate pleurocarps) are monophyletic in most molecular analyses (eg Goffinetet al 2001 Tsubota et al 2004 Bell et al 2007) with Ptychomniales being well-supported (Pedersen amp Newton 2007 Table 2) Clarifying relationships betweenHookeriales and Hypnales and within the latter is still a challenge but recent molecularstudies seem to support a sister group relationship of both orders (Bell et al 2007present study)
Phylogenetic utility of non-coding plastid markers
Non-coding plastid markers that comprise both variable and conserved regionssuch as the trnL
UAA intron have repeatedly been shown to possess potential for
resolving relationships at high taxonomic levels (eg Borsch et al 2003 Quandtet al 2004) Both the trnL intron and atpB-rbcL spacer were characterised indetail in mosses with respect to their structure and molecular evolution (Quandt ampStech 2005 Stech amp Quandt 2006) They include conservative regions that can beunambiguosly aligned and even parts of the more variable regions can be used ifrepeats hairpin loops etc are correctly identified and adequately treated in thephylogenetic analyses (eg Quandt et al 2003 Quandt amp Stech 2005) Using theatpB-rbcL spacer alone (Stech amp Quandt 2006) relationships of the major mosslineages were largely consistent with the ldquototal evidencerdquo molecular tree of Goffinetamp Buck (2004) However in addition to general limitations that result from singlemarker analyses the use of non-coding markers may pose further problems suchas a high amount of homoplasy resulting in low resolution or low statistical supportfor many clades Therefore several recent molecular studies of relationships withinBryidae have employed both coding and non-coding markers (Table 2)Nevertheless the usefulness of analyses of combined non-coding plastid markerscannot be ruled out In fact Fig 1 and Table 2 indicate a phylogenetic signal inthe present data set as many clades are recovered that are usually also resolvedin analyses of coding or combined coding and non-coding markers Especiallywith regard to statistical support however the present analysis is inferior tothose of other recent data sets especially Bell et al (2007) and Quandt et al(2007) In addition the non-coding markers used here are of different suitabilityand even the two intergenic spacers differ considerably from each other ThepsbA-trnH spacer contributes much less to the trees resolution than the atpB-rbcL spacer first because it is much shorter and second because relatively largeparts are attributed to hairpin loops or otherwise hypervariable regions These
13
results indicate that future studies should evaluate the molecular evolution andphylogenetic potential of new markers both coding and con-coding and choosethe most suitable ones in a combined analysis to resolve the remaining uncertaintiesin moss phylogeny
Taxonomy
Takakiaceae Stech amp WFrey stat nov
Plantae virides nusquam rhizophorae sine protonemate e caudicis rhizomatis erectae Caudicesrhizomati et axes geotropi radiformes frequenter intercalariter ramificantes sine phyllidiis cumpapillis mucilaginis rostratis Caules phyllidiiferi saepe furcati Phyllidia sine lamina et costadistincta profunde 2-4(-5)-lobata pluristratosa tristicha sed torsione spiraliter disposita Filumcentralium in ambabus generationibus (axibus gametophyti et setis) adest Plantae dioicae Antheridiaet archegonia nuda Sporophytum terminale solitarium Seta persistens Capsula tortilis admaturitatem schizocarpa secus unam rimam spiralem longitudinalem dehiscens Stomata etoperculum absunt peristomium nullum Calyptra mitriformis
TYPUS Takakia SHatt amp Inoue J Hattori Bot Lab 19 137 1958
Takakiaceae SHatt amp Inoue J Hattori Bot Lab 19 137 1958 nom inval (Art 411)
Takakiales Stech amp WFrey stat nov
Based on Takakiaceae Stech amp WFrey Nova Hedwigia 86 13 2008
TYPUS Takakia SHatt amp Inoue J Hattori Bot Lab 19 137 1958
Takakiales SHatt amp Inoue J Hattori Bot Lab 19 137 1958 nom inval
Takakiales SHatt amp Inoue ex RMSchust J Hattori Bot Lab 26 224 1963 nom inval (cumdescr latin)
Takakiopsida Stech amp WFrey statnov
Based on Takakiaceae Stech amp WFrey Nova Hedwigia 86 13 2008
TYPUS Takakia SHatt amp Inoue J Hattori Bot Lab 19 137 1958
Takakiopsida Goffinet amp WRBuck Monogr Syst Bot Missouri Bot Gard 98 232 2004 nominval
Takakiopsida Jia et al Acta Phytotax Sin 41 350 351 2003 nom nud
Takakiopsida Wang amp Wu Fl Bryophyt Sin 8 447 2004 nom inval (cum descr latin)
Takakiophytina Stech amp WFrey stat nov
Based on Takakiaceae Stech amp WFrey Nova Hedwigia 86 13 2008
TYPUS Takakia SHatt amp Inoue JHattori Bot Lab 19 137 1958
Gigaspermidae Stech amp WFrey subclass nov
Plantae acrocarpae terrestres stoloniferae ramis brevibus erectis Folia unicostata cellulis laxislaevibus Capsula plerumque valde rugosa gymnostomatica vel cleistocarpa stomata cum duabuscellulis sociis Ab Funariidis et Encalyptidis charactere phylogenomico (71-kb inversio abest)separatae
14
TYPUS Gigaspermum Lindb Oumlfversigt af Foumlrhandlingar Kongl Svenska Vetenskaps-Akademien21 599 1865
Amphidiaceae Stech stat nov
Based on Dicranaceae subfam Amphidioideae Ochyra in Ochyra Zarnowiec amp Bednarek-OchyraCens Cat Polish Mosses 110 2003
TYPUS Amphidium Schimp Coroll Bryol Eur 39 1856
Amphidiaceae AJESm Moss Fl Britain Ireland 2nd ed 657 2004 nom inval descr angl
Dicranellaceae Stech stat nov
Based on Dicranaceae subfam Dicranelloideae Lindb Utkast Eur Bladmoss 33 1878[lsquoUnderfamilje Dicranelleaersquo]
TYPUS Dicranella (MuumlllHal) Schimp Coroll Bryol Eur 13 1856
Oncophoraceae Stech stat nov
Based on Dicranaceae subfam Oncophoroideae Lindb Utkast Eur Bladmoss 34 1878[lsquoUnderfamilje Oncophoreaersquo]
TYPUS Oncophorus (Brid) Brid Bryol Univ 1 389 1826
Hypodontiaceae Stech fam nov
Plantae robustae characteribus morphologicis Pottiaceis et Calymperaceis similes sedcharacteribus molecularicis separatae Bracteae perichaetiales internae e basi vaginantes subulataevel aristatae Capsula aspectu succulenta cellulae exothecii incrassatae annulus magnopereabsens Peristomii dentes breves triangulati incurvati aurantiaci leves vel infirme verrucosiCalyptra cucullata
TYPUS Hypodontium MuumlllHal Hedwigia 38 96 1899
Helicophyllales Stech amp WFrey ord nov
Plantae acrocarpae prostratae tomentosae Folia dimorpha in duas series laterales et unam seriemventralem divisa Costa percurrens Cellulae hexagonae ad subquadratae papillosae Capsula immersacupulata ad oblonga infra orificium abrupte incurvata stomata destituta Peristomium nullum Sporaeisomorphae heteropolares granulatae
TYPUS Helicophyllum Brid Bryol Univ 2 771 1827
Synopsis of the suprageneric classification of BryophytaAuthor citations are in accordance with Art 492 of the Vienna Code (McNeill et al 2006)
Subdivision Takakiophytina Stech amp WFreyClass Takakiopsida Stech amp WFrey
Order Takakiales Stech amp WFreyTakakiaceae Stech amp WFrey
Subdivision Sphagnophytina DoweldClass Sphagnopsida Schimp
Order Sphagnales Limpr
15
Sphagnaceae DumortOrder Ambuchananiales Seppelt amp HACrum
Ambuchananiaceae Seppelt amp HACrumSubdivision Bryophytina Engler
Class Andreaeopsida JHSchaffnSubclass Andreaeidae Engl
Order Andreaeales LimprAndreaeaceae Dumort
Subclass Andreaeobryidae OchyraOrder Andreaeobryales BMMurray
Andreaeobryaceae Steere amp BMMurrayClass Oedipodiopsida Goffinet amp WRBuck
Order Oedipodiales Goffinet amp WRBuckOedipodiaceae Schimp
Class Tetraphidopsida Goffinet amp WRBuckOrder Tetraphidales MFleisch
Tetraphidaceae SchimpClass Polytrichopsida Doweld
Order Polytrichales MFleischPolytrichaceae Schwaumlgr
Class Bryopsida PaxSubclass Buxbaumiidae Doweld
Order Buxbaumiales MFleischBuxbaumiaceae Schimp
Subclass Diphysciidae OchyraOrder Diphysciales MFleisch
Diphysciaceae MFleischSubclass Timmiidae Ochyra
Order Timmiales OchyraTimmiaceae Schimp
Subclass Encalyptidae Ochyra Żarnowiec amp Bednarek-OchyraOrder Encalyptales Dixon
Encalyptaceae SchimpSubclass Funariidae Ochyra
Order Funariales MFleischFunariaceae Schwaumlgr Disceliaceae Schimp
Subclass Gigaspermidae Stech amp WFreyOrder Gigaspermales Goffinet Wickett OWerner Ros AJShaw amp CJCox
Gigaspermaceae LindbSubclass Dicranidae Doweld
Order Catoscopiales Ignatov amp IgnatovaCatoscopiaceae Broth
Order Scouleriales Goffinet amp WRBuckDrummondiaceae Goffinet Scouleriaceae SPChurchill
Order Bryoxiphiales HACrum amp LEAndersonBryoxiphiaceae Besch
16
Order Grimmiales MFleischGrimmiaceae Arn Ptychomitriaceae Schimp Seligeriaceae Schimp
Order Archidiales LimprArchidiaceae Schimp
Order Mitteniales ShawMitteniaceae Broth
Order Dicranales HPhilib ex MFleischAmphidiaceae Stech Aongstroemiaceae De Not BruchiaceaeSchimp Calymperaceae Kindb Dicranaceae Schimp Dicranel-laceae Stech Ditrichaceae Limpr Erpodiaceae Broth EustichiaceaeBroth Fissidentaceae Schimp Leucobryaceae Schimp Onco-phoraceae Stech Rhachitheciaceae HRob Schistostegaceae SchimpViridivelleraceae IGStone Wardiaceae Welch
Order Pottiales MFleischEphemeraceae Schimp Hypodontiaceae Stech PleurophascaceaeBroth Pottiaceae Schimp Serpotortellaceae WDReese amp RHZander
Subclass Bryidae EnglOrder Hedwigiales Ochyra
Hedwigiaceae Schimp Rhacocarpaceae KindbOrder Helicophyllales Stech amp WFrey
Helicophyllaceae BrothOrder Bartramiales DQuandt NEBell amp Stech
Bartramiaceae SchwaumlgrOrder Splachnales Ochyra
Meesiaceae Schimp Splachnaceae Grev amp ArnOrder Bryales Limpr
Bryaceae Schwaumlgr Leptostomataceae Schwaumlgr Mniaceae SchwaumlgrPhyllodrepaniaceae Crosby Pseudoditrichaceae Steere amp ZIwatsPulchrinodaceae DQuandt NEBell amp Stech
Order Orthotrichales DixonOrthotrichaceae Arn
Order Orthodontiales NEBell AENewton amp DQuandtOrthodontiaceae Goffinet
Order Aulacomniales NEBell AENewton amp DQuandtAulacomniaceae Schimp
Order Rhizogoniales Goffinet amp WRBuckRhizogoniaceae Broth
Order Hypnodendrales NEBell AENewton amp DQuandtBraithwaiteaceae NEBell AENewton amp DQuandt Hypnodendra-ceae Broth Pterobryellaceae WRBuck amp Vitt Racopilaceae Kindb
Order Ptychomniales WRBuck CJCox AJShaw amp GoffinetPtychomniaceae MFleisch
Order Hookeriales MFleischDaltoniaceae Schimp Hookeriaceae Schimp HypopterygiaceaeMitt Leucomiaceae Broth Pilotrichaceae Kindb SaulomataceaeWRBuck CJCox AJShaw amp Goffinet Schimperobryaceae WR
17
Buck CJCox AJShaw amp GoffinetOrder Hypnales WRBuck amp Vitt
Amblystegiaceae GRoth Anomodontaceae Kindb BrachytheciaceaeSchimp Calliergonaceae Vanderpoorten Hedenaumls CJCox amp AJShaw Catagoniaceae WRBuck amp Ireland Climaciaceae KindbCryphaeaceae Schimp Echinodiaceae Broth Entodontaceae KindbFabroniaceae Schimp Fontinalaceae Schimp Helodiaceae OchyraHeterocladiaceae Ignatov amp Ignatova Hylocomiaceae MFleischHypnaceae Schimp Lembophyllaceae Broth LeptodontaceaeSchimp Lepyrodontaceae Broth Leskeaceae Schimp Leucodon-taceae Schimp Meteoriaceae Kindb Microtheciellaceae HAMillamp AJHarr Myriniaceae Schimp Myuriaceae MFleisch NeckeraceaeSchimp Orthorrhynchiaceae SHLin Phyllogoniaceae KindbPlagiotheciaceae MFleisch Pleuroziopsidaceae Ireland Prionodon-taceae Broth Pseudoleskeaceae Schimp PseudoleskeellaceaeIgnatov amp Ignatova Pterigynandraceae Schimp PterobryaceaeKindb Pylaisiaceae Schimp Pylaisiadelphaceae Goffinet amp WRBuck Regmatodontaceae Broth Rhytidiaceae Broth RigodiaceaeHACrum Rutenbergiaceae MFleisch Scorpidiaceae Ignatov ampIgnatova Sematophyllaceae Broth Sorapillaceae MFleisch Ste-reophyllaceae WRBuck amp Ireland Symphyodontaceae MFleischTheliaceae MFleisch Thuidiaceae Schimp TrachylomataceaeWRBuck amp Vitt
Acknowledgements
Sincere thanks are due to JLReveal (Ithaca) as well as WFPrudhomme van Reine and JFVeldkamp(Leiden) for comments and discussions about suprafamilial taxonomy to DQuandt (Dresden) for providingDNA from Rhacocarpus and Bartramiaceae species and to BGiesicke (Berlin) for technical assistance
References
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BELL NE amp AE NEWTON (2004) Systematic studies of non-hypnanaean pleurocarps establishinga phylogenetic framework for investigating the origins of pleurocarpy - In GOFFINET BV HOLLOWELL amp R MAGILL (eds) Molecular systematics of bryophytes Monogr Syst BotMissouri Bot Gard 98 290-319
BELL NE amp AE NEWTON (2007) Pleurocarpy in the Rhizogoniaceous grade - In NEWTONAE amp RS TANGNEY (eds) Pleurocarpous mosses systematics and evolution SystematicsAssociation Special Volume Series 71 41-64
BELL NE D QUANDT TJ OBRIEN amp AE NEWTON (2007) Taxonomy and phylogeny inthe earliest diverging pleurocarps square holes and bifurcating pegs - Bryologist 110 533-560
BORSCH T KW HILU D QUANDT V WILDE C NEINHUIS amp W BARTHLOTT(2003) Non-coding plastid trnT-trnF sequences reveal a well resolved phylogeny of basal angiosperms- J Evol Biol 16 558-576
18
BUCK WR (2007) The history of pleurocarp classification two steps forward one step back - InNEWTON AE amp RS TANGNEY (eds) Pleurocarpous mosses systematics and evolutionSystematics Association Special Volume Series 71 1-18
BUCK WR amp B GOFFINET (2000) Morphology and classification of mosses - In SHAWAJ amp B GOFFINET (eds) Bryophyte Biology pp 71-123 Cambridge University PressCambridge
CHIANG TY BA SCHAAL amp CI PENG (1998) Universal primers for amplification andsequencing a noncoding spacer between atpB and rbcL genes of chloroplast DNA - Bot Bull AcadSin 39 245-250
COX CJ B GOFFINET AE NEWTON AJ SHAW amp TAJ HEDDERSON (2000)Phylogenetic relationships among the diplolepideous-alternate mosses (Bryidae) inferred from nuclearand chloroplast DNA sequences - Bryologist 103 224-241
COX CJ B GOFFINET AJ SHAW amp SB BOLES (2004) Phylogenetic relationships amongthe mosses based on heterogeneous Bayesian analysis of multiple genes from multiple genomiccompartments - Syst Bot 29 234-250
CRANDALL-STOTLER B (1986) Morphogenesis developmental anatomy and bryophytephylogenetics contra-indications of monophyly - J Bryol 14 1-23
CROSBY MR RE MAGILL B ALLEN amp S HE (1999) A checklist of the mosses - MissouriBotanical Garden St Louis Missouri
DOWELD A (2001) Prosyllabus Tracheophytorum - GEOS Moscow i-lxxx + 110 pp
DOYLE JJ amp JL DOYLE (1990) Isolation of plant DNA from fresh tissue - Focus 12 13-15
DUFF RJ JC VILLAREAL DC CARGILL amp KS RENZAGLIA (2007) Progress andchallenges towards developing a phylogeny and classification of the hornworts - Bryologist 110214-243
FLEISCHER M (1920) Natuumlrliches System der Laubmoose - Hedwigia 61 390-400
FORREST LL EC DAVIS DG LONG BJ CRANDALL-STOTLER A CLARK ampML HOLLINGSWORTH (2006) Unraveling the evolutionary history of the liverworts (Marchantio-phyta) multiple taxa genomes and analyses - Bryologist 109 303-334
FRAHM J-P amp W FREY (1987) Moosflora 2 Aufl - UTB 1250 Stuttgart
FREY W (1977) Neue Vorstellungen uumlber die Verwandtschaftsgruppen und die Stammesgeschichteder Laubmoose - In FREY W H HURKA amp F OBERWINKLER (Hrsg) Beitraumlge zur Biologieder Pflanzen pp 117-139 Stuttgart
FREY W amp M STECH (2005) A morpho-molecular classification of the liverworts (Hepa-ticophytina Bryophyta) - Nova Hedwigia 81 55-78
FREY W M STECH amp K MEIszligNER (1999) Chloroplast DNA-relationship in palaeoaustralLopidium concinnum (Hypopterygiaceae Musci) An example of steno-evolution in mosses Studiesin austral temperate rain forest bryophytes 2 - Plant Syst Evol 218 67-75
GOFFINET B amp WR BUCK (2004) Systematics of Bryophyta (mosses) from molecules to arevised classification - In GOFFINET B V HOLLOWELL amp R MAGILL (eds) Molecularsystematics of bryophytes Monogr Syst Bot Missouri Bot Gard 98 205-239
GOFFINET B CJ COX AJ SHAW amp TAJ HEDDERSON (2001) The Bryophyta (mosses)Systematic and evolutionary inferences from an rps4 gene (cpDNA) phylogeny - Ann Bot 87191-208
GOFFINET B NJ WICKETT O WERNER RM ROS AJ SHAW amp CJ COX (2007)Distribution and phylogenetic significance of the 71-kb inversion in the plastid genome in Funariidae(Bryophyta) - Ann Bot 99 747-753
19
GROTH-MALONEK M D PRUCHNER F GREWE amp V KNOOP (2005) Ancestors oftrans-splicing mitochondrial introns support serial sister group relationships of hornworts and mosseswith vascular plants - Mol Biol Evol 22 117-125
HATTORI S amp H INOUE (1958) Preliminary report on Takakia lepidozioides - J Hattori BotLab 19 133-137
HE-NYGREacuteN X A JUSLEacuteN I AHONEN D GLENNY amp S PIIPPO (2006) Illuminating theevolutionary history of liverworts (Marchantiophyta) - towards a natural classification - Cladistics22 1-31
HEDDERSON TAJ DJ MURRAY CJ COX amp TL NOWELL (2004) Phylogeneticrelationships of haplolepideous mosses (Dicranidae) inferred from rps4 gene sequences - Syst Bot29 29-41
LA FARGE C BD MISHER JA WHEELER DP WALL K JOHANNES S SCHAFFERamp AJ SHAW (2000) Phylogenetic relationships within the haplolepideous mosses - Bryologist103 257-276
LA FARGE C AJ SHAW amp DH VITT (2002) The circumscription of the Dicranaceae(Bryopsida) based on the chloroplast regions trnL-trnF and rps4 - Syst Bot 27 435-452
MAGOMBO ZLK (2003) The phylogeny of basal peristomate mosses evidence from cpDNAand implications for peristome evolution - Syst Bot 28 24-38
MCNEILL J FR BARRIE HM BURDET V DEMOULIN DL HAWKSWORTHK MARHOLD DH NICOLSON J PRADO PC SILVA JE SKOG JH WIERSEMA ampNJ TURLAND (2006) International Code of Botanical Nomenclature (Vienna Code) - RegnumVegetabile 146 1-568
MUumlLLER K (2004) PRAP - computation of Bremer support for large data sets - Mol PhylogenetEvol 31 780-782
MUumlLLER K (2005) SeqState - primer design and sequence statistics for phylogenetic DNA datasets - Appl Bioinformatics 4 65-69
MUumlLLER K D QUANDT J MUumlLLER amp C NEINHUIS (2005) PhyDE v0992 PhylogeneticData Editor - httpwwwphydede
MURRAY BM (1988) Systematics of the Andreaeopsida (Bryophyta) two orders with links toTakakia - Nova Hedwigia Beih 90 289-336
NEWTON AE amp RS TANGNEY (eds) (2007) Pleurocarpous mosses systematics and evolutionSystematics Association Special Volume Series 71 CRC Press Boca Raton 434 pp
NEWTON AE CJ COX JG DUCKETT JA WHEELER B GOFFINET TAJ HEDDER-SON amp BD MISHLER (2000) Evolution of the major moss lineages Phylogenetic analyses basedon multiple gene sequences and morphology - Bryologist 103 187-211
NEWTON AE N WIKSTROumlM NE BELL LL FORREST amp MS IGNATOV (2007)Dating the diversification of the pleurocarpous mosses - In NEWTON AE amp RS TANGNEY(eds) Pleurocarpous mosses systematics and evolution Systematics Association Special VolumeSeries 71 337-366
NIXON KC (1999) The parsimony ratchet a new method for rapid parsimony analysis - Cladistics15 407-411
OBRIEN TJ (2007) The phylogenetic distribution of pleurocarpous mosses evidence fromcpDNA sequences - In NEWTON AE amp RS TANGNEY (eds) Pleurocarpous mossessystematics and evolution Systematics Association Special Volume Series 71 19-41
OCHYRA R (2002) Nomenclatural changes in subfamilies of the Dicranaceae - CryptogamieBryol 23 345-349
20
OCHYRA R J ŻARNOWIEC amp H BEDNAREK-OCHYRA (2003) Census catalogue ofPolish mosses - Biodiv Poland 3 1-372
PEDERSEN N amp AE NEWTON (2007) Phylogenetic and morphological studies within thePtychomniales with emphasis on the evolution of dwarf males - In NEWTON AE amp RSTANGNEY (eds) Pleurocarpous mosses systematics and evolution Systematics AssociationSpecial Volume Series 71 367-392
QUANDT D amp M STECH (2005) Molecular evolution and secondary structure of the chloroplasttrnL intron in bryophytes - Mol Phylogenet Evol 36 429-443
QUANDT D K MUumlLLER amp S HUTTUNEN (2003) Characterisation of the chloroplast DNApsbT-H region and the influence of dyad symmetrical elements on phylogenetic reconstructions -Plant Biol 5 400-410
QUANDT D K MUumlLLER M STECH W FREY KW HILU amp T BORSCH (2004) Molecularevolution of the chloroplast trnL-F-region in land plants - In GOFFINET B V HOLLOWELL ampR MAGILL (eds) Molecular systematics of bryophytes Monogr Syst Bot Missouri Bot Gard98 13-37
QUANDT D NE BELL amp M STECH (2007) Unravelling the knot the Pulchrinodaceae famnov (Bryales) - In KUumlRSCHNER H T PFEIFFER amp M STECH (eds) A Festschrift to Wolf-gang Frey - a scientists life between deserts and rain forests Nova Hedwigia Beih 131 21-39
QIU Y-L Y CHO JC COX amp JD PALMER (1998) The gain of three mitochondrial intronsidentifies liverworts as the earliest land plants - Nature 394 671-674
QIU Y-L L LI B WANG Z CHEN V KNOOP M GROTH-MALONEK O DOM-BROVSKA J LEE L KENT J REST GF ESTABROOK TA HENDRY DW TAYLORCM TESTA M AMBROS B CRANDALL-STOTLER J DUFF M STECH W FREYD QUANDT amp CC DAVIS (2006) The deepest divergences in land plants inferred fromphylogenomic evidence - Proc Natl Acad Sci USA 103 15511-15516
RENZAGLIA KS S SCHUETTE RJ DUFF R LIGRONE AJ SHAW BD MISHLER ampJG DUCKETT (2007) Bryophyte phylogeny Advancing the molecular and morphological frontiers- Bryologist 110 179-213
SAMIGULLIN TH SP YACENTYUK GV DEGTYARYEVA KM VALIEJO-ROMANVK BOBROVA I CAPESIUS WF MARTIN AV TROITSKY VR FILIN amp ASANTONOV (2002) Paraphyly of bryophytes and close relationships of hornworts and vascularplants inferred from analysis of chloroplast rDNA ITS (cpITS) sequences - Arctoa 11 31-43
SANG T DJ CRAWFORD amp TF STUESSY (1997) Chloroplast DNA phylogeny reticulateevolution and biogeography of Paeonia (Paeoniaceae) - Amer J Bot 84 1120-1136
SHAW AJ amp KS RENZAGLIA (2004) Phylogeny and diversification of bryophytes - AmerJ Bot 91 1557-1581
SHAW AJ CJ COX amp B GOFFINET (2005) Global patterns of moss diversity taxonomic andmolecular inferences - Taxon 54 337-352
STECH M (1999a) A reclassification of Dicranaceae (Bryopsida) based on non-coding cpDNAsequence data - J Hattori Bot Lab 86 137-159
STECH M (1999b) A molecular systematic contribution to the position of Amphidium Schimp(Rhabdoweisiaceae Bryopsida) - Nova Hedwigia 68 291-300
STECH M (2004) Supraspecific circumscription and classification of Campylopus Brid(Dicranaceae Bryopsida) based on molecular data - Syst Bot 29 817-824
STECH M amp D QUANDT (2006) Molecular evolution of the chloroplast atpB-rbcL spacer inbryophytes - In SHARMA AK amp A SHARMA (eds) Plant Genome Biodiversity and EvolutionVol 2 Part B pp 409-431 Science Publishers Enfield New Hampshire
21
STECH M D QUANDT amp W FREY (2003) Molecular circumscription of the hornworts(Antho-cerotophyta) based on the chloroplast DNA trnL-trnF region - J Plant Res 116 389-398
STOTLER RE amp B CRANDALL-STOTLER (2005) A revised classification of theAnthocerotophyta and a checklist of the hornworts of North America north of Mexico - Bryologist108 16-26
SWOFFORD DL (2002) PAUP Phylogenetic analysis using parsimony (and other methods)version 40b10 - Sunderland MA
TABERLET P L GIELLY G PAUTOU amp J BOUVET (1991) Universal primers for amplificationof three non-coding regions of chloroplast DNA - Plant Mol Biol 17 1105-1109
TSUBOTA H Y AGENO B ESTEacuteBANEZ T YAMAGUCHI amp H DEGUCHI (2003)Molecular phylogeny of the Grimmiales (Musci) based on chloroplast rbcL sequences - Hikobia 1455-70
TSUBOTA H E DE LUNA D GONZAacuteLEZ MS IGNATOV amp H DEGUCHI (2004) Molecularphylogenetics and ordinal relationships based on analyses of a large-scale data set of 600 rbcLsequences of mosses - Hikobia 14 149-170
VITT DH (1984) Classification of the Bryopsida - In SCHUSTER RM (ed) New Manual ofBryology 2 696-759 Hattori Botanical Laboratory Nichinan Japan
VITT DH B GOFFINET amp T HEDDERSON (1998) 8 The ordinal classification of the mossesquestions and answers for the 1990s - In BATES JW NW ASHTON amp JG DUCKETT (eds)Bryology for the twenty-first century British Bryol Soc pp 113-123
Received 3 September 2007 accepted in revised form 30 October 2007
7
Discussion
Classification of mosses - recent progress and the current state
For a long time mosses were subdivided into three main lineages the subclassesSphagnidae Andreaeidae and Bryidae (eg Fleischer 1920 Vitt 1984 Frahm ampFrey 1987) the latter with a number of (super-)orders (eg Frey 1977) Howevermolecular data confirmed that mosses comprise a number of isolated basal lineagesrepresented by morphologically and ecologically distinct extant taxa such as TakakiaSphagnum Andreaea Andreaeobryum Oedipodium Tetraphis the Polytrichaceaeand Buxbaumia which probably have long independent phylogenetic histories (cfNewton et al 2007) As a result of molecular phylogenies and a re-evaluation ofmorphological-anatomical characters the classification of mosses has changedconsiderably in the last few years with the main lineages nowadays treated atsubdivision class and subclass levels within division Bryophyta (eg Doweld 2001Ochyra et al 2003 Goffinet amp Buck 2004 this study)
Takakia and Sphagnum are the earliest diverging moss taxa in molecular phylogenies(eg Newton et al 2000 Beckert et al 2001 Cox et al 2004 Qiu et al 2006Newton et al 2007) That Takakia is a moss and not a liverwort was confirmed byanalysis of DNA sequences and phylogenomic characters such as the distribution ofmitochondrial introns (eg Beckert et al 2001) Its taxonomic status however stillremains to be clarified On the one hand most molecular studies resolve Takakiaand Sphagnum as sister genera although only partly with high statistical supportThese molecular topologies do not support the recognition of division Takakiophytaas proposed by Crandall-Stotler (1986) One the other hand no morphologicalsynapomorphies unite Takakia with Sphagnum and significant molecular differencesseparating Takakia from all other mosses were also observed For example a regionin the plastid ITS3 is similar to that of other land plants but absent in mosses(Samigullin et al 2002) and a transition in the trnL
UAA gene changing the anticodon
to CAA was otherwise only found in leptosporangiate ferns and Ginkgo (Quandt etal 2004) Thus ldquoresolution of Sphagnum - Takakia clade may be an artifactrdquo (Shawamp Renzaglia 2004) Also Goffinet amp Buck (2004) did not unite Takakia and Sphagnumunder a formal taxonomic rank but placed them into different informal superclassesIn our opinion Takakia should be treated at the same level as Sphagnophytina andBryophytina (cf Doweld 2001) ie as a subdivision of Bryophyta However morefundamental nomenclatural changes are necessary as the family name Takakiaceaewas not validated in the original publication by Hattori amp Inoue (1958) (article411 of ICBN McNeill et al 2006) and consequently all higher taxa erected laterare invalid The corrected taxonomic treatment of Takakia is provided here withsporophytic characters included in the latin diagnosis of Takakiaceae (see taxonomy)
Within Bryophytina we recognise four morphologically and molecularly isolatedbasal lineages as separated from the arthrodontous mosses (Bryopsida) Andreaeopsida(with linear capsule dehiscence) the operculate but eperistomate Oedipodiopsida aswell as Polytrichopsida and Tetraphidopsida with nematodontous peristomes A fifthclass Andreaeobryopsida was erected by Buck amp Goffinet (2000) but re-includedin Andreaeopsida as a subclass by Ochyra et al (2003) The systematic status of
8
Andreaeobryum macrosporum Steere amp BMMurray and possible relationships withAndreaea and Takakia were discussed by Murray (1988) and summarised includingmolecular results by Shaw amp Renzaglia (2004)
On the next lower level a number of morphologically and molecularly divergentlineages are nowadays treated as subclasses of Bryopsida Buxbaumiidae andDiphysciidae are generally branching off first in molecular topologies (eg Beckertet al 2001 Magombo 2003 Cox et al 2004) followed by Timmiidae Encalyptidaeand Funariidae as well as Dicranidae (haplolepideous mosses) sister to Bryidae slThese subclasses (except Buxbaumiidae not included) are also well recognizable inthe present analysis of non-coding plastid sequences (Fig 1)
The morphologically very different Encalyptidae and Funariidae are revealed assister groups although mostly without high support in several molecular phylogenies(eg Goffinet et al 2001 Cox et al 2004 Hedderson et al 2004 Tsubota et al2003 2004) and also in the present study (Fig 1) Goffinet et al (2007) confirmedthis relationship by phylogenomic evidence namely a large (71 kb) inversion in thechloroplast genome of Funariaceae Disceliaceae and Encalyptaceae but not inGigaspermaceae Consequently the latter family was separated at ordinal level fromthe two remaining families of Funariales by Goffinet et al (2007) GigaspermalesFunariales and Encalyptales may share a common ancestor according to some butnot all molecular phylogenies (eg Goffinet et al 2001 2007 Hedderson et al2004 but not in Tsubota et al 2004) Although ontogenetic data from peristomedevelopment may support their common ancestry (Goffinet et al 2007) unambiguousmorphological synapomorphies are lacking We therefore propose to treatGigaspermaceae at subclass level within the Bryopsida (see taxonomy)
The haplolepideous mosses (Dicranidae) are clearly supported as a monophyleticlineage which obviously evolved from a diplolepideous ancestor according to theirposition in the molecular trees (eg Newton et al 2000 Tsubota et al 2003 Cox etal 2004 Goffinet amp Buck 2004) Molecular studies suitable for inferring ordinaland family level relationships within Dicranidae either focused on the haplolepideousmosses (eg Stech 1999ab 2004 LaFarge et al 2000 2002 Tsubota et al 2003Hedderson et al 2004) or included more than 15 haplolepideous taxa in analyses ofa broader range of mosses (eg Goffinet et al 2001 Tsubota et al 2004 this study)Major lineages supported by these analyses are for example Grimmiales(Grimmiaceae Ptychomitriaceae and Seligeriaceae) Leucobryaceae (incl formerDicranaceae-Campylopoideae and Paraleucobryoideae pp) Dicranaceae sstr(Dicranoideae plus former Dicnemonaceae and Paraleucobryoideae pp) Pottiaceae(incl Cinclidotaceae and Splachnobryum) and Calymperaceae (probably exclOctoblepharum) Furthermore several genera and families belong to Dicranidaewhose systematic positions have been controversial (eg Stech et al 1999b LaFarge et al 2002 Hedderson et al 2004 OBrien 2007 Quandt et al 2007 thisstudy) Amphidium Archidium Catoscopium Drummondia EphemeraceaeErpodiaceae Mittenia (cf OBrien 2007 sequences in some earlier analyses werebased on misdentified specimens) Rhachitheciaceae Schistostega Splachnobryumand Wardia On the contrary several problems remain such as the circumscriptionof Ditrichaceae and relationships of the major haplolepideous lineages in general
9
Fig 1 Strict consensus tree of 129 most parsimonious trees inferred from combined trnLUAA
intronatpB-rbcL spacer and psbA-trnH spacer sequences of 85 taxa of Bryopsida as well as Andreaearupestris (Andreaeopsida) and Pogonatum subulatum (Polytrichopsida) as outgroup representativesBootstrap support values gt50 are depicted above the branches
10
Consequently resolving the phylogeny of Dicranidae with confidence is one of themajor future challenges in moss systematics
As mentioned above Dicranaceae are monophyletic in a narrow circumscriptionaccording to molecular data In contrast to former Campylopoideae andParaleucobryoideae the status of Rhabdoweisioideae (= Oncophoroideae Ochyra2002) and Dicranelloideae needs further consideration Stech (1999ab) suggestedto recognise RhabdoweisioideaeRhabdoweisiaceae in a broad sense includingDicranoweisia Amphidium and Aongstroemia Subsequent molecular analysesconfirmed a close relationship of the genera Arctoa Cynodontium DicranoweisiaKiaeria Oncophorus Oreoweisia Oreas Rhabdoweisia and Symblepharis althoughwithout significant support (La Farge et al 2002 Tsubota et al 2003 Hedderson etal 2004) With respect to the molecular evidence available so far we propose toelevate Oncophoroideae to family level to accomodate these genera and perhapsGlyphomitrium (cf Tsubota et al 2003) whereas we consider AongstroemiaDichodontium and Diobelonella to belong to Aongstroemiaceae (cf Stech 1999a)Amphidium is neither closely related to Dicranaceae sstr nor to Oncophoroideae(La Farge et al 2002 Tsubota et al 2003 Hedderson et al 2004 Stech 2004 thisstudy) and should be treated at family level rather than placed in Dicranaceae assubfam Amphidioideae (Ochyra et al 2003) The circumscription of Dicranelloideaeis more difficult to evaluate as few representatives have been included in molecularanalyses However Dicranella heteromalla (Hedw) Schimp as well as the generaCampylopodium and Microcampylopus are clearly separated from Dicranaceae sstr(Stech 1999a 2004 La Farge et al 2002 Tsubota et al 2003 Hedderson et al2004) and consequently the subfamily deserves family status as well Finallymolecular data showed that the genus Hypodontium does not belong to Pottiaceae(Hedderson et al 2004 Tsubota et al 2004) Taxonomic conclusions have not beendrawn from these results which is made up here (see taxonomy)
All mosses with diplolepideous-alternate peristomes together with Splachnales witha diplolepideous-opposite (Funaria-type) peristome form a monophyletic group inmolecular analyses (eg Newton et al 2000 Beckert et al 2001 Goffinet et al2001 Cox et al 2004 Tsubota et al 2004 references in Table 2) Differentclassifications of this by far most species-rich group of mosses were proposed (egVitt et al 1998 Ochyra et al 2003 Goffinet amp Buck 2004) However at least someof the recognised subclasses and superorders are paraphyletic according to themolecular topologies and assigning formal ranks to all evolutionarily significantmonophyletic entities is problematic if the main taxonomic framework of Bryophytaand Bryopsida should be maintained (cf discussion in Bell et al 2007) Thereforein the present synopsis only one subclass Bryidae is recognised for all diplolepideous-alternate mosses and Splachnales This broadly defined Bryidae is subdivided into13 orders most of them resolved as monophyletic in the majority of the phylogeneticanalyses summarised in Table 2 although with different levels of statistical supportin maximum parsimony analyses To define monophyletic lineages at supraordinallevel informal node-based names may be chosen according to Bell et al (2007) Forexample the pleurocarpous mosses (pleurocarpy sensu Bell amp Newton 2007) andtheir closest acrocarpous relatives (Orthodontiales to Hypnales) were already
11
Table 2 Taxon sampling and bootstrap support (BS) for Dicranidae Bryidae and orders within theBryidae in recent phylogenetic analyses (MP only) based on combined molecular markers Markersare given in square brackets (non-coding regions in bold) numbers of included taxa in brackets ++respective clade present with ge 80 BS + clade present with lt 80 BS - clade not present no oronly one representative included
Bell amp Newton OBrien Quandt et al Bell et al this study(2004) (2007) (2007) (2007)
[rbcL rps4 [atpB atpB- [rbcL rps4 [rbcL rps4 [atpB-rbcLnad5] rbcL rbcL trnL-F nad5] trnL-F nad5] psbA-trnH
rps4 trnL-F] trnL]
Dicranidae + (2) + (4) ++ (3) (1) ++ (19)Bryidae ++ (57) + (53) ++ (52) ++ (98) ++ (58)Hedwigiales ++ (2) (1) ++ (2) ++ (2) - (3)Bartramiales ++ (2) ++ (4) ++ (4) ++ (3) - (4)Splachnales (0) ++ (2) ++ (3) ++ (2) ++ (5)Bryales - (4) - (5) ++ (18) + (17) - (8)Orthotrichales (1) ++ (3) ++ (3) ++ (2) ++ (4)Orthodontiales + (4) + (4) + (3) + (6) - (3)Aulacomniales + (6) + (7) ++ (2) + (7) + (3)Rhizogoniales ++ (13) + (8) ++ (5) ++ (14) - (3)Hypnodendrales ++ (13) + (7) ++ (4) ++ (29) ++ (6)Ptychomniales ++ (3) ++ (3) (1) ++ (4) (1)Hookeriales - (4) + (2) (1) + (2) + (8)Hypnales - (5) - (7) ++ (5) ++ (10) + (10)
summarised under the informal node based name pleurcarpids (Bell et al 2007)and can be distinguished from a basal grade of acrocarpous or cladocarpous lineages(Hedwigiales to Orthotrichales) Within the latter monophyly of BartramialesSplachnales and Orthotrichales is well-supported in all analyses including two ormore taxa except Bartramiales in the present data set (cf Fig 1) In contrast Bryalesreceive significant support less frequently (but see Bell et al 2007 Quandt et al2007) Hedwigiales are well supported if only Hedwigia (Hedwigiaceae) andRhacocarpus (Rhacocarpaceae) are included whereas the monospecific Helicophyllum(Helicophyllaceae) is not closely related to these taxa but shows affinities withBartramiales (Goffinet et al 2001 this study) With respect to the differentmorphologies of Helicophyllaceae and Bartramiaceae however the former shouldbe separated at ordinal level (see taxonomy)
Clarifying relationships of the Orthotrichales is still a difficult issue Analyses ofsingle chloroplast markers or parsimony analyses of combined markers from differentgenomes mostly indicated a close relationship either with Splachnales (eg Cox etal 2000 Newton et al 2000 Tsubota et al 2004 Quandt et al 2007) or with thepleurocarpids (Goffinet et al 2001 this study) Although none of these alternativesis well-supported the latter seems more likely with regard to the moderately tomaximally supported Orthotrichales - pleurocarpid sister group relationship in allanalyses of mitochondrial data and in likelihood analyses of combined plastidmitochondrial markers (Beckert et al 2001 Quandt et al 2007)
12
The molecular polyphyly of Rhizogoniaceae (eg Bell amp Newton 2004) was solvedby the transfer of rhizogonioid genera into broadly defined Aulacomniaceae andOrthodontiaceae (Bell et al 2007) which now include both acrocarpous andpleurocarpous taxa These systematic changes are also comprehensible by non-molecular characters such as morphological traits shared by Mesochaete andAulacomnium heterostichum (Hedw) Bruch amp Schimp or the variously reducedperistomes of Orthodontiaceae pp in contrast to the generally fully developed Bryum-type peristomes of rhizogonioid and hypnodendroid mosses (Bell et al 2007) Theposition of the solely pleurocarpous Hypnodendrales sister to the former Hypnidaeled to the recognition of the informal group core pleurocarps (Bell et al 2007)The former Hypnidae (Ptychomniales Hookeriales and Hypnales summarised ashomocostate pleurocarps) are monophyletic in most molecular analyses (eg Goffinetet al 2001 Tsubota et al 2004 Bell et al 2007) with Ptychomniales being well-supported (Pedersen amp Newton 2007 Table 2) Clarifying relationships betweenHookeriales and Hypnales and within the latter is still a challenge but recent molecularstudies seem to support a sister group relationship of both orders (Bell et al 2007present study)
Phylogenetic utility of non-coding plastid markers
Non-coding plastid markers that comprise both variable and conserved regionssuch as the trnL
UAA intron have repeatedly been shown to possess potential for
resolving relationships at high taxonomic levels (eg Borsch et al 2003 Quandtet al 2004) Both the trnL intron and atpB-rbcL spacer were characterised indetail in mosses with respect to their structure and molecular evolution (Quandt ampStech 2005 Stech amp Quandt 2006) They include conservative regions that can beunambiguosly aligned and even parts of the more variable regions can be used ifrepeats hairpin loops etc are correctly identified and adequately treated in thephylogenetic analyses (eg Quandt et al 2003 Quandt amp Stech 2005) Using theatpB-rbcL spacer alone (Stech amp Quandt 2006) relationships of the major mosslineages were largely consistent with the ldquototal evidencerdquo molecular tree of Goffinetamp Buck (2004) However in addition to general limitations that result from singlemarker analyses the use of non-coding markers may pose further problems suchas a high amount of homoplasy resulting in low resolution or low statistical supportfor many clades Therefore several recent molecular studies of relationships withinBryidae have employed both coding and non-coding markers (Table 2)Nevertheless the usefulness of analyses of combined non-coding plastid markerscannot be ruled out In fact Fig 1 and Table 2 indicate a phylogenetic signal inthe present data set as many clades are recovered that are usually also resolvedin analyses of coding or combined coding and non-coding markers Especiallywith regard to statistical support however the present analysis is inferior tothose of other recent data sets especially Bell et al (2007) and Quandt et al(2007) In addition the non-coding markers used here are of different suitabilityand even the two intergenic spacers differ considerably from each other ThepsbA-trnH spacer contributes much less to the trees resolution than the atpB-rbcL spacer first because it is much shorter and second because relatively largeparts are attributed to hairpin loops or otherwise hypervariable regions These
13
results indicate that future studies should evaluate the molecular evolution andphylogenetic potential of new markers both coding and con-coding and choosethe most suitable ones in a combined analysis to resolve the remaining uncertaintiesin moss phylogeny
Taxonomy
Takakiaceae Stech amp WFrey stat nov
Plantae virides nusquam rhizophorae sine protonemate e caudicis rhizomatis erectae Caudicesrhizomati et axes geotropi radiformes frequenter intercalariter ramificantes sine phyllidiis cumpapillis mucilaginis rostratis Caules phyllidiiferi saepe furcati Phyllidia sine lamina et costadistincta profunde 2-4(-5)-lobata pluristratosa tristicha sed torsione spiraliter disposita Filumcentralium in ambabus generationibus (axibus gametophyti et setis) adest Plantae dioicae Antheridiaet archegonia nuda Sporophytum terminale solitarium Seta persistens Capsula tortilis admaturitatem schizocarpa secus unam rimam spiralem longitudinalem dehiscens Stomata etoperculum absunt peristomium nullum Calyptra mitriformis
TYPUS Takakia SHatt amp Inoue J Hattori Bot Lab 19 137 1958
Takakiaceae SHatt amp Inoue J Hattori Bot Lab 19 137 1958 nom inval (Art 411)
Takakiales Stech amp WFrey stat nov
Based on Takakiaceae Stech amp WFrey Nova Hedwigia 86 13 2008
TYPUS Takakia SHatt amp Inoue J Hattori Bot Lab 19 137 1958
Takakiales SHatt amp Inoue J Hattori Bot Lab 19 137 1958 nom inval
Takakiales SHatt amp Inoue ex RMSchust J Hattori Bot Lab 26 224 1963 nom inval (cumdescr latin)
Takakiopsida Stech amp WFrey statnov
Based on Takakiaceae Stech amp WFrey Nova Hedwigia 86 13 2008
TYPUS Takakia SHatt amp Inoue J Hattori Bot Lab 19 137 1958
Takakiopsida Goffinet amp WRBuck Monogr Syst Bot Missouri Bot Gard 98 232 2004 nominval
Takakiopsida Jia et al Acta Phytotax Sin 41 350 351 2003 nom nud
Takakiopsida Wang amp Wu Fl Bryophyt Sin 8 447 2004 nom inval (cum descr latin)
Takakiophytina Stech amp WFrey stat nov
Based on Takakiaceae Stech amp WFrey Nova Hedwigia 86 13 2008
TYPUS Takakia SHatt amp Inoue JHattori Bot Lab 19 137 1958
Gigaspermidae Stech amp WFrey subclass nov
Plantae acrocarpae terrestres stoloniferae ramis brevibus erectis Folia unicostata cellulis laxislaevibus Capsula plerumque valde rugosa gymnostomatica vel cleistocarpa stomata cum duabuscellulis sociis Ab Funariidis et Encalyptidis charactere phylogenomico (71-kb inversio abest)separatae
14
TYPUS Gigaspermum Lindb Oumlfversigt af Foumlrhandlingar Kongl Svenska Vetenskaps-Akademien21 599 1865
Amphidiaceae Stech stat nov
Based on Dicranaceae subfam Amphidioideae Ochyra in Ochyra Zarnowiec amp Bednarek-OchyraCens Cat Polish Mosses 110 2003
TYPUS Amphidium Schimp Coroll Bryol Eur 39 1856
Amphidiaceae AJESm Moss Fl Britain Ireland 2nd ed 657 2004 nom inval descr angl
Dicranellaceae Stech stat nov
Based on Dicranaceae subfam Dicranelloideae Lindb Utkast Eur Bladmoss 33 1878[lsquoUnderfamilje Dicranelleaersquo]
TYPUS Dicranella (MuumlllHal) Schimp Coroll Bryol Eur 13 1856
Oncophoraceae Stech stat nov
Based on Dicranaceae subfam Oncophoroideae Lindb Utkast Eur Bladmoss 34 1878[lsquoUnderfamilje Oncophoreaersquo]
TYPUS Oncophorus (Brid) Brid Bryol Univ 1 389 1826
Hypodontiaceae Stech fam nov
Plantae robustae characteribus morphologicis Pottiaceis et Calymperaceis similes sedcharacteribus molecularicis separatae Bracteae perichaetiales internae e basi vaginantes subulataevel aristatae Capsula aspectu succulenta cellulae exothecii incrassatae annulus magnopereabsens Peristomii dentes breves triangulati incurvati aurantiaci leves vel infirme verrucosiCalyptra cucullata
TYPUS Hypodontium MuumlllHal Hedwigia 38 96 1899
Helicophyllales Stech amp WFrey ord nov
Plantae acrocarpae prostratae tomentosae Folia dimorpha in duas series laterales et unam seriemventralem divisa Costa percurrens Cellulae hexagonae ad subquadratae papillosae Capsula immersacupulata ad oblonga infra orificium abrupte incurvata stomata destituta Peristomium nullum Sporaeisomorphae heteropolares granulatae
TYPUS Helicophyllum Brid Bryol Univ 2 771 1827
Synopsis of the suprageneric classification of BryophytaAuthor citations are in accordance with Art 492 of the Vienna Code (McNeill et al 2006)
Subdivision Takakiophytina Stech amp WFreyClass Takakiopsida Stech amp WFrey
Order Takakiales Stech amp WFreyTakakiaceae Stech amp WFrey
Subdivision Sphagnophytina DoweldClass Sphagnopsida Schimp
Order Sphagnales Limpr
15
Sphagnaceae DumortOrder Ambuchananiales Seppelt amp HACrum
Ambuchananiaceae Seppelt amp HACrumSubdivision Bryophytina Engler
Class Andreaeopsida JHSchaffnSubclass Andreaeidae Engl
Order Andreaeales LimprAndreaeaceae Dumort
Subclass Andreaeobryidae OchyraOrder Andreaeobryales BMMurray
Andreaeobryaceae Steere amp BMMurrayClass Oedipodiopsida Goffinet amp WRBuck
Order Oedipodiales Goffinet amp WRBuckOedipodiaceae Schimp
Class Tetraphidopsida Goffinet amp WRBuckOrder Tetraphidales MFleisch
Tetraphidaceae SchimpClass Polytrichopsida Doweld
Order Polytrichales MFleischPolytrichaceae Schwaumlgr
Class Bryopsida PaxSubclass Buxbaumiidae Doweld
Order Buxbaumiales MFleischBuxbaumiaceae Schimp
Subclass Diphysciidae OchyraOrder Diphysciales MFleisch
Diphysciaceae MFleischSubclass Timmiidae Ochyra
Order Timmiales OchyraTimmiaceae Schimp
Subclass Encalyptidae Ochyra Żarnowiec amp Bednarek-OchyraOrder Encalyptales Dixon
Encalyptaceae SchimpSubclass Funariidae Ochyra
Order Funariales MFleischFunariaceae Schwaumlgr Disceliaceae Schimp
Subclass Gigaspermidae Stech amp WFreyOrder Gigaspermales Goffinet Wickett OWerner Ros AJShaw amp CJCox
Gigaspermaceae LindbSubclass Dicranidae Doweld
Order Catoscopiales Ignatov amp IgnatovaCatoscopiaceae Broth
Order Scouleriales Goffinet amp WRBuckDrummondiaceae Goffinet Scouleriaceae SPChurchill
Order Bryoxiphiales HACrum amp LEAndersonBryoxiphiaceae Besch
16
Order Grimmiales MFleischGrimmiaceae Arn Ptychomitriaceae Schimp Seligeriaceae Schimp
Order Archidiales LimprArchidiaceae Schimp
Order Mitteniales ShawMitteniaceae Broth
Order Dicranales HPhilib ex MFleischAmphidiaceae Stech Aongstroemiaceae De Not BruchiaceaeSchimp Calymperaceae Kindb Dicranaceae Schimp Dicranel-laceae Stech Ditrichaceae Limpr Erpodiaceae Broth EustichiaceaeBroth Fissidentaceae Schimp Leucobryaceae Schimp Onco-phoraceae Stech Rhachitheciaceae HRob Schistostegaceae SchimpViridivelleraceae IGStone Wardiaceae Welch
Order Pottiales MFleischEphemeraceae Schimp Hypodontiaceae Stech PleurophascaceaeBroth Pottiaceae Schimp Serpotortellaceae WDReese amp RHZander
Subclass Bryidae EnglOrder Hedwigiales Ochyra
Hedwigiaceae Schimp Rhacocarpaceae KindbOrder Helicophyllales Stech amp WFrey
Helicophyllaceae BrothOrder Bartramiales DQuandt NEBell amp Stech
Bartramiaceae SchwaumlgrOrder Splachnales Ochyra
Meesiaceae Schimp Splachnaceae Grev amp ArnOrder Bryales Limpr
Bryaceae Schwaumlgr Leptostomataceae Schwaumlgr Mniaceae SchwaumlgrPhyllodrepaniaceae Crosby Pseudoditrichaceae Steere amp ZIwatsPulchrinodaceae DQuandt NEBell amp Stech
Order Orthotrichales DixonOrthotrichaceae Arn
Order Orthodontiales NEBell AENewton amp DQuandtOrthodontiaceae Goffinet
Order Aulacomniales NEBell AENewton amp DQuandtAulacomniaceae Schimp
Order Rhizogoniales Goffinet amp WRBuckRhizogoniaceae Broth
Order Hypnodendrales NEBell AENewton amp DQuandtBraithwaiteaceae NEBell AENewton amp DQuandt Hypnodendra-ceae Broth Pterobryellaceae WRBuck amp Vitt Racopilaceae Kindb
Order Ptychomniales WRBuck CJCox AJShaw amp GoffinetPtychomniaceae MFleisch
Order Hookeriales MFleischDaltoniaceae Schimp Hookeriaceae Schimp HypopterygiaceaeMitt Leucomiaceae Broth Pilotrichaceae Kindb SaulomataceaeWRBuck CJCox AJShaw amp Goffinet Schimperobryaceae WR
17
Buck CJCox AJShaw amp GoffinetOrder Hypnales WRBuck amp Vitt
Amblystegiaceae GRoth Anomodontaceae Kindb BrachytheciaceaeSchimp Calliergonaceae Vanderpoorten Hedenaumls CJCox amp AJShaw Catagoniaceae WRBuck amp Ireland Climaciaceae KindbCryphaeaceae Schimp Echinodiaceae Broth Entodontaceae KindbFabroniaceae Schimp Fontinalaceae Schimp Helodiaceae OchyraHeterocladiaceae Ignatov amp Ignatova Hylocomiaceae MFleischHypnaceae Schimp Lembophyllaceae Broth LeptodontaceaeSchimp Lepyrodontaceae Broth Leskeaceae Schimp Leucodon-taceae Schimp Meteoriaceae Kindb Microtheciellaceae HAMillamp AJHarr Myriniaceae Schimp Myuriaceae MFleisch NeckeraceaeSchimp Orthorrhynchiaceae SHLin Phyllogoniaceae KindbPlagiotheciaceae MFleisch Pleuroziopsidaceae Ireland Prionodon-taceae Broth Pseudoleskeaceae Schimp PseudoleskeellaceaeIgnatov amp Ignatova Pterigynandraceae Schimp PterobryaceaeKindb Pylaisiaceae Schimp Pylaisiadelphaceae Goffinet amp WRBuck Regmatodontaceae Broth Rhytidiaceae Broth RigodiaceaeHACrum Rutenbergiaceae MFleisch Scorpidiaceae Ignatov ampIgnatova Sematophyllaceae Broth Sorapillaceae MFleisch Ste-reophyllaceae WRBuck amp Ireland Symphyodontaceae MFleischTheliaceae MFleisch Thuidiaceae Schimp TrachylomataceaeWRBuck amp Vitt
Acknowledgements
Sincere thanks are due to JLReveal (Ithaca) as well as WFPrudhomme van Reine and JFVeldkamp(Leiden) for comments and discussions about suprafamilial taxonomy to DQuandt (Dresden) for providingDNA from Rhacocarpus and Bartramiaceae species and to BGiesicke (Berlin) for technical assistance
References
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BELL NE amp AE NEWTON (2007) Pleurocarpy in the Rhizogoniaceous grade - In NEWTONAE amp RS TANGNEY (eds) Pleurocarpous mosses systematics and evolution SystematicsAssociation Special Volume Series 71 41-64
BELL NE D QUANDT TJ OBRIEN amp AE NEWTON (2007) Taxonomy and phylogeny inthe earliest diverging pleurocarps square holes and bifurcating pegs - Bryologist 110 533-560
BORSCH T KW HILU D QUANDT V WILDE C NEINHUIS amp W BARTHLOTT(2003) Non-coding plastid trnT-trnF sequences reveal a well resolved phylogeny of basal angiosperms- J Evol Biol 16 558-576
18
BUCK WR (2007) The history of pleurocarp classification two steps forward one step back - InNEWTON AE amp RS TANGNEY (eds) Pleurocarpous mosses systematics and evolutionSystematics Association Special Volume Series 71 1-18
BUCK WR amp B GOFFINET (2000) Morphology and classification of mosses - In SHAWAJ amp B GOFFINET (eds) Bryophyte Biology pp 71-123 Cambridge University PressCambridge
CHIANG TY BA SCHAAL amp CI PENG (1998) Universal primers for amplification andsequencing a noncoding spacer between atpB and rbcL genes of chloroplast DNA - Bot Bull AcadSin 39 245-250
COX CJ B GOFFINET AE NEWTON AJ SHAW amp TAJ HEDDERSON (2000)Phylogenetic relationships among the diplolepideous-alternate mosses (Bryidae) inferred from nuclearand chloroplast DNA sequences - Bryologist 103 224-241
COX CJ B GOFFINET AJ SHAW amp SB BOLES (2004) Phylogenetic relationships amongthe mosses based on heterogeneous Bayesian analysis of multiple genes from multiple genomiccompartments - Syst Bot 29 234-250
CRANDALL-STOTLER B (1986) Morphogenesis developmental anatomy and bryophytephylogenetics contra-indications of monophyly - J Bryol 14 1-23
CROSBY MR RE MAGILL B ALLEN amp S HE (1999) A checklist of the mosses - MissouriBotanical Garden St Louis Missouri
DOWELD A (2001) Prosyllabus Tracheophytorum - GEOS Moscow i-lxxx + 110 pp
DOYLE JJ amp JL DOYLE (1990) Isolation of plant DNA from fresh tissue - Focus 12 13-15
DUFF RJ JC VILLAREAL DC CARGILL amp KS RENZAGLIA (2007) Progress andchallenges towards developing a phylogeny and classification of the hornworts - Bryologist 110214-243
FLEISCHER M (1920) Natuumlrliches System der Laubmoose - Hedwigia 61 390-400
FORREST LL EC DAVIS DG LONG BJ CRANDALL-STOTLER A CLARK ampML HOLLINGSWORTH (2006) Unraveling the evolutionary history of the liverworts (Marchantio-phyta) multiple taxa genomes and analyses - Bryologist 109 303-334
FRAHM J-P amp W FREY (1987) Moosflora 2 Aufl - UTB 1250 Stuttgart
FREY W (1977) Neue Vorstellungen uumlber die Verwandtschaftsgruppen und die Stammesgeschichteder Laubmoose - In FREY W H HURKA amp F OBERWINKLER (Hrsg) Beitraumlge zur Biologieder Pflanzen pp 117-139 Stuttgart
FREY W amp M STECH (2005) A morpho-molecular classification of the liverworts (Hepa-ticophytina Bryophyta) - Nova Hedwigia 81 55-78
FREY W M STECH amp K MEIszligNER (1999) Chloroplast DNA-relationship in palaeoaustralLopidium concinnum (Hypopterygiaceae Musci) An example of steno-evolution in mosses Studiesin austral temperate rain forest bryophytes 2 - Plant Syst Evol 218 67-75
GOFFINET B amp WR BUCK (2004) Systematics of Bryophyta (mosses) from molecules to arevised classification - In GOFFINET B V HOLLOWELL amp R MAGILL (eds) Molecularsystematics of bryophytes Monogr Syst Bot Missouri Bot Gard 98 205-239
GOFFINET B CJ COX AJ SHAW amp TAJ HEDDERSON (2001) The Bryophyta (mosses)Systematic and evolutionary inferences from an rps4 gene (cpDNA) phylogeny - Ann Bot 87191-208
GOFFINET B NJ WICKETT O WERNER RM ROS AJ SHAW amp CJ COX (2007)Distribution and phylogenetic significance of the 71-kb inversion in the plastid genome in Funariidae(Bryophyta) - Ann Bot 99 747-753
19
GROTH-MALONEK M D PRUCHNER F GREWE amp V KNOOP (2005) Ancestors oftrans-splicing mitochondrial introns support serial sister group relationships of hornworts and mosseswith vascular plants - Mol Biol Evol 22 117-125
HATTORI S amp H INOUE (1958) Preliminary report on Takakia lepidozioides - J Hattori BotLab 19 133-137
HE-NYGREacuteN X A JUSLEacuteN I AHONEN D GLENNY amp S PIIPPO (2006) Illuminating theevolutionary history of liverworts (Marchantiophyta) - towards a natural classification - Cladistics22 1-31
HEDDERSON TAJ DJ MURRAY CJ COX amp TL NOWELL (2004) Phylogeneticrelationships of haplolepideous mosses (Dicranidae) inferred from rps4 gene sequences - Syst Bot29 29-41
LA FARGE C BD MISHER JA WHEELER DP WALL K JOHANNES S SCHAFFERamp AJ SHAW (2000) Phylogenetic relationships within the haplolepideous mosses - Bryologist103 257-276
LA FARGE C AJ SHAW amp DH VITT (2002) The circumscription of the Dicranaceae(Bryopsida) based on the chloroplast regions trnL-trnF and rps4 - Syst Bot 27 435-452
MAGOMBO ZLK (2003) The phylogeny of basal peristomate mosses evidence from cpDNAand implications for peristome evolution - Syst Bot 28 24-38
MCNEILL J FR BARRIE HM BURDET V DEMOULIN DL HAWKSWORTHK MARHOLD DH NICOLSON J PRADO PC SILVA JE SKOG JH WIERSEMA ampNJ TURLAND (2006) International Code of Botanical Nomenclature (Vienna Code) - RegnumVegetabile 146 1-568
MUumlLLER K (2004) PRAP - computation of Bremer support for large data sets - Mol PhylogenetEvol 31 780-782
MUumlLLER K (2005) SeqState - primer design and sequence statistics for phylogenetic DNA datasets - Appl Bioinformatics 4 65-69
MUumlLLER K D QUANDT J MUumlLLER amp C NEINHUIS (2005) PhyDE v0992 PhylogeneticData Editor - httpwwwphydede
MURRAY BM (1988) Systematics of the Andreaeopsida (Bryophyta) two orders with links toTakakia - Nova Hedwigia Beih 90 289-336
NEWTON AE amp RS TANGNEY (eds) (2007) Pleurocarpous mosses systematics and evolutionSystematics Association Special Volume Series 71 CRC Press Boca Raton 434 pp
NEWTON AE CJ COX JG DUCKETT JA WHEELER B GOFFINET TAJ HEDDER-SON amp BD MISHLER (2000) Evolution of the major moss lineages Phylogenetic analyses basedon multiple gene sequences and morphology - Bryologist 103 187-211
NEWTON AE N WIKSTROumlM NE BELL LL FORREST amp MS IGNATOV (2007)Dating the diversification of the pleurocarpous mosses - In NEWTON AE amp RS TANGNEY(eds) Pleurocarpous mosses systematics and evolution Systematics Association Special VolumeSeries 71 337-366
NIXON KC (1999) The parsimony ratchet a new method for rapid parsimony analysis - Cladistics15 407-411
OBRIEN TJ (2007) The phylogenetic distribution of pleurocarpous mosses evidence fromcpDNA sequences - In NEWTON AE amp RS TANGNEY (eds) Pleurocarpous mossessystematics and evolution Systematics Association Special Volume Series 71 19-41
OCHYRA R (2002) Nomenclatural changes in subfamilies of the Dicranaceae - CryptogamieBryol 23 345-349
20
OCHYRA R J ŻARNOWIEC amp H BEDNAREK-OCHYRA (2003) Census catalogue ofPolish mosses - Biodiv Poland 3 1-372
PEDERSEN N amp AE NEWTON (2007) Phylogenetic and morphological studies within thePtychomniales with emphasis on the evolution of dwarf males - In NEWTON AE amp RSTANGNEY (eds) Pleurocarpous mosses systematics and evolution Systematics AssociationSpecial Volume Series 71 367-392
QUANDT D amp M STECH (2005) Molecular evolution and secondary structure of the chloroplasttrnL intron in bryophytes - Mol Phylogenet Evol 36 429-443
QUANDT D K MUumlLLER amp S HUTTUNEN (2003) Characterisation of the chloroplast DNApsbT-H region and the influence of dyad symmetrical elements on phylogenetic reconstructions -Plant Biol 5 400-410
QUANDT D K MUumlLLER M STECH W FREY KW HILU amp T BORSCH (2004) Molecularevolution of the chloroplast trnL-F-region in land plants - In GOFFINET B V HOLLOWELL ampR MAGILL (eds) Molecular systematics of bryophytes Monogr Syst Bot Missouri Bot Gard98 13-37
QUANDT D NE BELL amp M STECH (2007) Unravelling the knot the Pulchrinodaceae famnov (Bryales) - In KUumlRSCHNER H T PFEIFFER amp M STECH (eds) A Festschrift to Wolf-gang Frey - a scientists life between deserts and rain forests Nova Hedwigia Beih 131 21-39
QIU Y-L Y CHO JC COX amp JD PALMER (1998) The gain of three mitochondrial intronsidentifies liverworts as the earliest land plants - Nature 394 671-674
QIU Y-L L LI B WANG Z CHEN V KNOOP M GROTH-MALONEK O DOM-BROVSKA J LEE L KENT J REST GF ESTABROOK TA HENDRY DW TAYLORCM TESTA M AMBROS B CRANDALL-STOTLER J DUFF M STECH W FREYD QUANDT amp CC DAVIS (2006) The deepest divergences in land plants inferred fromphylogenomic evidence - Proc Natl Acad Sci USA 103 15511-15516
RENZAGLIA KS S SCHUETTE RJ DUFF R LIGRONE AJ SHAW BD MISHLER ampJG DUCKETT (2007) Bryophyte phylogeny Advancing the molecular and morphological frontiers- Bryologist 110 179-213
SAMIGULLIN TH SP YACENTYUK GV DEGTYARYEVA KM VALIEJO-ROMANVK BOBROVA I CAPESIUS WF MARTIN AV TROITSKY VR FILIN amp ASANTONOV (2002) Paraphyly of bryophytes and close relationships of hornworts and vascularplants inferred from analysis of chloroplast rDNA ITS (cpITS) sequences - Arctoa 11 31-43
SANG T DJ CRAWFORD amp TF STUESSY (1997) Chloroplast DNA phylogeny reticulateevolution and biogeography of Paeonia (Paeoniaceae) - Amer J Bot 84 1120-1136
SHAW AJ amp KS RENZAGLIA (2004) Phylogeny and diversification of bryophytes - AmerJ Bot 91 1557-1581
SHAW AJ CJ COX amp B GOFFINET (2005) Global patterns of moss diversity taxonomic andmolecular inferences - Taxon 54 337-352
STECH M (1999a) A reclassification of Dicranaceae (Bryopsida) based on non-coding cpDNAsequence data - J Hattori Bot Lab 86 137-159
STECH M (1999b) A molecular systematic contribution to the position of Amphidium Schimp(Rhabdoweisiaceae Bryopsida) - Nova Hedwigia 68 291-300
STECH M (2004) Supraspecific circumscription and classification of Campylopus Brid(Dicranaceae Bryopsida) based on molecular data - Syst Bot 29 817-824
STECH M amp D QUANDT (2006) Molecular evolution of the chloroplast atpB-rbcL spacer inbryophytes - In SHARMA AK amp A SHARMA (eds) Plant Genome Biodiversity and EvolutionVol 2 Part B pp 409-431 Science Publishers Enfield New Hampshire
21
STECH M D QUANDT amp W FREY (2003) Molecular circumscription of the hornworts(Antho-cerotophyta) based on the chloroplast DNA trnL-trnF region - J Plant Res 116 389-398
STOTLER RE amp B CRANDALL-STOTLER (2005) A revised classification of theAnthocerotophyta and a checklist of the hornworts of North America north of Mexico - Bryologist108 16-26
SWOFFORD DL (2002) PAUP Phylogenetic analysis using parsimony (and other methods)version 40b10 - Sunderland MA
TABERLET P L GIELLY G PAUTOU amp J BOUVET (1991) Universal primers for amplificationof three non-coding regions of chloroplast DNA - Plant Mol Biol 17 1105-1109
TSUBOTA H Y AGENO B ESTEacuteBANEZ T YAMAGUCHI amp H DEGUCHI (2003)Molecular phylogeny of the Grimmiales (Musci) based on chloroplast rbcL sequences - Hikobia 1455-70
TSUBOTA H E DE LUNA D GONZAacuteLEZ MS IGNATOV amp H DEGUCHI (2004) Molecularphylogenetics and ordinal relationships based on analyses of a large-scale data set of 600 rbcLsequences of mosses - Hikobia 14 149-170
VITT DH (1984) Classification of the Bryopsida - In SCHUSTER RM (ed) New Manual ofBryology 2 696-759 Hattori Botanical Laboratory Nichinan Japan
VITT DH B GOFFINET amp T HEDDERSON (1998) 8 The ordinal classification of the mossesquestions and answers for the 1990s - In BATES JW NW ASHTON amp JG DUCKETT (eds)Bryology for the twenty-first century British Bryol Soc pp 113-123
Received 3 September 2007 accepted in revised form 30 October 2007
8
Andreaeobryum macrosporum Steere amp BMMurray and possible relationships withAndreaea and Takakia were discussed by Murray (1988) and summarised includingmolecular results by Shaw amp Renzaglia (2004)
On the next lower level a number of morphologically and molecularly divergentlineages are nowadays treated as subclasses of Bryopsida Buxbaumiidae andDiphysciidae are generally branching off first in molecular topologies (eg Beckertet al 2001 Magombo 2003 Cox et al 2004) followed by Timmiidae Encalyptidaeand Funariidae as well as Dicranidae (haplolepideous mosses) sister to Bryidae slThese subclasses (except Buxbaumiidae not included) are also well recognizable inthe present analysis of non-coding plastid sequences (Fig 1)
The morphologically very different Encalyptidae and Funariidae are revealed assister groups although mostly without high support in several molecular phylogenies(eg Goffinet et al 2001 Cox et al 2004 Hedderson et al 2004 Tsubota et al2003 2004) and also in the present study (Fig 1) Goffinet et al (2007) confirmedthis relationship by phylogenomic evidence namely a large (71 kb) inversion in thechloroplast genome of Funariaceae Disceliaceae and Encalyptaceae but not inGigaspermaceae Consequently the latter family was separated at ordinal level fromthe two remaining families of Funariales by Goffinet et al (2007) GigaspermalesFunariales and Encalyptales may share a common ancestor according to some butnot all molecular phylogenies (eg Goffinet et al 2001 2007 Hedderson et al2004 but not in Tsubota et al 2004) Although ontogenetic data from peristomedevelopment may support their common ancestry (Goffinet et al 2007) unambiguousmorphological synapomorphies are lacking We therefore propose to treatGigaspermaceae at subclass level within the Bryopsida (see taxonomy)
The haplolepideous mosses (Dicranidae) are clearly supported as a monophyleticlineage which obviously evolved from a diplolepideous ancestor according to theirposition in the molecular trees (eg Newton et al 2000 Tsubota et al 2003 Cox etal 2004 Goffinet amp Buck 2004) Molecular studies suitable for inferring ordinaland family level relationships within Dicranidae either focused on the haplolepideousmosses (eg Stech 1999ab 2004 LaFarge et al 2000 2002 Tsubota et al 2003Hedderson et al 2004) or included more than 15 haplolepideous taxa in analyses ofa broader range of mosses (eg Goffinet et al 2001 Tsubota et al 2004 this study)Major lineages supported by these analyses are for example Grimmiales(Grimmiaceae Ptychomitriaceae and Seligeriaceae) Leucobryaceae (incl formerDicranaceae-Campylopoideae and Paraleucobryoideae pp) Dicranaceae sstr(Dicranoideae plus former Dicnemonaceae and Paraleucobryoideae pp) Pottiaceae(incl Cinclidotaceae and Splachnobryum) and Calymperaceae (probably exclOctoblepharum) Furthermore several genera and families belong to Dicranidaewhose systematic positions have been controversial (eg Stech et al 1999b LaFarge et al 2002 Hedderson et al 2004 OBrien 2007 Quandt et al 2007 thisstudy) Amphidium Archidium Catoscopium Drummondia EphemeraceaeErpodiaceae Mittenia (cf OBrien 2007 sequences in some earlier analyses werebased on misdentified specimens) Rhachitheciaceae Schistostega Splachnobryumand Wardia On the contrary several problems remain such as the circumscriptionof Ditrichaceae and relationships of the major haplolepideous lineages in general
9
Fig 1 Strict consensus tree of 129 most parsimonious trees inferred from combined trnLUAA
intronatpB-rbcL spacer and psbA-trnH spacer sequences of 85 taxa of Bryopsida as well as Andreaearupestris (Andreaeopsida) and Pogonatum subulatum (Polytrichopsida) as outgroup representativesBootstrap support values gt50 are depicted above the branches
10
Consequently resolving the phylogeny of Dicranidae with confidence is one of themajor future challenges in moss systematics
As mentioned above Dicranaceae are monophyletic in a narrow circumscriptionaccording to molecular data In contrast to former Campylopoideae andParaleucobryoideae the status of Rhabdoweisioideae (= Oncophoroideae Ochyra2002) and Dicranelloideae needs further consideration Stech (1999ab) suggestedto recognise RhabdoweisioideaeRhabdoweisiaceae in a broad sense includingDicranoweisia Amphidium and Aongstroemia Subsequent molecular analysesconfirmed a close relationship of the genera Arctoa Cynodontium DicranoweisiaKiaeria Oncophorus Oreoweisia Oreas Rhabdoweisia and Symblepharis althoughwithout significant support (La Farge et al 2002 Tsubota et al 2003 Hedderson etal 2004) With respect to the molecular evidence available so far we propose toelevate Oncophoroideae to family level to accomodate these genera and perhapsGlyphomitrium (cf Tsubota et al 2003) whereas we consider AongstroemiaDichodontium and Diobelonella to belong to Aongstroemiaceae (cf Stech 1999a)Amphidium is neither closely related to Dicranaceae sstr nor to Oncophoroideae(La Farge et al 2002 Tsubota et al 2003 Hedderson et al 2004 Stech 2004 thisstudy) and should be treated at family level rather than placed in Dicranaceae assubfam Amphidioideae (Ochyra et al 2003) The circumscription of Dicranelloideaeis more difficult to evaluate as few representatives have been included in molecularanalyses However Dicranella heteromalla (Hedw) Schimp as well as the generaCampylopodium and Microcampylopus are clearly separated from Dicranaceae sstr(Stech 1999a 2004 La Farge et al 2002 Tsubota et al 2003 Hedderson et al2004) and consequently the subfamily deserves family status as well Finallymolecular data showed that the genus Hypodontium does not belong to Pottiaceae(Hedderson et al 2004 Tsubota et al 2004) Taxonomic conclusions have not beendrawn from these results which is made up here (see taxonomy)
All mosses with diplolepideous-alternate peristomes together with Splachnales witha diplolepideous-opposite (Funaria-type) peristome form a monophyletic group inmolecular analyses (eg Newton et al 2000 Beckert et al 2001 Goffinet et al2001 Cox et al 2004 Tsubota et al 2004 references in Table 2) Differentclassifications of this by far most species-rich group of mosses were proposed (egVitt et al 1998 Ochyra et al 2003 Goffinet amp Buck 2004) However at least someof the recognised subclasses and superorders are paraphyletic according to themolecular topologies and assigning formal ranks to all evolutionarily significantmonophyletic entities is problematic if the main taxonomic framework of Bryophytaand Bryopsida should be maintained (cf discussion in Bell et al 2007) Thereforein the present synopsis only one subclass Bryidae is recognised for all diplolepideous-alternate mosses and Splachnales This broadly defined Bryidae is subdivided into13 orders most of them resolved as monophyletic in the majority of the phylogeneticanalyses summarised in Table 2 although with different levels of statistical supportin maximum parsimony analyses To define monophyletic lineages at supraordinallevel informal node-based names may be chosen according to Bell et al (2007) Forexample the pleurocarpous mosses (pleurocarpy sensu Bell amp Newton 2007) andtheir closest acrocarpous relatives (Orthodontiales to Hypnales) were already
11
Table 2 Taxon sampling and bootstrap support (BS) for Dicranidae Bryidae and orders within theBryidae in recent phylogenetic analyses (MP only) based on combined molecular markers Markersare given in square brackets (non-coding regions in bold) numbers of included taxa in brackets ++respective clade present with ge 80 BS + clade present with lt 80 BS - clade not present no oronly one representative included
Bell amp Newton OBrien Quandt et al Bell et al this study(2004) (2007) (2007) (2007)
[rbcL rps4 [atpB atpB- [rbcL rps4 [rbcL rps4 [atpB-rbcLnad5] rbcL rbcL trnL-F nad5] trnL-F nad5] psbA-trnH
rps4 trnL-F] trnL]
Dicranidae + (2) + (4) ++ (3) (1) ++ (19)Bryidae ++ (57) + (53) ++ (52) ++ (98) ++ (58)Hedwigiales ++ (2) (1) ++ (2) ++ (2) - (3)Bartramiales ++ (2) ++ (4) ++ (4) ++ (3) - (4)Splachnales (0) ++ (2) ++ (3) ++ (2) ++ (5)Bryales - (4) - (5) ++ (18) + (17) - (8)Orthotrichales (1) ++ (3) ++ (3) ++ (2) ++ (4)Orthodontiales + (4) + (4) + (3) + (6) - (3)Aulacomniales + (6) + (7) ++ (2) + (7) + (3)Rhizogoniales ++ (13) + (8) ++ (5) ++ (14) - (3)Hypnodendrales ++ (13) + (7) ++ (4) ++ (29) ++ (6)Ptychomniales ++ (3) ++ (3) (1) ++ (4) (1)Hookeriales - (4) + (2) (1) + (2) + (8)Hypnales - (5) - (7) ++ (5) ++ (10) + (10)
summarised under the informal node based name pleurcarpids (Bell et al 2007)and can be distinguished from a basal grade of acrocarpous or cladocarpous lineages(Hedwigiales to Orthotrichales) Within the latter monophyly of BartramialesSplachnales and Orthotrichales is well-supported in all analyses including two ormore taxa except Bartramiales in the present data set (cf Fig 1) In contrast Bryalesreceive significant support less frequently (but see Bell et al 2007 Quandt et al2007) Hedwigiales are well supported if only Hedwigia (Hedwigiaceae) andRhacocarpus (Rhacocarpaceae) are included whereas the monospecific Helicophyllum(Helicophyllaceae) is not closely related to these taxa but shows affinities withBartramiales (Goffinet et al 2001 this study) With respect to the differentmorphologies of Helicophyllaceae and Bartramiaceae however the former shouldbe separated at ordinal level (see taxonomy)
Clarifying relationships of the Orthotrichales is still a difficult issue Analyses ofsingle chloroplast markers or parsimony analyses of combined markers from differentgenomes mostly indicated a close relationship either with Splachnales (eg Cox etal 2000 Newton et al 2000 Tsubota et al 2004 Quandt et al 2007) or with thepleurocarpids (Goffinet et al 2001 this study) Although none of these alternativesis well-supported the latter seems more likely with regard to the moderately tomaximally supported Orthotrichales - pleurocarpid sister group relationship in allanalyses of mitochondrial data and in likelihood analyses of combined plastidmitochondrial markers (Beckert et al 2001 Quandt et al 2007)
12
The molecular polyphyly of Rhizogoniaceae (eg Bell amp Newton 2004) was solvedby the transfer of rhizogonioid genera into broadly defined Aulacomniaceae andOrthodontiaceae (Bell et al 2007) which now include both acrocarpous andpleurocarpous taxa These systematic changes are also comprehensible by non-molecular characters such as morphological traits shared by Mesochaete andAulacomnium heterostichum (Hedw) Bruch amp Schimp or the variously reducedperistomes of Orthodontiaceae pp in contrast to the generally fully developed Bryum-type peristomes of rhizogonioid and hypnodendroid mosses (Bell et al 2007) Theposition of the solely pleurocarpous Hypnodendrales sister to the former Hypnidaeled to the recognition of the informal group core pleurocarps (Bell et al 2007)The former Hypnidae (Ptychomniales Hookeriales and Hypnales summarised ashomocostate pleurocarps) are monophyletic in most molecular analyses (eg Goffinetet al 2001 Tsubota et al 2004 Bell et al 2007) with Ptychomniales being well-supported (Pedersen amp Newton 2007 Table 2) Clarifying relationships betweenHookeriales and Hypnales and within the latter is still a challenge but recent molecularstudies seem to support a sister group relationship of both orders (Bell et al 2007present study)
Phylogenetic utility of non-coding plastid markers
Non-coding plastid markers that comprise both variable and conserved regionssuch as the trnL
UAA intron have repeatedly been shown to possess potential for
resolving relationships at high taxonomic levels (eg Borsch et al 2003 Quandtet al 2004) Both the trnL intron and atpB-rbcL spacer were characterised indetail in mosses with respect to their structure and molecular evolution (Quandt ampStech 2005 Stech amp Quandt 2006) They include conservative regions that can beunambiguosly aligned and even parts of the more variable regions can be used ifrepeats hairpin loops etc are correctly identified and adequately treated in thephylogenetic analyses (eg Quandt et al 2003 Quandt amp Stech 2005) Using theatpB-rbcL spacer alone (Stech amp Quandt 2006) relationships of the major mosslineages were largely consistent with the ldquototal evidencerdquo molecular tree of Goffinetamp Buck (2004) However in addition to general limitations that result from singlemarker analyses the use of non-coding markers may pose further problems suchas a high amount of homoplasy resulting in low resolution or low statistical supportfor many clades Therefore several recent molecular studies of relationships withinBryidae have employed both coding and non-coding markers (Table 2)Nevertheless the usefulness of analyses of combined non-coding plastid markerscannot be ruled out In fact Fig 1 and Table 2 indicate a phylogenetic signal inthe present data set as many clades are recovered that are usually also resolvedin analyses of coding or combined coding and non-coding markers Especiallywith regard to statistical support however the present analysis is inferior tothose of other recent data sets especially Bell et al (2007) and Quandt et al(2007) In addition the non-coding markers used here are of different suitabilityand even the two intergenic spacers differ considerably from each other ThepsbA-trnH spacer contributes much less to the trees resolution than the atpB-rbcL spacer first because it is much shorter and second because relatively largeparts are attributed to hairpin loops or otherwise hypervariable regions These
13
results indicate that future studies should evaluate the molecular evolution andphylogenetic potential of new markers both coding and con-coding and choosethe most suitable ones in a combined analysis to resolve the remaining uncertaintiesin moss phylogeny
Taxonomy
Takakiaceae Stech amp WFrey stat nov
Plantae virides nusquam rhizophorae sine protonemate e caudicis rhizomatis erectae Caudicesrhizomati et axes geotropi radiformes frequenter intercalariter ramificantes sine phyllidiis cumpapillis mucilaginis rostratis Caules phyllidiiferi saepe furcati Phyllidia sine lamina et costadistincta profunde 2-4(-5)-lobata pluristratosa tristicha sed torsione spiraliter disposita Filumcentralium in ambabus generationibus (axibus gametophyti et setis) adest Plantae dioicae Antheridiaet archegonia nuda Sporophytum terminale solitarium Seta persistens Capsula tortilis admaturitatem schizocarpa secus unam rimam spiralem longitudinalem dehiscens Stomata etoperculum absunt peristomium nullum Calyptra mitriformis
TYPUS Takakia SHatt amp Inoue J Hattori Bot Lab 19 137 1958
Takakiaceae SHatt amp Inoue J Hattori Bot Lab 19 137 1958 nom inval (Art 411)
Takakiales Stech amp WFrey stat nov
Based on Takakiaceae Stech amp WFrey Nova Hedwigia 86 13 2008
TYPUS Takakia SHatt amp Inoue J Hattori Bot Lab 19 137 1958
Takakiales SHatt amp Inoue J Hattori Bot Lab 19 137 1958 nom inval
Takakiales SHatt amp Inoue ex RMSchust J Hattori Bot Lab 26 224 1963 nom inval (cumdescr latin)
Takakiopsida Stech amp WFrey statnov
Based on Takakiaceae Stech amp WFrey Nova Hedwigia 86 13 2008
TYPUS Takakia SHatt amp Inoue J Hattori Bot Lab 19 137 1958
Takakiopsida Goffinet amp WRBuck Monogr Syst Bot Missouri Bot Gard 98 232 2004 nominval
Takakiopsida Jia et al Acta Phytotax Sin 41 350 351 2003 nom nud
Takakiopsida Wang amp Wu Fl Bryophyt Sin 8 447 2004 nom inval (cum descr latin)
Takakiophytina Stech amp WFrey stat nov
Based on Takakiaceae Stech amp WFrey Nova Hedwigia 86 13 2008
TYPUS Takakia SHatt amp Inoue JHattori Bot Lab 19 137 1958
Gigaspermidae Stech amp WFrey subclass nov
Plantae acrocarpae terrestres stoloniferae ramis brevibus erectis Folia unicostata cellulis laxislaevibus Capsula plerumque valde rugosa gymnostomatica vel cleistocarpa stomata cum duabuscellulis sociis Ab Funariidis et Encalyptidis charactere phylogenomico (71-kb inversio abest)separatae
14
TYPUS Gigaspermum Lindb Oumlfversigt af Foumlrhandlingar Kongl Svenska Vetenskaps-Akademien21 599 1865
Amphidiaceae Stech stat nov
Based on Dicranaceae subfam Amphidioideae Ochyra in Ochyra Zarnowiec amp Bednarek-OchyraCens Cat Polish Mosses 110 2003
TYPUS Amphidium Schimp Coroll Bryol Eur 39 1856
Amphidiaceae AJESm Moss Fl Britain Ireland 2nd ed 657 2004 nom inval descr angl
Dicranellaceae Stech stat nov
Based on Dicranaceae subfam Dicranelloideae Lindb Utkast Eur Bladmoss 33 1878[lsquoUnderfamilje Dicranelleaersquo]
TYPUS Dicranella (MuumlllHal) Schimp Coroll Bryol Eur 13 1856
Oncophoraceae Stech stat nov
Based on Dicranaceae subfam Oncophoroideae Lindb Utkast Eur Bladmoss 34 1878[lsquoUnderfamilje Oncophoreaersquo]
TYPUS Oncophorus (Brid) Brid Bryol Univ 1 389 1826
Hypodontiaceae Stech fam nov
Plantae robustae characteribus morphologicis Pottiaceis et Calymperaceis similes sedcharacteribus molecularicis separatae Bracteae perichaetiales internae e basi vaginantes subulataevel aristatae Capsula aspectu succulenta cellulae exothecii incrassatae annulus magnopereabsens Peristomii dentes breves triangulati incurvati aurantiaci leves vel infirme verrucosiCalyptra cucullata
TYPUS Hypodontium MuumlllHal Hedwigia 38 96 1899
Helicophyllales Stech amp WFrey ord nov
Plantae acrocarpae prostratae tomentosae Folia dimorpha in duas series laterales et unam seriemventralem divisa Costa percurrens Cellulae hexagonae ad subquadratae papillosae Capsula immersacupulata ad oblonga infra orificium abrupte incurvata stomata destituta Peristomium nullum Sporaeisomorphae heteropolares granulatae
TYPUS Helicophyllum Brid Bryol Univ 2 771 1827
Synopsis of the suprageneric classification of BryophytaAuthor citations are in accordance with Art 492 of the Vienna Code (McNeill et al 2006)
Subdivision Takakiophytina Stech amp WFreyClass Takakiopsida Stech amp WFrey
Order Takakiales Stech amp WFreyTakakiaceae Stech amp WFrey
Subdivision Sphagnophytina DoweldClass Sphagnopsida Schimp
Order Sphagnales Limpr
15
Sphagnaceae DumortOrder Ambuchananiales Seppelt amp HACrum
Ambuchananiaceae Seppelt amp HACrumSubdivision Bryophytina Engler
Class Andreaeopsida JHSchaffnSubclass Andreaeidae Engl
Order Andreaeales LimprAndreaeaceae Dumort
Subclass Andreaeobryidae OchyraOrder Andreaeobryales BMMurray
Andreaeobryaceae Steere amp BMMurrayClass Oedipodiopsida Goffinet amp WRBuck
Order Oedipodiales Goffinet amp WRBuckOedipodiaceae Schimp
Class Tetraphidopsida Goffinet amp WRBuckOrder Tetraphidales MFleisch
Tetraphidaceae SchimpClass Polytrichopsida Doweld
Order Polytrichales MFleischPolytrichaceae Schwaumlgr
Class Bryopsida PaxSubclass Buxbaumiidae Doweld
Order Buxbaumiales MFleischBuxbaumiaceae Schimp
Subclass Diphysciidae OchyraOrder Diphysciales MFleisch
Diphysciaceae MFleischSubclass Timmiidae Ochyra
Order Timmiales OchyraTimmiaceae Schimp
Subclass Encalyptidae Ochyra Żarnowiec amp Bednarek-OchyraOrder Encalyptales Dixon
Encalyptaceae SchimpSubclass Funariidae Ochyra
Order Funariales MFleischFunariaceae Schwaumlgr Disceliaceae Schimp
Subclass Gigaspermidae Stech amp WFreyOrder Gigaspermales Goffinet Wickett OWerner Ros AJShaw amp CJCox
Gigaspermaceae LindbSubclass Dicranidae Doweld
Order Catoscopiales Ignatov amp IgnatovaCatoscopiaceae Broth
Order Scouleriales Goffinet amp WRBuckDrummondiaceae Goffinet Scouleriaceae SPChurchill
Order Bryoxiphiales HACrum amp LEAndersonBryoxiphiaceae Besch
16
Order Grimmiales MFleischGrimmiaceae Arn Ptychomitriaceae Schimp Seligeriaceae Schimp
Order Archidiales LimprArchidiaceae Schimp
Order Mitteniales ShawMitteniaceae Broth
Order Dicranales HPhilib ex MFleischAmphidiaceae Stech Aongstroemiaceae De Not BruchiaceaeSchimp Calymperaceae Kindb Dicranaceae Schimp Dicranel-laceae Stech Ditrichaceae Limpr Erpodiaceae Broth EustichiaceaeBroth Fissidentaceae Schimp Leucobryaceae Schimp Onco-phoraceae Stech Rhachitheciaceae HRob Schistostegaceae SchimpViridivelleraceae IGStone Wardiaceae Welch
Order Pottiales MFleischEphemeraceae Schimp Hypodontiaceae Stech PleurophascaceaeBroth Pottiaceae Schimp Serpotortellaceae WDReese amp RHZander
Subclass Bryidae EnglOrder Hedwigiales Ochyra
Hedwigiaceae Schimp Rhacocarpaceae KindbOrder Helicophyllales Stech amp WFrey
Helicophyllaceae BrothOrder Bartramiales DQuandt NEBell amp Stech
Bartramiaceae SchwaumlgrOrder Splachnales Ochyra
Meesiaceae Schimp Splachnaceae Grev amp ArnOrder Bryales Limpr
Bryaceae Schwaumlgr Leptostomataceae Schwaumlgr Mniaceae SchwaumlgrPhyllodrepaniaceae Crosby Pseudoditrichaceae Steere amp ZIwatsPulchrinodaceae DQuandt NEBell amp Stech
Order Orthotrichales DixonOrthotrichaceae Arn
Order Orthodontiales NEBell AENewton amp DQuandtOrthodontiaceae Goffinet
Order Aulacomniales NEBell AENewton amp DQuandtAulacomniaceae Schimp
Order Rhizogoniales Goffinet amp WRBuckRhizogoniaceae Broth
Order Hypnodendrales NEBell AENewton amp DQuandtBraithwaiteaceae NEBell AENewton amp DQuandt Hypnodendra-ceae Broth Pterobryellaceae WRBuck amp Vitt Racopilaceae Kindb
Order Ptychomniales WRBuck CJCox AJShaw amp GoffinetPtychomniaceae MFleisch
Order Hookeriales MFleischDaltoniaceae Schimp Hookeriaceae Schimp HypopterygiaceaeMitt Leucomiaceae Broth Pilotrichaceae Kindb SaulomataceaeWRBuck CJCox AJShaw amp Goffinet Schimperobryaceae WR
17
Buck CJCox AJShaw amp GoffinetOrder Hypnales WRBuck amp Vitt
Amblystegiaceae GRoth Anomodontaceae Kindb BrachytheciaceaeSchimp Calliergonaceae Vanderpoorten Hedenaumls CJCox amp AJShaw Catagoniaceae WRBuck amp Ireland Climaciaceae KindbCryphaeaceae Schimp Echinodiaceae Broth Entodontaceae KindbFabroniaceae Schimp Fontinalaceae Schimp Helodiaceae OchyraHeterocladiaceae Ignatov amp Ignatova Hylocomiaceae MFleischHypnaceae Schimp Lembophyllaceae Broth LeptodontaceaeSchimp Lepyrodontaceae Broth Leskeaceae Schimp Leucodon-taceae Schimp Meteoriaceae Kindb Microtheciellaceae HAMillamp AJHarr Myriniaceae Schimp Myuriaceae MFleisch NeckeraceaeSchimp Orthorrhynchiaceae SHLin Phyllogoniaceae KindbPlagiotheciaceae MFleisch Pleuroziopsidaceae Ireland Prionodon-taceae Broth Pseudoleskeaceae Schimp PseudoleskeellaceaeIgnatov amp Ignatova Pterigynandraceae Schimp PterobryaceaeKindb Pylaisiaceae Schimp Pylaisiadelphaceae Goffinet amp WRBuck Regmatodontaceae Broth Rhytidiaceae Broth RigodiaceaeHACrum Rutenbergiaceae MFleisch Scorpidiaceae Ignatov ampIgnatova Sematophyllaceae Broth Sorapillaceae MFleisch Ste-reophyllaceae WRBuck amp Ireland Symphyodontaceae MFleischTheliaceae MFleisch Thuidiaceae Schimp TrachylomataceaeWRBuck amp Vitt
Acknowledgements
Sincere thanks are due to JLReveal (Ithaca) as well as WFPrudhomme van Reine and JFVeldkamp(Leiden) for comments and discussions about suprafamilial taxonomy to DQuandt (Dresden) for providingDNA from Rhacocarpus and Bartramiaceae species and to BGiesicke (Berlin) for technical assistance
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18
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TABERLET P L GIELLY G PAUTOU amp J BOUVET (1991) Universal primers for amplificationof three non-coding regions of chloroplast DNA - Plant Mol Biol 17 1105-1109
TSUBOTA H Y AGENO B ESTEacuteBANEZ T YAMAGUCHI amp H DEGUCHI (2003)Molecular phylogeny of the Grimmiales (Musci) based on chloroplast rbcL sequences - Hikobia 1455-70
TSUBOTA H E DE LUNA D GONZAacuteLEZ MS IGNATOV amp H DEGUCHI (2004) Molecularphylogenetics and ordinal relationships based on analyses of a large-scale data set of 600 rbcLsequences of mosses - Hikobia 14 149-170
VITT DH (1984) Classification of the Bryopsida - In SCHUSTER RM (ed) New Manual ofBryology 2 696-759 Hattori Botanical Laboratory Nichinan Japan
VITT DH B GOFFINET amp T HEDDERSON (1998) 8 The ordinal classification of the mossesquestions and answers for the 1990s - In BATES JW NW ASHTON amp JG DUCKETT (eds)Bryology for the twenty-first century British Bryol Soc pp 113-123
Received 3 September 2007 accepted in revised form 30 October 2007
9
Fig 1 Strict consensus tree of 129 most parsimonious trees inferred from combined trnLUAA
intronatpB-rbcL spacer and psbA-trnH spacer sequences of 85 taxa of Bryopsida as well as Andreaearupestris (Andreaeopsida) and Pogonatum subulatum (Polytrichopsida) as outgroup representativesBootstrap support values gt50 are depicted above the branches
10
Consequently resolving the phylogeny of Dicranidae with confidence is one of themajor future challenges in moss systematics
As mentioned above Dicranaceae are monophyletic in a narrow circumscriptionaccording to molecular data In contrast to former Campylopoideae andParaleucobryoideae the status of Rhabdoweisioideae (= Oncophoroideae Ochyra2002) and Dicranelloideae needs further consideration Stech (1999ab) suggestedto recognise RhabdoweisioideaeRhabdoweisiaceae in a broad sense includingDicranoweisia Amphidium and Aongstroemia Subsequent molecular analysesconfirmed a close relationship of the genera Arctoa Cynodontium DicranoweisiaKiaeria Oncophorus Oreoweisia Oreas Rhabdoweisia and Symblepharis althoughwithout significant support (La Farge et al 2002 Tsubota et al 2003 Hedderson etal 2004) With respect to the molecular evidence available so far we propose toelevate Oncophoroideae to family level to accomodate these genera and perhapsGlyphomitrium (cf Tsubota et al 2003) whereas we consider AongstroemiaDichodontium and Diobelonella to belong to Aongstroemiaceae (cf Stech 1999a)Amphidium is neither closely related to Dicranaceae sstr nor to Oncophoroideae(La Farge et al 2002 Tsubota et al 2003 Hedderson et al 2004 Stech 2004 thisstudy) and should be treated at family level rather than placed in Dicranaceae assubfam Amphidioideae (Ochyra et al 2003) The circumscription of Dicranelloideaeis more difficult to evaluate as few representatives have been included in molecularanalyses However Dicranella heteromalla (Hedw) Schimp as well as the generaCampylopodium and Microcampylopus are clearly separated from Dicranaceae sstr(Stech 1999a 2004 La Farge et al 2002 Tsubota et al 2003 Hedderson et al2004) and consequently the subfamily deserves family status as well Finallymolecular data showed that the genus Hypodontium does not belong to Pottiaceae(Hedderson et al 2004 Tsubota et al 2004) Taxonomic conclusions have not beendrawn from these results which is made up here (see taxonomy)
All mosses with diplolepideous-alternate peristomes together with Splachnales witha diplolepideous-opposite (Funaria-type) peristome form a monophyletic group inmolecular analyses (eg Newton et al 2000 Beckert et al 2001 Goffinet et al2001 Cox et al 2004 Tsubota et al 2004 references in Table 2) Differentclassifications of this by far most species-rich group of mosses were proposed (egVitt et al 1998 Ochyra et al 2003 Goffinet amp Buck 2004) However at least someof the recognised subclasses and superorders are paraphyletic according to themolecular topologies and assigning formal ranks to all evolutionarily significantmonophyletic entities is problematic if the main taxonomic framework of Bryophytaand Bryopsida should be maintained (cf discussion in Bell et al 2007) Thereforein the present synopsis only one subclass Bryidae is recognised for all diplolepideous-alternate mosses and Splachnales This broadly defined Bryidae is subdivided into13 orders most of them resolved as monophyletic in the majority of the phylogeneticanalyses summarised in Table 2 although with different levels of statistical supportin maximum parsimony analyses To define monophyletic lineages at supraordinallevel informal node-based names may be chosen according to Bell et al (2007) Forexample the pleurocarpous mosses (pleurocarpy sensu Bell amp Newton 2007) andtheir closest acrocarpous relatives (Orthodontiales to Hypnales) were already
11
Table 2 Taxon sampling and bootstrap support (BS) for Dicranidae Bryidae and orders within theBryidae in recent phylogenetic analyses (MP only) based on combined molecular markers Markersare given in square brackets (non-coding regions in bold) numbers of included taxa in brackets ++respective clade present with ge 80 BS + clade present with lt 80 BS - clade not present no oronly one representative included
Bell amp Newton OBrien Quandt et al Bell et al this study(2004) (2007) (2007) (2007)
[rbcL rps4 [atpB atpB- [rbcL rps4 [rbcL rps4 [atpB-rbcLnad5] rbcL rbcL trnL-F nad5] trnL-F nad5] psbA-trnH
rps4 trnL-F] trnL]
Dicranidae + (2) + (4) ++ (3) (1) ++ (19)Bryidae ++ (57) + (53) ++ (52) ++ (98) ++ (58)Hedwigiales ++ (2) (1) ++ (2) ++ (2) - (3)Bartramiales ++ (2) ++ (4) ++ (4) ++ (3) - (4)Splachnales (0) ++ (2) ++ (3) ++ (2) ++ (5)Bryales - (4) - (5) ++ (18) + (17) - (8)Orthotrichales (1) ++ (3) ++ (3) ++ (2) ++ (4)Orthodontiales + (4) + (4) + (3) + (6) - (3)Aulacomniales + (6) + (7) ++ (2) + (7) + (3)Rhizogoniales ++ (13) + (8) ++ (5) ++ (14) - (3)Hypnodendrales ++ (13) + (7) ++ (4) ++ (29) ++ (6)Ptychomniales ++ (3) ++ (3) (1) ++ (4) (1)Hookeriales - (4) + (2) (1) + (2) + (8)Hypnales - (5) - (7) ++ (5) ++ (10) + (10)
summarised under the informal node based name pleurcarpids (Bell et al 2007)and can be distinguished from a basal grade of acrocarpous or cladocarpous lineages(Hedwigiales to Orthotrichales) Within the latter monophyly of BartramialesSplachnales and Orthotrichales is well-supported in all analyses including two ormore taxa except Bartramiales in the present data set (cf Fig 1) In contrast Bryalesreceive significant support less frequently (but see Bell et al 2007 Quandt et al2007) Hedwigiales are well supported if only Hedwigia (Hedwigiaceae) andRhacocarpus (Rhacocarpaceae) are included whereas the monospecific Helicophyllum(Helicophyllaceae) is not closely related to these taxa but shows affinities withBartramiales (Goffinet et al 2001 this study) With respect to the differentmorphologies of Helicophyllaceae and Bartramiaceae however the former shouldbe separated at ordinal level (see taxonomy)
Clarifying relationships of the Orthotrichales is still a difficult issue Analyses ofsingle chloroplast markers or parsimony analyses of combined markers from differentgenomes mostly indicated a close relationship either with Splachnales (eg Cox etal 2000 Newton et al 2000 Tsubota et al 2004 Quandt et al 2007) or with thepleurocarpids (Goffinet et al 2001 this study) Although none of these alternativesis well-supported the latter seems more likely with regard to the moderately tomaximally supported Orthotrichales - pleurocarpid sister group relationship in allanalyses of mitochondrial data and in likelihood analyses of combined plastidmitochondrial markers (Beckert et al 2001 Quandt et al 2007)
12
The molecular polyphyly of Rhizogoniaceae (eg Bell amp Newton 2004) was solvedby the transfer of rhizogonioid genera into broadly defined Aulacomniaceae andOrthodontiaceae (Bell et al 2007) which now include both acrocarpous andpleurocarpous taxa These systematic changes are also comprehensible by non-molecular characters such as morphological traits shared by Mesochaete andAulacomnium heterostichum (Hedw) Bruch amp Schimp or the variously reducedperistomes of Orthodontiaceae pp in contrast to the generally fully developed Bryum-type peristomes of rhizogonioid and hypnodendroid mosses (Bell et al 2007) Theposition of the solely pleurocarpous Hypnodendrales sister to the former Hypnidaeled to the recognition of the informal group core pleurocarps (Bell et al 2007)The former Hypnidae (Ptychomniales Hookeriales and Hypnales summarised ashomocostate pleurocarps) are monophyletic in most molecular analyses (eg Goffinetet al 2001 Tsubota et al 2004 Bell et al 2007) with Ptychomniales being well-supported (Pedersen amp Newton 2007 Table 2) Clarifying relationships betweenHookeriales and Hypnales and within the latter is still a challenge but recent molecularstudies seem to support a sister group relationship of both orders (Bell et al 2007present study)
Phylogenetic utility of non-coding plastid markers
Non-coding plastid markers that comprise both variable and conserved regionssuch as the trnL
UAA intron have repeatedly been shown to possess potential for
resolving relationships at high taxonomic levels (eg Borsch et al 2003 Quandtet al 2004) Both the trnL intron and atpB-rbcL spacer were characterised indetail in mosses with respect to their structure and molecular evolution (Quandt ampStech 2005 Stech amp Quandt 2006) They include conservative regions that can beunambiguosly aligned and even parts of the more variable regions can be used ifrepeats hairpin loops etc are correctly identified and adequately treated in thephylogenetic analyses (eg Quandt et al 2003 Quandt amp Stech 2005) Using theatpB-rbcL spacer alone (Stech amp Quandt 2006) relationships of the major mosslineages were largely consistent with the ldquototal evidencerdquo molecular tree of Goffinetamp Buck (2004) However in addition to general limitations that result from singlemarker analyses the use of non-coding markers may pose further problems suchas a high amount of homoplasy resulting in low resolution or low statistical supportfor many clades Therefore several recent molecular studies of relationships withinBryidae have employed both coding and non-coding markers (Table 2)Nevertheless the usefulness of analyses of combined non-coding plastid markerscannot be ruled out In fact Fig 1 and Table 2 indicate a phylogenetic signal inthe present data set as many clades are recovered that are usually also resolvedin analyses of coding or combined coding and non-coding markers Especiallywith regard to statistical support however the present analysis is inferior tothose of other recent data sets especially Bell et al (2007) and Quandt et al(2007) In addition the non-coding markers used here are of different suitabilityand even the two intergenic spacers differ considerably from each other ThepsbA-trnH spacer contributes much less to the trees resolution than the atpB-rbcL spacer first because it is much shorter and second because relatively largeparts are attributed to hairpin loops or otherwise hypervariable regions These
13
results indicate that future studies should evaluate the molecular evolution andphylogenetic potential of new markers both coding and con-coding and choosethe most suitable ones in a combined analysis to resolve the remaining uncertaintiesin moss phylogeny
Taxonomy
Takakiaceae Stech amp WFrey stat nov
Plantae virides nusquam rhizophorae sine protonemate e caudicis rhizomatis erectae Caudicesrhizomati et axes geotropi radiformes frequenter intercalariter ramificantes sine phyllidiis cumpapillis mucilaginis rostratis Caules phyllidiiferi saepe furcati Phyllidia sine lamina et costadistincta profunde 2-4(-5)-lobata pluristratosa tristicha sed torsione spiraliter disposita Filumcentralium in ambabus generationibus (axibus gametophyti et setis) adest Plantae dioicae Antheridiaet archegonia nuda Sporophytum terminale solitarium Seta persistens Capsula tortilis admaturitatem schizocarpa secus unam rimam spiralem longitudinalem dehiscens Stomata etoperculum absunt peristomium nullum Calyptra mitriformis
TYPUS Takakia SHatt amp Inoue J Hattori Bot Lab 19 137 1958
Takakiaceae SHatt amp Inoue J Hattori Bot Lab 19 137 1958 nom inval (Art 411)
Takakiales Stech amp WFrey stat nov
Based on Takakiaceae Stech amp WFrey Nova Hedwigia 86 13 2008
TYPUS Takakia SHatt amp Inoue J Hattori Bot Lab 19 137 1958
Takakiales SHatt amp Inoue J Hattori Bot Lab 19 137 1958 nom inval
Takakiales SHatt amp Inoue ex RMSchust J Hattori Bot Lab 26 224 1963 nom inval (cumdescr latin)
Takakiopsida Stech amp WFrey statnov
Based on Takakiaceae Stech amp WFrey Nova Hedwigia 86 13 2008
TYPUS Takakia SHatt amp Inoue J Hattori Bot Lab 19 137 1958
Takakiopsida Goffinet amp WRBuck Monogr Syst Bot Missouri Bot Gard 98 232 2004 nominval
Takakiopsida Jia et al Acta Phytotax Sin 41 350 351 2003 nom nud
Takakiopsida Wang amp Wu Fl Bryophyt Sin 8 447 2004 nom inval (cum descr latin)
Takakiophytina Stech amp WFrey stat nov
Based on Takakiaceae Stech amp WFrey Nova Hedwigia 86 13 2008
TYPUS Takakia SHatt amp Inoue JHattori Bot Lab 19 137 1958
Gigaspermidae Stech amp WFrey subclass nov
Plantae acrocarpae terrestres stoloniferae ramis brevibus erectis Folia unicostata cellulis laxislaevibus Capsula plerumque valde rugosa gymnostomatica vel cleistocarpa stomata cum duabuscellulis sociis Ab Funariidis et Encalyptidis charactere phylogenomico (71-kb inversio abest)separatae
14
TYPUS Gigaspermum Lindb Oumlfversigt af Foumlrhandlingar Kongl Svenska Vetenskaps-Akademien21 599 1865
Amphidiaceae Stech stat nov
Based on Dicranaceae subfam Amphidioideae Ochyra in Ochyra Zarnowiec amp Bednarek-OchyraCens Cat Polish Mosses 110 2003
TYPUS Amphidium Schimp Coroll Bryol Eur 39 1856
Amphidiaceae AJESm Moss Fl Britain Ireland 2nd ed 657 2004 nom inval descr angl
Dicranellaceae Stech stat nov
Based on Dicranaceae subfam Dicranelloideae Lindb Utkast Eur Bladmoss 33 1878[lsquoUnderfamilje Dicranelleaersquo]
TYPUS Dicranella (MuumlllHal) Schimp Coroll Bryol Eur 13 1856
Oncophoraceae Stech stat nov
Based on Dicranaceae subfam Oncophoroideae Lindb Utkast Eur Bladmoss 34 1878[lsquoUnderfamilje Oncophoreaersquo]
TYPUS Oncophorus (Brid) Brid Bryol Univ 1 389 1826
Hypodontiaceae Stech fam nov
Plantae robustae characteribus morphologicis Pottiaceis et Calymperaceis similes sedcharacteribus molecularicis separatae Bracteae perichaetiales internae e basi vaginantes subulataevel aristatae Capsula aspectu succulenta cellulae exothecii incrassatae annulus magnopereabsens Peristomii dentes breves triangulati incurvati aurantiaci leves vel infirme verrucosiCalyptra cucullata
TYPUS Hypodontium MuumlllHal Hedwigia 38 96 1899
Helicophyllales Stech amp WFrey ord nov
Plantae acrocarpae prostratae tomentosae Folia dimorpha in duas series laterales et unam seriemventralem divisa Costa percurrens Cellulae hexagonae ad subquadratae papillosae Capsula immersacupulata ad oblonga infra orificium abrupte incurvata stomata destituta Peristomium nullum Sporaeisomorphae heteropolares granulatae
TYPUS Helicophyllum Brid Bryol Univ 2 771 1827
Synopsis of the suprageneric classification of BryophytaAuthor citations are in accordance with Art 492 of the Vienna Code (McNeill et al 2006)
Subdivision Takakiophytina Stech amp WFreyClass Takakiopsida Stech amp WFrey
Order Takakiales Stech amp WFreyTakakiaceae Stech amp WFrey
Subdivision Sphagnophytina DoweldClass Sphagnopsida Schimp
Order Sphagnales Limpr
15
Sphagnaceae DumortOrder Ambuchananiales Seppelt amp HACrum
Ambuchananiaceae Seppelt amp HACrumSubdivision Bryophytina Engler
Class Andreaeopsida JHSchaffnSubclass Andreaeidae Engl
Order Andreaeales LimprAndreaeaceae Dumort
Subclass Andreaeobryidae OchyraOrder Andreaeobryales BMMurray
Andreaeobryaceae Steere amp BMMurrayClass Oedipodiopsida Goffinet amp WRBuck
Order Oedipodiales Goffinet amp WRBuckOedipodiaceae Schimp
Class Tetraphidopsida Goffinet amp WRBuckOrder Tetraphidales MFleisch
Tetraphidaceae SchimpClass Polytrichopsida Doweld
Order Polytrichales MFleischPolytrichaceae Schwaumlgr
Class Bryopsida PaxSubclass Buxbaumiidae Doweld
Order Buxbaumiales MFleischBuxbaumiaceae Schimp
Subclass Diphysciidae OchyraOrder Diphysciales MFleisch
Diphysciaceae MFleischSubclass Timmiidae Ochyra
Order Timmiales OchyraTimmiaceae Schimp
Subclass Encalyptidae Ochyra Żarnowiec amp Bednarek-OchyraOrder Encalyptales Dixon
Encalyptaceae SchimpSubclass Funariidae Ochyra
Order Funariales MFleischFunariaceae Schwaumlgr Disceliaceae Schimp
Subclass Gigaspermidae Stech amp WFreyOrder Gigaspermales Goffinet Wickett OWerner Ros AJShaw amp CJCox
Gigaspermaceae LindbSubclass Dicranidae Doweld
Order Catoscopiales Ignatov amp IgnatovaCatoscopiaceae Broth
Order Scouleriales Goffinet amp WRBuckDrummondiaceae Goffinet Scouleriaceae SPChurchill
Order Bryoxiphiales HACrum amp LEAndersonBryoxiphiaceae Besch
16
Order Grimmiales MFleischGrimmiaceae Arn Ptychomitriaceae Schimp Seligeriaceae Schimp
Order Archidiales LimprArchidiaceae Schimp
Order Mitteniales ShawMitteniaceae Broth
Order Dicranales HPhilib ex MFleischAmphidiaceae Stech Aongstroemiaceae De Not BruchiaceaeSchimp Calymperaceae Kindb Dicranaceae Schimp Dicranel-laceae Stech Ditrichaceae Limpr Erpodiaceae Broth EustichiaceaeBroth Fissidentaceae Schimp Leucobryaceae Schimp Onco-phoraceae Stech Rhachitheciaceae HRob Schistostegaceae SchimpViridivelleraceae IGStone Wardiaceae Welch
Order Pottiales MFleischEphemeraceae Schimp Hypodontiaceae Stech PleurophascaceaeBroth Pottiaceae Schimp Serpotortellaceae WDReese amp RHZander
Subclass Bryidae EnglOrder Hedwigiales Ochyra
Hedwigiaceae Schimp Rhacocarpaceae KindbOrder Helicophyllales Stech amp WFrey
Helicophyllaceae BrothOrder Bartramiales DQuandt NEBell amp Stech
Bartramiaceae SchwaumlgrOrder Splachnales Ochyra
Meesiaceae Schimp Splachnaceae Grev amp ArnOrder Bryales Limpr
Bryaceae Schwaumlgr Leptostomataceae Schwaumlgr Mniaceae SchwaumlgrPhyllodrepaniaceae Crosby Pseudoditrichaceae Steere amp ZIwatsPulchrinodaceae DQuandt NEBell amp Stech
Order Orthotrichales DixonOrthotrichaceae Arn
Order Orthodontiales NEBell AENewton amp DQuandtOrthodontiaceae Goffinet
Order Aulacomniales NEBell AENewton amp DQuandtAulacomniaceae Schimp
Order Rhizogoniales Goffinet amp WRBuckRhizogoniaceae Broth
Order Hypnodendrales NEBell AENewton amp DQuandtBraithwaiteaceae NEBell AENewton amp DQuandt Hypnodendra-ceae Broth Pterobryellaceae WRBuck amp Vitt Racopilaceae Kindb
Order Ptychomniales WRBuck CJCox AJShaw amp GoffinetPtychomniaceae MFleisch
Order Hookeriales MFleischDaltoniaceae Schimp Hookeriaceae Schimp HypopterygiaceaeMitt Leucomiaceae Broth Pilotrichaceae Kindb SaulomataceaeWRBuck CJCox AJShaw amp Goffinet Schimperobryaceae WR
17
Buck CJCox AJShaw amp GoffinetOrder Hypnales WRBuck amp Vitt
Amblystegiaceae GRoth Anomodontaceae Kindb BrachytheciaceaeSchimp Calliergonaceae Vanderpoorten Hedenaumls CJCox amp AJShaw Catagoniaceae WRBuck amp Ireland Climaciaceae KindbCryphaeaceae Schimp Echinodiaceae Broth Entodontaceae KindbFabroniaceae Schimp Fontinalaceae Schimp Helodiaceae OchyraHeterocladiaceae Ignatov amp Ignatova Hylocomiaceae MFleischHypnaceae Schimp Lembophyllaceae Broth LeptodontaceaeSchimp Lepyrodontaceae Broth Leskeaceae Schimp Leucodon-taceae Schimp Meteoriaceae Kindb Microtheciellaceae HAMillamp AJHarr Myriniaceae Schimp Myuriaceae MFleisch NeckeraceaeSchimp Orthorrhynchiaceae SHLin Phyllogoniaceae KindbPlagiotheciaceae MFleisch Pleuroziopsidaceae Ireland Prionodon-taceae Broth Pseudoleskeaceae Schimp PseudoleskeellaceaeIgnatov amp Ignatova Pterigynandraceae Schimp PterobryaceaeKindb Pylaisiaceae Schimp Pylaisiadelphaceae Goffinet amp WRBuck Regmatodontaceae Broth Rhytidiaceae Broth RigodiaceaeHACrum Rutenbergiaceae MFleisch Scorpidiaceae Ignatov ampIgnatova Sematophyllaceae Broth Sorapillaceae MFleisch Ste-reophyllaceae WRBuck amp Ireland Symphyodontaceae MFleischTheliaceae MFleisch Thuidiaceae Schimp TrachylomataceaeWRBuck amp Vitt
Acknowledgements
Sincere thanks are due to JLReveal (Ithaca) as well as WFPrudhomme van Reine and JFVeldkamp(Leiden) for comments and discussions about suprafamilial taxonomy to DQuandt (Dresden) for providingDNA from Rhacocarpus and Bartramiaceae species and to BGiesicke (Berlin) for technical assistance
References
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BELL NE amp AE NEWTON (2007) Pleurocarpy in the Rhizogoniaceous grade - In NEWTONAE amp RS TANGNEY (eds) Pleurocarpous mosses systematics and evolution SystematicsAssociation Special Volume Series 71 41-64
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18
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FREY W amp M STECH (2005) A morpho-molecular classification of the liverworts (Hepa-ticophytina Bryophyta) - Nova Hedwigia 81 55-78
FREY W M STECH amp K MEIszligNER (1999) Chloroplast DNA-relationship in palaeoaustralLopidium concinnum (Hypopterygiaceae Musci) An example of steno-evolution in mosses Studiesin austral temperate rain forest bryophytes 2 - Plant Syst Evol 218 67-75
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GOFFINET B NJ WICKETT O WERNER RM ROS AJ SHAW amp CJ COX (2007)Distribution and phylogenetic significance of the 71-kb inversion in the plastid genome in Funariidae(Bryophyta) - Ann Bot 99 747-753
19
GROTH-MALONEK M D PRUCHNER F GREWE amp V KNOOP (2005) Ancestors oftrans-splicing mitochondrial introns support serial sister group relationships of hornworts and mosseswith vascular plants - Mol Biol Evol 22 117-125
HATTORI S amp H INOUE (1958) Preliminary report on Takakia lepidozioides - J Hattori BotLab 19 133-137
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LA FARGE C BD MISHER JA WHEELER DP WALL K JOHANNES S SCHAFFERamp AJ SHAW (2000) Phylogenetic relationships within the haplolepideous mosses - Bryologist103 257-276
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MCNEILL J FR BARRIE HM BURDET V DEMOULIN DL HAWKSWORTHK MARHOLD DH NICOLSON J PRADO PC SILVA JE SKOG JH WIERSEMA ampNJ TURLAND (2006) International Code of Botanical Nomenclature (Vienna Code) - RegnumVegetabile 146 1-568
MUumlLLER K (2004) PRAP - computation of Bremer support for large data sets - Mol PhylogenetEvol 31 780-782
MUumlLLER K (2005) SeqState - primer design and sequence statistics for phylogenetic DNA datasets - Appl Bioinformatics 4 65-69
MUumlLLER K D QUANDT J MUumlLLER amp C NEINHUIS (2005) PhyDE v0992 PhylogeneticData Editor - httpwwwphydede
MURRAY BM (1988) Systematics of the Andreaeopsida (Bryophyta) two orders with links toTakakia - Nova Hedwigia Beih 90 289-336
NEWTON AE amp RS TANGNEY (eds) (2007) Pleurocarpous mosses systematics and evolutionSystematics Association Special Volume Series 71 CRC Press Boca Raton 434 pp
NEWTON AE CJ COX JG DUCKETT JA WHEELER B GOFFINET TAJ HEDDER-SON amp BD MISHLER (2000) Evolution of the major moss lineages Phylogenetic analyses basedon multiple gene sequences and morphology - Bryologist 103 187-211
NEWTON AE N WIKSTROumlM NE BELL LL FORREST amp MS IGNATOV (2007)Dating the diversification of the pleurocarpous mosses - In NEWTON AE amp RS TANGNEY(eds) Pleurocarpous mosses systematics and evolution Systematics Association Special VolumeSeries 71 337-366
NIXON KC (1999) The parsimony ratchet a new method for rapid parsimony analysis - Cladistics15 407-411
OBRIEN TJ (2007) The phylogenetic distribution of pleurocarpous mosses evidence fromcpDNA sequences - In NEWTON AE amp RS TANGNEY (eds) Pleurocarpous mossessystematics and evolution Systematics Association Special Volume Series 71 19-41
OCHYRA R (2002) Nomenclatural changes in subfamilies of the Dicranaceae - CryptogamieBryol 23 345-349
20
OCHYRA R J ŻARNOWIEC amp H BEDNAREK-OCHYRA (2003) Census catalogue ofPolish mosses - Biodiv Poland 3 1-372
PEDERSEN N amp AE NEWTON (2007) Phylogenetic and morphological studies within thePtychomniales with emphasis on the evolution of dwarf males - In NEWTON AE amp RSTANGNEY (eds) Pleurocarpous mosses systematics and evolution Systematics AssociationSpecial Volume Series 71 367-392
QUANDT D amp M STECH (2005) Molecular evolution and secondary structure of the chloroplasttrnL intron in bryophytes - Mol Phylogenet Evol 36 429-443
QUANDT D K MUumlLLER amp S HUTTUNEN (2003) Characterisation of the chloroplast DNApsbT-H region and the influence of dyad symmetrical elements on phylogenetic reconstructions -Plant Biol 5 400-410
QUANDT D K MUumlLLER M STECH W FREY KW HILU amp T BORSCH (2004) Molecularevolution of the chloroplast trnL-F-region in land plants - In GOFFINET B V HOLLOWELL ampR MAGILL (eds) Molecular systematics of bryophytes Monogr Syst Bot Missouri Bot Gard98 13-37
QUANDT D NE BELL amp M STECH (2007) Unravelling the knot the Pulchrinodaceae famnov (Bryales) - In KUumlRSCHNER H T PFEIFFER amp M STECH (eds) A Festschrift to Wolf-gang Frey - a scientists life between deserts and rain forests Nova Hedwigia Beih 131 21-39
QIU Y-L Y CHO JC COX amp JD PALMER (1998) The gain of three mitochondrial intronsidentifies liverworts as the earliest land plants - Nature 394 671-674
QIU Y-L L LI B WANG Z CHEN V KNOOP M GROTH-MALONEK O DOM-BROVSKA J LEE L KENT J REST GF ESTABROOK TA HENDRY DW TAYLORCM TESTA M AMBROS B CRANDALL-STOTLER J DUFF M STECH W FREYD QUANDT amp CC DAVIS (2006) The deepest divergences in land plants inferred fromphylogenomic evidence - Proc Natl Acad Sci USA 103 15511-15516
RENZAGLIA KS S SCHUETTE RJ DUFF R LIGRONE AJ SHAW BD MISHLER ampJG DUCKETT (2007) Bryophyte phylogeny Advancing the molecular and morphological frontiers- Bryologist 110 179-213
SAMIGULLIN TH SP YACENTYUK GV DEGTYARYEVA KM VALIEJO-ROMANVK BOBROVA I CAPESIUS WF MARTIN AV TROITSKY VR FILIN amp ASANTONOV (2002) Paraphyly of bryophytes and close relationships of hornworts and vascularplants inferred from analysis of chloroplast rDNA ITS (cpITS) sequences - Arctoa 11 31-43
SANG T DJ CRAWFORD amp TF STUESSY (1997) Chloroplast DNA phylogeny reticulateevolution and biogeography of Paeonia (Paeoniaceae) - Amer J Bot 84 1120-1136
SHAW AJ amp KS RENZAGLIA (2004) Phylogeny and diversification of bryophytes - AmerJ Bot 91 1557-1581
SHAW AJ CJ COX amp B GOFFINET (2005) Global patterns of moss diversity taxonomic andmolecular inferences - Taxon 54 337-352
STECH M (1999a) A reclassification of Dicranaceae (Bryopsida) based on non-coding cpDNAsequence data - J Hattori Bot Lab 86 137-159
STECH M (1999b) A molecular systematic contribution to the position of Amphidium Schimp(Rhabdoweisiaceae Bryopsida) - Nova Hedwigia 68 291-300
STECH M (2004) Supraspecific circumscription and classification of Campylopus Brid(Dicranaceae Bryopsida) based on molecular data - Syst Bot 29 817-824
STECH M amp D QUANDT (2006) Molecular evolution of the chloroplast atpB-rbcL spacer inbryophytes - In SHARMA AK amp A SHARMA (eds) Plant Genome Biodiversity and EvolutionVol 2 Part B pp 409-431 Science Publishers Enfield New Hampshire
21
STECH M D QUANDT amp W FREY (2003) Molecular circumscription of the hornworts(Antho-cerotophyta) based on the chloroplast DNA trnL-trnF region - J Plant Res 116 389-398
STOTLER RE amp B CRANDALL-STOTLER (2005) A revised classification of theAnthocerotophyta and a checklist of the hornworts of North America north of Mexico - Bryologist108 16-26
SWOFFORD DL (2002) PAUP Phylogenetic analysis using parsimony (and other methods)version 40b10 - Sunderland MA
TABERLET P L GIELLY G PAUTOU amp J BOUVET (1991) Universal primers for amplificationof three non-coding regions of chloroplast DNA - Plant Mol Biol 17 1105-1109
TSUBOTA H Y AGENO B ESTEacuteBANEZ T YAMAGUCHI amp H DEGUCHI (2003)Molecular phylogeny of the Grimmiales (Musci) based on chloroplast rbcL sequences - Hikobia 1455-70
TSUBOTA H E DE LUNA D GONZAacuteLEZ MS IGNATOV amp H DEGUCHI (2004) Molecularphylogenetics and ordinal relationships based on analyses of a large-scale data set of 600 rbcLsequences of mosses - Hikobia 14 149-170
VITT DH (1984) Classification of the Bryopsida - In SCHUSTER RM (ed) New Manual ofBryology 2 696-759 Hattori Botanical Laboratory Nichinan Japan
VITT DH B GOFFINET amp T HEDDERSON (1998) 8 The ordinal classification of the mossesquestions and answers for the 1990s - In BATES JW NW ASHTON amp JG DUCKETT (eds)Bryology for the twenty-first century British Bryol Soc pp 113-123
Received 3 September 2007 accepted in revised form 30 October 2007
10
Consequently resolving the phylogeny of Dicranidae with confidence is one of themajor future challenges in moss systematics
As mentioned above Dicranaceae are monophyletic in a narrow circumscriptionaccording to molecular data In contrast to former Campylopoideae andParaleucobryoideae the status of Rhabdoweisioideae (= Oncophoroideae Ochyra2002) and Dicranelloideae needs further consideration Stech (1999ab) suggestedto recognise RhabdoweisioideaeRhabdoweisiaceae in a broad sense includingDicranoweisia Amphidium and Aongstroemia Subsequent molecular analysesconfirmed a close relationship of the genera Arctoa Cynodontium DicranoweisiaKiaeria Oncophorus Oreoweisia Oreas Rhabdoweisia and Symblepharis althoughwithout significant support (La Farge et al 2002 Tsubota et al 2003 Hedderson etal 2004) With respect to the molecular evidence available so far we propose toelevate Oncophoroideae to family level to accomodate these genera and perhapsGlyphomitrium (cf Tsubota et al 2003) whereas we consider AongstroemiaDichodontium and Diobelonella to belong to Aongstroemiaceae (cf Stech 1999a)Amphidium is neither closely related to Dicranaceae sstr nor to Oncophoroideae(La Farge et al 2002 Tsubota et al 2003 Hedderson et al 2004 Stech 2004 thisstudy) and should be treated at family level rather than placed in Dicranaceae assubfam Amphidioideae (Ochyra et al 2003) The circumscription of Dicranelloideaeis more difficult to evaluate as few representatives have been included in molecularanalyses However Dicranella heteromalla (Hedw) Schimp as well as the generaCampylopodium and Microcampylopus are clearly separated from Dicranaceae sstr(Stech 1999a 2004 La Farge et al 2002 Tsubota et al 2003 Hedderson et al2004) and consequently the subfamily deserves family status as well Finallymolecular data showed that the genus Hypodontium does not belong to Pottiaceae(Hedderson et al 2004 Tsubota et al 2004) Taxonomic conclusions have not beendrawn from these results which is made up here (see taxonomy)
All mosses with diplolepideous-alternate peristomes together with Splachnales witha diplolepideous-opposite (Funaria-type) peristome form a monophyletic group inmolecular analyses (eg Newton et al 2000 Beckert et al 2001 Goffinet et al2001 Cox et al 2004 Tsubota et al 2004 references in Table 2) Differentclassifications of this by far most species-rich group of mosses were proposed (egVitt et al 1998 Ochyra et al 2003 Goffinet amp Buck 2004) However at least someof the recognised subclasses and superorders are paraphyletic according to themolecular topologies and assigning formal ranks to all evolutionarily significantmonophyletic entities is problematic if the main taxonomic framework of Bryophytaand Bryopsida should be maintained (cf discussion in Bell et al 2007) Thereforein the present synopsis only one subclass Bryidae is recognised for all diplolepideous-alternate mosses and Splachnales This broadly defined Bryidae is subdivided into13 orders most of them resolved as monophyletic in the majority of the phylogeneticanalyses summarised in Table 2 although with different levels of statistical supportin maximum parsimony analyses To define monophyletic lineages at supraordinallevel informal node-based names may be chosen according to Bell et al (2007) Forexample the pleurocarpous mosses (pleurocarpy sensu Bell amp Newton 2007) andtheir closest acrocarpous relatives (Orthodontiales to Hypnales) were already
11
Table 2 Taxon sampling and bootstrap support (BS) for Dicranidae Bryidae and orders within theBryidae in recent phylogenetic analyses (MP only) based on combined molecular markers Markersare given in square brackets (non-coding regions in bold) numbers of included taxa in brackets ++respective clade present with ge 80 BS + clade present with lt 80 BS - clade not present no oronly one representative included
Bell amp Newton OBrien Quandt et al Bell et al this study(2004) (2007) (2007) (2007)
[rbcL rps4 [atpB atpB- [rbcL rps4 [rbcL rps4 [atpB-rbcLnad5] rbcL rbcL trnL-F nad5] trnL-F nad5] psbA-trnH
rps4 trnL-F] trnL]
Dicranidae + (2) + (4) ++ (3) (1) ++ (19)Bryidae ++ (57) + (53) ++ (52) ++ (98) ++ (58)Hedwigiales ++ (2) (1) ++ (2) ++ (2) - (3)Bartramiales ++ (2) ++ (4) ++ (4) ++ (3) - (4)Splachnales (0) ++ (2) ++ (3) ++ (2) ++ (5)Bryales - (4) - (5) ++ (18) + (17) - (8)Orthotrichales (1) ++ (3) ++ (3) ++ (2) ++ (4)Orthodontiales + (4) + (4) + (3) + (6) - (3)Aulacomniales + (6) + (7) ++ (2) + (7) + (3)Rhizogoniales ++ (13) + (8) ++ (5) ++ (14) - (3)Hypnodendrales ++ (13) + (7) ++ (4) ++ (29) ++ (6)Ptychomniales ++ (3) ++ (3) (1) ++ (4) (1)Hookeriales - (4) + (2) (1) + (2) + (8)Hypnales - (5) - (7) ++ (5) ++ (10) + (10)
summarised under the informal node based name pleurcarpids (Bell et al 2007)and can be distinguished from a basal grade of acrocarpous or cladocarpous lineages(Hedwigiales to Orthotrichales) Within the latter monophyly of BartramialesSplachnales and Orthotrichales is well-supported in all analyses including two ormore taxa except Bartramiales in the present data set (cf Fig 1) In contrast Bryalesreceive significant support less frequently (but see Bell et al 2007 Quandt et al2007) Hedwigiales are well supported if only Hedwigia (Hedwigiaceae) andRhacocarpus (Rhacocarpaceae) are included whereas the monospecific Helicophyllum(Helicophyllaceae) is not closely related to these taxa but shows affinities withBartramiales (Goffinet et al 2001 this study) With respect to the differentmorphologies of Helicophyllaceae and Bartramiaceae however the former shouldbe separated at ordinal level (see taxonomy)
Clarifying relationships of the Orthotrichales is still a difficult issue Analyses ofsingle chloroplast markers or parsimony analyses of combined markers from differentgenomes mostly indicated a close relationship either with Splachnales (eg Cox etal 2000 Newton et al 2000 Tsubota et al 2004 Quandt et al 2007) or with thepleurocarpids (Goffinet et al 2001 this study) Although none of these alternativesis well-supported the latter seems more likely with regard to the moderately tomaximally supported Orthotrichales - pleurocarpid sister group relationship in allanalyses of mitochondrial data and in likelihood analyses of combined plastidmitochondrial markers (Beckert et al 2001 Quandt et al 2007)
12
The molecular polyphyly of Rhizogoniaceae (eg Bell amp Newton 2004) was solvedby the transfer of rhizogonioid genera into broadly defined Aulacomniaceae andOrthodontiaceae (Bell et al 2007) which now include both acrocarpous andpleurocarpous taxa These systematic changes are also comprehensible by non-molecular characters such as morphological traits shared by Mesochaete andAulacomnium heterostichum (Hedw) Bruch amp Schimp or the variously reducedperistomes of Orthodontiaceae pp in contrast to the generally fully developed Bryum-type peristomes of rhizogonioid and hypnodendroid mosses (Bell et al 2007) Theposition of the solely pleurocarpous Hypnodendrales sister to the former Hypnidaeled to the recognition of the informal group core pleurocarps (Bell et al 2007)The former Hypnidae (Ptychomniales Hookeriales and Hypnales summarised ashomocostate pleurocarps) are monophyletic in most molecular analyses (eg Goffinetet al 2001 Tsubota et al 2004 Bell et al 2007) with Ptychomniales being well-supported (Pedersen amp Newton 2007 Table 2) Clarifying relationships betweenHookeriales and Hypnales and within the latter is still a challenge but recent molecularstudies seem to support a sister group relationship of both orders (Bell et al 2007present study)
Phylogenetic utility of non-coding plastid markers
Non-coding plastid markers that comprise both variable and conserved regionssuch as the trnL
UAA intron have repeatedly been shown to possess potential for
resolving relationships at high taxonomic levels (eg Borsch et al 2003 Quandtet al 2004) Both the trnL intron and atpB-rbcL spacer were characterised indetail in mosses with respect to their structure and molecular evolution (Quandt ampStech 2005 Stech amp Quandt 2006) They include conservative regions that can beunambiguosly aligned and even parts of the more variable regions can be used ifrepeats hairpin loops etc are correctly identified and adequately treated in thephylogenetic analyses (eg Quandt et al 2003 Quandt amp Stech 2005) Using theatpB-rbcL spacer alone (Stech amp Quandt 2006) relationships of the major mosslineages were largely consistent with the ldquototal evidencerdquo molecular tree of Goffinetamp Buck (2004) However in addition to general limitations that result from singlemarker analyses the use of non-coding markers may pose further problems suchas a high amount of homoplasy resulting in low resolution or low statistical supportfor many clades Therefore several recent molecular studies of relationships withinBryidae have employed both coding and non-coding markers (Table 2)Nevertheless the usefulness of analyses of combined non-coding plastid markerscannot be ruled out In fact Fig 1 and Table 2 indicate a phylogenetic signal inthe present data set as many clades are recovered that are usually also resolvedin analyses of coding or combined coding and non-coding markers Especiallywith regard to statistical support however the present analysis is inferior tothose of other recent data sets especially Bell et al (2007) and Quandt et al(2007) In addition the non-coding markers used here are of different suitabilityand even the two intergenic spacers differ considerably from each other ThepsbA-trnH spacer contributes much less to the trees resolution than the atpB-rbcL spacer first because it is much shorter and second because relatively largeparts are attributed to hairpin loops or otherwise hypervariable regions These
13
results indicate that future studies should evaluate the molecular evolution andphylogenetic potential of new markers both coding and con-coding and choosethe most suitable ones in a combined analysis to resolve the remaining uncertaintiesin moss phylogeny
Taxonomy
Takakiaceae Stech amp WFrey stat nov
Plantae virides nusquam rhizophorae sine protonemate e caudicis rhizomatis erectae Caudicesrhizomati et axes geotropi radiformes frequenter intercalariter ramificantes sine phyllidiis cumpapillis mucilaginis rostratis Caules phyllidiiferi saepe furcati Phyllidia sine lamina et costadistincta profunde 2-4(-5)-lobata pluristratosa tristicha sed torsione spiraliter disposita Filumcentralium in ambabus generationibus (axibus gametophyti et setis) adest Plantae dioicae Antheridiaet archegonia nuda Sporophytum terminale solitarium Seta persistens Capsula tortilis admaturitatem schizocarpa secus unam rimam spiralem longitudinalem dehiscens Stomata etoperculum absunt peristomium nullum Calyptra mitriformis
TYPUS Takakia SHatt amp Inoue J Hattori Bot Lab 19 137 1958
Takakiaceae SHatt amp Inoue J Hattori Bot Lab 19 137 1958 nom inval (Art 411)
Takakiales Stech amp WFrey stat nov
Based on Takakiaceae Stech amp WFrey Nova Hedwigia 86 13 2008
TYPUS Takakia SHatt amp Inoue J Hattori Bot Lab 19 137 1958
Takakiales SHatt amp Inoue J Hattori Bot Lab 19 137 1958 nom inval
Takakiales SHatt amp Inoue ex RMSchust J Hattori Bot Lab 26 224 1963 nom inval (cumdescr latin)
Takakiopsida Stech amp WFrey statnov
Based on Takakiaceae Stech amp WFrey Nova Hedwigia 86 13 2008
TYPUS Takakia SHatt amp Inoue J Hattori Bot Lab 19 137 1958
Takakiopsida Goffinet amp WRBuck Monogr Syst Bot Missouri Bot Gard 98 232 2004 nominval
Takakiopsida Jia et al Acta Phytotax Sin 41 350 351 2003 nom nud
Takakiopsida Wang amp Wu Fl Bryophyt Sin 8 447 2004 nom inval (cum descr latin)
Takakiophytina Stech amp WFrey stat nov
Based on Takakiaceae Stech amp WFrey Nova Hedwigia 86 13 2008
TYPUS Takakia SHatt amp Inoue JHattori Bot Lab 19 137 1958
Gigaspermidae Stech amp WFrey subclass nov
Plantae acrocarpae terrestres stoloniferae ramis brevibus erectis Folia unicostata cellulis laxislaevibus Capsula plerumque valde rugosa gymnostomatica vel cleistocarpa stomata cum duabuscellulis sociis Ab Funariidis et Encalyptidis charactere phylogenomico (71-kb inversio abest)separatae
14
TYPUS Gigaspermum Lindb Oumlfversigt af Foumlrhandlingar Kongl Svenska Vetenskaps-Akademien21 599 1865
Amphidiaceae Stech stat nov
Based on Dicranaceae subfam Amphidioideae Ochyra in Ochyra Zarnowiec amp Bednarek-OchyraCens Cat Polish Mosses 110 2003
TYPUS Amphidium Schimp Coroll Bryol Eur 39 1856
Amphidiaceae AJESm Moss Fl Britain Ireland 2nd ed 657 2004 nom inval descr angl
Dicranellaceae Stech stat nov
Based on Dicranaceae subfam Dicranelloideae Lindb Utkast Eur Bladmoss 33 1878[lsquoUnderfamilje Dicranelleaersquo]
TYPUS Dicranella (MuumlllHal) Schimp Coroll Bryol Eur 13 1856
Oncophoraceae Stech stat nov
Based on Dicranaceae subfam Oncophoroideae Lindb Utkast Eur Bladmoss 34 1878[lsquoUnderfamilje Oncophoreaersquo]
TYPUS Oncophorus (Brid) Brid Bryol Univ 1 389 1826
Hypodontiaceae Stech fam nov
Plantae robustae characteribus morphologicis Pottiaceis et Calymperaceis similes sedcharacteribus molecularicis separatae Bracteae perichaetiales internae e basi vaginantes subulataevel aristatae Capsula aspectu succulenta cellulae exothecii incrassatae annulus magnopereabsens Peristomii dentes breves triangulati incurvati aurantiaci leves vel infirme verrucosiCalyptra cucullata
TYPUS Hypodontium MuumlllHal Hedwigia 38 96 1899
Helicophyllales Stech amp WFrey ord nov
Plantae acrocarpae prostratae tomentosae Folia dimorpha in duas series laterales et unam seriemventralem divisa Costa percurrens Cellulae hexagonae ad subquadratae papillosae Capsula immersacupulata ad oblonga infra orificium abrupte incurvata stomata destituta Peristomium nullum Sporaeisomorphae heteropolares granulatae
TYPUS Helicophyllum Brid Bryol Univ 2 771 1827
Synopsis of the suprageneric classification of BryophytaAuthor citations are in accordance with Art 492 of the Vienna Code (McNeill et al 2006)
Subdivision Takakiophytina Stech amp WFreyClass Takakiopsida Stech amp WFrey
Order Takakiales Stech amp WFreyTakakiaceae Stech amp WFrey
Subdivision Sphagnophytina DoweldClass Sphagnopsida Schimp
Order Sphagnales Limpr
15
Sphagnaceae DumortOrder Ambuchananiales Seppelt amp HACrum
Ambuchananiaceae Seppelt amp HACrumSubdivision Bryophytina Engler
Class Andreaeopsida JHSchaffnSubclass Andreaeidae Engl
Order Andreaeales LimprAndreaeaceae Dumort
Subclass Andreaeobryidae OchyraOrder Andreaeobryales BMMurray
Andreaeobryaceae Steere amp BMMurrayClass Oedipodiopsida Goffinet amp WRBuck
Order Oedipodiales Goffinet amp WRBuckOedipodiaceae Schimp
Class Tetraphidopsida Goffinet amp WRBuckOrder Tetraphidales MFleisch
Tetraphidaceae SchimpClass Polytrichopsida Doweld
Order Polytrichales MFleischPolytrichaceae Schwaumlgr
Class Bryopsida PaxSubclass Buxbaumiidae Doweld
Order Buxbaumiales MFleischBuxbaumiaceae Schimp
Subclass Diphysciidae OchyraOrder Diphysciales MFleisch
Diphysciaceae MFleischSubclass Timmiidae Ochyra
Order Timmiales OchyraTimmiaceae Schimp
Subclass Encalyptidae Ochyra Żarnowiec amp Bednarek-OchyraOrder Encalyptales Dixon
Encalyptaceae SchimpSubclass Funariidae Ochyra
Order Funariales MFleischFunariaceae Schwaumlgr Disceliaceae Schimp
Subclass Gigaspermidae Stech amp WFreyOrder Gigaspermales Goffinet Wickett OWerner Ros AJShaw amp CJCox
Gigaspermaceae LindbSubclass Dicranidae Doweld
Order Catoscopiales Ignatov amp IgnatovaCatoscopiaceae Broth
Order Scouleriales Goffinet amp WRBuckDrummondiaceae Goffinet Scouleriaceae SPChurchill
Order Bryoxiphiales HACrum amp LEAndersonBryoxiphiaceae Besch
16
Order Grimmiales MFleischGrimmiaceae Arn Ptychomitriaceae Schimp Seligeriaceae Schimp
Order Archidiales LimprArchidiaceae Schimp
Order Mitteniales ShawMitteniaceae Broth
Order Dicranales HPhilib ex MFleischAmphidiaceae Stech Aongstroemiaceae De Not BruchiaceaeSchimp Calymperaceae Kindb Dicranaceae Schimp Dicranel-laceae Stech Ditrichaceae Limpr Erpodiaceae Broth EustichiaceaeBroth Fissidentaceae Schimp Leucobryaceae Schimp Onco-phoraceae Stech Rhachitheciaceae HRob Schistostegaceae SchimpViridivelleraceae IGStone Wardiaceae Welch
Order Pottiales MFleischEphemeraceae Schimp Hypodontiaceae Stech PleurophascaceaeBroth Pottiaceae Schimp Serpotortellaceae WDReese amp RHZander
Subclass Bryidae EnglOrder Hedwigiales Ochyra
Hedwigiaceae Schimp Rhacocarpaceae KindbOrder Helicophyllales Stech amp WFrey
Helicophyllaceae BrothOrder Bartramiales DQuandt NEBell amp Stech
Bartramiaceae SchwaumlgrOrder Splachnales Ochyra
Meesiaceae Schimp Splachnaceae Grev amp ArnOrder Bryales Limpr
Bryaceae Schwaumlgr Leptostomataceae Schwaumlgr Mniaceae SchwaumlgrPhyllodrepaniaceae Crosby Pseudoditrichaceae Steere amp ZIwatsPulchrinodaceae DQuandt NEBell amp Stech
Order Orthotrichales DixonOrthotrichaceae Arn
Order Orthodontiales NEBell AENewton amp DQuandtOrthodontiaceae Goffinet
Order Aulacomniales NEBell AENewton amp DQuandtAulacomniaceae Schimp
Order Rhizogoniales Goffinet amp WRBuckRhizogoniaceae Broth
Order Hypnodendrales NEBell AENewton amp DQuandtBraithwaiteaceae NEBell AENewton amp DQuandt Hypnodendra-ceae Broth Pterobryellaceae WRBuck amp Vitt Racopilaceae Kindb
Order Ptychomniales WRBuck CJCox AJShaw amp GoffinetPtychomniaceae MFleisch
Order Hookeriales MFleischDaltoniaceae Schimp Hookeriaceae Schimp HypopterygiaceaeMitt Leucomiaceae Broth Pilotrichaceae Kindb SaulomataceaeWRBuck CJCox AJShaw amp Goffinet Schimperobryaceae WR
17
Buck CJCox AJShaw amp GoffinetOrder Hypnales WRBuck amp Vitt
Amblystegiaceae GRoth Anomodontaceae Kindb BrachytheciaceaeSchimp Calliergonaceae Vanderpoorten Hedenaumls CJCox amp AJShaw Catagoniaceae WRBuck amp Ireland Climaciaceae KindbCryphaeaceae Schimp Echinodiaceae Broth Entodontaceae KindbFabroniaceae Schimp Fontinalaceae Schimp Helodiaceae OchyraHeterocladiaceae Ignatov amp Ignatova Hylocomiaceae MFleischHypnaceae Schimp Lembophyllaceae Broth LeptodontaceaeSchimp Lepyrodontaceae Broth Leskeaceae Schimp Leucodon-taceae Schimp Meteoriaceae Kindb Microtheciellaceae HAMillamp AJHarr Myriniaceae Schimp Myuriaceae MFleisch NeckeraceaeSchimp Orthorrhynchiaceae SHLin Phyllogoniaceae KindbPlagiotheciaceae MFleisch Pleuroziopsidaceae Ireland Prionodon-taceae Broth Pseudoleskeaceae Schimp PseudoleskeellaceaeIgnatov amp Ignatova Pterigynandraceae Schimp PterobryaceaeKindb Pylaisiaceae Schimp Pylaisiadelphaceae Goffinet amp WRBuck Regmatodontaceae Broth Rhytidiaceae Broth RigodiaceaeHACrum Rutenbergiaceae MFleisch Scorpidiaceae Ignatov ampIgnatova Sematophyllaceae Broth Sorapillaceae MFleisch Ste-reophyllaceae WRBuck amp Ireland Symphyodontaceae MFleischTheliaceae MFleisch Thuidiaceae Schimp TrachylomataceaeWRBuck amp Vitt
Acknowledgements
Sincere thanks are due to JLReveal (Ithaca) as well as WFPrudhomme van Reine and JFVeldkamp(Leiden) for comments and discussions about suprafamilial taxonomy to DQuandt (Dresden) for providingDNA from Rhacocarpus and Bartramiaceae species and to BGiesicke (Berlin) for technical assistance
References
BECKERT S H MUHLE D PRUCHNER amp V KNOOP (2001) The mitochondrial nad2 geneas a novel marker locus for phylogenetic analysis of early land plants a comparative analysis inmosses - Mol Phylogenet Evol 18 117-126
BELL NE amp AE NEWTON (2004) Systematic studies of non-hypnanaean pleurocarps establishinga phylogenetic framework for investigating the origins of pleurocarpy - In GOFFINET BV HOLLOWELL amp R MAGILL (eds) Molecular systematics of bryophytes Monogr Syst BotMissouri Bot Gard 98 290-319
BELL NE amp AE NEWTON (2007) Pleurocarpy in the Rhizogoniaceous grade - In NEWTONAE amp RS TANGNEY (eds) Pleurocarpous mosses systematics and evolution SystematicsAssociation Special Volume Series 71 41-64
BELL NE D QUANDT TJ OBRIEN amp AE NEWTON (2007) Taxonomy and phylogeny inthe earliest diverging pleurocarps square holes and bifurcating pegs - Bryologist 110 533-560
BORSCH T KW HILU D QUANDT V WILDE C NEINHUIS amp W BARTHLOTT(2003) Non-coding plastid trnT-trnF sequences reveal a well resolved phylogeny of basal angiosperms- J Evol Biol 16 558-576
18
BUCK WR (2007) The history of pleurocarp classification two steps forward one step back - InNEWTON AE amp RS TANGNEY (eds) Pleurocarpous mosses systematics and evolutionSystematics Association Special Volume Series 71 1-18
BUCK WR amp B GOFFINET (2000) Morphology and classification of mosses - In SHAWAJ amp B GOFFINET (eds) Bryophyte Biology pp 71-123 Cambridge University PressCambridge
CHIANG TY BA SCHAAL amp CI PENG (1998) Universal primers for amplification andsequencing a noncoding spacer between atpB and rbcL genes of chloroplast DNA - Bot Bull AcadSin 39 245-250
COX CJ B GOFFINET AE NEWTON AJ SHAW amp TAJ HEDDERSON (2000)Phylogenetic relationships among the diplolepideous-alternate mosses (Bryidae) inferred from nuclearand chloroplast DNA sequences - Bryologist 103 224-241
COX CJ B GOFFINET AJ SHAW amp SB BOLES (2004) Phylogenetic relationships amongthe mosses based on heterogeneous Bayesian analysis of multiple genes from multiple genomiccompartments - Syst Bot 29 234-250
CRANDALL-STOTLER B (1986) Morphogenesis developmental anatomy and bryophytephylogenetics contra-indications of monophyly - J Bryol 14 1-23
CROSBY MR RE MAGILL B ALLEN amp S HE (1999) A checklist of the mosses - MissouriBotanical Garden St Louis Missouri
DOWELD A (2001) Prosyllabus Tracheophytorum - GEOS Moscow i-lxxx + 110 pp
DOYLE JJ amp JL DOYLE (1990) Isolation of plant DNA from fresh tissue - Focus 12 13-15
DUFF RJ JC VILLAREAL DC CARGILL amp KS RENZAGLIA (2007) Progress andchallenges towards developing a phylogeny and classification of the hornworts - Bryologist 110214-243
FLEISCHER M (1920) Natuumlrliches System der Laubmoose - Hedwigia 61 390-400
FORREST LL EC DAVIS DG LONG BJ CRANDALL-STOTLER A CLARK ampML HOLLINGSWORTH (2006) Unraveling the evolutionary history of the liverworts (Marchantio-phyta) multiple taxa genomes and analyses - Bryologist 109 303-334
FRAHM J-P amp W FREY (1987) Moosflora 2 Aufl - UTB 1250 Stuttgart
FREY W (1977) Neue Vorstellungen uumlber die Verwandtschaftsgruppen und die Stammesgeschichteder Laubmoose - In FREY W H HURKA amp F OBERWINKLER (Hrsg) Beitraumlge zur Biologieder Pflanzen pp 117-139 Stuttgart
FREY W amp M STECH (2005) A morpho-molecular classification of the liverworts (Hepa-ticophytina Bryophyta) - Nova Hedwigia 81 55-78
FREY W M STECH amp K MEIszligNER (1999) Chloroplast DNA-relationship in palaeoaustralLopidium concinnum (Hypopterygiaceae Musci) An example of steno-evolution in mosses Studiesin austral temperate rain forest bryophytes 2 - Plant Syst Evol 218 67-75
GOFFINET B amp WR BUCK (2004) Systematics of Bryophyta (mosses) from molecules to arevised classification - In GOFFINET B V HOLLOWELL amp R MAGILL (eds) Molecularsystematics of bryophytes Monogr Syst Bot Missouri Bot Gard 98 205-239
GOFFINET B CJ COX AJ SHAW amp TAJ HEDDERSON (2001) The Bryophyta (mosses)Systematic and evolutionary inferences from an rps4 gene (cpDNA) phylogeny - Ann Bot 87191-208
GOFFINET B NJ WICKETT O WERNER RM ROS AJ SHAW amp CJ COX (2007)Distribution and phylogenetic significance of the 71-kb inversion in the plastid genome in Funariidae(Bryophyta) - Ann Bot 99 747-753
19
GROTH-MALONEK M D PRUCHNER F GREWE amp V KNOOP (2005) Ancestors oftrans-splicing mitochondrial introns support serial sister group relationships of hornworts and mosseswith vascular plants - Mol Biol Evol 22 117-125
HATTORI S amp H INOUE (1958) Preliminary report on Takakia lepidozioides - J Hattori BotLab 19 133-137
HE-NYGREacuteN X A JUSLEacuteN I AHONEN D GLENNY amp S PIIPPO (2006) Illuminating theevolutionary history of liverworts (Marchantiophyta) - towards a natural classification - Cladistics22 1-31
HEDDERSON TAJ DJ MURRAY CJ COX amp TL NOWELL (2004) Phylogeneticrelationships of haplolepideous mosses (Dicranidae) inferred from rps4 gene sequences - Syst Bot29 29-41
LA FARGE C BD MISHER JA WHEELER DP WALL K JOHANNES S SCHAFFERamp AJ SHAW (2000) Phylogenetic relationships within the haplolepideous mosses - Bryologist103 257-276
LA FARGE C AJ SHAW amp DH VITT (2002) The circumscription of the Dicranaceae(Bryopsida) based on the chloroplast regions trnL-trnF and rps4 - Syst Bot 27 435-452
MAGOMBO ZLK (2003) The phylogeny of basal peristomate mosses evidence from cpDNAand implications for peristome evolution - Syst Bot 28 24-38
MCNEILL J FR BARRIE HM BURDET V DEMOULIN DL HAWKSWORTHK MARHOLD DH NICOLSON J PRADO PC SILVA JE SKOG JH WIERSEMA ampNJ TURLAND (2006) International Code of Botanical Nomenclature (Vienna Code) - RegnumVegetabile 146 1-568
MUumlLLER K (2004) PRAP - computation of Bremer support for large data sets - Mol PhylogenetEvol 31 780-782
MUumlLLER K (2005) SeqState - primer design and sequence statistics for phylogenetic DNA datasets - Appl Bioinformatics 4 65-69
MUumlLLER K D QUANDT J MUumlLLER amp C NEINHUIS (2005) PhyDE v0992 PhylogeneticData Editor - httpwwwphydede
MURRAY BM (1988) Systematics of the Andreaeopsida (Bryophyta) two orders with links toTakakia - Nova Hedwigia Beih 90 289-336
NEWTON AE amp RS TANGNEY (eds) (2007) Pleurocarpous mosses systematics and evolutionSystematics Association Special Volume Series 71 CRC Press Boca Raton 434 pp
NEWTON AE CJ COX JG DUCKETT JA WHEELER B GOFFINET TAJ HEDDER-SON amp BD MISHLER (2000) Evolution of the major moss lineages Phylogenetic analyses basedon multiple gene sequences and morphology - Bryologist 103 187-211
NEWTON AE N WIKSTROumlM NE BELL LL FORREST amp MS IGNATOV (2007)Dating the diversification of the pleurocarpous mosses - In NEWTON AE amp RS TANGNEY(eds) Pleurocarpous mosses systematics and evolution Systematics Association Special VolumeSeries 71 337-366
NIXON KC (1999) The parsimony ratchet a new method for rapid parsimony analysis - Cladistics15 407-411
OBRIEN TJ (2007) The phylogenetic distribution of pleurocarpous mosses evidence fromcpDNA sequences - In NEWTON AE amp RS TANGNEY (eds) Pleurocarpous mossessystematics and evolution Systematics Association Special Volume Series 71 19-41
OCHYRA R (2002) Nomenclatural changes in subfamilies of the Dicranaceae - CryptogamieBryol 23 345-349
20
OCHYRA R J ŻARNOWIEC amp H BEDNAREK-OCHYRA (2003) Census catalogue ofPolish mosses - Biodiv Poland 3 1-372
PEDERSEN N amp AE NEWTON (2007) Phylogenetic and morphological studies within thePtychomniales with emphasis on the evolution of dwarf males - In NEWTON AE amp RSTANGNEY (eds) Pleurocarpous mosses systematics and evolution Systematics AssociationSpecial Volume Series 71 367-392
QUANDT D amp M STECH (2005) Molecular evolution and secondary structure of the chloroplasttrnL intron in bryophytes - Mol Phylogenet Evol 36 429-443
QUANDT D K MUumlLLER amp S HUTTUNEN (2003) Characterisation of the chloroplast DNApsbT-H region and the influence of dyad symmetrical elements on phylogenetic reconstructions -Plant Biol 5 400-410
QUANDT D K MUumlLLER M STECH W FREY KW HILU amp T BORSCH (2004) Molecularevolution of the chloroplast trnL-F-region in land plants - In GOFFINET B V HOLLOWELL ampR MAGILL (eds) Molecular systematics of bryophytes Monogr Syst Bot Missouri Bot Gard98 13-37
QUANDT D NE BELL amp M STECH (2007) Unravelling the knot the Pulchrinodaceae famnov (Bryales) - In KUumlRSCHNER H T PFEIFFER amp M STECH (eds) A Festschrift to Wolf-gang Frey - a scientists life between deserts and rain forests Nova Hedwigia Beih 131 21-39
QIU Y-L Y CHO JC COX amp JD PALMER (1998) The gain of three mitochondrial intronsidentifies liverworts as the earliest land plants - Nature 394 671-674
QIU Y-L L LI B WANG Z CHEN V KNOOP M GROTH-MALONEK O DOM-BROVSKA J LEE L KENT J REST GF ESTABROOK TA HENDRY DW TAYLORCM TESTA M AMBROS B CRANDALL-STOTLER J DUFF M STECH W FREYD QUANDT amp CC DAVIS (2006) The deepest divergences in land plants inferred fromphylogenomic evidence - Proc Natl Acad Sci USA 103 15511-15516
RENZAGLIA KS S SCHUETTE RJ DUFF R LIGRONE AJ SHAW BD MISHLER ampJG DUCKETT (2007) Bryophyte phylogeny Advancing the molecular and morphological frontiers- Bryologist 110 179-213
SAMIGULLIN TH SP YACENTYUK GV DEGTYARYEVA KM VALIEJO-ROMANVK BOBROVA I CAPESIUS WF MARTIN AV TROITSKY VR FILIN amp ASANTONOV (2002) Paraphyly of bryophytes and close relationships of hornworts and vascularplants inferred from analysis of chloroplast rDNA ITS (cpITS) sequences - Arctoa 11 31-43
SANG T DJ CRAWFORD amp TF STUESSY (1997) Chloroplast DNA phylogeny reticulateevolution and biogeography of Paeonia (Paeoniaceae) - Amer J Bot 84 1120-1136
SHAW AJ amp KS RENZAGLIA (2004) Phylogeny and diversification of bryophytes - AmerJ Bot 91 1557-1581
SHAW AJ CJ COX amp B GOFFINET (2005) Global patterns of moss diversity taxonomic andmolecular inferences - Taxon 54 337-352
STECH M (1999a) A reclassification of Dicranaceae (Bryopsida) based on non-coding cpDNAsequence data - J Hattori Bot Lab 86 137-159
STECH M (1999b) A molecular systematic contribution to the position of Amphidium Schimp(Rhabdoweisiaceae Bryopsida) - Nova Hedwigia 68 291-300
STECH M (2004) Supraspecific circumscription and classification of Campylopus Brid(Dicranaceae Bryopsida) based on molecular data - Syst Bot 29 817-824
STECH M amp D QUANDT (2006) Molecular evolution of the chloroplast atpB-rbcL spacer inbryophytes - In SHARMA AK amp A SHARMA (eds) Plant Genome Biodiversity and EvolutionVol 2 Part B pp 409-431 Science Publishers Enfield New Hampshire
21
STECH M D QUANDT amp W FREY (2003) Molecular circumscription of the hornworts(Antho-cerotophyta) based on the chloroplast DNA trnL-trnF region - J Plant Res 116 389-398
STOTLER RE amp B CRANDALL-STOTLER (2005) A revised classification of theAnthocerotophyta and a checklist of the hornworts of North America north of Mexico - Bryologist108 16-26
SWOFFORD DL (2002) PAUP Phylogenetic analysis using parsimony (and other methods)version 40b10 - Sunderland MA
TABERLET P L GIELLY G PAUTOU amp J BOUVET (1991) Universal primers for amplificationof three non-coding regions of chloroplast DNA - Plant Mol Biol 17 1105-1109
TSUBOTA H Y AGENO B ESTEacuteBANEZ T YAMAGUCHI amp H DEGUCHI (2003)Molecular phylogeny of the Grimmiales (Musci) based on chloroplast rbcL sequences - Hikobia 1455-70
TSUBOTA H E DE LUNA D GONZAacuteLEZ MS IGNATOV amp H DEGUCHI (2004) Molecularphylogenetics and ordinal relationships based on analyses of a large-scale data set of 600 rbcLsequences of mosses - Hikobia 14 149-170
VITT DH (1984) Classification of the Bryopsida - In SCHUSTER RM (ed) New Manual ofBryology 2 696-759 Hattori Botanical Laboratory Nichinan Japan
VITT DH B GOFFINET amp T HEDDERSON (1998) 8 The ordinal classification of the mossesquestions and answers for the 1990s - In BATES JW NW ASHTON amp JG DUCKETT (eds)Bryology for the twenty-first century British Bryol Soc pp 113-123
Received 3 September 2007 accepted in revised form 30 October 2007
11
Table 2 Taxon sampling and bootstrap support (BS) for Dicranidae Bryidae and orders within theBryidae in recent phylogenetic analyses (MP only) based on combined molecular markers Markersare given in square brackets (non-coding regions in bold) numbers of included taxa in brackets ++respective clade present with ge 80 BS + clade present with lt 80 BS - clade not present no oronly one representative included
Bell amp Newton OBrien Quandt et al Bell et al this study(2004) (2007) (2007) (2007)
[rbcL rps4 [atpB atpB- [rbcL rps4 [rbcL rps4 [atpB-rbcLnad5] rbcL rbcL trnL-F nad5] trnL-F nad5] psbA-trnH
rps4 trnL-F] trnL]
Dicranidae + (2) + (4) ++ (3) (1) ++ (19)Bryidae ++ (57) + (53) ++ (52) ++ (98) ++ (58)Hedwigiales ++ (2) (1) ++ (2) ++ (2) - (3)Bartramiales ++ (2) ++ (4) ++ (4) ++ (3) - (4)Splachnales (0) ++ (2) ++ (3) ++ (2) ++ (5)Bryales - (4) - (5) ++ (18) + (17) - (8)Orthotrichales (1) ++ (3) ++ (3) ++ (2) ++ (4)Orthodontiales + (4) + (4) + (3) + (6) - (3)Aulacomniales + (6) + (7) ++ (2) + (7) + (3)Rhizogoniales ++ (13) + (8) ++ (5) ++ (14) - (3)Hypnodendrales ++ (13) + (7) ++ (4) ++ (29) ++ (6)Ptychomniales ++ (3) ++ (3) (1) ++ (4) (1)Hookeriales - (4) + (2) (1) + (2) + (8)Hypnales - (5) - (7) ++ (5) ++ (10) + (10)
summarised under the informal node based name pleurcarpids (Bell et al 2007)and can be distinguished from a basal grade of acrocarpous or cladocarpous lineages(Hedwigiales to Orthotrichales) Within the latter monophyly of BartramialesSplachnales and Orthotrichales is well-supported in all analyses including two ormore taxa except Bartramiales in the present data set (cf Fig 1) In contrast Bryalesreceive significant support less frequently (but see Bell et al 2007 Quandt et al2007) Hedwigiales are well supported if only Hedwigia (Hedwigiaceae) andRhacocarpus (Rhacocarpaceae) are included whereas the monospecific Helicophyllum(Helicophyllaceae) is not closely related to these taxa but shows affinities withBartramiales (Goffinet et al 2001 this study) With respect to the differentmorphologies of Helicophyllaceae and Bartramiaceae however the former shouldbe separated at ordinal level (see taxonomy)
Clarifying relationships of the Orthotrichales is still a difficult issue Analyses ofsingle chloroplast markers or parsimony analyses of combined markers from differentgenomes mostly indicated a close relationship either with Splachnales (eg Cox etal 2000 Newton et al 2000 Tsubota et al 2004 Quandt et al 2007) or with thepleurocarpids (Goffinet et al 2001 this study) Although none of these alternativesis well-supported the latter seems more likely with regard to the moderately tomaximally supported Orthotrichales - pleurocarpid sister group relationship in allanalyses of mitochondrial data and in likelihood analyses of combined plastidmitochondrial markers (Beckert et al 2001 Quandt et al 2007)
12
The molecular polyphyly of Rhizogoniaceae (eg Bell amp Newton 2004) was solvedby the transfer of rhizogonioid genera into broadly defined Aulacomniaceae andOrthodontiaceae (Bell et al 2007) which now include both acrocarpous andpleurocarpous taxa These systematic changes are also comprehensible by non-molecular characters such as morphological traits shared by Mesochaete andAulacomnium heterostichum (Hedw) Bruch amp Schimp or the variously reducedperistomes of Orthodontiaceae pp in contrast to the generally fully developed Bryum-type peristomes of rhizogonioid and hypnodendroid mosses (Bell et al 2007) Theposition of the solely pleurocarpous Hypnodendrales sister to the former Hypnidaeled to the recognition of the informal group core pleurocarps (Bell et al 2007)The former Hypnidae (Ptychomniales Hookeriales and Hypnales summarised ashomocostate pleurocarps) are monophyletic in most molecular analyses (eg Goffinetet al 2001 Tsubota et al 2004 Bell et al 2007) with Ptychomniales being well-supported (Pedersen amp Newton 2007 Table 2) Clarifying relationships betweenHookeriales and Hypnales and within the latter is still a challenge but recent molecularstudies seem to support a sister group relationship of both orders (Bell et al 2007present study)
Phylogenetic utility of non-coding plastid markers
Non-coding plastid markers that comprise both variable and conserved regionssuch as the trnL
UAA intron have repeatedly been shown to possess potential for
resolving relationships at high taxonomic levels (eg Borsch et al 2003 Quandtet al 2004) Both the trnL intron and atpB-rbcL spacer were characterised indetail in mosses with respect to their structure and molecular evolution (Quandt ampStech 2005 Stech amp Quandt 2006) They include conservative regions that can beunambiguosly aligned and even parts of the more variable regions can be used ifrepeats hairpin loops etc are correctly identified and adequately treated in thephylogenetic analyses (eg Quandt et al 2003 Quandt amp Stech 2005) Using theatpB-rbcL spacer alone (Stech amp Quandt 2006) relationships of the major mosslineages were largely consistent with the ldquototal evidencerdquo molecular tree of Goffinetamp Buck (2004) However in addition to general limitations that result from singlemarker analyses the use of non-coding markers may pose further problems suchas a high amount of homoplasy resulting in low resolution or low statistical supportfor many clades Therefore several recent molecular studies of relationships withinBryidae have employed both coding and non-coding markers (Table 2)Nevertheless the usefulness of analyses of combined non-coding plastid markerscannot be ruled out In fact Fig 1 and Table 2 indicate a phylogenetic signal inthe present data set as many clades are recovered that are usually also resolvedin analyses of coding or combined coding and non-coding markers Especiallywith regard to statistical support however the present analysis is inferior tothose of other recent data sets especially Bell et al (2007) and Quandt et al(2007) In addition the non-coding markers used here are of different suitabilityand even the two intergenic spacers differ considerably from each other ThepsbA-trnH spacer contributes much less to the trees resolution than the atpB-rbcL spacer first because it is much shorter and second because relatively largeparts are attributed to hairpin loops or otherwise hypervariable regions These
13
results indicate that future studies should evaluate the molecular evolution andphylogenetic potential of new markers both coding and con-coding and choosethe most suitable ones in a combined analysis to resolve the remaining uncertaintiesin moss phylogeny
Taxonomy
Takakiaceae Stech amp WFrey stat nov
Plantae virides nusquam rhizophorae sine protonemate e caudicis rhizomatis erectae Caudicesrhizomati et axes geotropi radiformes frequenter intercalariter ramificantes sine phyllidiis cumpapillis mucilaginis rostratis Caules phyllidiiferi saepe furcati Phyllidia sine lamina et costadistincta profunde 2-4(-5)-lobata pluristratosa tristicha sed torsione spiraliter disposita Filumcentralium in ambabus generationibus (axibus gametophyti et setis) adest Plantae dioicae Antheridiaet archegonia nuda Sporophytum terminale solitarium Seta persistens Capsula tortilis admaturitatem schizocarpa secus unam rimam spiralem longitudinalem dehiscens Stomata etoperculum absunt peristomium nullum Calyptra mitriformis
TYPUS Takakia SHatt amp Inoue J Hattori Bot Lab 19 137 1958
Takakiaceae SHatt amp Inoue J Hattori Bot Lab 19 137 1958 nom inval (Art 411)
Takakiales Stech amp WFrey stat nov
Based on Takakiaceae Stech amp WFrey Nova Hedwigia 86 13 2008
TYPUS Takakia SHatt amp Inoue J Hattori Bot Lab 19 137 1958
Takakiales SHatt amp Inoue J Hattori Bot Lab 19 137 1958 nom inval
Takakiales SHatt amp Inoue ex RMSchust J Hattori Bot Lab 26 224 1963 nom inval (cumdescr latin)
Takakiopsida Stech amp WFrey statnov
Based on Takakiaceae Stech amp WFrey Nova Hedwigia 86 13 2008
TYPUS Takakia SHatt amp Inoue J Hattori Bot Lab 19 137 1958
Takakiopsida Goffinet amp WRBuck Monogr Syst Bot Missouri Bot Gard 98 232 2004 nominval
Takakiopsida Jia et al Acta Phytotax Sin 41 350 351 2003 nom nud
Takakiopsida Wang amp Wu Fl Bryophyt Sin 8 447 2004 nom inval (cum descr latin)
Takakiophytina Stech amp WFrey stat nov
Based on Takakiaceae Stech amp WFrey Nova Hedwigia 86 13 2008
TYPUS Takakia SHatt amp Inoue JHattori Bot Lab 19 137 1958
Gigaspermidae Stech amp WFrey subclass nov
Plantae acrocarpae terrestres stoloniferae ramis brevibus erectis Folia unicostata cellulis laxislaevibus Capsula plerumque valde rugosa gymnostomatica vel cleistocarpa stomata cum duabuscellulis sociis Ab Funariidis et Encalyptidis charactere phylogenomico (71-kb inversio abest)separatae
14
TYPUS Gigaspermum Lindb Oumlfversigt af Foumlrhandlingar Kongl Svenska Vetenskaps-Akademien21 599 1865
Amphidiaceae Stech stat nov
Based on Dicranaceae subfam Amphidioideae Ochyra in Ochyra Zarnowiec amp Bednarek-OchyraCens Cat Polish Mosses 110 2003
TYPUS Amphidium Schimp Coroll Bryol Eur 39 1856
Amphidiaceae AJESm Moss Fl Britain Ireland 2nd ed 657 2004 nom inval descr angl
Dicranellaceae Stech stat nov
Based on Dicranaceae subfam Dicranelloideae Lindb Utkast Eur Bladmoss 33 1878[lsquoUnderfamilje Dicranelleaersquo]
TYPUS Dicranella (MuumlllHal) Schimp Coroll Bryol Eur 13 1856
Oncophoraceae Stech stat nov
Based on Dicranaceae subfam Oncophoroideae Lindb Utkast Eur Bladmoss 34 1878[lsquoUnderfamilje Oncophoreaersquo]
TYPUS Oncophorus (Brid) Brid Bryol Univ 1 389 1826
Hypodontiaceae Stech fam nov
Plantae robustae characteribus morphologicis Pottiaceis et Calymperaceis similes sedcharacteribus molecularicis separatae Bracteae perichaetiales internae e basi vaginantes subulataevel aristatae Capsula aspectu succulenta cellulae exothecii incrassatae annulus magnopereabsens Peristomii dentes breves triangulati incurvati aurantiaci leves vel infirme verrucosiCalyptra cucullata
TYPUS Hypodontium MuumlllHal Hedwigia 38 96 1899
Helicophyllales Stech amp WFrey ord nov
Plantae acrocarpae prostratae tomentosae Folia dimorpha in duas series laterales et unam seriemventralem divisa Costa percurrens Cellulae hexagonae ad subquadratae papillosae Capsula immersacupulata ad oblonga infra orificium abrupte incurvata stomata destituta Peristomium nullum Sporaeisomorphae heteropolares granulatae
TYPUS Helicophyllum Brid Bryol Univ 2 771 1827
Synopsis of the suprageneric classification of BryophytaAuthor citations are in accordance with Art 492 of the Vienna Code (McNeill et al 2006)
Subdivision Takakiophytina Stech amp WFreyClass Takakiopsida Stech amp WFrey
Order Takakiales Stech amp WFreyTakakiaceae Stech amp WFrey
Subdivision Sphagnophytina DoweldClass Sphagnopsida Schimp
Order Sphagnales Limpr
15
Sphagnaceae DumortOrder Ambuchananiales Seppelt amp HACrum
Ambuchananiaceae Seppelt amp HACrumSubdivision Bryophytina Engler
Class Andreaeopsida JHSchaffnSubclass Andreaeidae Engl
Order Andreaeales LimprAndreaeaceae Dumort
Subclass Andreaeobryidae OchyraOrder Andreaeobryales BMMurray
Andreaeobryaceae Steere amp BMMurrayClass Oedipodiopsida Goffinet amp WRBuck
Order Oedipodiales Goffinet amp WRBuckOedipodiaceae Schimp
Class Tetraphidopsida Goffinet amp WRBuckOrder Tetraphidales MFleisch
Tetraphidaceae SchimpClass Polytrichopsida Doweld
Order Polytrichales MFleischPolytrichaceae Schwaumlgr
Class Bryopsida PaxSubclass Buxbaumiidae Doweld
Order Buxbaumiales MFleischBuxbaumiaceae Schimp
Subclass Diphysciidae OchyraOrder Diphysciales MFleisch
Diphysciaceae MFleischSubclass Timmiidae Ochyra
Order Timmiales OchyraTimmiaceae Schimp
Subclass Encalyptidae Ochyra Żarnowiec amp Bednarek-OchyraOrder Encalyptales Dixon
Encalyptaceae SchimpSubclass Funariidae Ochyra
Order Funariales MFleischFunariaceae Schwaumlgr Disceliaceae Schimp
Subclass Gigaspermidae Stech amp WFreyOrder Gigaspermales Goffinet Wickett OWerner Ros AJShaw amp CJCox
Gigaspermaceae LindbSubclass Dicranidae Doweld
Order Catoscopiales Ignatov amp IgnatovaCatoscopiaceae Broth
Order Scouleriales Goffinet amp WRBuckDrummondiaceae Goffinet Scouleriaceae SPChurchill
Order Bryoxiphiales HACrum amp LEAndersonBryoxiphiaceae Besch
16
Order Grimmiales MFleischGrimmiaceae Arn Ptychomitriaceae Schimp Seligeriaceae Schimp
Order Archidiales LimprArchidiaceae Schimp
Order Mitteniales ShawMitteniaceae Broth
Order Dicranales HPhilib ex MFleischAmphidiaceae Stech Aongstroemiaceae De Not BruchiaceaeSchimp Calymperaceae Kindb Dicranaceae Schimp Dicranel-laceae Stech Ditrichaceae Limpr Erpodiaceae Broth EustichiaceaeBroth Fissidentaceae Schimp Leucobryaceae Schimp Onco-phoraceae Stech Rhachitheciaceae HRob Schistostegaceae SchimpViridivelleraceae IGStone Wardiaceae Welch
Order Pottiales MFleischEphemeraceae Schimp Hypodontiaceae Stech PleurophascaceaeBroth Pottiaceae Schimp Serpotortellaceae WDReese amp RHZander
Subclass Bryidae EnglOrder Hedwigiales Ochyra
Hedwigiaceae Schimp Rhacocarpaceae KindbOrder Helicophyllales Stech amp WFrey
Helicophyllaceae BrothOrder Bartramiales DQuandt NEBell amp Stech
Bartramiaceae SchwaumlgrOrder Splachnales Ochyra
Meesiaceae Schimp Splachnaceae Grev amp ArnOrder Bryales Limpr
Bryaceae Schwaumlgr Leptostomataceae Schwaumlgr Mniaceae SchwaumlgrPhyllodrepaniaceae Crosby Pseudoditrichaceae Steere amp ZIwatsPulchrinodaceae DQuandt NEBell amp Stech
Order Orthotrichales DixonOrthotrichaceae Arn
Order Orthodontiales NEBell AENewton amp DQuandtOrthodontiaceae Goffinet
Order Aulacomniales NEBell AENewton amp DQuandtAulacomniaceae Schimp
Order Rhizogoniales Goffinet amp WRBuckRhizogoniaceae Broth
Order Hypnodendrales NEBell AENewton amp DQuandtBraithwaiteaceae NEBell AENewton amp DQuandt Hypnodendra-ceae Broth Pterobryellaceae WRBuck amp Vitt Racopilaceae Kindb
Order Ptychomniales WRBuck CJCox AJShaw amp GoffinetPtychomniaceae MFleisch
Order Hookeriales MFleischDaltoniaceae Schimp Hookeriaceae Schimp HypopterygiaceaeMitt Leucomiaceae Broth Pilotrichaceae Kindb SaulomataceaeWRBuck CJCox AJShaw amp Goffinet Schimperobryaceae WR
17
Buck CJCox AJShaw amp GoffinetOrder Hypnales WRBuck amp Vitt
Amblystegiaceae GRoth Anomodontaceae Kindb BrachytheciaceaeSchimp Calliergonaceae Vanderpoorten Hedenaumls CJCox amp AJShaw Catagoniaceae WRBuck amp Ireland Climaciaceae KindbCryphaeaceae Schimp Echinodiaceae Broth Entodontaceae KindbFabroniaceae Schimp Fontinalaceae Schimp Helodiaceae OchyraHeterocladiaceae Ignatov amp Ignatova Hylocomiaceae MFleischHypnaceae Schimp Lembophyllaceae Broth LeptodontaceaeSchimp Lepyrodontaceae Broth Leskeaceae Schimp Leucodon-taceae Schimp Meteoriaceae Kindb Microtheciellaceae HAMillamp AJHarr Myriniaceae Schimp Myuriaceae MFleisch NeckeraceaeSchimp Orthorrhynchiaceae SHLin Phyllogoniaceae KindbPlagiotheciaceae MFleisch Pleuroziopsidaceae Ireland Prionodon-taceae Broth Pseudoleskeaceae Schimp PseudoleskeellaceaeIgnatov amp Ignatova Pterigynandraceae Schimp PterobryaceaeKindb Pylaisiaceae Schimp Pylaisiadelphaceae Goffinet amp WRBuck Regmatodontaceae Broth Rhytidiaceae Broth RigodiaceaeHACrum Rutenbergiaceae MFleisch Scorpidiaceae Ignatov ampIgnatova Sematophyllaceae Broth Sorapillaceae MFleisch Ste-reophyllaceae WRBuck amp Ireland Symphyodontaceae MFleischTheliaceae MFleisch Thuidiaceae Schimp TrachylomataceaeWRBuck amp Vitt
Acknowledgements
Sincere thanks are due to JLReveal (Ithaca) as well as WFPrudhomme van Reine and JFVeldkamp(Leiden) for comments and discussions about suprafamilial taxonomy to DQuandt (Dresden) for providingDNA from Rhacocarpus and Bartramiaceae species and to BGiesicke (Berlin) for technical assistance
References
BECKERT S H MUHLE D PRUCHNER amp V KNOOP (2001) The mitochondrial nad2 geneas a novel marker locus for phylogenetic analysis of early land plants a comparative analysis inmosses - Mol Phylogenet Evol 18 117-126
BELL NE amp AE NEWTON (2004) Systematic studies of non-hypnanaean pleurocarps establishinga phylogenetic framework for investigating the origins of pleurocarpy - In GOFFINET BV HOLLOWELL amp R MAGILL (eds) Molecular systematics of bryophytes Monogr Syst BotMissouri Bot Gard 98 290-319
BELL NE amp AE NEWTON (2007) Pleurocarpy in the Rhizogoniaceous grade - In NEWTONAE amp RS TANGNEY (eds) Pleurocarpous mosses systematics and evolution SystematicsAssociation Special Volume Series 71 41-64
BELL NE D QUANDT TJ OBRIEN amp AE NEWTON (2007) Taxonomy and phylogeny inthe earliest diverging pleurocarps square holes and bifurcating pegs - Bryologist 110 533-560
BORSCH T KW HILU D QUANDT V WILDE C NEINHUIS amp W BARTHLOTT(2003) Non-coding plastid trnT-trnF sequences reveal a well resolved phylogeny of basal angiosperms- J Evol Biol 16 558-576
18
BUCK WR (2007) The history of pleurocarp classification two steps forward one step back - InNEWTON AE amp RS TANGNEY (eds) Pleurocarpous mosses systematics and evolutionSystematics Association Special Volume Series 71 1-18
BUCK WR amp B GOFFINET (2000) Morphology and classification of mosses - In SHAWAJ amp B GOFFINET (eds) Bryophyte Biology pp 71-123 Cambridge University PressCambridge
CHIANG TY BA SCHAAL amp CI PENG (1998) Universal primers for amplification andsequencing a noncoding spacer between atpB and rbcL genes of chloroplast DNA - Bot Bull AcadSin 39 245-250
COX CJ B GOFFINET AE NEWTON AJ SHAW amp TAJ HEDDERSON (2000)Phylogenetic relationships among the diplolepideous-alternate mosses (Bryidae) inferred from nuclearand chloroplast DNA sequences - Bryologist 103 224-241
COX CJ B GOFFINET AJ SHAW amp SB BOLES (2004) Phylogenetic relationships amongthe mosses based on heterogeneous Bayesian analysis of multiple genes from multiple genomiccompartments - Syst Bot 29 234-250
CRANDALL-STOTLER B (1986) Morphogenesis developmental anatomy and bryophytephylogenetics contra-indications of monophyly - J Bryol 14 1-23
CROSBY MR RE MAGILL B ALLEN amp S HE (1999) A checklist of the mosses - MissouriBotanical Garden St Louis Missouri
DOWELD A (2001) Prosyllabus Tracheophytorum - GEOS Moscow i-lxxx + 110 pp
DOYLE JJ amp JL DOYLE (1990) Isolation of plant DNA from fresh tissue - Focus 12 13-15
DUFF RJ JC VILLAREAL DC CARGILL amp KS RENZAGLIA (2007) Progress andchallenges towards developing a phylogeny and classification of the hornworts - Bryologist 110214-243
FLEISCHER M (1920) Natuumlrliches System der Laubmoose - Hedwigia 61 390-400
FORREST LL EC DAVIS DG LONG BJ CRANDALL-STOTLER A CLARK ampML HOLLINGSWORTH (2006) Unraveling the evolutionary history of the liverworts (Marchantio-phyta) multiple taxa genomes and analyses - Bryologist 109 303-334
FRAHM J-P amp W FREY (1987) Moosflora 2 Aufl - UTB 1250 Stuttgart
FREY W (1977) Neue Vorstellungen uumlber die Verwandtschaftsgruppen und die Stammesgeschichteder Laubmoose - In FREY W H HURKA amp F OBERWINKLER (Hrsg) Beitraumlge zur Biologieder Pflanzen pp 117-139 Stuttgart
FREY W amp M STECH (2005) A morpho-molecular classification of the liverworts (Hepa-ticophytina Bryophyta) - Nova Hedwigia 81 55-78
FREY W M STECH amp K MEIszligNER (1999) Chloroplast DNA-relationship in palaeoaustralLopidium concinnum (Hypopterygiaceae Musci) An example of steno-evolution in mosses Studiesin austral temperate rain forest bryophytes 2 - Plant Syst Evol 218 67-75
GOFFINET B amp WR BUCK (2004) Systematics of Bryophyta (mosses) from molecules to arevised classification - In GOFFINET B V HOLLOWELL amp R MAGILL (eds) Molecularsystematics of bryophytes Monogr Syst Bot Missouri Bot Gard 98 205-239
GOFFINET B CJ COX AJ SHAW amp TAJ HEDDERSON (2001) The Bryophyta (mosses)Systematic and evolutionary inferences from an rps4 gene (cpDNA) phylogeny - Ann Bot 87191-208
GOFFINET B NJ WICKETT O WERNER RM ROS AJ SHAW amp CJ COX (2007)Distribution and phylogenetic significance of the 71-kb inversion in the plastid genome in Funariidae(Bryophyta) - Ann Bot 99 747-753
19
GROTH-MALONEK M D PRUCHNER F GREWE amp V KNOOP (2005) Ancestors oftrans-splicing mitochondrial introns support serial sister group relationships of hornworts and mosseswith vascular plants - Mol Biol Evol 22 117-125
HATTORI S amp H INOUE (1958) Preliminary report on Takakia lepidozioides - J Hattori BotLab 19 133-137
HE-NYGREacuteN X A JUSLEacuteN I AHONEN D GLENNY amp S PIIPPO (2006) Illuminating theevolutionary history of liverworts (Marchantiophyta) - towards a natural classification - Cladistics22 1-31
HEDDERSON TAJ DJ MURRAY CJ COX amp TL NOWELL (2004) Phylogeneticrelationships of haplolepideous mosses (Dicranidae) inferred from rps4 gene sequences - Syst Bot29 29-41
LA FARGE C BD MISHER JA WHEELER DP WALL K JOHANNES S SCHAFFERamp AJ SHAW (2000) Phylogenetic relationships within the haplolepideous mosses - Bryologist103 257-276
LA FARGE C AJ SHAW amp DH VITT (2002) The circumscription of the Dicranaceae(Bryopsida) based on the chloroplast regions trnL-trnF and rps4 - Syst Bot 27 435-452
MAGOMBO ZLK (2003) The phylogeny of basal peristomate mosses evidence from cpDNAand implications for peristome evolution - Syst Bot 28 24-38
MCNEILL J FR BARRIE HM BURDET V DEMOULIN DL HAWKSWORTHK MARHOLD DH NICOLSON J PRADO PC SILVA JE SKOG JH WIERSEMA ampNJ TURLAND (2006) International Code of Botanical Nomenclature (Vienna Code) - RegnumVegetabile 146 1-568
MUumlLLER K (2004) PRAP - computation of Bremer support for large data sets - Mol PhylogenetEvol 31 780-782
MUumlLLER K (2005) SeqState - primer design and sequence statistics for phylogenetic DNA datasets - Appl Bioinformatics 4 65-69
MUumlLLER K D QUANDT J MUumlLLER amp C NEINHUIS (2005) PhyDE v0992 PhylogeneticData Editor - httpwwwphydede
MURRAY BM (1988) Systematics of the Andreaeopsida (Bryophyta) two orders with links toTakakia - Nova Hedwigia Beih 90 289-336
NEWTON AE amp RS TANGNEY (eds) (2007) Pleurocarpous mosses systematics and evolutionSystematics Association Special Volume Series 71 CRC Press Boca Raton 434 pp
NEWTON AE CJ COX JG DUCKETT JA WHEELER B GOFFINET TAJ HEDDER-SON amp BD MISHLER (2000) Evolution of the major moss lineages Phylogenetic analyses basedon multiple gene sequences and morphology - Bryologist 103 187-211
NEWTON AE N WIKSTROumlM NE BELL LL FORREST amp MS IGNATOV (2007)Dating the diversification of the pleurocarpous mosses - In NEWTON AE amp RS TANGNEY(eds) Pleurocarpous mosses systematics and evolution Systematics Association Special VolumeSeries 71 337-366
NIXON KC (1999) The parsimony ratchet a new method for rapid parsimony analysis - Cladistics15 407-411
OBRIEN TJ (2007) The phylogenetic distribution of pleurocarpous mosses evidence fromcpDNA sequences - In NEWTON AE amp RS TANGNEY (eds) Pleurocarpous mossessystematics and evolution Systematics Association Special Volume Series 71 19-41
OCHYRA R (2002) Nomenclatural changes in subfamilies of the Dicranaceae - CryptogamieBryol 23 345-349
20
OCHYRA R J ŻARNOWIEC amp H BEDNAREK-OCHYRA (2003) Census catalogue ofPolish mosses - Biodiv Poland 3 1-372
PEDERSEN N amp AE NEWTON (2007) Phylogenetic and morphological studies within thePtychomniales with emphasis on the evolution of dwarf males - In NEWTON AE amp RSTANGNEY (eds) Pleurocarpous mosses systematics and evolution Systematics AssociationSpecial Volume Series 71 367-392
QUANDT D amp M STECH (2005) Molecular evolution and secondary structure of the chloroplasttrnL intron in bryophytes - Mol Phylogenet Evol 36 429-443
QUANDT D K MUumlLLER amp S HUTTUNEN (2003) Characterisation of the chloroplast DNApsbT-H region and the influence of dyad symmetrical elements on phylogenetic reconstructions -Plant Biol 5 400-410
QUANDT D K MUumlLLER M STECH W FREY KW HILU amp T BORSCH (2004) Molecularevolution of the chloroplast trnL-F-region in land plants - In GOFFINET B V HOLLOWELL ampR MAGILL (eds) Molecular systematics of bryophytes Monogr Syst Bot Missouri Bot Gard98 13-37
QUANDT D NE BELL amp M STECH (2007) Unravelling the knot the Pulchrinodaceae famnov (Bryales) - In KUumlRSCHNER H T PFEIFFER amp M STECH (eds) A Festschrift to Wolf-gang Frey - a scientists life between deserts and rain forests Nova Hedwigia Beih 131 21-39
QIU Y-L Y CHO JC COX amp JD PALMER (1998) The gain of three mitochondrial intronsidentifies liverworts as the earliest land plants - Nature 394 671-674
QIU Y-L L LI B WANG Z CHEN V KNOOP M GROTH-MALONEK O DOM-BROVSKA J LEE L KENT J REST GF ESTABROOK TA HENDRY DW TAYLORCM TESTA M AMBROS B CRANDALL-STOTLER J DUFF M STECH W FREYD QUANDT amp CC DAVIS (2006) The deepest divergences in land plants inferred fromphylogenomic evidence - Proc Natl Acad Sci USA 103 15511-15516
RENZAGLIA KS S SCHUETTE RJ DUFF R LIGRONE AJ SHAW BD MISHLER ampJG DUCKETT (2007) Bryophyte phylogeny Advancing the molecular and morphological frontiers- Bryologist 110 179-213
SAMIGULLIN TH SP YACENTYUK GV DEGTYARYEVA KM VALIEJO-ROMANVK BOBROVA I CAPESIUS WF MARTIN AV TROITSKY VR FILIN amp ASANTONOV (2002) Paraphyly of bryophytes and close relationships of hornworts and vascularplants inferred from analysis of chloroplast rDNA ITS (cpITS) sequences - Arctoa 11 31-43
SANG T DJ CRAWFORD amp TF STUESSY (1997) Chloroplast DNA phylogeny reticulateevolution and biogeography of Paeonia (Paeoniaceae) - Amer J Bot 84 1120-1136
SHAW AJ amp KS RENZAGLIA (2004) Phylogeny and diversification of bryophytes - AmerJ Bot 91 1557-1581
SHAW AJ CJ COX amp B GOFFINET (2005) Global patterns of moss diversity taxonomic andmolecular inferences - Taxon 54 337-352
STECH M (1999a) A reclassification of Dicranaceae (Bryopsida) based on non-coding cpDNAsequence data - J Hattori Bot Lab 86 137-159
STECH M (1999b) A molecular systematic contribution to the position of Amphidium Schimp(Rhabdoweisiaceae Bryopsida) - Nova Hedwigia 68 291-300
STECH M (2004) Supraspecific circumscription and classification of Campylopus Brid(Dicranaceae Bryopsida) based on molecular data - Syst Bot 29 817-824
STECH M amp D QUANDT (2006) Molecular evolution of the chloroplast atpB-rbcL spacer inbryophytes - In SHARMA AK amp A SHARMA (eds) Plant Genome Biodiversity and EvolutionVol 2 Part B pp 409-431 Science Publishers Enfield New Hampshire
21
STECH M D QUANDT amp W FREY (2003) Molecular circumscription of the hornworts(Antho-cerotophyta) based on the chloroplast DNA trnL-trnF region - J Plant Res 116 389-398
STOTLER RE amp B CRANDALL-STOTLER (2005) A revised classification of theAnthocerotophyta and a checklist of the hornworts of North America north of Mexico - Bryologist108 16-26
SWOFFORD DL (2002) PAUP Phylogenetic analysis using parsimony (and other methods)version 40b10 - Sunderland MA
TABERLET P L GIELLY G PAUTOU amp J BOUVET (1991) Universal primers for amplificationof three non-coding regions of chloroplast DNA - Plant Mol Biol 17 1105-1109
TSUBOTA H Y AGENO B ESTEacuteBANEZ T YAMAGUCHI amp H DEGUCHI (2003)Molecular phylogeny of the Grimmiales (Musci) based on chloroplast rbcL sequences - Hikobia 1455-70
TSUBOTA H E DE LUNA D GONZAacuteLEZ MS IGNATOV amp H DEGUCHI (2004) Molecularphylogenetics and ordinal relationships based on analyses of a large-scale data set of 600 rbcLsequences of mosses - Hikobia 14 149-170
VITT DH (1984) Classification of the Bryopsida - In SCHUSTER RM (ed) New Manual ofBryology 2 696-759 Hattori Botanical Laboratory Nichinan Japan
VITT DH B GOFFINET amp T HEDDERSON (1998) 8 The ordinal classification of the mossesquestions and answers for the 1990s - In BATES JW NW ASHTON amp JG DUCKETT (eds)Bryology for the twenty-first century British Bryol Soc pp 113-123
Received 3 September 2007 accepted in revised form 30 October 2007
12
The molecular polyphyly of Rhizogoniaceae (eg Bell amp Newton 2004) was solvedby the transfer of rhizogonioid genera into broadly defined Aulacomniaceae andOrthodontiaceae (Bell et al 2007) which now include both acrocarpous andpleurocarpous taxa These systematic changes are also comprehensible by non-molecular characters such as morphological traits shared by Mesochaete andAulacomnium heterostichum (Hedw) Bruch amp Schimp or the variously reducedperistomes of Orthodontiaceae pp in contrast to the generally fully developed Bryum-type peristomes of rhizogonioid and hypnodendroid mosses (Bell et al 2007) Theposition of the solely pleurocarpous Hypnodendrales sister to the former Hypnidaeled to the recognition of the informal group core pleurocarps (Bell et al 2007)The former Hypnidae (Ptychomniales Hookeriales and Hypnales summarised ashomocostate pleurocarps) are monophyletic in most molecular analyses (eg Goffinetet al 2001 Tsubota et al 2004 Bell et al 2007) with Ptychomniales being well-supported (Pedersen amp Newton 2007 Table 2) Clarifying relationships betweenHookeriales and Hypnales and within the latter is still a challenge but recent molecularstudies seem to support a sister group relationship of both orders (Bell et al 2007present study)
Phylogenetic utility of non-coding plastid markers
Non-coding plastid markers that comprise both variable and conserved regionssuch as the trnL
UAA intron have repeatedly been shown to possess potential for
resolving relationships at high taxonomic levels (eg Borsch et al 2003 Quandtet al 2004) Both the trnL intron and atpB-rbcL spacer were characterised indetail in mosses with respect to their structure and molecular evolution (Quandt ampStech 2005 Stech amp Quandt 2006) They include conservative regions that can beunambiguosly aligned and even parts of the more variable regions can be used ifrepeats hairpin loops etc are correctly identified and adequately treated in thephylogenetic analyses (eg Quandt et al 2003 Quandt amp Stech 2005) Using theatpB-rbcL spacer alone (Stech amp Quandt 2006) relationships of the major mosslineages were largely consistent with the ldquototal evidencerdquo molecular tree of Goffinetamp Buck (2004) However in addition to general limitations that result from singlemarker analyses the use of non-coding markers may pose further problems suchas a high amount of homoplasy resulting in low resolution or low statistical supportfor many clades Therefore several recent molecular studies of relationships withinBryidae have employed both coding and non-coding markers (Table 2)Nevertheless the usefulness of analyses of combined non-coding plastid markerscannot be ruled out In fact Fig 1 and Table 2 indicate a phylogenetic signal inthe present data set as many clades are recovered that are usually also resolvedin analyses of coding or combined coding and non-coding markers Especiallywith regard to statistical support however the present analysis is inferior tothose of other recent data sets especially Bell et al (2007) and Quandt et al(2007) In addition the non-coding markers used here are of different suitabilityand even the two intergenic spacers differ considerably from each other ThepsbA-trnH spacer contributes much less to the trees resolution than the atpB-rbcL spacer first because it is much shorter and second because relatively largeparts are attributed to hairpin loops or otherwise hypervariable regions These
13
results indicate that future studies should evaluate the molecular evolution andphylogenetic potential of new markers both coding and con-coding and choosethe most suitable ones in a combined analysis to resolve the remaining uncertaintiesin moss phylogeny
Taxonomy
Takakiaceae Stech amp WFrey stat nov
Plantae virides nusquam rhizophorae sine protonemate e caudicis rhizomatis erectae Caudicesrhizomati et axes geotropi radiformes frequenter intercalariter ramificantes sine phyllidiis cumpapillis mucilaginis rostratis Caules phyllidiiferi saepe furcati Phyllidia sine lamina et costadistincta profunde 2-4(-5)-lobata pluristratosa tristicha sed torsione spiraliter disposita Filumcentralium in ambabus generationibus (axibus gametophyti et setis) adest Plantae dioicae Antheridiaet archegonia nuda Sporophytum terminale solitarium Seta persistens Capsula tortilis admaturitatem schizocarpa secus unam rimam spiralem longitudinalem dehiscens Stomata etoperculum absunt peristomium nullum Calyptra mitriformis
TYPUS Takakia SHatt amp Inoue J Hattori Bot Lab 19 137 1958
Takakiaceae SHatt amp Inoue J Hattori Bot Lab 19 137 1958 nom inval (Art 411)
Takakiales Stech amp WFrey stat nov
Based on Takakiaceae Stech amp WFrey Nova Hedwigia 86 13 2008
TYPUS Takakia SHatt amp Inoue J Hattori Bot Lab 19 137 1958
Takakiales SHatt amp Inoue J Hattori Bot Lab 19 137 1958 nom inval
Takakiales SHatt amp Inoue ex RMSchust J Hattori Bot Lab 26 224 1963 nom inval (cumdescr latin)
Takakiopsida Stech amp WFrey statnov
Based on Takakiaceae Stech amp WFrey Nova Hedwigia 86 13 2008
TYPUS Takakia SHatt amp Inoue J Hattori Bot Lab 19 137 1958
Takakiopsida Goffinet amp WRBuck Monogr Syst Bot Missouri Bot Gard 98 232 2004 nominval
Takakiopsida Jia et al Acta Phytotax Sin 41 350 351 2003 nom nud
Takakiopsida Wang amp Wu Fl Bryophyt Sin 8 447 2004 nom inval (cum descr latin)
Takakiophytina Stech amp WFrey stat nov
Based on Takakiaceae Stech amp WFrey Nova Hedwigia 86 13 2008
TYPUS Takakia SHatt amp Inoue JHattori Bot Lab 19 137 1958
Gigaspermidae Stech amp WFrey subclass nov
Plantae acrocarpae terrestres stoloniferae ramis brevibus erectis Folia unicostata cellulis laxislaevibus Capsula plerumque valde rugosa gymnostomatica vel cleistocarpa stomata cum duabuscellulis sociis Ab Funariidis et Encalyptidis charactere phylogenomico (71-kb inversio abest)separatae
14
TYPUS Gigaspermum Lindb Oumlfversigt af Foumlrhandlingar Kongl Svenska Vetenskaps-Akademien21 599 1865
Amphidiaceae Stech stat nov
Based on Dicranaceae subfam Amphidioideae Ochyra in Ochyra Zarnowiec amp Bednarek-OchyraCens Cat Polish Mosses 110 2003
TYPUS Amphidium Schimp Coroll Bryol Eur 39 1856
Amphidiaceae AJESm Moss Fl Britain Ireland 2nd ed 657 2004 nom inval descr angl
Dicranellaceae Stech stat nov
Based on Dicranaceae subfam Dicranelloideae Lindb Utkast Eur Bladmoss 33 1878[lsquoUnderfamilje Dicranelleaersquo]
TYPUS Dicranella (MuumlllHal) Schimp Coroll Bryol Eur 13 1856
Oncophoraceae Stech stat nov
Based on Dicranaceae subfam Oncophoroideae Lindb Utkast Eur Bladmoss 34 1878[lsquoUnderfamilje Oncophoreaersquo]
TYPUS Oncophorus (Brid) Brid Bryol Univ 1 389 1826
Hypodontiaceae Stech fam nov
Plantae robustae characteribus morphologicis Pottiaceis et Calymperaceis similes sedcharacteribus molecularicis separatae Bracteae perichaetiales internae e basi vaginantes subulataevel aristatae Capsula aspectu succulenta cellulae exothecii incrassatae annulus magnopereabsens Peristomii dentes breves triangulati incurvati aurantiaci leves vel infirme verrucosiCalyptra cucullata
TYPUS Hypodontium MuumlllHal Hedwigia 38 96 1899
Helicophyllales Stech amp WFrey ord nov
Plantae acrocarpae prostratae tomentosae Folia dimorpha in duas series laterales et unam seriemventralem divisa Costa percurrens Cellulae hexagonae ad subquadratae papillosae Capsula immersacupulata ad oblonga infra orificium abrupte incurvata stomata destituta Peristomium nullum Sporaeisomorphae heteropolares granulatae
TYPUS Helicophyllum Brid Bryol Univ 2 771 1827
Synopsis of the suprageneric classification of BryophytaAuthor citations are in accordance with Art 492 of the Vienna Code (McNeill et al 2006)
Subdivision Takakiophytina Stech amp WFreyClass Takakiopsida Stech amp WFrey
Order Takakiales Stech amp WFreyTakakiaceae Stech amp WFrey
Subdivision Sphagnophytina DoweldClass Sphagnopsida Schimp
Order Sphagnales Limpr
15
Sphagnaceae DumortOrder Ambuchananiales Seppelt amp HACrum
Ambuchananiaceae Seppelt amp HACrumSubdivision Bryophytina Engler
Class Andreaeopsida JHSchaffnSubclass Andreaeidae Engl
Order Andreaeales LimprAndreaeaceae Dumort
Subclass Andreaeobryidae OchyraOrder Andreaeobryales BMMurray
Andreaeobryaceae Steere amp BMMurrayClass Oedipodiopsida Goffinet amp WRBuck
Order Oedipodiales Goffinet amp WRBuckOedipodiaceae Schimp
Class Tetraphidopsida Goffinet amp WRBuckOrder Tetraphidales MFleisch
Tetraphidaceae SchimpClass Polytrichopsida Doweld
Order Polytrichales MFleischPolytrichaceae Schwaumlgr
Class Bryopsida PaxSubclass Buxbaumiidae Doweld
Order Buxbaumiales MFleischBuxbaumiaceae Schimp
Subclass Diphysciidae OchyraOrder Diphysciales MFleisch
Diphysciaceae MFleischSubclass Timmiidae Ochyra
Order Timmiales OchyraTimmiaceae Schimp
Subclass Encalyptidae Ochyra Żarnowiec amp Bednarek-OchyraOrder Encalyptales Dixon
Encalyptaceae SchimpSubclass Funariidae Ochyra
Order Funariales MFleischFunariaceae Schwaumlgr Disceliaceae Schimp
Subclass Gigaspermidae Stech amp WFreyOrder Gigaspermales Goffinet Wickett OWerner Ros AJShaw amp CJCox
Gigaspermaceae LindbSubclass Dicranidae Doweld
Order Catoscopiales Ignatov amp IgnatovaCatoscopiaceae Broth
Order Scouleriales Goffinet amp WRBuckDrummondiaceae Goffinet Scouleriaceae SPChurchill
Order Bryoxiphiales HACrum amp LEAndersonBryoxiphiaceae Besch
16
Order Grimmiales MFleischGrimmiaceae Arn Ptychomitriaceae Schimp Seligeriaceae Schimp
Order Archidiales LimprArchidiaceae Schimp
Order Mitteniales ShawMitteniaceae Broth
Order Dicranales HPhilib ex MFleischAmphidiaceae Stech Aongstroemiaceae De Not BruchiaceaeSchimp Calymperaceae Kindb Dicranaceae Schimp Dicranel-laceae Stech Ditrichaceae Limpr Erpodiaceae Broth EustichiaceaeBroth Fissidentaceae Schimp Leucobryaceae Schimp Onco-phoraceae Stech Rhachitheciaceae HRob Schistostegaceae SchimpViridivelleraceae IGStone Wardiaceae Welch
Order Pottiales MFleischEphemeraceae Schimp Hypodontiaceae Stech PleurophascaceaeBroth Pottiaceae Schimp Serpotortellaceae WDReese amp RHZander
Subclass Bryidae EnglOrder Hedwigiales Ochyra
Hedwigiaceae Schimp Rhacocarpaceae KindbOrder Helicophyllales Stech amp WFrey
Helicophyllaceae BrothOrder Bartramiales DQuandt NEBell amp Stech
Bartramiaceae SchwaumlgrOrder Splachnales Ochyra
Meesiaceae Schimp Splachnaceae Grev amp ArnOrder Bryales Limpr
Bryaceae Schwaumlgr Leptostomataceae Schwaumlgr Mniaceae SchwaumlgrPhyllodrepaniaceae Crosby Pseudoditrichaceae Steere amp ZIwatsPulchrinodaceae DQuandt NEBell amp Stech
Order Orthotrichales DixonOrthotrichaceae Arn
Order Orthodontiales NEBell AENewton amp DQuandtOrthodontiaceae Goffinet
Order Aulacomniales NEBell AENewton amp DQuandtAulacomniaceae Schimp
Order Rhizogoniales Goffinet amp WRBuckRhizogoniaceae Broth
Order Hypnodendrales NEBell AENewton amp DQuandtBraithwaiteaceae NEBell AENewton amp DQuandt Hypnodendra-ceae Broth Pterobryellaceae WRBuck amp Vitt Racopilaceae Kindb
Order Ptychomniales WRBuck CJCox AJShaw amp GoffinetPtychomniaceae MFleisch
Order Hookeriales MFleischDaltoniaceae Schimp Hookeriaceae Schimp HypopterygiaceaeMitt Leucomiaceae Broth Pilotrichaceae Kindb SaulomataceaeWRBuck CJCox AJShaw amp Goffinet Schimperobryaceae WR
17
Buck CJCox AJShaw amp GoffinetOrder Hypnales WRBuck amp Vitt
Amblystegiaceae GRoth Anomodontaceae Kindb BrachytheciaceaeSchimp Calliergonaceae Vanderpoorten Hedenaumls CJCox amp AJShaw Catagoniaceae WRBuck amp Ireland Climaciaceae KindbCryphaeaceae Schimp Echinodiaceae Broth Entodontaceae KindbFabroniaceae Schimp Fontinalaceae Schimp Helodiaceae OchyraHeterocladiaceae Ignatov amp Ignatova Hylocomiaceae MFleischHypnaceae Schimp Lembophyllaceae Broth LeptodontaceaeSchimp Lepyrodontaceae Broth Leskeaceae Schimp Leucodon-taceae Schimp Meteoriaceae Kindb Microtheciellaceae HAMillamp AJHarr Myriniaceae Schimp Myuriaceae MFleisch NeckeraceaeSchimp Orthorrhynchiaceae SHLin Phyllogoniaceae KindbPlagiotheciaceae MFleisch Pleuroziopsidaceae Ireland Prionodon-taceae Broth Pseudoleskeaceae Schimp PseudoleskeellaceaeIgnatov amp Ignatova Pterigynandraceae Schimp PterobryaceaeKindb Pylaisiaceae Schimp Pylaisiadelphaceae Goffinet amp WRBuck Regmatodontaceae Broth Rhytidiaceae Broth RigodiaceaeHACrum Rutenbergiaceae MFleisch Scorpidiaceae Ignatov ampIgnatova Sematophyllaceae Broth Sorapillaceae MFleisch Ste-reophyllaceae WRBuck amp Ireland Symphyodontaceae MFleischTheliaceae MFleisch Thuidiaceae Schimp TrachylomataceaeWRBuck amp Vitt
Acknowledgements
Sincere thanks are due to JLReveal (Ithaca) as well as WFPrudhomme van Reine and JFVeldkamp(Leiden) for comments and discussions about suprafamilial taxonomy to DQuandt (Dresden) for providingDNA from Rhacocarpus and Bartramiaceae species and to BGiesicke (Berlin) for technical assistance
References
BECKERT S H MUHLE D PRUCHNER amp V KNOOP (2001) The mitochondrial nad2 geneas a novel marker locus for phylogenetic analysis of early land plants a comparative analysis inmosses - Mol Phylogenet Evol 18 117-126
BELL NE amp AE NEWTON (2004) Systematic studies of non-hypnanaean pleurocarps establishinga phylogenetic framework for investigating the origins of pleurocarpy - In GOFFINET BV HOLLOWELL amp R MAGILL (eds) Molecular systematics of bryophytes Monogr Syst BotMissouri Bot Gard 98 290-319
BELL NE amp AE NEWTON (2007) Pleurocarpy in the Rhizogoniaceous grade - In NEWTONAE amp RS TANGNEY (eds) Pleurocarpous mosses systematics and evolution SystematicsAssociation Special Volume Series 71 41-64
BELL NE D QUANDT TJ OBRIEN amp AE NEWTON (2007) Taxonomy and phylogeny inthe earliest diverging pleurocarps square holes and bifurcating pegs - Bryologist 110 533-560
BORSCH T KW HILU D QUANDT V WILDE C NEINHUIS amp W BARTHLOTT(2003) Non-coding plastid trnT-trnF sequences reveal a well resolved phylogeny of basal angiosperms- J Evol Biol 16 558-576
18
BUCK WR (2007) The history of pleurocarp classification two steps forward one step back - InNEWTON AE amp RS TANGNEY (eds) Pleurocarpous mosses systematics and evolutionSystematics Association Special Volume Series 71 1-18
BUCK WR amp B GOFFINET (2000) Morphology and classification of mosses - In SHAWAJ amp B GOFFINET (eds) Bryophyte Biology pp 71-123 Cambridge University PressCambridge
CHIANG TY BA SCHAAL amp CI PENG (1998) Universal primers for amplification andsequencing a noncoding spacer between atpB and rbcL genes of chloroplast DNA - Bot Bull AcadSin 39 245-250
COX CJ B GOFFINET AE NEWTON AJ SHAW amp TAJ HEDDERSON (2000)Phylogenetic relationships among the diplolepideous-alternate mosses (Bryidae) inferred from nuclearand chloroplast DNA sequences - Bryologist 103 224-241
COX CJ B GOFFINET AJ SHAW amp SB BOLES (2004) Phylogenetic relationships amongthe mosses based on heterogeneous Bayesian analysis of multiple genes from multiple genomiccompartments - Syst Bot 29 234-250
CRANDALL-STOTLER B (1986) Morphogenesis developmental anatomy and bryophytephylogenetics contra-indications of monophyly - J Bryol 14 1-23
CROSBY MR RE MAGILL B ALLEN amp S HE (1999) A checklist of the mosses - MissouriBotanical Garden St Louis Missouri
DOWELD A (2001) Prosyllabus Tracheophytorum - GEOS Moscow i-lxxx + 110 pp
DOYLE JJ amp JL DOYLE (1990) Isolation of plant DNA from fresh tissue - Focus 12 13-15
DUFF RJ JC VILLAREAL DC CARGILL amp KS RENZAGLIA (2007) Progress andchallenges towards developing a phylogeny and classification of the hornworts - Bryologist 110214-243
FLEISCHER M (1920) Natuumlrliches System der Laubmoose - Hedwigia 61 390-400
FORREST LL EC DAVIS DG LONG BJ CRANDALL-STOTLER A CLARK ampML HOLLINGSWORTH (2006) Unraveling the evolutionary history of the liverworts (Marchantio-phyta) multiple taxa genomes and analyses - Bryologist 109 303-334
FRAHM J-P amp W FREY (1987) Moosflora 2 Aufl - UTB 1250 Stuttgart
FREY W (1977) Neue Vorstellungen uumlber die Verwandtschaftsgruppen und die Stammesgeschichteder Laubmoose - In FREY W H HURKA amp F OBERWINKLER (Hrsg) Beitraumlge zur Biologieder Pflanzen pp 117-139 Stuttgart
FREY W amp M STECH (2005) A morpho-molecular classification of the liverworts (Hepa-ticophytina Bryophyta) - Nova Hedwigia 81 55-78
FREY W M STECH amp K MEIszligNER (1999) Chloroplast DNA-relationship in palaeoaustralLopidium concinnum (Hypopterygiaceae Musci) An example of steno-evolution in mosses Studiesin austral temperate rain forest bryophytes 2 - Plant Syst Evol 218 67-75
GOFFINET B amp WR BUCK (2004) Systematics of Bryophyta (mosses) from molecules to arevised classification - In GOFFINET B V HOLLOWELL amp R MAGILL (eds) Molecularsystematics of bryophytes Monogr Syst Bot Missouri Bot Gard 98 205-239
GOFFINET B CJ COX AJ SHAW amp TAJ HEDDERSON (2001) The Bryophyta (mosses)Systematic and evolutionary inferences from an rps4 gene (cpDNA) phylogeny - Ann Bot 87191-208
GOFFINET B NJ WICKETT O WERNER RM ROS AJ SHAW amp CJ COX (2007)Distribution and phylogenetic significance of the 71-kb inversion in the plastid genome in Funariidae(Bryophyta) - Ann Bot 99 747-753
19
GROTH-MALONEK M D PRUCHNER F GREWE amp V KNOOP (2005) Ancestors oftrans-splicing mitochondrial introns support serial sister group relationships of hornworts and mosseswith vascular plants - Mol Biol Evol 22 117-125
HATTORI S amp H INOUE (1958) Preliminary report on Takakia lepidozioides - J Hattori BotLab 19 133-137
HE-NYGREacuteN X A JUSLEacuteN I AHONEN D GLENNY amp S PIIPPO (2006) Illuminating theevolutionary history of liverworts (Marchantiophyta) - towards a natural classification - Cladistics22 1-31
HEDDERSON TAJ DJ MURRAY CJ COX amp TL NOWELL (2004) Phylogeneticrelationships of haplolepideous mosses (Dicranidae) inferred from rps4 gene sequences - Syst Bot29 29-41
LA FARGE C BD MISHER JA WHEELER DP WALL K JOHANNES S SCHAFFERamp AJ SHAW (2000) Phylogenetic relationships within the haplolepideous mosses - Bryologist103 257-276
LA FARGE C AJ SHAW amp DH VITT (2002) The circumscription of the Dicranaceae(Bryopsida) based on the chloroplast regions trnL-trnF and rps4 - Syst Bot 27 435-452
MAGOMBO ZLK (2003) The phylogeny of basal peristomate mosses evidence from cpDNAand implications for peristome evolution - Syst Bot 28 24-38
MCNEILL J FR BARRIE HM BURDET V DEMOULIN DL HAWKSWORTHK MARHOLD DH NICOLSON J PRADO PC SILVA JE SKOG JH WIERSEMA ampNJ TURLAND (2006) International Code of Botanical Nomenclature (Vienna Code) - RegnumVegetabile 146 1-568
MUumlLLER K (2004) PRAP - computation of Bremer support for large data sets - Mol PhylogenetEvol 31 780-782
MUumlLLER K (2005) SeqState - primer design and sequence statistics for phylogenetic DNA datasets - Appl Bioinformatics 4 65-69
MUumlLLER K D QUANDT J MUumlLLER amp C NEINHUIS (2005) PhyDE v0992 PhylogeneticData Editor - httpwwwphydede
MURRAY BM (1988) Systematics of the Andreaeopsida (Bryophyta) two orders with links toTakakia - Nova Hedwigia Beih 90 289-336
NEWTON AE amp RS TANGNEY (eds) (2007) Pleurocarpous mosses systematics and evolutionSystematics Association Special Volume Series 71 CRC Press Boca Raton 434 pp
NEWTON AE CJ COX JG DUCKETT JA WHEELER B GOFFINET TAJ HEDDER-SON amp BD MISHLER (2000) Evolution of the major moss lineages Phylogenetic analyses basedon multiple gene sequences and morphology - Bryologist 103 187-211
NEWTON AE N WIKSTROumlM NE BELL LL FORREST amp MS IGNATOV (2007)Dating the diversification of the pleurocarpous mosses - In NEWTON AE amp RS TANGNEY(eds) Pleurocarpous mosses systematics and evolution Systematics Association Special VolumeSeries 71 337-366
NIXON KC (1999) The parsimony ratchet a new method for rapid parsimony analysis - Cladistics15 407-411
OBRIEN TJ (2007) The phylogenetic distribution of pleurocarpous mosses evidence fromcpDNA sequences - In NEWTON AE amp RS TANGNEY (eds) Pleurocarpous mossessystematics and evolution Systematics Association Special Volume Series 71 19-41
OCHYRA R (2002) Nomenclatural changes in subfamilies of the Dicranaceae - CryptogamieBryol 23 345-349
20
OCHYRA R J ŻARNOWIEC amp H BEDNAREK-OCHYRA (2003) Census catalogue ofPolish mosses - Biodiv Poland 3 1-372
PEDERSEN N amp AE NEWTON (2007) Phylogenetic and morphological studies within thePtychomniales with emphasis on the evolution of dwarf males - In NEWTON AE amp RSTANGNEY (eds) Pleurocarpous mosses systematics and evolution Systematics AssociationSpecial Volume Series 71 367-392
QUANDT D amp M STECH (2005) Molecular evolution and secondary structure of the chloroplasttrnL intron in bryophytes - Mol Phylogenet Evol 36 429-443
QUANDT D K MUumlLLER amp S HUTTUNEN (2003) Characterisation of the chloroplast DNApsbT-H region and the influence of dyad symmetrical elements on phylogenetic reconstructions -Plant Biol 5 400-410
QUANDT D K MUumlLLER M STECH W FREY KW HILU amp T BORSCH (2004) Molecularevolution of the chloroplast trnL-F-region in land plants - In GOFFINET B V HOLLOWELL ampR MAGILL (eds) Molecular systematics of bryophytes Monogr Syst Bot Missouri Bot Gard98 13-37
QUANDT D NE BELL amp M STECH (2007) Unravelling the knot the Pulchrinodaceae famnov (Bryales) - In KUumlRSCHNER H T PFEIFFER amp M STECH (eds) A Festschrift to Wolf-gang Frey - a scientists life between deserts and rain forests Nova Hedwigia Beih 131 21-39
QIU Y-L Y CHO JC COX amp JD PALMER (1998) The gain of three mitochondrial intronsidentifies liverworts as the earliest land plants - Nature 394 671-674
QIU Y-L L LI B WANG Z CHEN V KNOOP M GROTH-MALONEK O DOM-BROVSKA J LEE L KENT J REST GF ESTABROOK TA HENDRY DW TAYLORCM TESTA M AMBROS B CRANDALL-STOTLER J DUFF M STECH W FREYD QUANDT amp CC DAVIS (2006) The deepest divergences in land plants inferred fromphylogenomic evidence - Proc Natl Acad Sci USA 103 15511-15516
RENZAGLIA KS S SCHUETTE RJ DUFF R LIGRONE AJ SHAW BD MISHLER ampJG DUCKETT (2007) Bryophyte phylogeny Advancing the molecular and morphological frontiers- Bryologist 110 179-213
SAMIGULLIN TH SP YACENTYUK GV DEGTYARYEVA KM VALIEJO-ROMANVK BOBROVA I CAPESIUS WF MARTIN AV TROITSKY VR FILIN amp ASANTONOV (2002) Paraphyly of bryophytes and close relationships of hornworts and vascularplants inferred from analysis of chloroplast rDNA ITS (cpITS) sequences - Arctoa 11 31-43
SANG T DJ CRAWFORD amp TF STUESSY (1997) Chloroplast DNA phylogeny reticulateevolution and biogeography of Paeonia (Paeoniaceae) - Amer J Bot 84 1120-1136
SHAW AJ amp KS RENZAGLIA (2004) Phylogeny and diversification of bryophytes - AmerJ Bot 91 1557-1581
SHAW AJ CJ COX amp B GOFFINET (2005) Global patterns of moss diversity taxonomic andmolecular inferences - Taxon 54 337-352
STECH M (1999a) A reclassification of Dicranaceae (Bryopsida) based on non-coding cpDNAsequence data - J Hattori Bot Lab 86 137-159
STECH M (1999b) A molecular systematic contribution to the position of Amphidium Schimp(Rhabdoweisiaceae Bryopsida) - Nova Hedwigia 68 291-300
STECH M (2004) Supraspecific circumscription and classification of Campylopus Brid(Dicranaceae Bryopsida) based on molecular data - Syst Bot 29 817-824
STECH M amp D QUANDT (2006) Molecular evolution of the chloroplast atpB-rbcL spacer inbryophytes - In SHARMA AK amp A SHARMA (eds) Plant Genome Biodiversity and EvolutionVol 2 Part B pp 409-431 Science Publishers Enfield New Hampshire
21
STECH M D QUANDT amp W FREY (2003) Molecular circumscription of the hornworts(Antho-cerotophyta) based on the chloroplast DNA trnL-trnF region - J Plant Res 116 389-398
STOTLER RE amp B CRANDALL-STOTLER (2005) A revised classification of theAnthocerotophyta and a checklist of the hornworts of North America north of Mexico - Bryologist108 16-26
SWOFFORD DL (2002) PAUP Phylogenetic analysis using parsimony (and other methods)version 40b10 - Sunderland MA
TABERLET P L GIELLY G PAUTOU amp J BOUVET (1991) Universal primers for amplificationof three non-coding regions of chloroplast DNA - Plant Mol Biol 17 1105-1109
TSUBOTA H Y AGENO B ESTEacuteBANEZ T YAMAGUCHI amp H DEGUCHI (2003)Molecular phylogeny of the Grimmiales (Musci) based on chloroplast rbcL sequences - Hikobia 1455-70
TSUBOTA H E DE LUNA D GONZAacuteLEZ MS IGNATOV amp H DEGUCHI (2004) Molecularphylogenetics and ordinal relationships based on analyses of a large-scale data set of 600 rbcLsequences of mosses - Hikobia 14 149-170
VITT DH (1984) Classification of the Bryopsida - In SCHUSTER RM (ed) New Manual ofBryology 2 696-759 Hattori Botanical Laboratory Nichinan Japan
VITT DH B GOFFINET amp T HEDDERSON (1998) 8 The ordinal classification of the mossesquestions and answers for the 1990s - In BATES JW NW ASHTON amp JG DUCKETT (eds)Bryology for the twenty-first century British Bryol Soc pp 113-123
Received 3 September 2007 accepted in revised form 30 October 2007
13
results indicate that future studies should evaluate the molecular evolution andphylogenetic potential of new markers both coding and con-coding and choosethe most suitable ones in a combined analysis to resolve the remaining uncertaintiesin moss phylogeny
Taxonomy
Takakiaceae Stech amp WFrey stat nov
Plantae virides nusquam rhizophorae sine protonemate e caudicis rhizomatis erectae Caudicesrhizomati et axes geotropi radiformes frequenter intercalariter ramificantes sine phyllidiis cumpapillis mucilaginis rostratis Caules phyllidiiferi saepe furcati Phyllidia sine lamina et costadistincta profunde 2-4(-5)-lobata pluristratosa tristicha sed torsione spiraliter disposita Filumcentralium in ambabus generationibus (axibus gametophyti et setis) adest Plantae dioicae Antheridiaet archegonia nuda Sporophytum terminale solitarium Seta persistens Capsula tortilis admaturitatem schizocarpa secus unam rimam spiralem longitudinalem dehiscens Stomata etoperculum absunt peristomium nullum Calyptra mitriformis
TYPUS Takakia SHatt amp Inoue J Hattori Bot Lab 19 137 1958
Takakiaceae SHatt amp Inoue J Hattori Bot Lab 19 137 1958 nom inval (Art 411)
Takakiales Stech amp WFrey stat nov
Based on Takakiaceae Stech amp WFrey Nova Hedwigia 86 13 2008
TYPUS Takakia SHatt amp Inoue J Hattori Bot Lab 19 137 1958
Takakiales SHatt amp Inoue J Hattori Bot Lab 19 137 1958 nom inval
Takakiales SHatt amp Inoue ex RMSchust J Hattori Bot Lab 26 224 1963 nom inval (cumdescr latin)
Takakiopsida Stech amp WFrey statnov
Based on Takakiaceae Stech amp WFrey Nova Hedwigia 86 13 2008
TYPUS Takakia SHatt amp Inoue J Hattori Bot Lab 19 137 1958
Takakiopsida Goffinet amp WRBuck Monogr Syst Bot Missouri Bot Gard 98 232 2004 nominval
Takakiopsida Jia et al Acta Phytotax Sin 41 350 351 2003 nom nud
Takakiopsida Wang amp Wu Fl Bryophyt Sin 8 447 2004 nom inval (cum descr latin)
Takakiophytina Stech amp WFrey stat nov
Based on Takakiaceae Stech amp WFrey Nova Hedwigia 86 13 2008
TYPUS Takakia SHatt amp Inoue JHattori Bot Lab 19 137 1958
Gigaspermidae Stech amp WFrey subclass nov
Plantae acrocarpae terrestres stoloniferae ramis brevibus erectis Folia unicostata cellulis laxislaevibus Capsula plerumque valde rugosa gymnostomatica vel cleistocarpa stomata cum duabuscellulis sociis Ab Funariidis et Encalyptidis charactere phylogenomico (71-kb inversio abest)separatae
14
TYPUS Gigaspermum Lindb Oumlfversigt af Foumlrhandlingar Kongl Svenska Vetenskaps-Akademien21 599 1865
Amphidiaceae Stech stat nov
Based on Dicranaceae subfam Amphidioideae Ochyra in Ochyra Zarnowiec amp Bednarek-OchyraCens Cat Polish Mosses 110 2003
TYPUS Amphidium Schimp Coroll Bryol Eur 39 1856
Amphidiaceae AJESm Moss Fl Britain Ireland 2nd ed 657 2004 nom inval descr angl
Dicranellaceae Stech stat nov
Based on Dicranaceae subfam Dicranelloideae Lindb Utkast Eur Bladmoss 33 1878[lsquoUnderfamilje Dicranelleaersquo]
TYPUS Dicranella (MuumlllHal) Schimp Coroll Bryol Eur 13 1856
Oncophoraceae Stech stat nov
Based on Dicranaceae subfam Oncophoroideae Lindb Utkast Eur Bladmoss 34 1878[lsquoUnderfamilje Oncophoreaersquo]
TYPUS Oncophorus (Brid) Brid Bryol Univ 1 389 1826
Hypodontiaceae Stech fam nov
Plantae robustae characteribus morphologicis Pottiaceis et Calymperaceis similes sedcharacteribus molecularicis separatae Bracteae perichaetiales internae e basi vaginantes subulataevel aristatae Capsula aspectu succulenta cellulae exothecii incrassatae annulus magnopereabsens Peristomii dentes breves triangulati incurvati aurantiaci leves vel infirme verrucosiCalyptra cucullata
TYPUS Hypodontium MuumlllHal Hedwigia 38 96 1899
Helicophyllales Stech amp WFrey ord nov
Plantae acrocarpae prostratae tomentosae Folia dimorpha in duas series laterales et unam seriemventralem divisa Costa percurrens Cellulae hexagonae ad subquadratae papillosae Capsula immersacupulata ad oblonga infra orificium abrupte incurvata stomata destituta Peristomium nullum Sporaeisomorphae heteropolares granulatae
TYPUS Helicophyllum Brid Bryol Univ 2 771 1827
Synopsis of the suprageneric classification of BryophytaAuthor citations are in accordance with Art 492 of the Vienna Code (McNeill et al 2006)
Subdivision Takakiophytina Stech amp WFreyClass Takakiopsida Stech amp WFrey
Order Takakiales Stech amp WFreyTakakiaceae Stech amp WFrey
Subdivision Sphagnophytina DoweldClass Sphagnopsida Schimp
Order Sphagnales Limpr
15
Sphagnaceae DumortOrder Ambuchananiales Seppelt amp HACrum
Ambuchananiaceae Seppelt amp HACrumSubdivision Bryophytina Engler
Class Andreaeopsida JHSchaffnSubclass Andreaeidae Engl
Order Andreaeales LimprAndreaeaceae Dumort
Subclass Andreaeobryidae OchyraOrder Andreaeobryales BMMurray
Andreaeobryaceae Steere amp BMMurrayClass Oedipodiopsida Goffinet amp WRBuck
Order Oedipodiales Goffinet amp WRBuckOedipodiaceae Schimp
Class Tetraphidopsida Goffinet amp WRBuckOrder Tetraphidales MFleisch
Tetraphidaceae SchimpClass Polytrichopsida Doweld
Order Polytrichales MFleischPolytrichaceae Schwaumlgr
Class Bryopsida PaxSubclass Buxbaumiidae Doweld
Order Buxbaumiales MFleischBuxbaumiaceae Schimp
Subclass Diphysciidae OchyraOrder Diphysciales MFleisch
Diphysciaceae MFleischSubclass Timmiidae Ochyra
Order Timmiales OchyraTimmiaceae Schimp
Subclass Encalyptidae Ochyra Żarnowiec amp Bednarek-OchyraOrder Encalyptales Dixon
Encalyptaceae SchimpSubclass Funariidae Ochyra
Order Funariales MFleischFunariaceae Schwaumlgr Disceliaceae Schimp
Subclass Gigaspermidae Stech amp WFreyOrder Gigaspermales Goffinet Wickett OWerner Ros AJShaw amp CJCox
Gigaspermaceae LindbSubclass Dicranidae Doweld
Order Catoscopiales Ignatov amp IgnatovaCatoscopiaceae Broth
Order Scouleriales Goffinet amp WRBuckDrummondiaceae Goffinet Scouleriaceae SPChurchill
Order Bryoxiphiales HACrum amp LEAndersonBryoxiphiaceae Besch
16
Order Grimmiales MFleischGrimmiaceae Arn Ptychomitriaceae Schimp Seligeriaceae Schimp
Order Archidiales LimprArchidiaceae Schimp
Order Mitteniales ShawMitteniaceae Broth
Order Dicranales HPhilib ex MFleischAmphidiaceae Stech Aongstroemiaceae De Not BruchiaceaeSchimp Calymperaceae Kindb Dicranaceae Schimp Dicranel-laceae Stech Ditrichaceae Limpr Erpodiaceae Broth EustichiaceaeBroth Fissidentaceae Schimp Leucobryaceae Schimp Onco-phoraceae Stech Rhachitheciaceae HRob Schistostegaceae SchimpViridivelleraceae IGStone Wardiaceae Welch
Order Pottiales MFleischEphemeraceae Schimp Hypodontiaceae Stech PleurophascaceaeBroth Pottiaceae Schimp Serpotortellaceae WDReese amp RHZander
Subclass Bryidae EnglOrder Hedwigiales Ochyra
Hedwigiaceae Schimp Rhacocarpaceae KindbOrder Helicophyllales Stech amp WFrey
Helicophyllaceae BrothOrder Bartramiales DQuandt NEBell amp Stech
Bartramiaceae SchwaumlgrOrder Splachnales Ochyra
Meesiaceae Schimp Splachnaceae Grev amp ArnOrder Bryales Limpr
Bryaceae Schwaumlgr Leptostomataceae Schwaumlgr Mniaceae SchwaumlgrPhyllodrepaniaceae Crosby Pseudoditrichaceae Steere amp ZIwatsPulchrinodaceae DQuandt NEBell amp Stech
Order Orthotrichales DixonOrthotrichaceae Arn
Order Orthodontiales NEBell AENewton amp DQuandtOrthodontiaceae Goffinet
Order Aulacomniales NEBell AENewton amp DQuandtAulacomniaceae Schimp
Order Rhizogoniales Goffinet amp WRBuckRhizogoniaceae Broth
Order Hypnodendrales NEBell AENewton amp DQuandtBraithwaiteaceae NEBell AENewton amp DQuandt Hypnodendra-ceae Broth Pterobryellaceae WRBuck amp Vitt Racopilaceae Kindb
Order Ptychomniales WRBuck CJCox AJShaw amp GoffinetPtychomniaceae MFleisch
Order Hookeriales MFleischDaltoniaceae Schimp Hookeriaceae Schimp HypopterygiaceaeMitt Leucomiaceae Broth Pilotrichaceae Kindb SaulomataceaeWRBuck CJCox AJShaw amp Goffinet Schimperobryaceae WR
17
Buck CJCox AJShaw amp GoffinetOrder Hypnales WRBuck amp Vitt
Amblystegiaceae GRoth Anomodontaceae Kindb BrachytheciaceaeSchimp Calliergonaceae Vanderpoorten Hedenaumls CJCox amp AJShaw Catagoniaceae WRBuck amp Ireland Climaciaceae KindbCryphaeaceae Schimp Echinodiaceae Broth Entodontaceae KindbFabroniaceae Schimp Fontinalaceae Schimp Helodiaceae OchyraHeterocladiaceae Ignatov amp Ignatova Hylocomiaceae MFleischHypnaceae Schimp Lembophyllaceae Broth LeptodontaceaeSchimp Lepyrodontaceae Broth Leskeaceae Schimp Leucodon-taceae Schimp Meteoriaceae Kindb Microtheciellaceae HAMillamp AJHarr Myriniaceae Schimp Myuriaceae MFleisch NeckeraceaeSchimp Orthorrhynchiaceae SHLin Phyllogoniaceae KindbPlagiotheciaceae MFleisch Pleuroziopsidaceae Ireland Prionodon-taceae Broth Pseudoleskeaceae Schimp PseudoleskeellaceaeIgnatov amp Ignatova Pterigynandraceae Schimp PterobryaceaeKindb Pylaisiaceae Schimp Pylaisiadelphaceae Goffinet amp WRBuck Regmatodontaceae Broth Rhytidiaceae Broth RigodiaceaeHACrum Rutenbergiaceae MFleisch Scorpidiaceae Ignatov ampIgnatova Sematophyllaceae Broth Sorapillaceae MFleisch Ste-reophyllaceae WRBuck amp Ireland Symphyodontaceae MFleischTheliaceae MFleisch Thuidiaceae Schimp TrachylomataceaeWRBuck amp Vitt
Acknowledgements
Sincere thanks are due to JLReveal (Ithaca) as well as WFPrudhomme van Reine and JFVeldkamp(Leiden) for comments and discussions about suprafamilial taxonomy to DQuandt (Dresden) for providingDNA from Rhacocarpus and Bartramiaceae species and to BGiesicke (Berlin) for technical assistance
References
BECKERT S H MUHLE D PRUCHNER amp V KNOOP (2001) The mitochondrial nad2 geneas a novel marker locus for phylogenetic analysis of early land plants a comparative analysis inmosses - Mol Phylogenet Evol 18 117-126
BELL NE amp AE NEWTON (2004) Systematic studies of non-hypnanaean pleurocarps establishinga phylogenetic framework for investigating the origins of pleurocarpy - In GOFFINET BV HOLLOWELL amp R MAGILL (eds) Molecular systematics of bryophytes Monogr Syst BotMissouri Bot Gard 98 290-319
BELL NE amp AE NEWTON (2007) Pleurocarpy in the Rhizogoniaceous grade - In NEWTONAE amp RS TANGNEY (eds) Pleurocarpous mosses systematics and evolution SystematicsAssociation Special Volume Series 71 41-64
BELL NE D QUANDT TJ OBRIEN amp AE NEWTON (2007) Taxonomy and phylogeny inthe earliest diverging pleurocarps square holes and bifurcating pegs - Bryologist 110 533-560
BORSCH T KW HILU D QUANDT V WILDE C NEINHUIS amp W BARTHLOTT(2003) Non-coding plastid trnT-trnF sequences reveal a well resolved phylogeny of basal angiosperms- J Evol Biol 16 558-576
18
BUCK WR (2007) The history of pleurocarp classification two steps forward one step back - InNEWTON AE amp RS TANGNEY (eds) Pleurocarpous mosses systematics and evolutionSystematics Association Special Volume Series 71 1-18
BUCK WR amp B GOFFINET (2000) Morphology and classification of mosses - In SHAWAJ amp B GOFFINET (eds) Bryophyte Biology pp 71-123 Cambridge University PressCambridge
CHIANG TY BA SCHAAL amp CI PENG (1998) Universal primers for amplification andsequencing a noncoding spacer between atpB and rbcL genes of chloroplast DNA - Bot Bull AcadSin 39 245-250
COX CJ B GOFFINET AE NEWTON AJ SHAW amp TAJ HEDDERSON (2000)Phylogenetic relationships among the diplolepideous-alternate mosses (Bryidae) inferred from nuclearand chloroplast DNA sequences - Bryologist 103 224-241
COX CJ B GOFFINET AJ SHAW amp SB BOLES (2004) Phylogenetic relationships amongthe mosses based on heterogeneous Bayesian analysis of multiple genes from multiple genomiccompartments - Syst Bot 29 234-250
CRANDALL-STOTLER B (1986) Morphogenesis developmental anatomy and bryophytephylogenetics contra-indications of monophyly - J Bryol 14 1-23
CROSBY MR RE MAGILL B ALLEN amp S HE (1999) A checklist of the mosses - MissouriBotanical Garden St Louis Missouri
DOWELD A (2001) Prosyllabus Tracheophytorum - GEOS Moscow i-lxxx + 110 pp
DOYLE JJ amp JL DOYLE (1990) Isolation of plant DNA from fresh tissue - Focus 12 13-15
DUFF RJ JC VILLAREAL DC CARGILL amp KS RENZAGLIA (2007) Progress andchallenges towards developing a phylogeny and classification of the hornworts - Bryologist 110214-243
FLEISCHER M (1920) Natuumlrliches System der Laubmoose - Hedwigia 61 390-400
FORREST LL EC DAVIS DG LONG BJ CRANDALL-STOTLER A CLARK ampML HOLLINGSWORTH (2006) Unraveling the evolutionary history of the liverworts (Marchantio-phyta) multiple taxa genomes and analyses - Bryologist 109 303-334
FRAHM J-P amp W FREY (1987) Moosflora 2 Aufl - UTB 1250 Stuttgart
FREY W (1977) Neue Vorstellungen uumlber die Verwandtschaftsgruppen und die Stammesgeschichteder Laubmoose - In FREY W H HURKA amp F OBERWINKLER (Hrsg) Beitraumlge zur Biologieder Pflanzen pp 117-139 Stuttgart
FREY W amp M STECH (2005) A morpho-molecular classification of the liverworts (Hepa-ticophytina Bryophyta) - Nova Hedwigia 81 55-78
FREY W M STECH amp K MEIszligNER (1999) Chloroplast DNA-relationship in palaeoaustralLopidium concinnum (Hypopterygiaceae Musci) An example of steno-evolution in mosses Studiesin austral temperate rain forest bryophytes 2 - Plant Syst Evol 218 67-75
GOFFINET B amp WR BUCK (2004) Systematics of Bryophyta (mosses) from molecules to arevised classification - In GOFFINET B V HOLLOWELL amp R MAGILL (eds) Molecularsystematics of bryophytes Monogr Syst Bot Missouri Bot Gard 98 205-239
GOFFINET B CJ COX AJ SHAW amp TAJ HEDDERSON (2001) The Bryophyta (mosses)Systematic and evolutionary inferences from an rps4 gene (cpDNA) phylogeny - Ann Bot 87191-208
GOFFINET B NJ WICKETT O WERNER RM ROS AJ SHAW amp CJ COX (2007)Distribution and phylogenetic significance of the 71-kb inversion in the plastid genome in Funariidae(Bryophyta) - Ann Bot 99 747-753
19
GROTH-MALONEK M D PRUCHNER F GREWE amp V KNOOP (2005) Ancestors oftrans-splicing mitochondrial introns support serial sister group relationships of hornworts and mosseswith vascular plants - Mol Biol Evol 22 117-125
HATTORI S amp H INOUE (1958) Preliminary report on Takakia lepidozioides - J Hattori BotLab 19 133-137
HE-NYGREacuteN X A JUSLEacuteN I AHONEN D GLENNY amp S PIIPPO (2006) Illuminating theevolutionary history of liverworts (Marchantiophyta) - towards a natural classification - Cladistics22 1-31
HEDDERSON TAJ DJ MURRAY CJ COX amp TL NOWELL (2004) Phylogeneticrelationships of haplolepideous mosses (Dicranidae) inferred from rps4 gene sequences - Syst Bot29 29-41
LA FARGE C BD MISHER JA WHEELER DP WALL K JOHANNES S SCHAFFERamp AJ SHAW (2000) Phylogenetic relationships within the haplolepideous mosses - Bryologist103 257-276
LA FARGE C AJ SHAW amp DH VITT (2002) The circumscription of the Dicranaceae(Bryopsida) based on the chloroplast regions trnL-trnF and rps4 - Syst Bot 27 435-452
MAGOMBO ZLK (2003) The phylogeny of basal peristomate mosses evidence from cpDNAand implications for peristome evolution - Syst Bot 28 24-38
MCNEILL J FR BARRIE HM BURDET V DEMOULIN DL HAWKSWORTHK MARHOLD DH NICOLSON J PRADO PC SILVA JE SKOG JH WIERSEMA ampNJ TURLAND (2006) International Code of Botanical Nomenclature (Vienna Code) - RegnumVegetabile 146 1-568
MUumlLLER K (2004) PRAP - computation of Bremer support for large data sets - Mol PhylogenetEvol 31 780-782
MUumlLLER K (2005) SeqState - primer design and sequence statistics for phylogenetic DNA datasets - Appl Bioinformatics 4 65-69
MUumlLLER K D QUANDT J MUumlLLER amp C NEINHUIS (2005) PhyDE v0992 PhylogeneticData Editor - httpwwwphydede
MURRAY BM (1988) Systematics of the Andreaeopsida (Bryophyta) two orders with links toTakakia - Nova Hedwigia Beih 90 289-336
NEWTON AE amp RS TANGNEY (eds) (2007) Pleurocarpous mosses systematics and evolutionSystematics Association Special Volume Series 71 CRC Press Boca Raton 434 pp
NEWTON AE CJ COX JG DUCKETT JA WHEELER B GOFFINET TAJ HEDDER-SON amp BD MISHLER (2000) Evolution of the major moss lineages Phylogenetic analyses basedon multiple gene sequences and morphology - Bryologist 103 187-211
NEWTON AE N WIKSTROumlM NE BELL LL FORREST amp MS IGNATOV (2007)Dating the diversification of the pleurocarpous mosses - In NEWTON AE amp RS TANGNEY(eds) Pleurocarpous mosses systematics and evolution Systematics Association Special VolumeSeries 71 337-366
NIXON KC (1999) The parsimony ratchet a new method for rapid parsimony analysis - Cladistics15 407-411
OBRIEN TJ (2007) The phylogenetic distribution of pleurocarpous mosses evidence fromcpDNA sequences - In NEWTON AE amp RS TANGNEY (eds) Pleurocarpous mossessystematics and evolution Systematics Association Special Volume Series 71 19-41
OCHYRA R (2002) Nomenclatural changes in subfamilies of the Dicranaceae - CryptogamieBryol 23 345-349
20
OCHYRA R J ŻARNOWIEC amp H BEDNAREK-OCHYRA (2003) Census catalogue ofPolish mosses - Biodiv Poland 3 1-372
PEDERSEN N amp AE NEWTON (2007) Phylogenetic and morphological studies within thePtychomniales with emphasis on the evolution of dwarf males - In NEWTON AE amp RSTANGNEY (eds) Pleurocarpous mosses systematics and evolution Systematics AssociationSpecial Volume Series 71 367-392
QUANDT D amp M STECH (2005) Molecular evolution and secondary structure of the chloroplasttrnL intron in bryophytes - Mol Phylogenet Evol 36 429-443
QUANDT D K MUumlLLER amp S HUTTUNEN (2003) Characterisation of the chloroplast DNApsbT-H region and the influence of dyad symmetrical elements on phylogenetic reconstructions -Plant Biol 5 400-410
QUANDT D K MUumlLLER M STECH W FREY KW HILU amp T BORSCH (2004) Molecularevolution of the chloroplast trnL-F-region in land plants - In GOFFINET B V HOLLOWELL ampR MAGILL (eds) Molecular systematics of bryophytes Monogr Syst Bot Missouri Bot Gard98 13-37
QUANDT D NE BELL amp M STECH (2007) Unravelling the knot the Pulchrinodaceae famnov (Bryales) - In KUumlRSCHNER H T PFEIFFER amp M STECH (eds) A Festschrift to Wolf-gang Frey - a scientists life between deserts and rain forests Nova Hedwigia Beih 131 21-39
QIU Y-L Y CHO JC COX amp JD PALMER (1998) The gain of three mitochondrial intronsidentifies liverworts as the earliest land plants - Nature 394 671-674
QIU Y-L L LI B WANG Z CHEN V KNOOP M GROTH-MALONEK O DOM-BROVSKA J LEE L KENT J REST GF ESTABROOK TA HENDRY DW TAYLORCM TESTA M AMBROS B CRANDALL-STOTLER J DUFF M STECH W FREYD QUANDT amp CC DAVIS (2006) The deepest divergences in land plants inferred fromphylogenomic evidence - Proc Natl Acad Sci USA 103 15511-15516
RENZAGLIA KS S SCHUETTE RJ DUFF R LIGRONE AJ SHAW BD MISHLER ampJG DUCKETT (2007) Bryophyte phylogeny Advancing the molecular and morphological frontiers- Bryologist 110 179-213
SAMIGULLIN TH SP YACENTYUK GV DEGTYARYEVA KM VALIEJO-ROMANVK BOBROVA I CAPESIUS WF MARTIN AV TROITSKY VR FILIN amp ASANTONOV (2002) Paraphyly of bryophytes and close relationships of hornworts and vascularplants inferred from analysis of chloroplast rDNA ITS (cpITS) sequences - Arctoa 11 31-43
SANG T DJ CRAWFORD amp TF STUESSY (1997) Chloroplast DNA phylogeny reticulateevolution and biogeography of Paeonia (Paeoniaceae) - Amer J Bot 84 1120-1136
SHAW AJ amp KS RENZAGLIA (2004) Phylogeny and diversification of bryophytes - AmerJ Bot 91 1557-1581
SHAW AJ CJ COX amp B GOFFINET (2005) Global patterns of moss diversity taxonomic andmolecular inferences - Taxon 54 337-352
STECH M (1999a) A reclassification of Dicranaceae (Bryopsida) based on non-coding cpDNAsequence data - J Hattori Bot Lab 86 137-159
STECH M (1999b) A molecular systematic contribution to the position of Amphidium Schimp(Rhabdoweisiaceae Bryopsida) - Nova Hedwigia 68 291-300
STECH M (2004) Supraspecific circumscription and classification of Campylopus Brid(Dicranaceae Bryopsida) based on molecular data - Syst Bot 29 817-824
STECH M amp D QUANDT (2006) Molecular evolution of the chloroplast atpB-rbcL spacer inbryophytes - In SHARMA AK amp A SHARMA (eds) Plant Genome Biodiversity and EvolutionVol 2 Part B pp 409-431 Science Publishers Enfield New Hampshire
21
STECH M D QUANDT amp W FREY (2003) Molecular circumscription of the hornworts(Antho-cerotophyta) based on the chloroplast DNA trnL-trnF region - J Plant Res 116 389-398
STOTLER RE amp B CRANDALL-STOTLER (2005) A revised classification of theAnthocerotophyta and a checklist of the hornworts of North America north of Mexico - Bryologist108 16-26
SWOFFORD DL (2002) PAUP Phylogenetic analysis using parsimony (and other methods)version 40b10 - Sunderland MA
TABERLET P L GIELLY G PAUTOU amp J BOUVET (1991) Universal primers for amplificationof three non-coding regions of chloroplast DNA - Plant Mol Biol 17 1105-1109
TSUBOTA H Y AGENO B ESTEacuteBANEZ T YAMAGUCHI amp H DEGUCHI (2003)Molecular phylogeny of the Grimmiales (Musci) based on chloroplast rbcL sequences - Hikobia 1455-70
TSUBOTA H E DE LUNA D GONZAacuteLEZ MS IGNATOV amp H DEGUCHI (2004) Molecularphylogenetics and ordinal relationships based on analyses of a large-scale data set of 600 rbcLsequences of mosses - Hikobia 14 149-170
VITT DH (1984) Classification of the Bryopsida - In SCHUSTER RM (ed) New Manual ofBryology 2 696-759 Hattori Botanical Laboratory Nichinan Japan
VITT DH B GOFFINET amp T HEDDERSON (1998) 8 The ordinal classification of the mossesquestions and answers for the 1990s - In BATES JW NW ASHTON amp JG DUCKETT (eds)Bryology for the twenty-first century British Bryol Soc pp 113-123
Received 3 September 2007 accepted in revised form 30 October 2007
14
TYPUS Gigaspermum Lindb Oumlfversigt af Foumlrhandlingar Kongl Svenska Vetenskaps-Akademien21 599 1865
Amphidiaceae Stech stat nov
Based on Dicranaceae subfam Amphidioideae Ochyra in Ochyra Zarnowiec amp Bednarek-OchyraCens Cat Polish Mosses 110 2003
TYPUS Amphidium Schimp Coroll Bryol Eur 39 1856
Amphidiaceae AJESm Moss Fl Britain Ireland 2nd ed 657 2004 nom inval descr angl
Dicranellaceae Stech stat nov
Based on Dicranaceae subfam Dicranelloideae Lindb Utkast Eur Bladmoss 33 1878[lsquoUnderfamilje Dicranelleaersquo]
TYPUS Dicranella (MuumlllHal) Schimp Coroll Bryol Eur 13 1856
Oncophoraceae Stech stat nov
Based on Dicranaceae subfam Oncophoroideae Lindb Utkast Eur Bladmoss 34 1878[lsquoUnderfamilje Oncophoreaersquo]
TYPUS Oncophorus (Brid) Brid Bryol Univ 1 389 1826
Hypodontiaceae Stech fam nov
Plantae robustae characteribus morphologicis Pottiaceis et Calymperaceis similes sedcharacteribus molecularicis separatae Bracteae perichaetiales internae e basi vaginantes subulataevel aristatae Capsula aspectu succulenta cellulae exothecii incrassatae annulus magnopereabsens Peristomii dentes breves triangulati incurvati aurantiaci leves vel infirme verrucosiCalyptra cucullata
TYPUS Hypodontium MuumlllHal Hedwigia 38 96 1899
Helicophyllales Stech amp WFrey ord nov
Plantae acrocarpae prostratae tomentosae Folia dimorpha in duas series laterales et unam seriemventralem divisa Costa percurrens Cellulae hexagonae ad subquadratae papillosae Capsula immersacupulata ad oblonga infra orificium abrupte incurvata stomata destituta Peristomium nullum Sporaeisomorphae heteropolares granulatae
TYPUS Helicophyllum Brid Bryol Univ 2 771 1827
Synopsis of the suprageneric classification of BryophytaAuthor citations are in accordance with Art 492 of the Vienna Code (McNeill et al 2006)
Subdivision Takakiophytina Stech amp WFreyClass Takakiopsida Stech amp WFrey
Order Takakiales Stech amp WFreyTakakiaceae Stech amp WFrey
Subdivision Sphagnophytina DoweldClass Sphagnopsida Schimp
Order Sphagnales Limpr
15
Sphagnaceae DumortOrder Ambuchananiales Seppelt amp HACrum
Ambuchananiaceae Seppelt amp HACrumSubdivision Bryophytina Engler
Class Andreaeopsida JHSchaffnSubclass Andreaeidae Engl
Order Andreaeales LimprAndreaeaceae Dumort
Subclass Andreaeobryidae OchyraOrder Andreaeobryales BMMurray
Andreaeobryaceae Steere amp BMMurrayClass Oedipodiopsida Goffinet amp WRBuck
Order Oedipodiales Goffinet amp WRBuckOedipodiaceae Schimp
Class Tetraphidopsida Goffinet amp WRBuckOrder Tetraphidales MFleisch
Tetraphidaceae SchimpClass Polytrichopsida Doweld
Order Polytrichales MFleischPolytrichaceae Schwaumlgr
Class Bryopsida PaxSubclass Buxbaumiidae Doweld
Order Buxbaumiales MFleischBuxbaumiaceae Schimp
Subclass Diphysciidae OchyraOrder Diphysciales MFleisch
Diphysciaceae MFleischSubclass Timmiidae Ochyra
Order Timmiales OchyraTimmiaceae Schimp
Subclass Encalyptidae Ochyra Żarnowiec amp Bednarek-OchyraOrder Encalyptales Dixon
Encalyptaceae SchimpSubclass Funariidae Ochyra
Order Funariales MFleischFunariaceae Schwaumlgr Disceliaceae Schimp
Subclass Gigaspermidae Stech amp WFreyOrder Gigaspermales Goffinet Wickett OWerner Ros AJShaw amp CJCox
Gigaspermaceae LindbSubclass Dicranidae Doweld
Order Catoscopiales Ignatov amp IgnatovaCatoscopiaceae Broth
Order Scouleriales Goffinet amp WRBuckDrummondiaceae Goffinet Scouleriaceae SPChurchill
Order Bryoxiphiales HACrum amp LEAndersonBryoxiphiaceae Besch
16
Order Grimmiales MFleischGrimmiaceae Arn Ptychomitriaceae Schimp Seligeriaceae Schimp
Order Archidiales LimprArchidiaceae Schimp
Order Mitteniales ShawMitteniaceae Broth
Order Dicranales HPhilib ex MFleischAmphidiaceae Stech Aongstroemiaceae De Not BruchiaceaeSchimp Calymperaceae Kindb Dicranaceae Schimp Dicranel-laceae Stech Ditrichaceae Limpr Erpodiaceae Broth EustichiaceaeBroth Fissidentaceae Schimp Leucobryaceae Schimp Onco-phoraceae Stech Rhachitheciaceae HRob Schistostegaceae SchimpViridivelleraceae IGStone Wardiaceae Welch
Order Pottiales MFleischEphemeraceae Schimp Hypodontiaceae Stech PleurophascaceaeBroth Pottiaceae Schimp Serpotortellaceae WDReese amp RHZander
Subclass Bryidae EnglOrder Hedwigiales Ochyra
Hedwigiaceae Schimp Rhacocarpaceae KindbOrder Helicophyllales Stech amp WFrey
Helicophyllaceae BrothOrder Bartramiales DQuandt NEBell amp Stech
Bartramiaceae SchwaumlgrOrder Splachnales Ochyra
Meesiaceae Schimp Splachnaceae Grev amp ArnOrder Bryales Limpr
Bryaceae Schwaumlgr Leptostomataceae Schwaumlgr Mniaceae SchwaumlgrPhyllodrepaniaceae Crosby Pseudoditrichaceae Steere amp ZIwatsPulchrinodaceae DQuandt NEBell amp Stech
Order Orthotrichales DixonOrthotrichaceae Arn
Order Orthodontiales NEBell AENewton amp DQuandtOrthodontiaceae Goffinet
Order Aulacomniales NEBell AENewton amp DQuandtAulacomniaceae Schimp
Order Rhizogoniales Goffinet amp WRBuckRhizogoniaceae Broth
Order Hypnodendrales NEBell AENewton amp DQuandtBraithwaiteaceae NEBell AENewton amp DQuandt Hypnodendra-ceae Broth Pterobryellaceae WRBuck amp Vitt Racopilaceae Kindb
Order Ptychomniales WRBuck CJCox AJShaw amp GoffinetPtychomniaceae MFleisch
Order Hookeriales MFleischDaltoniaceae Schimp Hookeriaceae Schimp HypopterygiaceaeMitt Leucomiaceae Broth Pilotrichaceae Kindb SaulomataceaeWRBuck CJCox AJShaw amp Goffinet Schimperobryaceae WR
17
Buck CJCox AJShaw amp GoffinetOrder Hypnales WRBuck amp Vitt
Amblystegiaceae GRoth Anomodontaceae Kindb BrachytheciaceaeSchimp Calliergonaceae Vanderpoorten Hedenaumls CJCox amp AJShaw Catagoniaceae WRBuck amp Ireland Climaciaceae KindbCryphaeaceae Schimp Echinodiaceae Broth Entodontaceae KindbFabroniaceae Schimp Fontinalaceae Schimp Helodiaceae OchyraHeterocladiaceae Ignatov amp Ignatova Hylocomiaceae MFleischHypnaceae Schimp Lembophyllaceae Broth LeptodontaceaeSchimp Lepyrodontaceae Broth Leskeaceae Schimp Leucodon-taceae Schimp Meteoriaceae Kindb Microtheciellaceae HAMillamp AJHarr Myriniaceae Schimp Myuriaceae MFleisch NeckeraceaeSchimp Orthorrhynchiaceae SHLin Phyllogoniaceae KindbPlagiotheciaceae MFleisch Pleuroziopsidaceae Ireland Prionodon-taceae Broth Pseudoleskeaceae Schimp PseudoleskeellaceaeIgnatov amp Ignatova Pterigynandraceae Schimp PterobryaceaeKindb Pylaisiaceae Schimp Pylaisiadelphaceae Goffinet amp WRBuck Regmatodontaceae Broth Rhytidiaceae Broth RigodiaceaeHACrum Rutenbergiaceae MFleisch Scorpidiaceae Ignatov ampIgnatova Sematophyllaceae Broth Sorapillaceae MFleisch Ste-reophyllaceae WRBuck amp Ireland Symphyodontaceae MFleischTheliaceae MFleisch Thuidiaceae Schimp TrachylomataceaeWRBuck amp Vitt
Acknowledgements
Sincere thanks are due to JLReveal (Ithaca) as well as WFPrudhomme van Reine and JFVeldkamp(Leiden) for comments and discussions about suprafamilial taxonomy to DQuandt (Dresden) for providingDNA from Rhacocarpus and Bartramiaceae species and to BGiesicke (Berlin) for technical assistance
References
BECKERT S H MUHLE D PRUCHNER amp V KNOOP (2001) The mitochondrial nad2 geneas a novel marker locus for phylogenetic analysis of early land plants a comparative analysis inmosses - Mol Phylogenet Evol 18 117-126
BELL NE amp AE NEWTON (2004) Systematic studies of non-hypnanaean pleurocarps establishinga phylogenetic framework for investigating the origins of pleurocarpy - In GOFFINET BV HOLLOWELL amp R MAGILL (eds) Molecular systematics of bryophytes Monogr Syst BotMissouri Bot Gard 98 290-319
BELL NE amp AE NEWTON (2007) Pleurocarpy in the Rhizogoniaceous grade - In NEWTONAE amp RS TANGNEY (eds) Pleurocarpous mosses systematics and evolution SystematicsAssociation Special Volume Series 71 41-64
BELL NE D QUANDT TJ OBRIEN amp AE NEWTON (2007) Taxonomy and phylogeny inthe earliest diverging pleurocarps square holes and bifurcating pegs - Bryologist 110 533-560
BORSCH T KW HILU D QUANDT V WILDE C NEINHUIS amp W BARTHLOTT(2003) Non-coding plastid trnT-trnF sequences reveal a well resolved phylogeny of basal angiosperms- J Evol Biol 16 558-576
18
BUCK WR (2007) The history of pleurocarp classification two steps forward one step back - InNEWTON AE amp RS TANGNEY (eds) Pleurocarpous mosses systematics and evolutionSystematics Association Special Volume Series 71 1-18
BUCK WR amp B GOFFINET (2000) Morphology and classification of mosses - In SHAWAJ amp B GOFFINET (eds) Bryophyte Biology pp 71-123 Cambridge University PressCambridge
CHIANG TY BA SCHAAL amp CI PENG (1998) Universal primers for amplification andsequencing a noncoding spacer between atpB and rbcL genes of chloroplast DNA - Bot Bull AcadSin 39 245-250
COX CJ B GOFFINET AE NEWTON AJ SHAW amp TAJ HEDDERSON (2000)Phylogenetic relationships among the diplolepideous-alternate mosses (Bryidae) inferred from nuclearand chloroplast DNA sequences - Bryologist 103 224-241
COX CJ B GOFFINET AJ SHAW amp SB BOLES (2004) Phylogenetic relationships amongthe mosses based on heterogeneous Bayesian analysis of multiple genes from multiple genomiccompartments - Syst Bot 29 234-250
CRANDALL-STOTLER B (1986) Morphogenesis developmental anatomy and bryophytephylogenetics contra-indications of monophyly - J Bryol 14 1-23
CROSBY MR RE MAGILL B ALLEN amp S HE (1999) A checklist of the mosses - MissouriBotanical Garden St Louis Missouri
DOWELD A (2001) Prosyllabus Tracheophytorum - GEOS Moscow i-lxxx + 110 pp
DOYLE JJ amp JL DOYLE (1990) Isolation of plant DNA from fresh tissue - Focus 12 13-15
DUFF RJ JC VILLAREAL DC CARGILL amp KS RENZAGLIA (2007) Progress andchallenges towards developing a phylogeny and classification of the hornworts - Bryologist 110214-243
FLEISCHER M (1920) Natuumlrliches System der Laubmoose - Hedwigia 61 390-400
FORREST LL EC DAVIS DG LONG BJ CRANDALL-STOTLER A CLARK ampML HOLLINGSWORTH (2006) Unraveling the evolutionary history of the liverworts (Marchantio-phyta) multiple taxa genomes and analyses - Bryologist 109 303-334
FRAHM J-P amp W FREY (1987) Moosflora 2 Aufl - UTB 1250 Stuttgart
FREY W (1977) Neue Vorstellungen uumlber die Verwandtschaftsgruppen und die Stammesgeschichteder Laubmoose - In FREY W H HURKA amp F OBERWINKLER (Hrsg) Beitraumlge zur Biologieder Pflanzen pp 117-139 Stuttgart
FREY W amp M STECH (2005) A morpho-molecular classification of the liverworts (Hepa-ticophytina Bryophyta) - Nova Hedwigia 81 55-78
FREY W M STECH amp K MEIszligNER (1999) Chloroplast DNA-relationship in palaeoaustralLopidium concinnum (Hypopterygiaceae Musci) An example of steno-evolution in mosses Studiesin austral temperate rain forest bryophytes 2 - Plant Syst Evol 218 67-75
GOFFINET B amp WR BUCK (2004) Systematics of Bryophyta (mosses) from molecules to arevised classification - In GOFFINET B V HOLLOWELL amp R MAGILL (eds) Molecularsystematics of bryophytes Monogr Syst Bot Missouri Bot Gard 98 205-239
GOFFINET B CJ COX AJ SHAW amp TAJ HEDDERSON (2001) The Bryophyta (mosses)Systematic and evolutionary inferences from an rps4 gene (cpDNA) phylogeny - Ann Bot 87191-208
GOFFINET B NJ WICKETT O WERNER RM ROS AJ SHAW amp CJ COX (2007)Distribution and phylogenetic significance of the 71-kb inversion in the plastid genome in Funariidae(Bryophyta) - Ann Bot 99 747-753
19
GROTH-MALONEK M D PRUCHNER F GREWE amp V KNOOP (2005) Ancestors oftrans-splicing mitochondrial introns support serial sister group relationships of hornworts and mosseswith vascular plants - Mol Biol Evol 22 117-125
HATTORI S amp H INOUE (1958) Preliminary report on Takakia lepidozioides - J Hattori BotLab 19 133-137
HE-NYGREacuteN X A JUSLEacuteN I AHONEN D GLENNY amp S PIIPPO (2006) Illuminating theevolutionary history of liverworts (Marchantiophyta) - towards a natural classification - Cladistics22 1-31
HEDDERSON TAJ DJ MURRAY CJ COX amp TL NOWELL (2004) Phylogeneticrelationships of haplolepideous mosses (Dicranidae) inferred from rps4 gene sequences - Syst Bot29 29-41
LA FARGE C BD MISHER JA WHEELER DP WALL K JOHANNES S SCHAFFERamp AJ SHAW (2000) Phylogenetic relationships within the haplolepideous mosses - Bryologist103 257-276
LA FARGE C AJ SHAW amp DH VITT (2002) The circumscription of the Dicranaceae(Bryopsida) based on the chloroplast regions trnL-trnF and rps4 - Syst Bot 27 435-452
MAGOMBO ZLK (2003) The phylogeny of basal peristomate mosses evidence from cpDNAand implications for peristome evolution - Syst Bot 28 24-38
MCNEILL J FR BARRIE HM BURDET V DEMOULIN DL HAWKSWORTHK MARHOLD DH NICOLSON J PRADO PC SILVA JE SKOG JH WIERSEMA ampNJ TURLAND (2006) International Code of Botanical Nomenclature (Vienna Code) - RegnumVegetabile 146 1-568
MUumlLLER K (2004) PRAP - computation of Bremer support for large data sets - Mol PhylogenetEvol 31 780-782
MUumlLLER K (2005) SeqState - primer design and sequence statistics for phylogenetic DNA datasets - Appl Bioinformatics 4 65-69
MUumlLLER K D QUANDT J MUumlLLER amp C NEINHUIS (2005) PhyDE v0992 PhylogeneticData Editor - httpwwwphydede
MURRAY BM (1988) Systematics of the Andreaeopsida (Bryophyta) two orders with links toTakakia - Nova Hedwigia Beih 90 289-336
NEWTON AE amp RS TANGNEY (eds) (2007) Pleurocarpous mosses systematics and evolutionSystematics Association Special Volume Series 71 CRC Press Boca Raton 434 pp
NEWTON AE CJ COX JG DUCKETT JA WHEELER B GOFFINET TAJ HEDDER-SON amp BD MISHLER (2000) Evolution of the major moss lineages Phylogenetic analyses basedon multiple gene sequences and morphology - Bryologist 103 187-211
NEWTON AE N WIKSTROumlM NE BELL LL FORREST amp MS IGNATOV (2007)Dating the diversification of the pleurocarpous mosses - In NEWTON AE amp RS TANGNEY(eds) Pleurocarpous mosses systematics and evolution Systematics Association Special VolumeSeries 71 337-366
NIXON KC (1999) The parsimony ratchet a new method for rapid parsimony analysis - Cladistics15 407-411
OBRIEN TJ (2007) The phylogenetic distribution of pleurocarpous mosses evidence fromcpDNA sequences - In NEWTON AE amp RS TANGNEY (eds) Pleurocarpous mossessystematics and evolution Systematics Association Special Volume Series 71 19-41
OCHYRA R (2002) Nomenclatural changes in subfamilies of the Dicranaceae - CryptogamieBryol 23 345-349
20
OCHYRA R J ŻARNOWIEC amp H BEDNAREK-OCHYRA (2003) Census catalogue ofPolish mosses - Biodiv Poland 3 1-372
PEDERSEN N amp AE NEWTON (2007) Phylogenetic and morphological studies within thePtychomniales with emphasis on the evolution of dwarf males - In NEWTON AE amp RSTANGNEY (eds) Pleurocarpous mosses systematics and evolution Systematics AssociationSpecial Volume Series 71 367-392
QUANDT D amp M STECH (2005) Molecular evolution and secondary structure of the chloroplasttrnL intron in bryophytes - Mol Phylogenet Evol 36 429-443
QUANDT D K MUumlLLER amp S HUTTUNEN (2003) Characterisation of the chloroplast DNApsbT-H region and the influence of dyad symmetrical elements on phylogenetic reconstructions -Plant Biol 5 400-410
QUANDT D K MUumlLLER M STECH W FREY KW HILU amp T BORSCH (2004) Molecularevolution of the chloroplast trnL-F-region in land plants - In GOFFINET B V HOLLOWELL ampR MAGILL (eds) Molecular systematics of bryophytes Monogr Syst Bot Missouri Bot Gard98 13-37
QUANDT D NE BELL amp M STECH (2007) Unravelling the knot the Pulchrinodaceae famnov (Bryales) - In KUumlRSCHNER H T PFEIFFER amp M STECH (eds) A Festschrift to Wolf-gang Frey - a scientists life between deserts and rain forests Nova Hedwigia Beih 131 21-39
QIU Y-L Y CHO JC COX amp JD PALMER (1998) The gain of three mitochondrial intronsidentifies liverworts as the earliest land plants - Nature 394 671-674
QIU Y-L L LI B WANG Z CHEN V KNOOP M GROTH-MALONEK O DOM-BROVSKA J LEE L KENT J REST GF ESTABROOK TA HENDRY DW TAYLORCM TESTA M AMBROS B CRANDALL-STOTLER J DUFF M STECH W FREYD QUANDT amp CC DAVIS (2006) The deepest divergences in land plants inferred fromphylogenomic evidence - Proc Natl Acad Sci USA 103 15511-15516
RENZAGLIA KS S SCHUETTE RJ DUFF R LIGRONE AJ SHAW BD MISHLER ampJG DUCKETT (2007) Bryophyte phylogeny Advancing the molecular and morphological frontiers- Bryologist 110 179-213
SAMIGULLIN TH SP YACENTYUK GV DEGTYARYEVA KM VALIEJO-ROMANVK BOBROVA I CAPESIUS WF MARTIN AV TROITSKY VR FILIN amp ASANTONOV (2002) Paraphyly of bryophytes and close relationships of hornworts and vascularplants inferred from analysis of chloroplast rDNA ITS (cpITS) sequences - Arctoa 11 31-43
SANG T DJ CRAWFORD amp TF STUESSY (1997) Chloroplast DNA phylogeny reticulateevolution and biogeography of Paeonia (Paeoniaceae) - Amer J Bot 84 1120-1136
SHAW AJ amp KS RENZAGLIA (2004) Phylogeny and diversification of bryophytes - AmerJ Bot 91 1557-1581
SHAW AJ CJ COX amp B GOFFINET (2005) Global patterns of moss diversity taxonomic andmolecular inferences - Taxon 54 337-352
STECH M (1999a) A reclassification of Dicranaceae (Bryopsida) based on non-coding cpDNAsequence data - J Hattori Bot Lab 86 137-159
STECH M (1999b) A molecular systematic contribution to the position of Amphidium Schimp(Rhabdoweisiaceae Bryopsida) - Nova Hedwigia 68 291-300
STECH M (2004) Supraspecific circumscription and classification of Campylopus Brid(Dicranaceae Bryopsida) based on molecular data - Syst Bot 29 817-824
STECH M amp D QUANDT (2006) Molecular evolution of the chloroplast atpB-rbcL spacer inbryophytes - In SHARMA AK amp A SHARMA (eds) Plant Genome Biodiversity and EvolutionVol 2 Part B pp 409-431 Science Publishers Enfield New Hampshire
21
STECH M D QUANDT amp W FREY (2003) Molecular circumscription of the hornworts(Antho-cerotophyta) based on the chloroplast DNA trnL-trnF region - J Plant Res 116 389-398
STOTLER RE amp B CRANDALL-STOTLER (2005) A revised classification of theAnthocerotophyta and a checklist of the hornworts of North America north of Mexico - Bryologist108 16-26
SWOFFORD DL (2002) PAUP Phylogenetic analysis using parsimony (and other methods)version 40b10 - Sunderland MA
TABERLET P L GIELLY G PAUTOU amp J BOUVET (1991) Universal primers for amplificationof three non-coding regions of chloroplast DNA - Plant Mol Biol 17 1105-1109
TSUBOTA H Y AGENO B ESTEacuteBANEZ T YAMAGUCHI amp H DEGUCHI (2003)Molecular phylogeny of the Grimmiales (Musci) based on chloroplast rbcL sequences - Hikobia 1455-70
TSUBOTA H E DE LUNA D GONZAacuteLEZ MS IGNATOV amp H DEGUCHI (2004) Molecularphylogenetics and ordinal relationships based on analyses of a large-scale data set of 600 rbcLsequences of mosses - Hikobia 14 149-170
VITT DH (1984) Classification of the Bryopsida - In SCHUSTER RM (ed) New Manual ofBryology 2 696-759 Hattori Botanical Laboratory Nichinan Japan
VITT DH B GOFFINET amp T HEDDERSON (1998) 8 The ordinal classification of the mossesquestions and answers for the 1990s - In BATES JW NW ASHTON amp JG DUCKETT (eds)Bryology for the twenty-first century British Bryol Soc pp 113-123
Received 3 September 2007 accepted in revised form 30 October 2007
15
Sphagnaceae DumortOrder Ambuchananiales Seppelt amp HACrum
Ambuchananiaceae Seppelt amp HACrumSubdivision Bryophytina Engler
Class Andreaeopsida JHSchaffnSubclass Andreaeidae Engl
Order Andreaeales LimprAndreaeaceae Dumort
Subclass Andreaeobryidae OchyraOrder Andreaeobryales BMMurray
Andreaeobryaceae Steere amp BMMurrayClass Oedipodiopsida Goffinet amp WRBuck
Order Oedipodiales Goffinet amp WRBuckOedipodiaceae Schimp
Class Tetraphidopsida Goffinet amp WRBuckOrder Tetraphidales MFleisch
Tetraphidaceae SchimpClass Polytrichopsida Doweld
Order Polytrichales MFleischPolytrichaceae Schwaumlgr
Class Bryopsida PaxSubclass Buxbaumiidae Doweld
Order Buxbaumiales MFleischBuxbaumiaceae Schimp
Subclass Diphysciidae OchyraOrder Diphysciales MFleisch
Diphysciaceae MFleischSubclass Timmiidae Ochyra
Order Timmiales OchyraTimmiaceae Schimp
Subclass Encalyptidae Ochyra Żarnowiec amp Bednarek-OchyraOrder Encalyptales Dixon
Encalyptaceae SchimpSubclass Funariidae Ochyra
Order Funariales MFleischFunariaceae Schwaumlgr Disceliaceae Schimp
Subclass Gigaspermidae Stech amp WFreyOrder Gigaspermales Goffinet Wickett OWerner Ros AJShaw amp CJCox
Gigaspermaceae LindbSubclass Dicranidae Doweld
Order Catoscopiales Ignatov amp IgnatovaCatoscopiaceae Broth
Order Scouleriales Goffinet amp WRBuckDrummondiaceae Goffinet Scouleriaceae SPChurchill
Order Bryoxiphiales HACrum amp LEAndersonBryoxiphiaceae Besch
16
Order Grimmiales MFleischGrimmiaceae Arn Ptychomitriaceae Schimp Seligeriaceae Schimp
Order Archidiales LimprArchidiaceae Schimp
Order Mitteniales ShawMitteniaceae Broth
Order Dicranales HPhilib ex MFleischAmphidiaceae Stech Aongstroemiaceae De Not BruchiaceaeSchimp Calymperaceae Kindb Dicranaceae Schimp Dicranel-laceae Stech Ditrichaceae Limpr Erpodiaceae Broth EustichiaceaeBroth Fissidentaceae Schimp Leucobryaceae Schimp Onco-phoraceae Stech Rhachitheciaceae HRob Schistostegaceae SchimpViridivelleraceae IGStone Wardiaceae Welch
Order Pottiales MFleischEphemeraceae Schimp Hypodontiaceae Stech PleurophascaceaeBroth Pottiaceae Schimp Serpotortellaceae WDReese amp RHZander
Subclass Bryidae EnglOrder Hedwigiales Ochyra
Hedwigiaceae Schimp Rhacocarpaceae KindbOrder Helicophyllales Stech amp WFrey
Helicophyllaceae BrothOrder Bartramiales DQuandt NEBell amp Stech
Bartramiaceae SchwaumlgrOrder Splachnales Ochyra
Meesiaceae Schimp Splachnaceae Grev amp ArnOrder Bryales Limpr
Bryaceae Schwaumlgr Leptostomataceae Schwaumlgr Mniaceae SchwaumlgrPhyllodrepaniaceae Crosby Pseudoditrichaceae Steere amp ZIwatsPulchrinodaceae DQuandt NEBell amp Stech
Order Orthotrichales DixonOrthotrichaceae Arn
Order Orthodontiales NEBell AENewton amp DQuandtOrthodontiaceae Goffinet
Order Aulacomniales NEBell AENewton amp DQuandtAulacomniaceae Schimp
Order Rhizogoniales Goffinet amp WRBuckRhizogoniaceae Broth
Order Hypnodendrales NEBell AENewton amp DQuandtBraithwaiteaceae NEBell AENewton amp DQuandt Hypnodendra-ceae Broth Pterobryellaceae WRBuck amp Vitt Racopilaceae Kindb
Order Ptychomniales WRBuck CJCox AJShaw amp GoffinetPtychomniaceae MFleisch
Order Hookeriales MFleischDaltoniaceae Schimp Hookeriaceae Schimp HypopterygiaceaeMitt Leucomiaceae Broth Pilotrichaceae Kindb SaulomataceaeWRBuck CJCox AJShaw amp Goffinet Schimperobryaceae WR
17
Buck CJCox AJShaw amp GoffinetOrder Hypnales WRBuck amp Vitt
Amblystegiaceae GRoth Anomodontaceae Kindb BrachytheciaceaeSchimp Calliergonaceae Vanderpoorten Hedenaumls CJCox amp AJShaw Catagoniaceae WRBuck amp Ireland Climaciaceae KindbCryphaeaceae Schimp Echinodiaceae Broth Entodontaceae KindbFabroniaceae Schimp Fontinalaceae Schimp Helodiaceae OchyraHeterocladiaceae Ignatov amp Ignatova Hylocomiaceae MFleischHypnaceae Schimp Lembophyllaceae Broth LeptodontaceaeSchimp Lepyrodontaceae Broth Leskeaceae Schimp Leucodon-taceae Schimp Meteoriaceae Kindb Microtheciellaceae HAMillamp AJHarr Myriniaceae Schimp Myuriaceae MFleisch NeckeraceaeSchimp Orthorrhynchiaceae SHLin Phyllogoniaceae KindbPlagiotheciaceae MFleisch Pleuroziopsidaceae Ireland Prionodon-taceae Broth Pseudoleskeaceae Schimp PseudoleskeellaceaeIgnatov amp Ignatova Pterigynandraceae Schimp PterobryaceaeKindb Pylaisiaceae Schimp Pylaisiadelphaceae Goffinet amp WRBuck Regmatodontaceae Broth Rhytidiaceae Broth RigodiaceaeHACrum Rutenbergiaceae MFleisch Scorpidiaceae Ignatov ampIgnatova Sematophyllaceae Broth Sorapillaceae MFleisch Ste-reophyllaceae WRBuck amp Ireland Symphyodontaceae MFleischTheliaceae MFleisch Thuidiaceae Schimp TrachylomataceaeWRBuck amp Vitt
Acknowledgements
Sincere thanks are due to JLReveal (Ithaca) as well as WFPrudhomme van Reine and JFVeldkamp(Leiden) for comments and discussions about suprafamilial taxonomy to DQuandt (Dresden) for providingDNA from Rhacocarpus and Bartramiaceae species and to BGiesicke (Berlin) for technical assistance
References
BECKERT S H MUHLE D PRUCHNER amp V KNOOP (2001) The mitochondrial nad2 geneas a novel marker locus for phylogenetic analysis of early land plants a comparative analysis inmosses - Mol Phylogenet Evol 18 117-126
BELL NE amp AE NEWTON (2004) Systematic studies of non-hypnanaean pleurocarps establishinga phylogenetic framework for investigating the origins of pleurocarpy - In GOFFINET BV HOLLOWELL amp R MAGILL (eds) Molecular systematics of bryophytes Monogr Syst BotMissouri Bot Gard 98 290-319
BELL NE amp AE NEWTON (2007) Pleurocarpy in the Rhizogoniaceous grade - In NEWTONAE amp RS TANGNEY (eds) Pleurocarpous mosses systematics and evolution SystematicsAssociation Special Volume Series 71 41-64
BELL NE D QUANDT TJ OBRIEN amp AE NEWTON (2007) Taxonomy and phylogeny inthe earliest diverging pleurocarps square holes and bifurcating pegs - Bryologist 110 533-560
BORSCH T KW HILU D QUANDT V WILDE C NEINHUIS amp W BARTHLOTT(2003) Non-coding plastid trnT-trnF sequences reveal a well resolved phylogeny of basal angiosperms- J Evol Biol 16 558-576
18
BUCK WR (2007) The history of pleurocarp classification two steps forward one step back - InNEWTON AE amp RS TANGNEY (eds) Pleurocarpous mosses systematics and evolutionSystematics Association Special Volume Series 71 1-18
BUCK WR amp B GOFFINET (2000) Morphology and classification of mosses - In SHAWAJ amp B GOFFINET (eds) Bryophyte Biology pp 71-123 Cambridge University PressCambridge
CHIANG TY BA SCHAAL amp CI PENG (1998) Universal primers for amplification andsequencing a noncoding spacer between atpB and rbcL genes of chloroplast DNA - Bot Bull AcadSin 39 245-250
COX CJ B GOFFINET AE NEWTON AJ SHAW amp TAJ HEDDERSON (2000)Phylogenetic relationships among the diplolepideous-alternate mosses (Bryidae) inferred from nuclearand chloroplast DNA sequences - Bryologist 103 224-241
COX CJ B GOFFINET AJ SHAW amp SB BOLES (2004) Phylogenetic relationships amongthe mosses based on heterogeneous Bayesian analysis of multiple genes from multiple genomiccompartments - Syst Bot 29 234-250
CRANDALL-STOTLER B (1986) Morphogenesis developmental anatomy and bryophytephylogenetics contra-indications of monophyly - J Bryol 14 1-23
CROSBY MR RE MAGILL B ALLEN amp S HE (1999) A checklist of the mosses - MissouriBotanical Garden St Louis Missouri
DOWELD A (2001) Prosyllabus Tracheophytorum - GEOS Moscow i-lxxx + 110 pp
DOYLE JJ amp JL DOYLE (1990) Isolation of plant DNA from fresh tissue - Focus 12 13-15
DUFF RJ JC VILLAREAL DC CARGILL amp KS RENZAGLIA (2007) Progress andchallenges towards developing a phylogeny and classification of the hornworts - Bryologist 110214-243
FLEISCHER M (1920) Natuumlrliches System der Laubmoose - Hedwigia 61 390-400
FORREST LL EC DAVIS DG LONG BJ CRANDALL-STOTLER A CLARK ampML HOLLINGSWORTH (2006) Unraveling the evolutionary history of the liverworts (Marchantio-phyta) multiple taxa genomes and analyses - Bryologist 109 303-334
FRAHM J-P amp W FREY (1987) Moosflora 2 Aufl - UTB 1250 Stuttgart
FREY W (1977) Neue Vorstellungen uumlber die Verwandtschaftsgruppen und die Stammesgeschichteder Laubmoose - In FREY W H HURKA amp F OBERWINKLER (Hrsg) Beitraumlge zur Biologieder Pflanzen pp 117-139 Stuttgart
FREY W amp M STECH (2005) A morpho-molecular classification of the liverworts (Hepa-ticophytina Bryophyta) - Nova Hedwigia 81 55-78
FREY W M STECH amp K MEIszligNER (1999) Chloroplast DNA-relationship in palaeoaustralLopidium concinnum (Hypopterygiaceae Musci) An example of steno-evolution in mosses Studiesin austral temperate rain forest bryophytes 2 - Plant Syst Evol 218 67-75
GOFFINET B amp WR BUCK (2004) Systematics of Bryophyta (mosses) from molecules to arevised classification - In GOFFINET B V HOLLOWELL amp R MAGILL (eds) Molecularsystematics of bryophytes Monogr Syst Bot Missouri Bot Gard 98 205-239
GOFFINET B CJ COX AJ SHAW amp TAJ HEDDERSON (2001) The Bryophyta (mosses)Systematic and evolutionary inferences from an rps4 gene (cpDNA) phylogeny - Ann Bot 87191-208
GOFFINET B NJ WICKETT O WERNER RM ROS AJ SHAW amp CJ COX (2007)Distribution and phylogenetic significance of the 71-kb inversion in the plastid genome in Funariidae(Bryophyta) - Ann Bot 99 747-753
19
GROTH-MALONEK M D PRUCHNER F GREWE amp V KNOOP (2005) Ancestors oftrans-splicing mitochondrial introns support serial sister group relationships of hornworts and mosseswith vascular plants - Mol Biol Evol 22 117-125
HATTORI S amp H INOUE (1958) Preliminary report on Takakia lepidozioides - J Hattori BotLab 19 133-137
HE-NYGREacuteN X A JUSLEacuteN I AHONEN D GLENNY amp S PIIPPO (2006) Illuminating theevolutionary history of liverworts (Marchantiophyta) - towards a natural classification - Cladistics22 1-31
HEDDERSON TAJ DJ MURRAY CJ COX amp TL NOWELL (2004) Phylogeneticrelationships of haplolepideous mosses (Dicranidae) inferred from rps4 gene sequences - Syst Bot29 29-41
LA FARGE C BD MISHER JA WHEELER DP WALL K JOHANNES S SCHAFFERamp AJ SHAW (2000) Phylogenetic relationships within the haplolepideous mosses - Bryologist103 257-276
LA FARGE C AJ SHAW amp DH VITT (2002) The circumscription of the Dicranaceae(Bryopsida) based on the chloroplast regions trnL-trnF and rps4 - Syst Bot 27 435-452
MAGOMBO ZLK (2003) The phylogeny of basal peristomate mosses evidence from cpDNAand implications for peristome evolution - Syst Bot 28 24-38
MCNEILL J FR BARRIE HM BURDET V DEMOULIN DL HAWKSWORTHK MARHOLD DH NICOLSON J PRADO PC SILVA JE SKOG JH WIERSEMA ampNJ TURLAND (2006) International Code of Botanical Nomenclature (Vienna Code) - RegnumVegetabile 146 1-568
MUumlLLER K (2004) PRAP - computation of Bremer support for large data sets - Mol PhylogenetEvol 31 780-782
MUumlLLER K (2005) SeqState - primer design and sequence statistics for phylogenetic DNA datasets - Appl Bioinformatics 4 65-69
MUumlLLER K D QUANDT J MUumlLLER amp C NEINHUIS (2005) PhyDE v0992 PhylogeneticData Editor - httpwwwphydede
MURRAY BM (1988) Systematics of the Andreaeopsida (Bryophyta) two orders with links toTakakia - Nova Hedwigia Beih 90 289-336
NEWTON AE amp RS TANGNEY (eds) (2007) Pleurocarpous mosses systematics and evolutionSystematics Association Special Volume Series 71 CRC Press Boca Raton 434 pp
NEWTON AE CJ COX JG DUCKETT JA WHEELER B GOFFINET TAJ HEDDER-SON amp BD MISHLER (2000) Evolution of the major moss lineages Phylogenetic analyses basedon multiple gene sequences and morphology - Bryologist 103 187-211
NEWTON AE N WIKSTROumlM NE BELL LL FORREST amp MS IGNATOV (2007)Dating the diversification of the pleurocarpous mosses - In NEWTON AE amp RS TANGNEY(eds) Pleurocarpous mosses systematics and evolution Systematics Association Special VolumeSeries 71 337-366
NIXON KC (1999) The parsimony ratchet a new method for rapid parsimony analysis - Cladistics15 407-411
OBRIEN TJ (2007) The phylogenetic distribution of pleurocarpous mosses evidence fromcpDNA sequences - In NEWTON AE amp RS TANGNEY (eds) Pleurocarpous mossessystematics and evolution Systematics Association Special Volume Series 71 19-41
OCHYRA R (2002) Nomenclatural changes in subfamilies of the Dicranaceae - CryptogamieBryol 23 345-349
20
OCHYRA R J ŻARNOWIEC amp H BEDNAREK-OCHYRA (2003) Census catalogue ofPolish mosses - Biodiv Poland 3 1-372
PEDERSEN N amp AE NEWTON (2007) Phylogenetic and morphological studies within thePtychomniales with emphasis on the evolution of dwarf males - In NEWTON AE amp RSTANGNEY (eds) Pleurocarpous mosses systematics and evolution Systematics AssociationSpecial Volume Series 71 367-392
QUANDT D amp M STECH (2005) Molecular evolution and secondary structure of the chloroplasttrnL intron in bryophytes - Mol Phylogenet Evol 36 429-443
QUANDT D K MUumlLLER amp S HUTTUNEN (2003) Characterisation of the chloroplast DNApsbT-H region and the influence of dyad symmetrical elements on phylogenetic reconstructions -Plant Biol 5 400-410
QUANDT D K MUumlLLER M STECH W FREY KW HILU amp T BORSCH (2004) Molecularevolution of the chloroplast trnL-F-region in land plants - In GOFFINET B V HOLLOWELL ampR MAGILL (eds) Molecular systematics of bryophytes Monogr Syst Bot Missouri Bot Gard98 13-37
QUANDT D NE BELL amp M STECH (2007) Unravelling the knot the Pulchrinodaceae famnov (Bryales) - In KUumlRSCHNER H T PFEIFFER amp M STECH (eds) A Festschrift to Wolf-gang Frey - a scientists life between deserts and rain forests Nova Hedwigia Beih 131 21-39
QIU Y-L Y CHO JC COX amp JD PALMER (1998) The gain of three mitochondrial intronsidentifies liverworts as the earliest land plants - Nature 394 671-674
QIU Y-L L LI B WANG Z CHEN V KNOOP M GROTH-MALONEK O DOM-BROVSKA J LEE L KENT J REST GF ESTABROOK TA HENDRY DW TAYLORCM TESTA M AMBROS B CRANDALL-STOTLER J DUFF M STECH W FREYD QUANDT amp CC DAVIS (2006) The deepest divergences in land plants inferred fromphylogenomic evidence - Proc Natl Acad Sci USA 103 15511-15516
RENZAGLIA KS S SCHUETTE RJ DUFF R LIGRONE AJ SHAW BD MISHLER ampJG DUCKETT (2007) Bryophyte phylogeny Advancing the molecular and morphological frontiers- Bryologist 110 179-213
SAMIGULLIN TH SP YACENTYUK GV DEGTYARYEVA KM VALIEJO-ROMANVK BOBROVA I CAPESIUS WF MARTIN AV TROITSKY VR FILIN amp ASANTONOV (2002) Paraphyly of bryophytes and close relationships of hornworts and vascularplants inferred from analysis of chloroplast rDNA ITS (cpITS) sequences - Arctoa 11 31-43
SANG T DJ CRAWFORD amp TF STUESSY (1997) Chloroplast DNA phylogeny reticulateevolution and biogeography of Paeonia (Paeoniaceae) - Amer J Bot 84 1120-1136
SHAW AJ amp KS RENZAGLIA (2004) Phylogeny and diversification of bryophytes - AmerJ Bot 91 1557-1581
SHAW AJ CJ COX amp B GOFFINET (2005) Global patterns of moss diversity taxonomic andmolecular inferences - Taxon 54 337-352
STECH M (1999a) A reclassification of Dicranaceae (Bryopsida) based on non-coding cpDNAsequence data - J Hattori Bot Lab 86 137-159
STECH M (1999b) A molecular systematic contribution to the position of Amphidium Schimp(Rhabdoweisiaceae Bryopsida) - Nova Hedwigia 68 291-300
STECH M (2004) Supraspecific circumscription and classification of Campylopus Brid(Dicranaceae Bryopsida) based on molecular data - Syst Bot 29 817-824
STECH M amp D QUANDT (2006) Molecular evolution of the chloroplast atpB-rbcL spacer inbryophytes - In SHARMA AK amp A SHARMA (eds) Plant Genome Biodiversity and EvolutionVol 2 Part B pp 409-431 Science Publishers Enfield New Hampshire
21
STECH M D QUANDT amp W FREY (2003) Molecular circumscription of the hornworts(Antho-cerotophyta) based on the chloroplast DNA trnL-trnF region - J Plant Res 116 389-398
STOTLER RE amp B CRANDALL-STOTLER (2005) A revised classification of theAnthocerotophyta and a checklist of the hornworts of North America north of Mexico - Bryologist108 16-26
SWOFFORD DL (2002) PAUP Phylogenetic analysis using parsimony (and other methods)version 40b10 - Sunderland MA
TABERLET P L GIELLY G PAUTOU amp J BOUVET (1991) Universal primers for amplificationof three non-coding regions of chloroplast DNA - Plant Mol Biol 17 1105-1109
TSUBOTA H Y AGENO B ESTEacuteBANEZ T YAMAGUCHI amp H DEGUCHI (2003)Molecular phylogeny of the Grimmiales (Musci) based on chloroplast rbcL sequences - Hikobia 1455-70
TSUBOTA H E DE LUNA D GONZAacuteLEZ MS IGNATOV amp H DEGUCHI (2004) Molecularphylogenetics and ordinal relationships based on analyses of a large-scale data set of 600 rbcLsequences of mosses - Hikobia 14 149-170
VITT DH (1984) Classification of the Bryopsida - In SCHUSTER RM (ed) New Manual ofBryology 2 696-759 Hattori Botanical Laboratory Nichinan Japan
VITT DH B GOFFINET amp T HEDDERSON (1998) 8 The ordinal classification of the mossesquestions and answers for the 1990s - In BATES JW NW ASHTON amp JG DUCKETT (eds)Bryology for the twenty-first century British Bryol Soc pp 113-123
Received 3 September 2007 accepted in revised form 30 October 2007
16
Order Grimmiales MFleischGrimmiaceae Arn Ptychomitriaceae Schimp Seligeriaceae Schimp
Order Archidiales LimprArchidiaceae Schimp
Order Mitteniales ShawMitteniaceae Broth
Order Dicranales HPhilib ex MFleischAmphidiaceae Stech Aongstroemiaceae De Not BruchiaceaeSchimp Calymperaceae Kindb Dicranaceae Schimp Dicranel-laceae Stech Ditrichaceae Limpr Erpodiaceae Broth EustichiaceaeBroth Fissidentaceae Schimp Leucobryaceae Schimp Onco-phoraceae Stech Rhachitheciaceae HRob Schistostegaceae SchimpViridivelleraceae IGStone Wardiaceae Welch
Order Pottiales MFleischEphemeraceae Schimp Hypodontiaceae Stech PleurophascaceaeBroth Pottiaceae Schimp Serpotortellaceae WDReese amp RHZander
Subclass Bryidae EnglOrder Hedwigiales Ochyra
Hedwigiaceae Schimp Rhacocarpaceae KindbOrder Helicophyllales Stech amp WFrey
Helicophyllaceae BrothOrder Bartramiales DQuandt NEBell amp Stech
Bartramiaceae SchwaumlgrOrder Splachnales Ochyra
Meesiaceae Schimp Splachnaceae Grev amp ArnOrder Bryales Limpr
Bryaceae Schwaumlgr Leptostomataceae Schwaumlgr Mniaceae SchwaumlgrPhyllodrepaniaceae Crosby Pseudoditrichaceae Steere amp ZIwatsPulchrinodaceae DQuandt NEBell amp Stech
Order Orthotrichales DixonOrthotrichaceae Arn
Order Orthodontiales NEBell AENewton amp DQuandtOrthodontiaceae Goffinet
Order Aulacomniales NEBell AENewton amp DQuandtAulacomniaceae Schimp
Order Rhizogoniales Goffinet amp WRBuckRhizogoniaceae Broth
Order Hypnodendrales NEBell AENewton amp DQuandtBraithwaiteaceae NEBell AENewton amp DQuandt Hypnodendra-ceae Broth Pterobryellaceae WRBuck amp Vitt Racopilaceae Kindb
Order Ptychomniales WRBuck CJCox AJShaw amp GoffinetPtychomniaceae MFleisch
Order Hookeriales MFleischDaltoniaceae Schimp Hookeriaceae Schimp HypopterygiaceaeMitt Leucomiaceae Broth Pilotrichaceae Kindb SaulomataceaeWRBuck CJCox AJShaw amp Goffinet Schimperobryaceae WR
17
Buck CJCox AJShaw amp GoffinetOrder Hypnales WRBuck amp Vitt
Amblystegiaceae GRoth Anomodontaceae Kindb BrachytheciaceaeSchimp Calliergonaceae Vanderpoorten Hedenaumls CJCox amp AJShaw Catagoniaceae WRBuck amp Ireland Climaciaceae KindbCryphaeaceae Schimp Echinodiaceae Broth Entodontaceae KindbFabroniaceae Schimp Fontinalaceae Schimp Helodiaceae OchyraHeterocladiaceae Ignatov amp Ignatova Hylocomiaceae MFleischHypnaceae Schimp Lembophyllaceae Broth LeptodontaceaeSchimp Lepyrodontaceae Broth Leskeaceae Schimp Leucodon-taceae Schimp Meteoriaceae Kindb Microtheciellaceae HAMillamp AJHarr Myriniaceae Schimp Myuriaceae MFleisch NeckeraceaeSchimp Orthorrhynchiaceae SHLin Phyllogoniaceae KindbPlagiotheciaceae MFleisch Pleuroziopsidaceae Ireland Prionodon-taceae Broth Pseudoleskeaceae Schimp PseudoleskeellaceaeIgnatov amp Ignatova Pterigynandraceae Schimp PterobryaceaeKindb Pylaisiaceae Schimp Pylaisiadelphaceae Goffinet amp WRBuck Regmatodontaceae Broth Rhytidiaceae Broth RigodiaceaeHACrum Rutenbergiaceae MFleisch Scorpidiaceae Ignatov ampIgnatova Sematophyllaceae Broth Sorapillaceae MFleisch Ste-reophyllaceae WRBuck amp Ireland Symphyodontaceae MFleischTheliaceae MFleisch Thuidiaceae Schimp TrachylomataceaeWRBuck amp Vitt
Acknowledgements
Sincere thanks are due to JLReveal (Ithaca) as well as WFPrudhomme van Reine and JFVeldkamp(Leiden) for comments and discussions about suprafamilial taxonomy to DQuandt (Dresden) for providingDNA from Rhacocarpus and Bartramiaceae species and to BGiesicke (Berlin) for technical assistance
References
BECKERT S H MUHLE D PRUCHNER amp V KNOOP (2001) The mitochondrial nad2 geneas a novel marker locus for phylogenetic analysis of early land plants a comparative analysis inmosses - Mol Phylogenet Evol 18 117-126
BELL NE amp AE NEWTON (2004) Systematic studies of non-hypnanaean pleurocarps establishinga phylogenetic framework for investigating the origins of pleurocarpy - In GOFFINET BV HOLLOWELL amp R MAGILL (eds) Molecular systematics of bryophytes Monogr Syst BotMissouri Bot Gard 98 290-319
BELL NE amp AE NEWTON (2007) Pleurocarpy in the Rhizogoniaceous grade - In NEWTONAE amp RS TANGNEY (eds) Pleurocarpous mosses systematics and evolution SystematicsAssociation Special Volume Series 71 41-64
BELL NE D QUANDT TJ OBRIEN amp AE NEWTON (2007) Taxonomy and phylogeny inthe earliest diverging pleurocarps square holes and bifurcating pegs - Bryologist 110 533-560
BORSCH T KW HILU D QUANDT V WILDE C NEINHUIS amp W BARTHLOTT(2003) Non-coding plastid trnT-trnF sequences reveal a well resolved phylogeny of basal angiosperms- J Evol Biol 16 558-576
18
BUCK WR (2007) The history of pleurocarp classification two steps forward one step back - InNEWTON AE amp RS TANGNEY (eds) Pleurocarpous mosses systematics and evolutionSystematics Association Special Volume Series 71 1-18
BUCK WR amp B GOFFINET (2000) Morphology and classification of mosses - In SHAWAJ amp B GOFFINET (eds) Bryophyte Biology pp 71-123 Cambridge University PressCambridge
CHIANG TY BA SCHAAL amp CI PENG (1998) Universal primers for amplification andsequencing a noncoding spacer between atpB and rbcL genes of chloroplast DNA - Bot Bull AcadSin 39 245-250
COX CJ B GOFFINET AE NEWTON AJ SHAW amp TAJ HEDDERSON (2000)Phylogenetic relationships among the diplolepideous-alternate mosses (Bryidae) inferred from nuclearand chloroplast DNA sequences - Bryologist 103 224-241
COX CJ B GOFFINET AJ SHAW amp SB BOLES (2004) Phylogenetic relationships amongthe mosses based on heterogeneous Bayesian analysis of multiple genes from multiple genomiccompartments - Syst Bot 29 234-250
CRANDALL-STOTLER B (1986) Morphogenesis developmental anatomy and bryophytephylogenetics contra-indications of monophyly - J Bryol 14 1-23
CROSBY MR RE MAGILL B ALLEN amp S HE (1999) A checklist of the mosses - MissouriBotanical Garden St Louis Missouri
DOWELD A (2001) Prosyllabus Tracheophytorum - GEOS Moscow i-lxxx + 110 pp
DOYLE JJ amp JL DOYLE (1990) Isolation of plant DNA from fresh tissue - Focus 12 13-15
DUFF RJ JC VILLAREAL DC CARGILL amp KS RENZAGLIA (2007) Progress andchallenges towards developing a phylogeny and classification of the hornworts - Bryologist 110214-243
FLEISCHER M (1920) Natuumlrliches System der Laubmoose - Hedwigia 61 390-400
FORREST LL EC DAVIS DG LONG BJ CRANDALL-STOTLER A CLARK ampML HOLLINGSWORTH (2006) Unraveling the evolutionary history of the liverworts (Marchantio-phyta) multiple taxa genomes and analyses - Bryologist 109 303-334
FRAHM J-P amp W FREY (1987) Moosflora 2 Aufl - UTB 1250 Stuttgart
FREY W (1977) Neue Vorstellungen uumlber die Verwandtschaftsgruppen und die Stammesgeschichteder Laubmoose - In FREY W H HURKA amp F OBERWINKLER (Hrsg) Beitraumlge zur Biologieder Pflanzen pp 117-139 Stuttgart
FREY W amp M STECH (2005) A morpho-molecular classification of the liverworts (Hepa-ticophytina Bryophyta) - Nova Hedwigia 81 55-78
FREY W M STECH amp K MEIszligNER (1999) Chloroplast DNA-relationship in palaeoaustralLopidium concinnum (Hypopterygiaceae Musci) An example of steno-evolution in mosses Studiesin austral temperate rain forest bryophytes 2 - Plant Syst Evol 218 67-75
GOFFINET B amp WR BUCK (2004) Systematics of Bryophyta (mosses) from molecules to arevised classification - In GOFFINET B V HOLLOWELL amp R MAGILL (eds) Molecularsystematics of bryophytes Monogr Syst Bot Missouri Bot Gard 98 205-239
GOFFINET B CJ COX AJ SHAW amp TAJ HEDDERSON (2001) The Bryophyta (mosses)Systematic and evolutionary inferences from an rps4 gene (cpDNA) phylogeny - Ann Bot 87191-208
GOFFINET B NJ WICKETT O WERNER RM ROS AJ SHAW amp CJ COX (2007)Distribution and phylogenetic significance of the 71-kb inversion in the plastid genome in Funariidae(Bryophyta) - Ann Bot 99 747-753
19
GROTH-MALONEK M D PRUCHNER F GREWE amp V KNOOP (2005) Ancestors oftrans-splicing mitochondrial introns support serial sister group relationships of hornworts and mosseswith vascular plants - Mol Biol Evol 22 117-125
HATTORI S amp H INOUE (1958) Preliminary report on Takakia lepidozioides - J Hattori BotLab 19 133-137
HE-NYGREacuteN X A JUSLEacuteN I AHONEN D GLENNY amp S PIIPPO (2006) Illuminating theevolutionary history of liverworts (Marchantiophyta) - towards a natural classification - Cladistics22 1-31
HEDDERSON TAJ DJ MURRAY CJ COX amp TL NOWELL (2004) Phylogeneticrelationships of haplolepideous mosses (Dicranidae) inferred from rps4 gene sequences - Syst Bot29 29-41
LA FARGE C BD MISHER JA WHEELER DP WALL K JOHANNES S SCHAFFERamp AJ SHAW (2000) Phylogenetic relationships within the haplolepideous mosses - Bryologist103 257-276
LA FARGE C AJ SHAW amp DH VITT (2002) The circumscription of the Dicranaceae(Bryopsida) based on the chloroplast regions trnL-trnF and rps4 - Syst Bot 27 435-452
MAGOMBO ZLK (2003) The phylogeny of basal peristomate mosses evidence from cpDNAand implications for peristome evolution - Syst Bot 28 24-38
MCNEILL J FR BARRIE HM BURDET V DEMOULIN DL HAWKSWORTHK MARHOLD DH NICOLSON J PRADO PC SILVA JE SKOG JH WIERSEMA ampNJ TURLAND (2006) International Code of Botanical Nomenclature (Vienna Code) - RegnumVegetabile 146 1-568
MUumlLLER K (2004) PRAP - computation of Bremer support for large data sets - Mol PhylogenetEvol 31 780-782
MUumlLLER K (2005) SeqState - primer design and sequence statistics for phylogenetic DNA datasets - Appl Bioinformatics 4 65-69
MUumlLLER K D QUANDT J MUumlLLER amp C NEINHUIS (2005) PhyDE v0992 PhylogeneticData Editor - httpwwwphydede
MURRAY BM (1988) Systematics of the Andreaeopsida (Bryophyta) two orders with links toTakakia - Nova Hedwigia Beih 90 289-336
NEWTON AE amp RS TANGNEY (eds) (2007) Pleurocarpous mosses systematics and evolutionSystematics Association Special Volume Series 71 CRC Press Boca Raton 434 pp
NEWTON AE CJ COX JG DUCKETT JA WHEELER B GOFFINET TAJ HEDDER-SON amp BD MISHLER (2000) Evolution of the major moss lineages Phylogenetic analyses basedon multiple gene sequences and morphology - Bryologist 103 187-211
NEWTON AE N WIKSTROumlM NE BELL LL FORREST amp MS IGNATOV (2007)Dating the diversification of the pleurocarpous mosses - In NEWTON AE amp RS TANGNEY(eds) Pleurocarpous mosses systematics and evolution Systematics Association Special VolumeSeries 71 337-366
NIXON KC (1999) The parsimony ratchet a new method for rapid parsimony analysis - Cladistics15 407-411
OBRIEN TJ (2007) The phylogenetic distribution of pleurocarpous mosses evidence fromcpDNA sequences - In NEWTON AE amp RS TANGNEY (eds) Pleurocarpous mossessystematics and evolution Systematics Association Special Volume Series 71 19-41
OCHYRA R (2002) Nomenclatural changes in subfamilies of the Dicranaceae - CryptogamieBryol 23 345-349
20
OCHYRA R J ŻARNOWIEC amp H BEDNAREK-OCHYRA (2003) Census catalogue ofPolish mosses - Biodiv Poland 3 1-372
PEDERSEN N amp AE NEWTON (2007) Phylogenetic and morphological studies within thePtychomniales with emphasis on the evolution of dwarf males - In NEWTON AE amp RSTANGNEY (eds) Pleurocarpous mosses systematics and evolution Systematics AssociationSpecial Volume Series 71 367-392
QUANDT D amp M STECH (2005) Molecular evolution and secondary structure of the chloroplasttrnL intron in bryophytes - Mol Phylogenet Evol 36 429-443
QUANDT D K MUumlLLER amp S HUTTUNEN (2003) Characterisation of the chloroplast DNApsbT-H region and the influence of dyad symmetrical elements on phylogenetic reconstructions -Plant Biol 5 400-410
QUANDT D K MUumlLLER M STECH W FREY KW HILU amp T BORSCH (2004) Molecularevolution of the chloroplast trnL-F-region in land plants - In GOFFINET B V HOLLOWELL ampR MAGILL (eds) Molecular systematics of bryophytes Monogr Syst Bot Missouri Bot Gard98 13-37
QUANDT D NE BELL amp M STECH (2007) Unravelling the knot the Pulchrinodaceae famnov (Bryales) - In KUumlRSCHNER H T PFEIFFER amp M STECH (eds) A Festschrift to Wolf-gang Frey - a scientists life between deserts and rain forests Nova Hedwigia Beih 131 21-39
QIU Y-L Y CHO JC COX amp JD PALMER (1998) The gain of three mitochondrial intronsidentifies liverworts as the earliest land plants - Nature 394 671-674
QIU Y-L L LI B WANG Z CHEN V KNOOP M GROTH-MALONEK O DOM-BROVSKA J LEE L KENT J REST GF ESTABROOK TA HENDRY DW TAYLORCM TESTA M AMBROS B CRANDALL-STOTLER J DUFF M STECH W FREYD QUANDT amp CC DAVIS (2006) The deepest divergences in land plants inferred fromphylogenomic evidence - Proc Natl Acad Sci USA 103 15511-15516
RENZAGLIA KS S SCHUETTE RJ DUFF R LIGRONE AJ SHAW BD MISHLER ampJG DUCKETT (2007) Bryophyte phylogeny Advancing the molecular and morphological frontiers- Bryologist 110 179-213
SAMIGULLIN TH SP YACENTYUK GV DEGTYARYEVA KM VALIEJO-ROMANVK BOBROVA I CAPESIUS WF MARTIN AV TROITSKY VR FILIN amp ASANTONOV (2002) Paraphyly of bryophytes and close relationships of hornworts and vascularplants inferred from analysis of chloroplast rDNA ITS (cpITS) sequences - Arctoa 11 31-43
SANG T DJ CRAWFORD amp TF STUESSY (1997) Chloroplast DNA phylogeny reticulateevolution and biogeography of Paeonia (Paeoniaceae) - Amer J Bot 84 1120-1136
SHAW AJ amp KS RENZAGLIA (2004) Phylogeny and diversification of bryophytes - AmerJ Bot 91 1557-1581
SHAW AJ CJ COX amp B GOFFINET (2005) Global patterns of moss diversity taxonomic andmolecular inferences - Taxon 54 337-352
STECH M (1999a) A reclassification of Dicranaceae (Bryopsida) based on non-coding cpDNAsequence data - J Hattori Bot Lab 86 137-159
STECH M (1999b) A molecular systematic contribution to the position of Amphidium Schimp(Rhabdoweisiaceae Bryopsida) - Nova Hedwigia 68 291-300
STECH M (2004) Supraspecific circumscription and classification of Campylopus Brid(Dicranaceae Bryopsida) based on molecular data - Syst Bot 29 817-824
STECH M amp D QUANDT (2006) Molecular evolution of the chloroplast atpB-rbcL spacer inbryophytes - In SHARMA AK amp A SHARMA (eds) Plant Genome Biodiversity and EvolutionVol 2 Part B pp 409-431 Science Publishers Enfield New Hampshire
21
STECH M D QUANDT amp W FREY (2003) Molecular circumscription of the hornworts(Antho-cerotophyta) based on the chloroplast DNA trnL-trnF region - J Plant Res 116 389-398
STOTLER RE amp B CRANDALL-STOTLER (2005) A revised classification of theAnthocerotophyta and a checklist of the hornworts of North America north of Mexico - Bryologist108 16-26
SWOFFORD DL (2002) PAUP Phylogenetic analysis using parsimony (and other methods)version 40b10 - Sunderland MA
TABERLET P L GIELLY G PAUTOU amp J BOUVET (1991) Universal primers for amplificationof three non-coding regions of chloroplast DNA - Plant Mol Biol 17 1105-1109
TSUBOTA H Y AGENO B ESTEacuteBANEZ T YAMAGUCHI amp H DEGUCHI (2003)Molecular phylogeny of the Grimmiales (Musci) based on chloroplast rbcL sequences - Hikobia 1455-70
TSUBOTA H E DE LUNA D GONZAacuteLEZ MS IGNATOV amp H DEGUCHI (2004) Molecularphylogenetics and ordinal relationships based on analyses of a large-scale data set of 600 rbcLsequences of mosses - Hikobia 14 149-170
VITT DH (1984) Classification of the Bryopsida - In SCHUSTER RM (ed) New Manual ofBryology 2 696-759 Hattori Botanical Laboratory Nichinan Japan
VITT DH B GOFFINET amp T HEDDERSON (1998) 8 The ordinal classification of the mossesquestions and answers for the 1990s - In BATES JW NW ASHTON amp JG DUCKETT (eds)Bryology for the twenty-first century British Bryol Soc pp 113-123
Received 3 September 2007 accepted in revised form 30 October 2007
17
Buck CJCox AJShaw amp GoffinetOrder Hypnales WRBuck amp Vitt
Amblystegiaceae GRoth Anomodontaceae Kindb BrachytheciaceaeSchimp Calliergonaceae Vanderpoorten Hedenaumls CJCox amp AJShaw Catagoniaceae WRBuck amp Ireland Climaciaceae KindbCryphaeaceae Schimp Echinodiaceae Broth Entodontaceae KindbFabroniaceae Schimp Fontinalaceae Schimp Helodiaceae OchyraHeterocladiaceae Ignatov amp Ignatova Hylocomiaceae MFleischHypnaceae Schimp Lembophyllaceae Broth LeptodontaceaeSchimp Lepyrodontaceae Broth Leskeaceae Schimp Leucodon-taceae Schimp Meteoriaceae Kindb Microtheciellaceae HAMillamp AJHarr Myriniaceae Schimp Myuriaceae MFleisch NeckeraceaeSchimp Orthorrhynchiaceae SHLin Phyllogoniaceae KindbPlagiotheciaceae MFleisch Pleuroziopsidaceae Ireland Prionodon-taceae Broth Pseudoleskeaceae Schimp PseudoleskeellaceaeIgnatov amp Ignatova Pterigynandraceae Schimp PterobryaceaeKindb Pylaisiaceae Schimp Pylaisiadelphaceae Goffinet amp WRBuck Regmatodontaceae Broth Rhytidiaceae Broth RigodiaceaeHACrum Rutenbergiaceae MFleisch Scorpidiaceae Ignatov ampIgnatova Sematophyllaceae Broth Sorapillaceae MFleisch Ste-reophyllaceae WRBuck amp Ireland Symphyodontaceae MFleischTheliaceae MFleisch Thuidiaceae Schimp TrachylomataceaeWRBuck amp Vitt
Acknowledgements
Sincere thanks are due to JLReveal (Ithaca) as well as WFPrudhomme van Reine and JFVeldkamp(Leiden) for comments and discussions about suprafamilial taxonomy to DQuandt (Dresden) for providingDNA from Rhacocarpus and Bartramiaceae species and to BGiesicke (Berlin) for technical assistance
References
BECKERT S H MUHLE D PRUCHNER amp V KNOOP (2001) The mitochondrial nad2 geneas a novel marker locus for phylogenetic analysis of early land plants a comparative analysis inmosses - Mol Phylogenet Evol 18 117-126
BELL NE amp AE NEWTON (2004) Systematic studies of non-hypnanaean pleurocarps establishinga phylogenetic framework for investigating the origins of pleurocarpy - In GOFFINET BV HOLLOWELL amp R MAGILL (eds) Molecular systematics of bryophytes Monogr Syst BotMissouri Bot Gard 98 290-319
BELL NE amp AE NEWTON (2007) Pleurocarpy in the Rhizogoniaceous grade - In NEWTONAE amp RS TANGNEY (eds) Pleurocarpous mosses systematics and evolution SystematicsAssociation Special Volume Series 71 41-64
BELL NE D QUANDT TJ OBRIEN amp AE NEWTON (2007) Taxonomy and phylogeny inthe earliest diverging pleurocarps square holes and bifurcating pegs - Bryologist 110 533-560
BORSCH T KW HILU D QUANDT V WILDE C NEINHUIS amp W BARTHLOTT(2003) Non-coding plastid trnT-trnF sequences reveal a well resolved phylogeny of basal angiosperms- J Evol Biol 16 558-576
18
BUCK WR (2007) The history of pleurocarp classification two steps forward one step back - InNEWTON AE amp RS TANGNEY (eds) Pleurocarpous mosses systematics and evolutionSystematics Association Special Volume Series 71 1-18
BUCK WR amp B GOFFINET (2000) Morphology and classification of mosses - In SHAWAJ amp B GOFFINET (eds) Bryophyte Biology pp 71-123 Cambridge University PressCambridge
CHIANG TY BA SCHAAL amp CI PENG (1998) Universal primers for amplification andsequencing a noncoding spacer between atpB and rbcL genes of chloroplast DNA - Bot Bull AcadSin 39 245-250
COX CJ B GOFFINET AE NEWTON AJ SHAW amp TAJ HEDDERSON (2000)Phylogenetic relationships among the diplolepideous-alternate mosses (Bryidae) inferred from nuclearand chloroplast DNA sequences - Bryologist 103 224-241
COX CJ B GOFFINET AJ SHAW amp SB BOLES (2004) Phylogenetic relationships amongthe mosses based on heterogeneous Bayesian analysis of multiple genes from multiple genomiccompartments - Syst Bot 29 234-250
CRANDALL-STOTLER B (1986) Morphogenesis developmental anatomy and bryophytephylogenetics contra-indications of monophyly - J Bryol 14 1-23
CROSBY MR RE MAGILL B ALLEN amp S HE (1999) A checklist of the mosses - MissouriBotanical Garden St Louis Missouri
DOWELD A (2001) Prosyllabus Tracheophytorum - GEOS Moscow i-lxxx + 110 pp
DOYLE JJ amp JL DOYLE (1990) Isolation of plant DNA from fresh tissue - Focus 12 13-15
DUFF RJ JC VILLAREAL DC CARGILL amp KS RENZAGLIA (2007) Progress andchallenges towards developing a phylogeny and classification of the hornworts - Bryologist 110214-243
FLEISCHER M (1920) Natuumlrliches System der Laubmoose - Hedwigia 61 390-400
FORREST LL EC DAVIS DG LONG BJ CRANDALL-STOTLER A CLARK ampML HOLLINGSWORTH (2006) Unraveling the evolutionary history of the liverworts (Marchantio-phyta) multiple taxa genomes and analyses - Bryologist 109 303-334
FRAHM J-P amp W FREY (1987) Moosflora 2 Aufl - UTB 1250 Stuttgart
FREY W (1977) Neue Vorstellungen uumlber die Verwandtschaftsgruppen und die Stammesgeschichteder Laubmoose - In FREY W H HURKA amp F OBERWINKLER (Hrsg) Beitraumlge zur Biologieder Pflanzen pp 117-139 Stuttgart
FREY W amp M STECH (2005) A morpho-molecular classification of the liverworts (Hepa-ticophytina Bryophyta) - Nova Hedwigia 81 55-78
FREY W M STECH amp K MEIszligNER (1999) Chloroplast DNA-relationship in palaeoaustralLopidium concinnum (Hypopterygiaceae Musci) An example of steno-evolution in mosses Studiesin austral temperate rain forest bryophytes 2 - Plant Syst Evol 218 67-75
GOFFINET B amp WR BUCK (2004) Systematics of Bryophyta (mosses) from molecules to arevised classification - In GOFFINET B V HOLLOWELL amp R MAGILL (eds) Molecularsystematics of bryophytes Monogr Syst Bot Missouri Bot Gard 98 205-239
GOFFINET B CJ COX AJ SHAW amp TAJ HEDDERSON (2001) The Bryophyta (mosses)Systematic and evolutionary inferences from an rps4 gene (cpDNA) phylogeny - Ann Bot 87191-208
GOFFINET B NJ WICKETT O WERNER RM ROS AJ SHAW amp CJ COX (2007)Distribution and phylogenetic significance of the 71-kb inversion in the plastid genome in Funariidae(Bryophyta) - Ann Bot 99 747-753
19
GROTH-MALONEK M D PRUCHNER F GREWE amp V KNOOP (2005) Ancestors oftrans-splicing mitochondrial introns support serial sister group relationships of hornworts and mosseswith vascular plants - Mol Biol Evol 22 117-125
HATTORI S amp H INOUE (1958) Preliminary report on Takakia lepidozioides - J Hattori BotLab 19 133-137
HE-NYGREacuteN X A JUSLEacuteN I AHONEN D GLENNY amp S PIIPPO (2006) Illuminating theevolutionary history of liverworts (Marchantiophyta) - towards a natural classification - Cladistics22 1-31
HEDDERSON TAJ DJ MURRAY CJ COX amp TL NOWELL (2004) Phylogeneticrelationships of haplolepideous mosses (Dicranidae) inferred from rps4 gene sequences - Syst Bot29 29-41
LA FARGE C BD MISHER JA WHEELER DP WALL K JOHANNES S SCHAFFERamp AJ SHAW (2000) Phylogenetic relationships within the haplolepideous mosses - Bryologist103 257-276
LA FARGE C AJ SHAW amp DH VITT (2002) The circumscription of the Dicranaceae(Bryopsida) based on the chloroplast regions trnL-trnF and rps4 - Syst Bot 27 435-452
MAGOMBO ZLK (2003) The phylogeny of basal peristomate mosses evidence from cpDNAand implications for peristome evolution - Syst Bot 28 24-38
MCNEILL J FR BARRIE HM BURDET V DEMOULIN DL HAWKSWORTHK MARHOLD DH NICOLSON J PRADO PC SILVA JE SKOG JH WIERSEMA ampNJ TURLAND (2006) International Code of Botanical Nomenclature (Vienna Code) - RegnumVegetabile 146 1-568
MUumlLLER K (2004) PRAP - computation of Bremer support for large data sets - Mol PhylogenetEvol 31 780-782
MUumlLLER K (2005) SeqState - primer design and sequence statistics for phylogenetic DNA datasets - Appl Bioinformatics 4 65-69
MUumlLLER K D QUANDT J MUumlLLER amp C NEINHUIS (2005) PhyDE v0992 PhylogeneticData Editor - httpwwwphydede
MURRAY BM (1988) Systematics of the Andreaeopsida (Bryophyta) two orders with links toTakakia - Nova Hedwigia Beih 90 289-336
NEWTON AE amp RS TANGNEY (eds) (2007) Pleurocarpous mosses systematics and evolutionSystematics Association Special Volume Series 71 CRC Press Boca Raton 434 pp
NEWTON AE CJ COX JG DUCKETT JA WHEELER B GOFFINET TAJ HEDDER-SON amp BD MISHLER (2000) Evolution of the major moss lineages Phylogenetic analyses basedon multiple gene sequences and morphology - Bryologist 103 187-211
NEWTON AE N WIKSTROumlM NE BELL LL FORREST amp MS IGNATOV (2007)Dating the diversification of the pleurocarpous mosses - In NEWTON AE amp RS TANGNEY(eds) Pleurocarpous mosses systematics and evolution Systematics Association Special VolumeSeries 71 337-366
NIXON KC (1999) The parsimony ratchet a new method for rapid parsimony analysis - Cladistics15 407-411
OBRIEN TJ (2007) The phylogenetic distribution of pleurocarpous mosses evidence fromcpDNA sequences - In NEWTON AE amp RS TANGNEY (eds) Pleurocarpous mossessystematics and evolution Systematics Association Special Volume Series 71 19-41
OCHYRA R (2002) Nomenclatural changes in subfamilies of the Dicranaceae - CryptogamieBryol 23 345-349
20
OCHYRA R J ŻARNOWIEC amp H BEDNAREK-OCHYRA (2003) Census catalogue ofPolish mosses - Biodiv Poland 3 1-372
PEDERSEN N amp AE NEWTON (2007) Phylogenetic and morphological studies within thePtychomniales with emphasis on the evolution of dwarf males - In NEWTON AE amp RSTANGNEY (eds) Pleurocarpous mosses systematics and evolution Systematics AssociationSpecial Volume Series 71 367-392
QUANDT D amp M STECH (2005) Molecular evolution and secondary structure of the chloroplasttrnL intron in bryophytes - Mol Phylogenet Evol 36 429-443
QUANDT D K MUumlLLER amp S HUTTUNEN (2003) Characterisation of the chloroplast DNApsbT-H region and the influence of dyad symmetrical elements on phylogenetic reconstructions -Plant Biol 5 400-410
QUANDT D K MUumlLLER M STECH W FREY KW HILU amp T BORSCH (2004) Molecularevolution of the chloroplast trnL-F-region in land plants - In GOFFINET B V HOLLOWELL ampR MAGILL (eds) Molecular systematics of bryophytes Monogr Syst Bot Missouri Bot Gard98 13-37
QUANDT D NE BELL amp M STECH (2007) Unravelling the knot the Pulchrinodaceae famnov (Bryales) - In KUumlRSCHNER H T PFEIFFER amp M STECH (eds) A Festschrift to Wolf-gang Frey - a scientists life between deserts and rain forests Nova Hedwigia Beih 131 21-39
QIU Y-L Y CHO JC COX amp JD PALMER (1998) The gain of three mitochondrial intronsidentifies liverworts as the earliest land plants - Nature 394 671-674
QIU Y-L L LI B WANG Z CHEN V KNOOP M GROTH-MALONEK O DOM-BROVSKA J LEE L KENT J REST GF ESTABROOK TA HENDRY DW TAYLORCM TESTA M AMBROS B CRANDALL-STOTLER J DUFF M STECH W FREYD QUANDT amp CC DAVIS (2006) The deepest divergences in land plants inferred fromphylogenomic evidence - Proc Natl Acad Sci USA 103 15511-15516
RENZAGLIA KS S SCHUETTE RJ DUFF R LIGRONE AJ SHAW BD MISHLER ampJG DUCKETT (2007) Bryophyte phylogeny Advancing the molecular and morphological frontiers- Bryologist 110 179-213
SAMIGULLIN TH SP YACENTYUK GV DEGTYARYEVA KM VALIEJO-ROMANVK BOBROVA I CAPESIUS WF MARTIN AV TROITSKY VR FILIN amp ASANTONOV (2002) Paraphyly of bryophytes and close relationships of hornworts and vascularplants inferred from analysis of chloroplast rDNA ITS (cpITS) sequences - Arctoa 11 31-43
SANG T DJ CRAWFORD amp TF STUESSY (1997) Chloroplast DNA phylogeny reticulateevolution and biogeography of Paeonia (Paeoniaceae) - Amer J Bot 84 1120-1136
SHAW AJ amp KS RENZAGLIA (2004) Phylogeny and diversification of bryophytes - AmerJ Bot 91 1557-1581
SHAW AJ CJ COX amp B GOFFINET (2005) Global patterns of moss diversity taxonomic andmolecular inferences - Taxon 54 337-352
STECH M (1999a) A reclassification of Dicranaceae (Bryopsida) based on non-coding cpDNAsequence data - J Hattori Bot Lab 86 137-159
STECH M (1999b) A molecular systematic contribution to the position of Amphidium Schimp(Rhabdoweisiaceae Bryopsida) - Nova Hedwigia 68 291-300
STECH M (2004) Supraspecific circumscription and classification of Campylopus Brid(Dicranaceae Bryopsida) based on molecular data - Syst Bot 29 817-824
STECH M amp D QUANDT (2006) Molecular evolution of the chloroplast atpB-rbcL spacer inbryophytes - In SHARMA AK amp A SHARMA (eds) Plant Genome Biodiversity and EvolutionVol 2 Part B pp 409-431 Science Publishers Enfield New Hampshire
21
STECH M D QUANDT amp W FREY (2003) Molecular circumscription of the hornworts(Antho-cerotophyta) based on the chloroplast DNA trnL-trnF region - J Plant Res 116 389-398
STOTLER RE amp B CRANDALL-STOTLER (2005) A revised classification of theAnthocerotophyta and a checklist of the hornworts of North America north of Mexico - Bryologist108 16-26
SWOFFORD DL (2002) PAUP Phylogenetic analysis using parsimony (and other methods)version 40b10 - Sunderland MA
TABERLET P L GIELLY G PAUTOU amp J BOUVET (1991) Universal primers for amplificationof three non-coding regions of chloroplast DNA - Plant Mol Biol 17 1105-1109
TSUBOTA H Y AGENO B ESTEacuteBANEZ T YAMAGUCHI amp H DEGUCHI (2003)Molecular phylogeny of the Grimmiales (Musci) based on chloroplast rbcL sequences - Hikobia 1455-70
TSUBOTA H E DE LUNA D GONZAacuteLEZ MS IGNATOV amp H DEGUCHI (2004) Molecularphylogenetics and ordinal relationships based on analyses of a large-scale data set of 600 rbcLsequences of mosses - Hikobia 14 149-170
VITT DH (1984) Classification of the Bryopsida - In SCHUSTER RM (ed) New Manual ofBryology 2 696-759 Hattori Botanical Laboratory Nichinan Japan
VITT DH B GOFFINET amp T HEDDERSON (1998) 8 The ordinal classification of the mossesquestions and answers for the 1990s - In BATES JW NW ASHTON amp JG DUCKETT (eds)Bryology for the twenty-first century British Bryol Soc pp 113-123
Received 3 September 2007 accepted in revised form 30 October 2007
18
BUCK WR (2007) The history of pleurocarp classification two steps forward one step back - InNEWTON AE amp RS TANGNEY (eds) Pleurocarpous mosses systematics and evolutionSystematics Association Special Volume Series 71 1-18
BUCK WR amp B GOFFINET (2000) Morphology and classification of mosses - In SHAWAJ amp B GOFFINET (eds) Bryophyte Biology pp 71-123 Cambridge University PressCambridge
CHIANG TY BA SCHAAL amp CI PENG (1998) Universal primers for amplification andsequencing a noncoding spacer between atpB and rbcL genes of chloroplast DNA - Bot Bull AcadSin 39 245-250
COX CJ B GOFFINET AE NEWTON AJ SHAW amp TAJ HEDDERSON (2000)Phylogenetic relationships among the diplolepideous-alternate mosses (Bryidae) inferred from nuclearand chloroplast DNA sequences - Bryologist 103 224-241
COX CJ B GOFFINET AJ SHAW amp SB BOLES (2004) Phylogenetic relationships amongthe mosses based on heterogeneous Bayesian analysis of multiple genes from multiple genomiccompartments - Syst Bot 29 234-250
CRANDALL-STOTLER B (1986) Morphogenesis developmental anatomy and bryophytephylogenetics contra-indications of monophyly - J Bryol 14 1-23
CROSBY MR RE MAGILL B ALLEN amp S HE (1999) A checklist of the mosses - MissouriBotanical Garden St Louis Missouri
DOWELD A (2001) Prosyllabus Tracheophytorum - GEOS Moscow i-lxxx + 110 pp
DOYLE JJ amp JL DOYLE (1990) Isolation of plant DNA from fresh tissue - Focus 12 13-15
DUFF RJ JC VILLAREAL DC CARGILL amp KS RENZAGLIA (2007) Progress andchallenges towards developing a phylogeny and classification of the hornworts - Bryologist 110214-243
FLEISCHER M (1920) Natuumlrliches System der Laubmoose - Hedwigia 61 390-400
FORREST LL EC DAVIS DG LONG BJ CRANDALL-STOTLER A CLARK ampML HOLLINGSWORTH (2006) Unraveling the evolutionary history of the liverworts (Marchantio-phyta) multiple taxa genomes and analyses - Bryologist 109 303-334
FRAHM J-P amp W FREY (1987) Moosflora 2 Aufl - UTB 1250 Stuttgart
FREY W (1977) Neue Vorstellungen uumlber die Verwandtschaftsgruppen und die Stammesgeschichteder Laubmoose - In FREY W H HURKA amp F OBERWINKLER (Hrsg) Beitraumlge zur Biologieder Pflanzen pp 117-139 Stuttgart
FREY W amp M STECH (2005) A morpho-molecular classification of the liverworts (Hepa-ticophytina Bryophyta) - Nova Hedwigia 81 55-78
FREY W M STECH amp K MEIszligNER (1999) Chloroplast DNA-relationship in palaeoaustralLopidium concinnum (Hypopterygiaceae Musci) An example of steno-evolution in mosses Studiesin austral temperate rain forest bryophytes 2 - Plant Syst Evol 218 67-75
GOFFINET B amp WR BUCK (2004) Systematics of Bryophyta (mosses) from molecules to arevised classification - In GOFFINET B V HOLLOWELL amp R MAGILL (eds) Molecularsystematics of bryophytes Monogr Syst Bot Missouri Bot Gard 98 205-239
GOFFINET B CJ COX AJ SHAW amp TAJ HEDDERSON (2001) The Bryophyta (mosses)Systematic and evolutionary inferences from an rps4 gene (cpDNA) phylogeny - Ann Bot 87191-208
GOFFINET B NJ WICKETT O WERNER RM ROS AJ SHAW amp CJ COX (2007)Distribution and phylogenetic significance of the 71-kb inversion in the plastid genome in Funariidae(Bryophyta) - Ann Bot 99 747-753
19
GROTH-MALONEK M D PRUCHNER F GREWE amp V KNOOP (2005) Ancestors oftrans-splicing mitochondrial introns support serial sister group relationships of hornworts and mosseswith vascular plants - Mol Biol Evol 22 117-125
HATTORI S amp H INOUE (1958) Preliminary report on Takakia lepidozioides - J Hattori BotLab 19 133-137
HE-NYGREacuteN X A JUSLEacuteN I AHONEN D GLENNY amp S PIIPPO (2006) Illuminating theevolutionary history of liverworts (Marchantiophyta) - towards a natural classification - Cladistics22 1-31
HEDDERSON TAJ DJ MURRAY CJ COX amp TL NOWELL (2004) Phylogeneticrelationships of haplolepideous mosses (Dicranidae) inferred from rps4 gene sequences - Syst Bot29 29-41
LA FARGE C BD MISHER JA WHEELER DP WALL K JOHANNES S SCHAFFERamp AJ SHAW (2000) Phylogenetic relationships within the haplolepideous mosses - Bryologist103 257-276
LA FARGE C AJ SHAW amp DH VITT (2002) The circumscription of the Dicranaceae(Bryopsida) based on the chloroplast regions trnL-trnF and rps4 - Syst Bot 27 435-452
MAGOMBO ZLK (2003) The phylogeny of basal peristomate mosses evidence from cpDNAand implications for peristome evolution - Syst Bot 28 24-38
MCNEILL J FR BARRIE HM BURDET V DEMOULIN DL HAWKSWORTHK MARHOLD DH NICOLSON J PRADO PC SILVA JE SKOG JH WIERSEMA ampNJ TURLAND (2006) International Code of Botanical Nomenclature (Vienna Code) - RegnumVegetabile 146 1-568
MUumlLLER K (2004) PRAP - computation of Bremer support for large data sets - Mol PhylogenetEvol 31 780-782
MUumlLLER K (2005) SeqState - primer design and sequence statistics for phylogenetic DNA datasets - Appl Bioinformatics 4 65-69
MUumlLLER K D QUANDT J MUumlLLER amp C NEINHUIS (2005) PhyDE v0992 PhylogeneticData Editor - httpwwwphydede
MURRAY BM (1988) Systematics of the Andreaeopsida (Bryophyta) two orders with links toTakakia - Nova Hedwigia Beih 90 289-336
NEWTON AE amp RS TANGNEY (eds) (2007) Pleurocarpous mosses systematics and evolutionSystematics Association Special Volume Series 71 CRC Press Boca Raton 434 pp
NEWTON AE CJ COX JG DUCKETT JA WHEELER B GOFFINET TAJ HEDDER-SON amp BD MISHLER (2000) Evolution of the major moss lineages Phylogenetic analyses basedon multiple gene sequences and morphology - Bryologist 103 187-211
NEWTON AE N WIKSTROumlM NE BELL LL FORREST amp MS IGNATOV (2007)Dating the diversification of the pleurocarpous mosses - In NEWTON AE amp RS TANGNEY(eds) Pleurocarpous mosses systematics and evolution Systematics Association Special VolumeSeries 71 337-366
NIXON KC (1999) The parsimony ratchet a new method for rapid parsimony analysis - Cladistics15 407-411
OBRIEN TJ (2007) The phylogenetic distribution of pleurocarpous mosses evidence fromcpDNA sequences - In NEWTON AE amp RS TANGNEY (eds) Pleurocarpous mossessystematics and evolution Systematics Association Special Volume Series 71 19-41
OCHYRA R (2002) Nomenclatural changes in subfamilies of the Dicranaceae - CryptogamieBryol 23 345-349
20
OCHYRA R J ŻARNOWIEC amp H BEDNAREK-OCHYRA (2003) Census catalogue ofPolish mosses - Biodiv Poland 3 1-372
PEDERSEN N amp AE NEWTON (2007) Phylogenetic and morphological studies within thePtychomniales with emphasis on the evolution of dwarf males - In NEWTON AE amp RSTANGNEY (eds) Pleurocarpous mosses systematics and evolution Systematics AssociationSpecial Volume Series 71 367-392
QUANDT D amp M STECH (2005) Molecular evolution and secondary structure of the chloroplasttrnL intron in bryophytes - Mol Phylogenet Evol 36 429-443
QUANDT D K MUumlLLER amp S HUTTUNEN (2003) Characterisation of the chloroplast DNApsbT-H region and the influence of dyad symmetrical elements on phylogenetic reconstructions -Plant Biol 5 400-410
QUANDT D K MUumlLLER M STECH W FREY KW HILU amp T BORSCH (2004) Molecularevolution of the chloroplast trnL-F-region in land plants - In GOFFINET B V HOLLOWELL ampR MAGILL (eds) Molecular systematics of bryophytes Monogr Syst Bot Missouri Bot Gard98 13-37
QUANDT D NE BELL amp M STECH (2007) Unravelling the knot the Pulchrinodaceae famnov (Bryales) - In KUumlRSCHNER H T PFEIFFER amp M STECH (eds) A Festschrift to Wolf-gang Frey - a scientists life between deserts and rain forests Nova Hedwigia Beih 131 21-39
QIU Y-L Y CHO JC COX amp JD PALMER (1998) The gain of three mitochondrial intronsidentifies liverworts as the earliest land plants - Nature 394 671-674
QIU Y-L L LI B WANG Z CHEN V KNOOP M GROTH-MALONEK O DOM-BROVSKA J LEE L KENT J REST GF ESTABROOK TA HENDRY DW TAYLORCM TESTA M AMBROS B CRANDALL-STOTLER J DUFF M STECH W FREYD QUANDT amp CC DAVIS (2006) The deepest divergences in land plants inferred fromphylogenomic evidence - Proc Natl Acad Sci USA 103 15511-15516
RENZAGLIA KS S SCHUETTE RJ DUFF R LIGRONE AJ SHAW BD MISHLER ampJG DUCKETT (2007) Bryophyte phylogeny Advancing the molecular and morphological frontiers- Bryologist 110 179-213
SAMIGULLIN TH SP YACENTYUK GV DEGTYARYEVA KM VALIEJO-ROMANVK BOBROVA I CAPESIUS WF MARTIN AV TROITSKY VR FILIN amp ASANTONOV (2002) Paraphyly of bryophytes and close relationships of hornworts and vascularplants inferred from analysis of chloroplast rDNA ITS (cpITS) sequences - Arctoa 11 31-43
SANG T DJ CRAWFORD amp TF STUESSY (1997) Chloroplast DNA phylogeny reticulateevolution and biogeography of Paeonia (Paeoniaceae) - Amer J Bot 84 1120-1136
SHAW AJ amp KS RENZAGLIA (2004) Phylogeny and diversification of bryophytes - AmerJ Bot 91 1557-1581
SHAW AJ CJ COX amp B GOFFINET (2005) Global patterns of moss diversity taxonomic andmolecular inferences - Taxon 54 337-352
STECH M (1999a) A reclassification of Dicranaceae (Bryopsida) based on non-coding cpDNAsequence data - J Hattori Bot Lab 86 137-159
STECH M (1999b) A molecular systematic contribution to the position of Amphidium Schimp(Rhabdoweisiaceae Bryopsida) - Nova Hedwigia 68 291-300
STECH M (2004) Supraspecific circumscription and classification of Campylopus Brid(Dicranaceae Bryopsida) based on molecular data - Syst Bot 29 817-824
STECH M amp D QUANDT (2006) Molecular evolution of the chloroplast atpB-rbcL spacer inbryophytes - In SHARMA AK amp A SHARMA (eds) Plant Genome Biodiversity and EvolutionVol 2 Part B pp 409-431 Science Publishers Enfield New Hampshire
21
STECH M D QUANDT amp W FREY (2003) Molecular circumscription of the hornworts(Antho-cerotophyta) based on the chloroplast DNA trnL-trnF region - J Plant Res 116 389-398
STOTLER RE amp B CRANDALL-STOTLER (2005) A revised classification of theAnthocerotophyta and a checklist of the hornworts of North America north of Mexico - Bryologist108 16-26
SWOFFORD DL (2002) PAUP Phylogenetic analysis using parsimony (and other methods)version 40b10 - Sunderland MA
TABERLET P L GIELLY G PAUTOU amp J BOUVET (1991) Universal primers for amplificationof three non-coding regions of chloroplast DNA - Plant Mol Biol 17 1105-1109
TSUBOTA H Y AGENO B ESTEacuteBANEZ T YAMAGUCHI amp H DEGUCHI (2003)Molecular phylogeny of the Grimmiales (Musci) based on chloroplast rbcL sequences - Hikobia 1455-70
TSUBOTA H E DE LUNA D GONZAacuteLEZ MS IGNATOV amp H DEGUCHI (2004) Molecularphylogenetics and ordinal relationships based on analyses of a large-scale data set of 600 rbcLsequences of mosses - Hikobia 14 149-170
VITT DH (1984) Classification of the Bryopsida - In SCHUSTER RM (ed) New Manual ofBryology 2 696-759 Hattori Botanical Laboratory Nichinan Japan
VITT DH B GOFFINET amp T HEDDERSON (1998) 8 The ordinal classification of the mossesquestions and answers for the 1990s - In BATES JW NW ASHTON amp JG DUCKETT (eds)Bryology for the twenty-first century British Bryol Soc pp 113-123
Received 3 September 2007 accepted in revised form 30 October 2007
19
GROTH-MALONEK M D PRUCHNER F GREWE amp V KNOOP (2005) Ancestors oftrans-splicing mitochondrial introns support serial sister group relationships of hornworts and mosseswith vascular plants - Mol Biol Evol 22 117-125
HATTORI S amp H INOUE (1958) Preliminary report on Takakia lepidozioides - J Hattori BotLab 19 133-137
HE-NYGREacuteN X A JUSLEacuteN I AHONEN D GLENNY amp S PIIPPO (2006) Illuminating theevolutionary history of liverworts (Marchantiophyta) - towards a natural classification - Cladistics22 1-31
HEDDERSON TAJ DJ MURRAY CJ COX amp TL NOWELL (2004) Phylogeneticrelationships of haplolepideous mosses (Dicranidae) inferred from rps4 gene sequences - Syst Bot29 29-41
LA FARGE C BD MISHER JA WHEELER DP WALL K JOHANNES S SCHAFFERamp AJ SHAW (2000) Phylogenetic relationships within the haplolepideous mosses - Bryologist103 257-276
LA FARGE C AJ SHAW amp DH VITT (2002) The circumscription of the Dicranaceae(Bryopsida) based on the chloroplast regions trnL-trnF and rps4 - Syst Bot 27 435-452
MAGOMBO ZLK (2003) The phylogeny of basal peristomate mosses evidence from cpDNAand implications for peristome evolution - Syst Bot 28 24-38
MCNEILL J FR BARRIE HM BURDET V DEMOULIN DL HAWKSWORTHK MARHOLD DH NICOLSON J PRADO PC SILVA JE SKOG JH WIERSEMA ampNJ TURLAND (2006) International Code of Botanical Nomenclature (Vienna Code) - RegnumVegetabile 146 1-568
MUumlLLER K (2004) PRAP - computation of Bremer support for large data sets - Mol PhylogenetEvol 31 780-782
MUumlLLER K (2005) SeqState - primer design and sequence statistics for phylogenetic DNA datasets - Appl Bioinformatics 4 65-69
MUumlLLER K D QUANDT J MUumlLLER amp C NEINHUIS (2005) PhyDE v0992 PhylogeneticData Editor - httpwwwphydede
MURRAY BM (1988) Systematics of the Andreaeopsida (Bryophyta) two orders with links toTakakia - Nova Hedwigia Beih 90 289-336
NEWTON AE amp RS TANGNEY (eds) (2007) Pleurocarpous mosses systematics and evolutionSystematics Association Special Volume Series 71 CRC Press Boca Raton 434 pp
NEWTON AE CJ COX JG DUCKETT JA WHEELER B GOFFINET TAJ HEDDER-SON amp BD MISHLER (2000) Evolution of the major moss lineages Phylogenetic analyses basedon multiple gene sequences and morphology - Bryologist 103 187-211
NEWTON AE N WIKSTROumlM NE BELL LL FORREST amp MS IGNATOV (2007)Dating the diversification of the pleurocarpous mosses - In NEWTON AE amp RS TANGNEY(eds) Pleurocarpous mosses systematics and evolution Systematics Association Special VolumeSeries 71 337-366
NIXON KC (1999) The parsimony ratchet a new method for rapid parsimony analysis - Cladistics15 407-411
OBRIEN TJ (2007) The phylogenetic distribution of pleurocarpous mosses evidence fromcpDNA sequences - In NEWTON AE amp RS TANGNEY (eds) Pleurocarpous mossessystematics and evolution Systematics Association Special Volume Series 71 19-41
OCHYRA R (2002) Nomenclatural changes in subfamilies of the Dicranaceae - CryptogamieBryol 23 345-349
20
OCHYRA R J ŻARNOWIEC amp H BEDNAREK-OCHYRA (2003) Census catalogue ofPolish mosses - Biodiv Poland 3 1-372
PEDERSEN N amp AE NEWTON (2007) Phylogenetic and morphological studies within thePtychomniales with emphasis on the evolution of dwarf males - In NEWTON AE amp RSTANGNEY (eds) Pleurocarpous mosses systematics and evolution Systematics AssociationSpecial Volume Series 71 367-392
QUANDT D amp M STECH (2005) Molecular evolution and secondary structure of the chloroplasttrnL intron in bryophytes - Mol Phylogenet Evol 36 429-443
QUANDT D K MUumlLLER amp S HUTTUNEN (2003) Characterisation of the chloroplast DNApsbT-H region and the influence of dyad symmetrical elements on phylogenetic reconstructions -Plant Biol 5 400-410
QUANDT D K MUumlLLER M STECH W FREY KW HILU amp T BORSCH (2004) Molecularevolution of the chloroplast trnL-F-region in land plants - In GOFFINET B V HOLLOWELL ampR MAGILL (eds) Molecular systematics of bryophytes Monogr Syst Bot Missouri Bot Gard98 13-37
QUANDT D NE BELL amp M STECH (2007) Unravelling the knot the Pulchrinodaceae famnov (Bryales) - In KUumlRSCHNER H T PFEIFFER amp M STECH (eds) A Festschrift to Wolf-gang Frey - a scientists life between deserts and rain forests Nova Hedwigia Beih 131 21-39
QIU Y-L Y CHO JC COX amp JD PALMER (1998) The gain of three mitochondrial intronsidentifies liverworts as the earliest land plants - Nature 394 671-674
QIU Y-L L LI B WANG Z CHEN V KNOOP M GROTH-MALONEK O DOM-BROVSKA J LEE L KENT J REST GF ESTABROOK TA HENDRY DW TAYLORCM TESTA M AMBROS B CRANDALL-STOTLER J DUFF M STECH W FREYD QUANDT amp CC DAVIS (2006) The deepest divergences in land plants inferred fromphylogenomic evidence - Proc Natl Acad Sci USA 103 15511-15516
RENZAGLIA KS S SCHUETTE RJ DUFF R LIGRONE AJ SHAW BD MISHLER ampJG DUCKETT (2007) Bryophyte phylogeny Advancing the molecular and morphological frontiers- Bryologist 110 179-213
SAMIGULLIN TH SP YACENTYUK GV DEGTYARYEVA KM VALIEJO-ROMANVK BOBROVA I CAPESIUS WF MARTIN AV TROITSKY VR FILIN amp ASANTONOV (2002) Paraphyly of bryophytes and close relationships of hornworts and vascularplants inferred from analysis of chloroplast rDNA ITS (cpITS) sequences - Arctoa 11 31-43
SANG T DJ CRAWFORD amp TF STUESSY (1997) Chloroplast DNA phylogeny reticulateevolution and biogeography of Paeonia (Paeoniaceae) - Amer J Bot 84 1120-1136
SHAW AJ amp KS RENZAGLIA (2004) Phylogeny and diversification of bryophytes - AmerJ Bot 91 1557-1581
SHAW AJ CJ COX amp B GOFFINET (2005) Global patterns of moss diversity taxonomic andmolecular inferences - Taxon 54 337-352
STECH M (1999a) A reclassification of Dicranaceae (Bryopsida) based on non-coding cpDNAsequence data - J Hattori Bot Lab 86 137-159
STECH M (1999b) A molecular systematic contribution to the position of Amphidium Schimp(Rhabdoweisiaceae Bryopsida) - Nova Hedwigia 68 291-300
STECH M (2004) Supraspecific circumscription and classification of Campylopus Brid(Dicranaceae Bryopsida) based on molecular data - Syst Bot 29 817-824
STECH M amp D QUANDT (2006) Molecular evolution of the chloroplast atpB-rbcL spacer inbryophytes - In SHARMA AK amp A SHARMA (eds) Plant Genome Biodiversity and EvolutionVol 2 Part B pp 409-431 Science Publishers Enfield New Hampshire
21
STECH M D QUANDT amp W FREY (2003) Molecular circumscription of the hornworts(Antho-cerotophyta) based on the chloroplast DNA trnL-trnF region - J Plant Res 116 389-398
STOTLER RE amp B CRANDALL-STOTLER (2005) A revised classification of theAnthocerotophyta and a checklist of the hornworts of North America north of Mexico - Bryologist108 16-26
SWOFFORD DL (2002) PAUP Phylogenetic analysis using parsimony (and other methods)version 40b10 - Sunderland MA
TABERLET P L GIELLY G PAUTOU amp J BOUVET (1991) Universal primers for amplificationof three non-coding regions of chloroplast DNA - Plant Mol Biol 17 1105-1109
TSUBOTA H Y AGENO B ESTEacuteBANEZ T YAMAGUCHI amp H DEGUCHI (2003)Molecular phylogeny of the Grimmiales (Musci) based on chloroplast rbcL sequences - Hikobia 1455-70
TSUBOTA H E DE LUNA D GONZAacuteLEZ MS IGNATOV amp H DEGUCHI (2004) Molecularphylogenetics and ordinal relationships based on analyses of a large-scale data set of 600 rbcLsequences of mosses - Hikobia 14 149-170
VITT DH (1984) Classification of the Bryopsida - In SCHUSTER RM (ed) New Manual ofBryology 2 696-759 Hattori Botanical Laboratory Nichinan Japan
VITT DH B GOFFINET amp T HEDDERSON (1998) 8 The ordinal classification of the mossesquestions and answers for the 1990s - In BATES JW NW ASHTON amp JG DUCKETT (eds)Bryology for the twenty-first century British Bryol Soc pp 113-123
Received 3 September 2007 accepted in revised form 30 October 2007
20
OCHYRA R J ŻARNOWIEC amp H BEDNAREK-OCHYRA (2003) Census catalogue ofPolish mosses - Biodiv Poland 3 1-372
PEDERSEN N amp AE NEWTON (2007) Phylogenetic and morphological studies within thePtychomniales with emphasis on the evolution of dwarf males - In NEWTON AE amp RSTANGNEY (eds) Pleurocarpous mosses systematics and evolution Systematics AssociationSpecial Volume Series 71 367-392
QUANDT D amp M STECH (2005) Molecular evolution and secondary structure of the chloroplasttrnL intron in bryophytes - Mol Phylogenet Evol 36 429-443
QUANDT D K MUumlLLER amp S HUTTUNEN (2003) Characterisation of the chloroplast DNApsbT-H region and the influence of dyad symmetrical elements on phylogenetic reconstructions -Plant Biol 5 400-410
QUANDT D K MUumlLLER M STECH W FREY KW HILU amp T BORSCH (2004) Molecularevolution of the chloroplast trnL-F-region in land plants - In GOFFINET B V HOLLOWELL ampR MAGILL (eds) Molecular systematics of bryophytes Monogr Syst Bot Missouri Bot Gard98 13-37
QUANDT D NE BELL amp M STECH (2007) Unravelling the knot the Pulchrinodaceae famnov (Bryales) - In KUumlRSCHNER H T PFEIFFER amp M STECH (eds) A Festschrift to Wolf-gang Frey - a scientists life between deserts and rain forests Nova Hedwigia Beih 131 21-39
QIU Y-L Y CHO JC COX amp JD PALMER (1998) The gain of three mitochondrial intronsidentifies liverworts as the earliest land plants - Nature 394 671-674
QIU Y-L L LI B WANG Z CHEN V KNOOP M GROTH-MALONEK O DOM-BROVSKA J LEE L KENT J REST GF ESTABROOK TA HENDRY DW TAYLORCM TESTA M AMBROS B CRANDALL-STOTLER J DUFF M STECH W FREYD QUANDT amp CC DAVIS (2006) The deepest divergences in land plants inferred fromphylogenomic evidence - Proc Natl Acad Sci USA 103 15511-15516
RENZAGLIA KS S SCHUETTE RJ DUFF R LIGRONE AJ SHAW BD MISHLER ampJG DUCKETT (2007) Bryophyte phylogeny Advancing the molecular and morphological frontiers- Bryologist 110 179-213
SAMIGULLIN TH SP YACENTYUK GV DEGTYARYEVA KM VALIEJO-ROMANVK BOBROVA I CAPESIUS WF MARTIN AV TROITSKY VR FILIN amp ASANTONOV (2002) Paraphyly of bryophytes and close relationships of hornworts and vascularplants inferred from analysis of chloroplast rDNA ITS (cpITS) sequences - Arctoa 11 31-43
SANG T DJ CRAWFORD amp TF STUESSY (1997) Chloroplast DNA phylogeny reticulateevolution and biogeography of Paeonia (Paeoniaceae) - Amer J Bot 84 1120-1136
SHAW AJ amp KS RENZAGLIA (2004) Phylogeny and diversification of bryophytes - AmerJ Bot 91 1557-1581
SHAW AJ CJ COX amp B GOFFINET (2005) Global patterns of moss diversity taxonomic andmolecular inferences - Taxon 54 337-352
STECH M (1999a) A reclassification of Dicranaceae (Bryopsida) based on non-coding cpDNAsequence data - J Hattori Bot Lab 86 137-159
STECH M (1999b) A molecular systematic contribution to the position of Amphidium Schimp(Rhabdoweisiaceae Bryopsida) - Nova Hedwigia 68 291-300
STECH M (2004) Supraspecific circumscription and classification of Campylopus Brid(Dicranaceae Bryopsida) based on molecular data - Syst Bot 29 817-824
STECH M amp D QUANDT (2006) Molecular evolution of the chloroplast atpB-rbcL spacer inbryophytes - In SHARMA AK amp A SHARMA (eds) Plant Genome Biodiversity and EvolutionVol 2 Part B pp 409-431 Science Publishers Enfield New Hampshire
21
STECH M D QUANDT amp W FREY (2003) Molecular circumscription of the hornworts(Antho-cerotophyta) based on the chloroplast DNA trnL-trnF region - J Plant Res 116 389-398
STOTLER RE amp B CRANDALL-STOTLER (2005) A revised classification of theAnthocerotophyta and a checklist of the hornworts of North America north of Mexico - Bryologist108 16-26
SWOFFORD DL (2002) PAUP Phylogenetic analysis using parsimony (and other methods)version 40b10 - Sunderland MA
TABERLET P L GIELLY G PAUTOU amp J BOUVET (1991) Universal primers for amplificationof three non-coding regions of chloroplast DNA - Plant Mol Biol 17 1105-1109
TSUBOTA H Y AGENO B ESTEacuteBANEZ T YAMAGUCHI amp H DEGUCHI (2003)Molecular phylogeny of the Grimmiales (Musci) based on chloroplast rbcL sequences - Hikobia 1455-70
TSUBOTA H E DE LUNA D GONZAacuteLEZ MS IGNATOV amp H DEGUCHI (2004) Molecularphylogenetics and ordinal relationships based on analyses of a large-scale data set of 600 rbcLsequences of mosses - Hikobia 14 149-170
VITT DH (1984) Classification of the Bryopsida - In SCHUSTER RM (ed) New Manual ofBryology 2 696-759 Hattori Botanical Laboratory Nichinan Japan
VITT DH B GOFFINET amp T HEDDERSON (1998) 8 The ordinal classification of the mossesquestions and answers for the 1990s - In BATES JW NW ASHTON amp JG DUCKETT (eds)Bryology for the twenty-first century British Bryol Soc pp 113-123
Received 3 September 2007 accepted in revised form 30 October 2007
21
STECH M D QUANDT amp W FREY (2003) Molecular circumscription of the hornworts(Antho-cerotophyta) based on the chloroplast DNA trnL-trnF region - J Plant Res 116 389-398
STOTLER RE amp B CRANDALL-STOTLER (2005) A revised classification of theAnthocerotophyta and a checklist of the hornworts of North America north of Mexico - Bryologist108 16-26
SWOFFORD DL (2002) PAUP Phylogenetic analysis using parsimony (and other methods)version 40b10 - Sunderland MA
TABERLET P L GIELLY G PAUTOU amp J BOUVET (1991) Universal primers for amplificationof three non-coding regions of chloroplast DNA - Plant Mol Biol 17 1105-1109
TSUBOTA H Y AGENO B ESTEacuteBANEZ T YAMAGUCHI amp H DEGUCHI (2003)Molecular phylogeny of the Grimmiales (Musci) based on chloroplast rbcL sequences - Hikobia 1455-70
TSUBOTA H E DE LUNA D GONZAacuteLEZ MS IGNATOV amp H DEGUCHI (2004) Molecularphylogenetics and ordinal relationships based on analyses of a large-scale data set of 600 rbcLsequences of mosses - Hikobia 14 149-170
VITT DH (1984) Classification of the Bryopsida - In SCHUSTER RM (ed) New Manual ofBryology 2 696-759 Hattori Botanical Laboratory Nichinan Japan
VITT DH B GOFFINET amp T HEDDERSON (1998) 8 The ordinal classification of the mossesquestions and answers for the 1990s - In BATES JW NW ASHTON amp JG DUCKETT (eds)Bryology for the twenty-first century British Bryol Soc pp 113-123
Received 3 September 2007 accepted in revised form 30 October 2007