The structure of the stigma and the style of Oxalis spp. (Oxalidaceae) 1

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The structure of the stigma and the style of Oxalis spp.(Oxalidaceae)Author(s): Sonia Rosenfeldt and Beatriz G. GalatiSource: The Journal of the Torrey Botanical Society, 136(1):33-45. 2009.Published By: Torrey Botanical SocietyDOI: http://dx.doi.org/10.3159/08-RA-090R.1URL: http://www.bioone.org/doi/full/10.3159/08-RA-090R.1

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The structure of the stigma and the style of Oxalisspp. (Oxalidaceae)1

Sonia Rosenfeldt2

DBBE, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Buenos Aires, Argentina

Beatriz G. Galati3

Catedra de Botanica, Facultad de Agronomıa, Universidad de Buenos Aires, Buenos Aires, Argentina

ROSENFELDT, S. (DBBE, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, BuenosAires, Argentina) AND B. G. GALATI (Catedra de Botanica, Facultad de Agronomıa, Universidad de BuenosAires, Buenos Aires, Argentina). The structure of the stigma and the style of Oxalis spp. (Oxalidaceae). J.Torrey Bot. Soc. 136: 33–45. 2009.—The anatomy of the stigma and style of three species of Oxalis (O.articulata, O. hispidula, and O. paludosa), belonging to different sections (Articulatae, Ionoxalis, andCorniculatae) was studied using light, scanning, and transmission electron microscopy. The stigmamorphology of each of the different flower morphs of the three species (longistylous, medistylous, andbrevistylous flowers) was compared in this work. The stigma is dry and has multicellular and multiseriatepapillae. The morphology of the papillae does not differ between flower morphs. According to the Ca2+

concentration in pre-anthesis, anthesis, and post-anthesis, we hypothesize that the stigmas of the differentmorphs are equally receptive. Oxalis style is solid type. The cytoplasm of the transmitting tissue cells is densewith few vacuoles and abundant organelles. The transmitting tissue cells have large amounts of intercellularsubstance, mainly at the corners. This substance has moderate electron density in the species O. articulataand O. hispidula and shows some laxer areas in O. paludosa. The transmitting cell wall of the two first specieshas wall ingrowths like fingers with low electron density that protrude into the cytoplasm. Theultrastructural characteristics of the transmitting cells allow to characterize three of the sections of the genus.

Key words: Oxalis, stigma, style, ultrastructure.

The morphology of the stigmatic surface cells

and the amount of secretion are very diverse.

However, there are very few papers that

describe the stigma structure in angiosperms.

According to Heslop-Harrison (1975), the

angiosperm stigmas are divided into two

categories, wet stigmas with a copious fluid

secretion, and dry stigmas with limited surface

secretion. Later, Heslop-Harrison and Shi-

vanna (1977) and Heslop-Harrison (1981)

extended this basic classification, based on the

degree of variation of the stigmatic surface

morphology, the amount of secretion and the

nature of the surface cells of almost 1,000

species of about 900 genera of 250 families.

However, according to Raghavan (1997), there

is an imprecise correlation between the mor-

phology of the stigmatic surface and the

amount of secretion during the receptive period.

Moreover, some genera of Amaryllidaceae,

Commelinaceae, Liliaceae, Onagraceae, and

Rosaceae have both stigma types. The species

of Oxalidaceae studied so far present dry

stigmas, with multicellular and multiseriate

papillae (Heslop-Harrison and Shivanna, 1977).

The ultrastructure of the stigmatic papillae

of some species have been studied by different

investigators. These cells are characterized by

the preponderant presence of mitochondria,

plastids, endoplasmic reticulum, dictyosomes,

ribosomes, and vesicles (Konar and Linskens

1966, Vasilev 1970, Dickinson and Lewis 1973,

Dumas et al. 1978, Sedgley and Buttrose 1978,

Herrero and Dickinson 1979, Clarke et al.

1980, Herd and Beadle 1980, J. Heslop-

Harrison and Y. Heslop-Harrison 1980, Tilton

and Horner 1980, Wilms 1980, Y. Heslop-

Harrison et al. 1981, Sedgley 1981, Uwate and

Lin 1981, Dickinson et al. 1982, Owens and

Horsfield 1982, Ciampolini et al. 1983, Sedgley

and Blesing 1983, Cresti et al. 1986, Kanda-

samy et al. 1989, Bystedt 1990, Wrobel and

Bednarska 1994, Ciampolini et al. 1990).

However, the ultrastructure of the stigmatic

papillae of the genus Oxalis is still unknown.

The morphology and the anatomy of the

style is highly variable. Of the three basic types

described for angiosperms (Vasil and Johri

1964, Vasil 1974), Oxalis style can be classified

as solid type, with a transmitting tissue.

1 This work was supported by Grant PIP5262from CONICET, Argentina and UBACyT X823.

2 We thank Dr. Marina M. Gotelli and Dr. LaraStrittmatter for reviewing the English.

3 Author for correspondence. E-mail: [email protected]

Received for publication August 21, 2008, and inrevised form November 16, 2008.

Journal of the Torrey Botanical Society 136(1), 2009, pp. 33–45

33

Several authors studied the ultrastructural

characteristics of the cell walls of this tissue

in some species, but nothing is known about

the ultrastructure of the transmitting tissue in

the genus Oxalis (Johri 1984, Raghavan 1997,

Cresti et al. 1976, Ciampolini and Cresti 1998,

Ciampolini et al. 1995, Ciampolini et al. 1996,

Ciampolini et al. 2001, Hristova et al. 1996,

Hudak et al. 1993, Shivanna et al. 1989).

Some species of Oxalis show a strong self-

incompatibility associated with three different

flower morphs (tristylous flowers). Each

morph has two types of stamens. In one

morph, the pistil is short, and the stamens are

long and intermediate (B morph); in the

second morph, the pistil is intermediate, and

the stamens are short and long (M morph); in

the third morph, the pistil is long, and the

stamens are short and intermediate (L morph).

The presence of tristylous flowers is a charac-

teristic postulated as the ancestral condition of

heterostylous species of this genus (Marco and

Arroyo 1998). Evolution of distyly occurred

from tristyly in Oxalidaceae, through loss of

one of the morphs, commonly the M morph

(Ornduff 1972, Weller and Denton 1976).

The aim of this research is to study the

anatomy of the stigma and style of three

species of Oxalis belonging to three different

sections of this genus using light microscopy

(LM), scanning electron microscopy (SEM),

and transmission electron microscopy (TEM).

The stigmatic characteristics of the different

morphs present in each studied species are

analyzed. The ultrastructural data on Oxalis

are summarized in relation to the taxonomic

position of each species.

Material and methods. The three species

studied included: Oxalis articulata Savign., O.

hispidula Zucc., and O. paludosa A. St.-Hil.

These species present tristylous flowers.

Total proteins were localized with Coomas-

sie Brilliant Blue (Heslop-Harrison et al.

1973), pectinaceous material with Ruthenium

Red (Heslop-Harrison 1979), total insoluble

polysaccharides with periodic acid-Schiff

(PAS) reagent (McGuckin and McKenzie

1958), and lipoidal material with Sudan Black

B (Pearse 1961).

For scanning electron microscopy (SEM)

studies, the material was transferred to ethanol

100%, and subsequently critically point-dried

with liquid CO2. It was sputter coated with

gold-palladium for 3 minutes. Scanning mi-

crographs were taken with a Philips XL 30

microscope. Chemical elements were detected

with a SEM/EDX Philips XL30 (Eindhover,

The Netherlands).

For transmission electron microscopy

(TEM) studies, the stigmas and styles were

pre-fixed in 2.5% glutaraldehyde in phosphate

buffer (pH 7.2) for two hours and then post-

fixed in OsO4 at 2uC in the same buffer for two

hours. Following dehydration in ethanol

series, the material was embedded in Spurr’s

resin. Thin sections (75–90 nm thick) were

made on a Sorvall ultramicrotome and then

stained with uranyl acetate and lead citrate

(O’Brien and McCully 1981). The sections

were observed and photographed with a

JEOL-JEM 1200 EX II TEM at 85.0 Kv.

For light microscopy (LM) studies, the

material was fixed in FAA (formalin, alcohol,

acetic-acid) and then embedded in paraffin.

Sections were cut on a rotary microtome at

10–11 mm. The slides were stained in a

safranin-fast green combination (D’Ambro-

gio, 1986). The material was viewed with a

Wild M20 microscope and photographed with

a Nikon Labophot AFX-II microscope.

Results. The genus Oxalis has five stylar

branches that end in five capitate stigmas.

Observations of fresh material at different

stages of development (pre-anthesis, anthesis,

and post-anthesis) revealed the lack of a

copious secretion on the stigma papillae.

Although papillae morphology does not

differ between flower morphs, the papillae are

pluricellular, multiseriate and can bifurcate at

the tip (Figs. 1–3). Their cells have thick

primary walls, and they are coated by a thin

cuticle (Fig. 4) and pellicle layer as revealed by

staining with Sudan Black B and Coomassie

Brilliant Blue. The wall is composed of two

different layers. The innermost is thin and has

moderate electron density and the outermost is

thick with inclusions of different density

(Figs. 4, 5). These cells are very vacuolated

and have chloroplasts with abundant starch

granules, mitochondria, endoplasmic reticulum

of rough type (RER), and scarce dictyosomes

(Fig. 4). The large vacuoles are rich in tannin.

During anthesis, pollen tubes grow through

the papillae cell walls. Chloroplasts at this

stage are not observed. The RER and the

dictyosomes are meagre to absent (Fig. 5).

Stigmas in different stages of development

(pre-anthesis, anthesis, and post-anthesis)

34 JOURNAL OF THE TORREY BOTANICAL SOCIETY [VOL. 136

differ in Ca2+ ions (Figs. 6, 7). This ion is

present in low concentration in the pre- and

post-anthesis and in high concentration

during anthesis (Figs. 6, 7). This variation

of the Ca2+ level is the same in the different

morphs.

The style possesses a uniseriate epidermis, a

cortical parenchyma with two periphloematic

vascular bands and a transmitting tissue

(Fig. 8).

Epidermal cells have thin walls and are

vacuolated (Fig. 8). There are two types of

FIGS. 1–5. 1. Oxalis hispidula. Detail of stigma photographed with scanning electron microscope (SEM).2. O. articulata. Longitudinal section (LS) of stigma and style with light microscope (LM). 3. O. paludosa.Detail of stigmatic papillae with LM. 4 and 5. O. articulata. Transmitting electron microscope (TEM). 4.Detail of stigmatic papilla cell. 5. Detail of pollen grain germinating. Cl 5 chloroplast; pg 5 pollen grain; Tt5 transmitting tissue. Scale bars: 1 5 40 mm; 2, 3 5 3 mm; 4 5 4 mm; 5 5 2 mm.

2009] ROSENFELDT AND GALATI: STIGMA AND STYLE OF OXALIS 35

FIG. 6. Oxalis hispidula. Ca2+ level in the brevi-style morph. A. pre-anthesis. B. anthesis. C. post-anthesis.


FIG. 7. Oxalis hispidula. Ca2+ level in the longi-style morph. A. pre-anthesis. B. anthesis. C. post-anthesis.


trichomes: a) simple or unbranched type,

unicellular, with thick and verrucose walls

(Figs. 9–11) and b) glandular type (1–4 cells)

(Figs. 12, 13). The species Oxalis hispidula and

O. paludosa possess glandular type trichomes

positioned in the end portion of the style, near

the stigma (Fig. 9).

In Oxalis paludosa, these hairs are formed

by two or four cells and in O. hispidula by one

or two. In the O. articulata, the glandular

trichomes are very scarce and they are

irregularly distributed on the lower portion

of the style, between the simple hairs.

The transmitting tissue cells are isodiametric

in transverse section and elongated with sharp

ends in longitudinal section (Figs. 14, 15).

These cells show a large nucleus with one or

numerous nucleolus (Figs. 16–20). The cyto-

plasm is dense with few vacuoles and abun-

dant organelles. Many mitochondria with a

dense matrix and well developed cristae,

abundant RER, plastids with starch grains

and dictyosomes with numerous vesicles can

be observed (Figs. 16–24).

The species Oxalis articulata and O. hispi-

dula have transmitting tissue cells with a large

amount of intercellular substance, mainly at

the corners (Figs. 16–20). This intercellular

substance stains positively for pectins and

polysaccharides but not at all for proteins.

At the ultrastructural level the intercellular

substance has a moderate electron density.

The primary wall is thin and wall ingrowths,

like fingers that protrude into the cytoplasm of

the cell can be observed (Figs. 16–20). These

ingrowths are observed with less electron

density that the external primary wall

(Fig. 19).

Oxalis paludosa has transmitting tissue cells

with a very thick and electron dense middle

FIGS. 8–13. 8. Oxalis articulata. Transversal section (TS) of style in anthesis with LM. 9–10. O. hispidulaobserved with SEM. 9. General aspect of stigma and style. 10. Detail of simple stylar trichomes. 11–13. O.paludosa observed with LM. 11. Simple stylar hair with verrucose wall. 12–13. Glandular hairs. gh 5glandular hairs; sh 5 simple hairs; Tt 5 transmitting tissue; vb 5 vascular bands. Scale bars: 8 5 6 mm; 9 5200 mm; 10 5 40 mm; 11, 12, 13 5 3 mm.


layer with some areas that show low electron

density (Figs. 21–22).

Many plasmodesmata between transmitting

tissue cells and cortical parenchyma cells can

be observed in Oxalis articulata and O.

hispidula (Figs. 16, 19, 20) whereas in O.

paludosa, these connections are very scarce

(Figs. 21–22).

After pollination, pollen tubes start to grow

through the intercellular substance of the

transmitting tissue. As a consequence, the

transmitting tissue cells are observed separated

FIGS. 14–20. Transmitting tissue in anthesis. 14–18. Oxalis articulata. 14–15. Detail of transmittingtissue cells observed with LM. 14. TS. 15. LS. 16–18. Detail of transmitting tissue cells in TS observed withTEM. 19–20. O. hispidula. Detail of transmitting tissue cells observed with TEM. 19. TS. 20. LS. Arrows 5plasmodesmata; Cl 5 chloroplasts; d 5 dictyosome; m 5 mitochondrion; Ml 5 middle layer; n 5 nucleus; p5 plastid; Pw 5 primary wall; RER 5 Rough endoplasmic reticulum; Wi 5 wall ingrowths. Scale bars: 14,15 5 0.75 mm; 16 5 2 mm; 17, 18 5 1 mm; 19, 20 5 2 mm.


(Fig. 25–28), with the primary walls thinner

than the previous stage and with or without

very few wall ingrowths (Figs. 25–28). At this

moment, most of these cells are vacuolated,

with few plastids and some mitochondria

(Figs. 25–28). In Oxalis paludosa, while pollen

tubes grow, the intercellular substance is very

lax and swollen and parts of the cytoplasm

delimited by RER lamella can be observed in

the transmitting tissue cells. During post-

anthesis, many of the transmitting tissue cells

are compressed or totally degraded (Fig. 27).

The three species studied in this research

belong to three sections of Oxalis: Articulatae,

Ionoxalis, and Corniculatae. The ultrastruc-

tural characteristics observed in the transmit-

ting cells allow to characterize these three

different sections of the genus. These charac-

teristics are summarized in the Table 1.

Discussion. The species of Oxalis studied in

this paper have a stigma without signs of

copious secretion in all floral developmental

stages. Therefore, we can define this stigma as

dry. The same type of stigma has been

described for the family Oxalidaceae (He-

slop-Harrison and Shivanna 1977, Heslop-

Harrison 1981).

FIGS. 21–24. Oxalis paludosa. Transmitting tissue in anthesis observed with TEM. 21–22. TS. 23–24. LS.D 5 dictyosome; Ml 5 middle layer; m 5 mitochondrion; p 5 plastid. Scale bars: 21 5 2 mm; 22 5 1 mm; 235 4 mm; 24 5 0.5 mm.


The nature of the papillae walls shows great

diversity between species. According to Dick-

inson and Lewis (1975), the papillae walls have

a layered structure. In grasses, vesicles with

proteins can be present in the wall (J. Heslop-

Harrison and Y. Heslop-Harrison 1980). In

Oxalis species investigated here, the papillae

walls have two layers differentiated by the

electronic density. The same characteristic was

described for Secale cereale (J. Heslop-Harri-

son and Y. Heslop-Harrison 1980), Zea mays

(Y. Heslop-Harrison et al. 1984) and Hyper-

icum calycinum (Shivanna et al. 1989). In

Oxalis, the inner layer, in contact with the

plasmalemma, is thin and has a moderate

electron density. The outer layer, contiguous

to the cuticle is thicker. Different inclusions

can be observed inside this layer, but its nature

was not determined.

The stigmatic papillae of Oxalis contain

RER before the anthesis, but it is not very

abundant. This organelle has been related with

the origin of the secretory vesicles that carry

lipophilic glandular fluid (Dumas 1973). The

scarce RER is typical of the stigma dry type

present in this genus.

In general, the papillae of Oxalis have fewer

organelles than those typical of glandular cells.

These observations are in agreement with that

of Shivanna et al. (1989) for Hypericum

calycinum. In both cases, the stigma is of the

dry type.

The presence of tannins in the vacuoles of

stigmatic cells was cited in the papillae of

Lycopersicum esculentum (Dumas et al. 1978),

Olea europaeae (Ciampolini et al. 1983),

Tibouchina semidecandra (Ciampolini et al.

1995), and Hypericum calycinum (Shivanna et

al. 1989). All the species of Oxalis observed in

this work have abundant tannins in their

stigmatic cells, but the significance of these is

not known (Raghavan 1997).

FIGS. 25–28. Oxalis articulata. Transmitting tissue (Tt) in post-anthesis observed with TEM. 25–27. TS.25. General aspect. 26–27. Detail of Tt cells. 28. Detail of Tt cells in LS. Ml 5 middle layer; m 5mitochondrion; n 5 nucleus. Scale bars: 25 5 1 mm; 26 5 2 mm; 27, 28 5 4 mm.


The stigmatic papillae of Oxalis contain

obvious chloroplasts. These organelles were

described by Jobson et al. (1983) in the

stigmatic cells of Acacia retinodes and some

species of Fabaceae. However, these chloro-

plasts were defined by these authors as

photosynthetically inactive.

The subcellular localization of Ca 2+ions in

Oxalis stigmas differs at each stage of the

stigma development (pre-anthesis, anthesis,

and post-anthesis), but it is the same in the

different morphs of each species at the same

stage. The higher concentration of this ion was

found in the anthesis stage. According to

Bednarska et al.(2005), the pollination induces

an accumulation of these ions in the apoplast

of the stigma epidermal cells. In a study

involving pollen grains of 86 species, including

79 genera representing 39 families, Brewbaker

and Kwack (1963) demonstrated an almost

universal requirement for Ca 2+ in the medium

to ensure pollen germination and pollen tube

growth. According to these accounts we might

suggest that the stigmas of the different

morphs are equally receptive to pollen germi-

nation.

According to the observations made until

anthesis for different species of Angiosperms,

the transmitting tissue cells are very active

metabolically. They have abundant free ribo-

somes, mitochondria, RER, dictyosomes, and

amyloplasts (Raghavan 1997). The cellular

ultrastructure of this tissue of Oxalis articu-

lata, O. hispidula, and O. paludosa shows all

these characteristics.

Many plasmodesmata are observed in the

transmitting cell walls of Oxalis. These con-

nections have been described for the cells of

this tissue in Petunia hibrida (Sassen 1974),

Lycopersicon peruvianum (Cresti et al. 1976),

Nicotiana tabacum (Bell and Hicks 1976),

Tibouchina semidecandra (Ciampolini et al.

1995), Corylus avellana (Ciampolini and Cresti

1998), and Oryza sativa (Ciampolini et al.

2001).

The cell walls of the transmitting tissue of

Oxalis paludosa and O. hispidula have in-

growths surrounded by the plasma membrane.

Similar observations were made in Petunia

hybrida by Herrero and Dickinson (1979).

According to these authors, this characteristic

associated to the plasmodesmata assures a

great efficiency in the cellular exchange. These

wall ingrowths resemble the ‘‘transfer cells’’

described by Gunning and Pate (1969).

Tab

le1.

Sty

lech

ara

cter

isti

cso

fth

eth

ree

spec

ies

of

Ox

ali

sex

am

ined

inth

isst

ud

y.

Sp

ecie

s

Tri

cho

mes

Tra

nsm

itti

ng

tiss

ue

Sim

ple

typ

eG

lan

du

lar

typ

eM

idd

lela

yer

Pri

mary

wa

ll

O.

art

icula

ta(S

ecti

on

Art

icu

lata

e)U

nic

ellu

lar,

wit

hver

ruco

sew

all

1-2

-cel

lula

r.D

istr

ibu

ted

on

the

low

erp

ort

ion

of

the

style

,b

etw

een

the

sim

ple

hair

s

Larg

eam

ou

nt

of

inte

rcel

lula

rsu

bst

an

ce,

main

lyat

the

corn

ers

Ho

mo

gen

eou

sin

elec

tro

nd

ensi

ty,

wit

hw

all

ingro

wth

sli

ke

fin

ger

s.A

bu

nd

an

tp

lam

od

esm

ata

are

pre

sen

tO

.palu

dosa

(Sec

tio

nC

orn

icu

lata

e)U

nic

ellu

lar,

wit

hver

ruco

sew

all

4-c

ellu

lar.

Dis

po

sed

inth

een

dp

ort

ion

of

the

style

,n

ear

the

stig

ma

Ver

yth

ick

an

del

ectr

on

den

sein

terc

ellu

lar

sub

stan

cew

ith

som

eare

as

laxer

,li

ke

vacu

ole

s

Ho

mo

gen

eou

sin

elec

tro

nd

ensi

ty,

wit

ho

ut

wall

ingro

wth

sli

ke

fin

ger

san

dsc

arc

ep

lasm

od

esm

ata

O.

his

pid

ula

(Sec

tio

nIo

no

xali

s)U

nic

ellu

lar,

wit

hver

ruco

sew

all

1-2

cell

ula

r.D

isp

ose

din

the

end

po

rtio

no

fth

est

yle

,n

ear

the

stig

ma

Larg

eam

ou

nt

of

inte

rcel

lula

rsu

bst

an

ce,

main

lyat

the

corn

ers

Het

ero

gen

eou

sin

elec

tro

nd

ensi

ty,

wit

hw

all

ingro

wth

sli

ke

fin

ger

sth

at

have

less

elec

tro

nd

ensi

ty.

Ab

un

dan

tp

lam

od

esm

ata

are

pre

sen

t


In the species of Oxalis studied in this

research, the wall ingrowths have different

electron density that the primary wall. Studies

made in the xylem transfer cells of wheat and

transfer cells of corn endosperm tissue using

field emission scanning electron microscopy

and inmunofluorescence confocal microscopy

show that the parallel organisation of cellulose

microfibrils in flange wall ingrowths is similar

to those in secondary walls (Talbot et al.

2007). This may be the same in transmitting

cells of the style of Oxalis.

According to Wardini et al. (2007), the

progression of wall ingrowths deposition is

positively correlated with intracellular sucrose

concentrations. Intracellular sucrose is likely to

increase in the transmitting tissue cells before

anthesis.

Abundant pectic substances were identified

in the transmitting tissue of Oxalis. The

ultrastructural characteristics of the cells of

this tissue, with many ribosomes, dictyosomes,

and RER, is probably related to the secretion

of this extracellular substance (Jensen and

Fisher 1969, Cresti et al. 1976).

The intercellular substance has greater

electron density than the cell walls. According

to Raghavan (1997), this is due to the

amorphous nature of intercellular substance,

that generally presents a mucilaginous base

with other substances as carbohydrates, pro-

teins, phenolic compounds, and tannins. This

mucilaginous matrix facilitates and guides

pollen tube growth (Clarke et al. 1977).

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Documents

The structure of the stigma and the style of Oxalis spp. (Oxalidaceae) 1