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Interplay between insects and plants: dynamic and complex interactions that have evolved over millions of years but act in milliseconds
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Interplay between insects and plants: dynamic and complex interactions that have evolved over millions of years but act in milliseconds
Toby Bruce
Overview – effect of time• Insect-plant interactions are dynamic and change over
time
▫Long timescale over which interactions have evolved contrasts with short time when interaction happens
▫The legacy of co-evolutionary history
Image via Linden Gledhill
Labandeira (2013) Curr. Opin. Plant Biol. 16: 414
DNA code has evolved over millions of years - subject to mutations that are deleterious or advantageous according to context- gene expression is modulated by epigenetic ‘stress imprints’
The different timescales associated with insect-plant interactions
Overview – effect of time• Order of exposure can change interaction
▫ INSECT: learning behaviour▫PLANT: induced defence
• Combination of plant cues at a point in time is important
How do insects recognise host plants?
1. Species-specific odour recognition:
taxonomically characteristic volatilesORN
Plant Volatile
CNS
ORN
Plant Volatile
CNS
Plant VolatilePlant Volatile
Plant Volatile
Plant VolatileORN
ORN
ORN
ORN
Bruce et al. (2005) TRENDS in Plant Science 10: 269
2. Ratio-specific odour recognition: specific combinations of volatiles, distributed generally among plant species
The challenge of host recognition
Helicoverpa armigera
• highly polyphagous• specialises on flowers
H OH
CH3
CH2
H
O
benzaldehyde phenylacetaldehyde
limonene linalool
Bruce & Cork (2001) J. Chem. Ecol. 27: 1119
Helicoverpa armigera
• host plants limited to wheat and a few related grasses
Sitodiplosis mosellana
Birkett et al. (2004) J. Chem. Ecol. 30: 1319
3-carene(Z)-3-hexenyl acetate
acetophenone
Ubiquitous compounds!
Sitodiplosis mosellana
Bruce et al. (2005) TRENDS in Plant Science 10: 269
Signals must be present at the same time!
Aphis fabae
• specialist on beans
• feeds in colonies
(E)-2-hexenal 1-hexanol (Z)-3-hexen-1-ol benzaldehyde 6-methyl-5-hepten-2-one octanal (Z)-3-hexen-1-yl acetate (R)-linalool methyl salicylate decanal undecanal (E)-caryophyllene (E)-β-farnesene (S)-(-)-germacrene (E,E)-4,8,12-trimethyl-1,3,7,11-tridecatetraene
Webster et al. (2008) J. Chem. Ecol. 34: 1153
Bioassay
• insect released in the centre
• time spent in treated arm compared with time spent in control arms
Response to volatiles collected from plants with and without eggs?
Webster et al. (2010) Animal Behaviour 79: 451
Aphis fabae – host odours must be present together at the same time
Tim
e sp
ent
(Min
)
0
2
- 3
9-comp synthet
ic blend
** * * *
*
* * *
*0
.1n
g(E
)-2
-h
exa
nal
1n
g
ben
zald
eh
yde 0
.01
ng
oct
an
al
0.0
1n
g (
Z)-
3-h
exe
nyl
ace
tate
0.1
ng
(R
)-li
an
lool
10
ng
meth
yl
sali
cyla
te
10
0n
g
deca
nal
0.0
1n
g (
S)-
germ
acr
en
e
D 0.1
ng
TM
TT
Attraction to blends
Bruce & Pickett (2011) Phytochem. 72: 1605
Right mix is needed…
Bruce & Pickett (2011) Phytochem. 72: 1605
Insect responses change over time
(image courtesy of Patrizia d'Ettorre and Mauro Patricelli)
Associative learning is used to help find rewarding forage and to maximise fitness
Manduca sexta hawkmoths• innate preference for night blooming flowers like jimsonweed• Switch to Agave palmeri if there is a shortage
Riffell et al. (2013) Science 339: 200-204
Manduca sexta hawkmoths• innate preference for night blooming flowers like jimsonweed• Switch to Agave palmeri if there is a shortage
Pollinatators coevolve mutually beneficial interactions
Insect herbivory: selection pressure pulling in opposite directions for the insect and the plant
Tomato leafminer, Tuta absoluta
Insect effectors supress or induce plant defence (depending if insect or plant is ‘ahead’)
Hogenhout & Bos (2011) Curr. Opin. Plant Biol. 14: 422
Defences:“constitutive”,“induced” and primed
Primed defence
plant is ready to mount quicker or stronger defences when subsequently attacked
Induced defence
these traits are always expressed
these traits need a signal to elicit them
- attacking organism
- volatile surrogate (plant activator)
Constitutive defence
Bruce & Pickett (2007) Current Opinion in Plant Biology 10: 387-392
Orange wheat blossom midge
OWBM damage
Oakley et al 2005 HGCA Project Report No. 363
Now approx. 60% of UK wheat is resistant
Timing matters
•See EBF video
• Inducible traits more effective & can be fine tuned
HIPV emission
(E)-caryophyllene
(E)-4,8-dimethyl-1,3,7-nonatriene
Maize landrace lines
Tamiru et al. (2011) Ecology Letters 14: 1075
Parasitoid response - landraces
Attracted to plants with eggs
Volatile profiles - landraces
(a) (E)-ocimene, (b) (R)-linalool, (c) (E)-4,8-dimethyl-1,3,7, nonatriene (DMNT), (d) methyl salicylate, (e) decanal, (f) methyleugenol, (g) (E)-(1R,9S)-caryophyllene, (h) (E)-β-farnesene, (i) (E,E)-4,8,12-trimethyl-1,3,7,11-tridecatetraene (TMTT).
Tamiru et al. (2011) Ecology Letters 14: 1075
Volatile profiles – standard commercial varieties
(a) (E)-ocimene, (b) (R)-linalool, (c) (E)-4,8-dimethyl-1,3,7, nonatriene (DMNT), (d) methyl salicylate, (e) decanal, (f) methyleugenol, (g) (E)-(1R,9S)-caryophyllene, (h) (E)-β-farnesene, (i) (E,E)-4,8,12-trimethyl-1,3,7,11-tridecatetraene (TMTT).
Tamiru et al. (2011) Ecology Letters 14: 1075
JA seed treatment induced defence: Mean number of eggs laid by 10 Tetranychus urticae females on 4 week old tomato leaves over 4 days
untreated JA0
20
40
60
80
100
120
140
Cultivar ‘Carousel’
n=10, P=0.021; seed treated with 3mM JA
mean n
o./
leaf
untreated JA treated0
10
20
30
40
50
60
70
80
90
100
Cultivar ‘Moneymaker’
ANOVA no significant difference; n=15; seed soaked in 3mM JA
Smart et al. (2013) J. Chem. Ecol. 39: 1297
*
Genotypic variation in inducible defence
T T T0
0.5
1
Genotype 1
Genotype 2
Genotype 3
Exp
ress
ion
lev
el o
f st
ress
res
po
nse
gen
e
Bruce 2014 Frontiers in Plant Science (online early)
cis-Jasmone
• Stress related volatile plant activator that induces defence mechanisms
• Identified from winter host volatiles of lettuce aphid, Nasonovia ribis-nigri
• Emitted by insect infested plants:– cotton plants damaged by Spodoptera– potato plants infested with potato aphid
• Biological effects observed >24h after spraying plants with cis-jasmone
• Non-toxic• No residue left as it is volatile
Aphids repelled by CJ treated wheat volatiles
Response: No. of entries into treated arm
0.00.51.01.52.02.53.03.54.04.55.0
treated control mean
Response: time spent
0.00.51.01.52.02.53.03.54.0
treated control mean
tim
e (
min
)
Settlement bioassay in simulator
• aphids (Sitobion avenae) released at downwind end
• numbers settled on wheat seedlings recorded
• Fewer aphids colonised cis-jasmone induced plants
Bruce et al. (2003) Pest Management Science 59: 1031 – 1036
0
10
20
30
40
50
60
70
-1 4 9 14 19 24
% s
ettle
men
t
time after release (h)
control
cis-jasmone
Bruce et al. (2003) Pest Management Science 59: 1031 – 1036
Field plot trial: spray application
• Aphids assessed every week May-July
• 100 tillers per plot
Bruce et al. (2003) Pest Management Science 59: 1031 – 1036
Response to cis-jasmone: Solstice > Consort > Hereward > Welford
3. Hereward
0
50
100
150
200
250
01-Jun 7 12 20 29 06-Jul
tota
l ap
hid
s/4
00
til
lers
control
CJ
4. Welford
0
20
40
60
80
100
120
140
160
180
200
01-Jun 7 12 20 29 06-Jul
tota
l ap
hid
s/4
00
til
lers
control
CJ
1. Solstice
0
50
100
150
200
250
300
350
01-Jun 7 12 20 29 06-Jul
tota
l ap
hid
s/4
00
til
lers
control
CJ
2. Consort
0
20
40
60
80
100
120
140
160
01-Jun 7 12 20 29 06-Jul
tota
l ap
hid
s/4
00
til
lers
control
CJ
Bruce et al. (2003) Pesticide Outlook 14: 96 – 98
Aphidius ervi foraging on cis-Jasmone treated wheat
• significantly longer time spent on induced plants
0
5
10
15
20
25
Treated Control
min
Arabidopsis - Myzus persicae – Aphidius ervi
Bruce et al. 2008 PNAS 105: 4553-4558
Myzus persicae: repelled by CJ treated volatiles
Olfactometer bioassay:
• Attracted to wild type Arabidopsis (Col 0) volatiles when untreated
• Repelled by CJ treated
Bruce et al. 2008 PNAS 105: 4553-4558
Aphidius ervi: forages for longer time periods on CJ treated Arabidopsis
0
2
4
6
8
10
12
14
Cleaning Still Walking Total Time
Tim
e s
pe
nt
(m
in)
control
CJ
P = 0.025
P = 0.021
Bruce et al. 2008 PNAS 105: 4553-4558
MI PS Nr. Putative function Log2(R/G) At5g22140 Putative protein -2 At2g44130 F-box protein -1.83 At2g04870 Hypothetical protein -1.61 At1g21310 Hypothetical protein -1.44 At3g28740 Cytochrome P450 -1.42 At1g55920 Serine acetyltransf erase -1.4 At5g44030 Cellulose synthase catalytic subunit-like -1.4 At2g28330 Hypothetical protein -1.34 At3g05110 Hypothetical protein -1.32 At1g78380 Glutathione S-transferase, similar to -1.32 At2g29490 Putative Glutathione S-transf erase -1.29 At1g55920 Serine acetyltransf erase -1.28 At5g24610 Putative protein -1.28 At5g14730 Putative protein -1.27 At4g39290 Putative protein -1.27 At5g21940 Putative protein -1.26 At1g78380 Similar to glutathione S-transf erase -1.25 At1g21310 Hypothetical protein -1.24 At1g69980 Hypothetical protein -1.23 At3g16920 Basic chitinase, putative -1.22 At4g12470 pEARL 1-like protein -1.2 At3g13750 Galactosidase putative -1.19 At1g76690 12-oxophytodienoate reductase (OPR1/ 2) -1.19 At3g25910 Unknown protein -1.18 At3g02300 Unknown protein/ chromatin modification -1.17 At1g07920 Elongation f actor 1-alpha -1.17 At4g12000 Putative protein -1.15 At1g09500 Putative cinnamyl alcohol dehydrogenase -1.12 At3g09270 Glutathione transf erase -1.11 At4g30920 Leucyl aminopeptidase like -1.11 At1g32940 Hypothetical protein -1.09 At1g21310 Hypothetical protein -1.08 At5g15630 Phytochelatine synthase, putative -1.08 At4g02520 Atpm24.1 glutathione transf erase -1.07 At1g17860 Hypothetical protein -1.06 At1g48090 Unknown protein -1.05 At4g21130 Hypothetical protein -1.04 At3g08790 Hypothetical protein -1.04 At2g18190 Putative AAA-type ATPase -1.04 At1g35580 I nvertase, putative -1.02 At3g13310 DNAJ protein, putative -1.01 At4g26050 Putative leucine rich repeat protein -1
Arabidopsis thaliana exposure to cis-jasmonecis-Jasmone upregulated sequences:
• OPR1/2
• Cell wall biosynthetic genes
• Cytochrome P450 (CYP81D11)
• F-box containing protein
Sequences unaffected by cis-jasmone:
• Defence genes (PR proteins, etc)
• Stress genes (HSPs, etc)
• Jasmonate-regulated genes (OPR3, LOX)
Myzus persicae responses to CYP81D11 overexpressing plants
Bruce et al. 2008 PNAS 105: 4553-4558
Aphidius ervi responses to CYP81D11 overexpressing plants
Bruce et al. 2008 PNAS 105: 4553-4558
Interactions with other organisms
Disease can alter interaction
• Volatiles from Fusarium graminearum infested wheat are repellent to grain aphid, Sitobion avenae
• EAG active compounds: ▫ 2-pentadecanone, ▫ 2-heptanone, ▫ phenyl actetic acid, ▫ α-gurjunene, ▫ 2-tridecanone, ▫ α -cedrene
• Key behaviourally active compounds: ▫ 2-pentadecanone ▫ 2-heptanone
-2.5
-2
-1.5
-1
-0.5
0
0.5
1
1.5
Mycorrhizal fungal networks communicate pest defence between plants via signalling through mycelia
Babikova et al. (2013) Ecology Letters 16: 835-43
Mycorrhizae can alter interaction
Donor plant with aphids
No barrier. Root and hyphal contact
Static 40 µm mesh. Hyphal contact, no root contact
0.5 µm mesh. No hyphal contact, no root contact
Rotated 40 µmmesh. No hyphal contact, no root contact
Roots
AM fungi
Babikova et al. (2013) Ecology Letters 16: 835-43
Experimental mesocosm
No hyphal connection
Receiver plants (no aphids)
0.5 µm 40 µm rotated
40 µmstatic
no barrier
Donor (with aphids)
Tim
e s
pen
t [
min
]
-3
-2
-1
0
1
2
3
Pea aphid
Hyphal connectionAttractive
Repellent
a
a
bb b
Babikova et al. (2013) Ecology Letters 16: 835-43
Response of pea aphid and its parasitoid wasp (Aphidius ervi) to volatiles in olfactometer bioassays
No hyphal connection
Receiver plants (no aphids)
0.5 µm 40 µm rotated
40 µmstatic
no barrier
Donor (with aphids)
Tim
e s
pen
t [
min
]
-3
-2
-1
0
1
2
3
Aphidius ervi
Hyphal connectionAttractive
Repellent
z
z
y yy
Babikova et al. (2013) Ecology Letters 16: 835-43
Response of pea aphid and its parasitoid wasp (Aphidius ervi) to volatiles in olfactometer bioassays
Conclusions
• Insect-plant interactions are complex and dynamic
•Time and space matter
•Combination of plant cues at a point in time is important
•History of exposure changes interaction
Thank you• Ben Webster• Christine Woodcock• Janet Martin• John Caulfield• John Pickett• Lesley Smart• Lester Wadhams• Mike Birkett• Zeyaur Khan (ICIPE)• Charles Midega (ICIPE)• Amanuel Tamiru (ICIPE)• Jassy Drakulic (University of Nottingham)• Jurriaan Ton (University of Sheffield)• Zdenka Babikova (University of Abderdeen)
