seb bruce insect-plant interactions

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

Insect host location

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

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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

Plant defence

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

Wound plug

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

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Cultivar ‘Carousel’

n=10, P=0.021; seed treated with 3mM JA

mean n

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leaf

untreated JA treated0

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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

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Genotype 2

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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

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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

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Bruce et al. (2003) Pesticide Outlook 14: 96 – 98

Aphidius ervi foraging on cis-Jasmone treated wheat

• significantly longer time spent on induced plants

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Treated Control

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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

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Cleaning Still Walking Total Time

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nt

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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

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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

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min

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-3

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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

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pen

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min

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-3

-2

-1

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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

Time has run out!

Conclusions

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)

Questions… ?