Insect-Plant Interactions: a dynamic co-evolutionary struggle highly relevant to future food security

Toby BruceUniversity of Nottingham, 12 May 2014

Modern agriculture:High yielding varieties (?)

High yield – only if there is adequate crop protection against pests

Overview of talk:

•Vulnerability of agro-ecosystems to pest attackImplications for Food Security

• Insect-plant interactions

•Techniques for managing pests

•Future directions

Vulnerability of agro-ecosystems to pest attack

Lush monocultures of high yielding varieties grown with fertiliser and irrigation are often more susceptible to pests

Bruce (2011) J. Exp. Bot. 63: 537-541

fewer effective

pesticides

legislation

reduced discovery and

approval of new products

rapid evolution and

spread of resistant biotypes

short generation

time

high reproductive rate

easy dispersal

global trade

consumer demand to

replace pesticides

fewer effective

pesticides

reduced genetic diversity in crops

THRIVING PESTS AND HIGH CROP

LOSSES

climate change can make conditions better for pests

less intrinsic resistance to insects and

pathogens, and less competitiveness with

weeds

fertilised crops more nutritious to insects

and pathogens

broad spectrum pesticides kill

natural enemies of pests

Bruce (2011) J. Exp. Bot. 63: 537-541

Impact of Pests, Weeds & Diseases

1965 – staple cereals

1992 – staple cereals

42% lost

36% lost

SOURCE: Oerke & Dehne (2004) Crop Prot 23:275–285

Crop losses caused by pests have not decreased since the 1960s, even with use of pesticides

Resistance to agrochemicals worldwide

EC Directive 2009-128

A framework “Promoting the use of IPM and of alternative approaches”

Research on “Alternatives” is urgently needed

Promoting IPM and use of alternatives

2009/128/EC on the Sustainable Use of Pesticides

Reducing risks and impacts of

pesticide use on human health

and environment

Research on “Alternatives” is urgently needed

More complicated than just banning pesticides

Bees

“Impacts of pesticides on human health and the environment”

… BUT WAIT, some impacts are positive

Human health ► increased affordability of

healthy food (e.g. fruit & veg)

► less mycotoxin contamination

Environment► more food can be

produced on less land with less water and fertiliser

► more efficient production – less GHG

• EU yields decline

• Increased selection pressure for resistance to remaining pesticides

• Food price increase

• Food production companies move out of Europe

• More land used for agriculture

Unintended consequences

1961

1964

1967

1970

1973

1976

1979

1982

1985

1988

1991

1994

1997

2000

2003

2006

2009

2012

2015

2018

2021

2024

2027

2030

2033

2036

2039

2042

2045

2048

0

1000000

2000000

3000000

4000000

5000000

6000000

7000000

8000000

9000000

10000000

Popu

lati

on

(1000s)

; C

ere

al

Pro

du

cti

on

(x 5

00

ton

nes)

Will future demand be met?

Source: FAOSTAT

human population

cereal production

Bruce (2010) Food Security 2: 133-141

To keep pace with growing demand,

global food production needs to increase by an estimated 70% by

2050 [United Nations]

New directions for Agriculture in the 21st Century

Royal Society: “There is a pressing need for the ‘sustainable intensification’ of global agriculture in which yields are increased without adverse environmental impact and without the cultivation of more land”.

Royal Society (2009) Policy document 11/09

A second green revolution which is knowledge intensive rather than input intensive?

So we need to learn more about insect-plant interactions…

…these are complicated and dynamic

Insect-plant interactions

The different timescales associated with insect-plant interactions 

Bruce (2014) JXB in press

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’

INDUCED PLANT DEFENCE

Insect effectors supress or induce plant defence (depending if insect or plant is ‘ahead’)

(image courtesy of Saskia Hogenhout)

Plant defence changes over time

(image courtesy of Jurriaan Ton and Marieke van Hulten)

Defences: traditionally divided into “constitutive” and “induced”

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

primed

not primed

Bruce et al. (2007) Plant Science 173: 603-608

primed

not primed

Bruce et al. (2007) Plant Science 173: 603-608

primed

not primed

Does priming leave an epigenetic mark?

AcAc AcAc

AcAc

AcAcMeMeMeMeMeMeMeMeMeMe

MeMeMeMeMeMeMeMeMeMe

Bruce et al. (2007) Plant Science 173: 603-608

INSECT HOST LOCATION

Rapid decisions by insects about plant colonisation, made in flight

Bruce (2014) JXB in press

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

GC-linked electroantennography

• The insect antenna is used as a biological detector

• Delicate manipulation with microelectrodes to connect an antenna to an electrical circuit

• Volatiles (GC effluent) passed over electrophysiological preparation

• There is increased depolarisation when the insect responds

• Insect released in the centre

• Time spent in treated arm compared with time spent in control arms

• Insects released at downwind end• Upwind flight and source contacts recorded

Olfactometer

Wind-tunnel

Behavioural Bioassays

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

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

Webster et al. (2010) Animal Behaviour 79: 451

Aphis fabae

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

Bruce et al. (2005) TRENDS in Plant Science 10: 269

Spatio-temporal resolution of signals

The challenge of host recognition

Insect responses change over time

(image courtesy of Patrizia d'Ettorre and Mauro Patricelli)

Techniques for managing pests

ORANGE WHEAT BLOSSOM MIDGE

Orange wheat blossom midge• varies from year to

year

• was difficult to decide in time which fields needed treating

• difficult to control with insecticide

•Females lay eggs, but larvae die when they start to feed

•A wound plug is formed at the feeding site due to lignification

•Antibiotic action of phenolic acids by the grain

Resistant varieties

Resistant varieties

Oakley et al 2005 HGCA Project Report No. 363

Now approx. 60% of UK wheat is resistant

Resistant varieties

Yellow rust on wheat OWBM resistant cultivar (Robigus)

Need for multiple resistance

OCOC3H7

OCOC3H7

2,7-nonanediyl dibutyrate

Sex pheromone

Monitoring systems

Bruce et al. (2007) Pest Man. Sci. 63: 49

• Allow rational use of pesticides

• Need based applications save costs and importantly slow down the development of resistance

• sex pheromone traps:

- provide a solution to the detection problem

- enable more accurate and effective spray timing

Bruce et al. (2007) Pest Man. Sci. 63: 49

• Pheromone traps widely used by wheat growers in the UK

Decision support system for OWBM

Bruce & Smart (2009) Outlooks Pest Management 20: 89-92

CIS-JASMONE

• 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

cis-Jasmone O

• aphids (Sitobion avenae) released at downwind end

• numbers settled on wheat seedlings recorded

• Fewer aphids colonised cis-jasmone induced plants

0

10

20

30

40

50

60

70

-1 4 9 14 19 24

time after release (h)

% s

ettle

men

t

control

cis-jasmone

Settlement bioassay in simulator

Bruce et al. (2003) Pest Management Science 59: 1031 – 1036

Field plot trial: spray application

0

0.2

0.4

0.6

0.8

1

1.2

28-May 8-Jun 16-Jun 24-Jun 6-Jul

Me

an

No

. Ap

hid

s /

Till

er

*

*

control

cis-jasmone

P = 0.036

Bruce et al. (2003) Pest Management Science 59: 1031 – 1036

Wheat Field Trial

significantly longer time spent on induced plants

0

5

10

15

20

25

Treated Control

min

Aphidius ervi foraging on cis-Jasmone treated wheat

CYP81D11• Insect responses to CYP81D11 OE plants are similar to

the responses observed with CJ treated plants

• We still do not know the function of this gene

Bruce et al. (2008) PNAS 105: 4553-4558

EGG ALERT

Stemborers

(E)-caryophyllene

(E)-4,8-dimethyl-1,3,7-nonatriene

Collecting volatiles from plants with eggs

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?

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

New Project: markers for egg induced volatile emission trait

Diverse seeds

HIPV induced by eggs in improved line

Improved maize line CKIR12001 emits DMNT when stemborer eggs are laid on it.

INTERACTIONS WITH OTHER ORGANISMS

New aphid repellents identified

• 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

natu

ral

2-trid

ecan

one

(1µg

)

α-gur

june

ne (1

µg)

phen

yl ac

etic a

cid

(1µg

)

α-cedr

ene

(1µg

)

2-he

ptan

one

(1µg

)

2-pe

ntad

ecan

one

(1µg

)

6-co

mp

blen

d

2-co

mp

blen

d

-2.5

-2

-1.5

-1

-0.5

0

0.5

1

1.5

MYCORRHIZAL SIGNALlING…

- volatiles produced from vegetative parts and roots can change significantly following aphid attack

- repellent to subsequent herbivores

- signalling molecules attract natural enemies

Babikova et al. (2013) Ecology Letters 16: 835-43

Herbivore-Induced Plant Volatiles

Common Mycorrhizal Networks

Hypothesis: Mycorrhizal fungal networks communicate pest defence between plants via signalling through mycelia

Babikova et al. (2013) Ecology Letters 16: 835-43

- arbuscular mycorrhizae are ubiquitous ancient plant mutualists -80 % of terrestrial plants

-due to lack of specificity of form CMNs connecting plants

- CMNs act as conduits of nutrients and water and also disease resistance signals

- role in transfer of signals released in response in insect damage in multitrophic interactions was unknown

Babikova et al. (2013) Ecology Letters 16: 835-43

Common Mycorrhizal Networks

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 Aphidius ervi

Hyphal connectionAttractive

Repellent

a

a

bb b

z

z

y yy

Response of pea aphid and its parasitoid wasp (Aphidius ervi) to volatiles in olfactometer bioassays: time spent in treated arm minus control (mean)

3

-2

-1

0

1

2

With MeS

Without MeS

Attractive

Repellent

Tim

e s

pen

t [

min

]

***-3

am

ount

of

meth

yl sa

licyla

te [

ng

/ m

l]

0

2

4

6

8

10

Meth

yl s

ali

cyl

ate

[n

g /

ml]

Response of pea aphid to volatiles in olfactometer bioassays: time spent in treated arm minus control (mean)

Babikova et al. (2013) Ecology Letters 16: 835-43

Future directions

IMPROVING BIOCONTROL

Biocontrol with natural enemies

• Natrual enemies of pests can be released to control them

• Successful in glasshouses e.g. Almaria in Spain

• Harder to use in open field environments

New Agri-tech Catalyst project: Lure-and-kill technology to manage beetle pests of field beans and peas

4-Methylheptane-3,5-dione

Beauveria bassiana spores adhering to Entostat particles

Sitona lineatus adults

♂ produced aggregation pheromone that attracts ♀s and ♂s

The main non-chemical control of aphids is based on parasitoids - either by release in glasshouses or encouraging natural populations outside.

Biocontrol in edible protected crops 2010/11 (UK)

Aphidius ervi used on 2072 ha: 350 ha tomatoes, 131 ha of cucumbers, 1511 ha of peppers

Data from Fera Pesticide Usage survey (ha are treated hectares and include repeat treatments)

Aphidius colemani used on 3160 ha:

2235 ha peppers, 487 ha of cucumbers, 426 other vegetables

Aphidius

Aphelinus

Praon

Dendrocerus Alloxysta PachyneuronAsaphes

Treated Control0

1

2

3

4

5

Tim

e (

min

s)Significant

Attraction inOlfactometerBioassay

*Attractant

IMPROVING CROP RESISTANCE

Introgressing resistance?

at least 10,000 years ago

wild einkorn wheat (Triticum urartu)

wild goat grass related to Aegilops speltoides

Triticum diccocoides, wild emmer wheat

prehistoric times

goat grass (Aegilops tauschii)

Bread wheat, Triticum aestivum

Blight resistant potato +Rpi-vnt1

5 fungicide sprays to protect

No pesticide needed

Aphid resistant wild potatoes

0

40

80

% Nymph survival

(after 7 days)

0

4

8

Nymphs produced

(after 24h)

012345

Adults settled (after 24h)

Two of the ten lines tested were very resistant with 0% aphid survival after 7 days.

Molecular recognition system in insects

Molecular recognition system in plants

Understanding resistance mechanisms

(image courtesy of Saskia Hogenhout)

Conclusion

Intensified agriculture is more dependent on crop protection

Lush monocultures of high yielding varieties grown with fertiliser are often more susceptible to pests

Value of Crop Protection – UK wheat

Oerke EC (2006) Crop losses to pests. The Journal of Agricultural Science 144:31-43.

Value of UK wheat production in 2011 (Defra - Agiculture in the UK dataset) £ 2 210 million

Crop losses with no crop protection (from Oerke 2006) %

weeds 23 £ 508 millionpests 8.7 £ 192 million

diseases 18.1 £ 400 millionTOTAL £1100 million

0

1000000

2000000

3000000

4000000

5000000

6000000

7000000

8000000

9000000

10000000

Popu

lati

on

(1000s)

; C

ere

al

Pro

du

cti

on

(x 5

00 t

on

nes)

Source: FAOSTAT

human population

cereal production

Will Future Demand be Met? Consider resources, planetary boundaries and climate change

Questions… ?