insect plant interactions
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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… ?
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