Push–pull farming systems

Push

–

pull

farming

systems

John

A

Pickett

,

Christine

M

Woodcock

,

Charles

AO

Midega

and

Zeyaur

R

Khan

Farmingsystemsforpestcontrol,basedonthe stimulo-deterrentdiversionarystrategyorpush–pullsystem,have becomeanimportanttargetforsustainableintensificationof foodproduction.Aprominentexampleispush–pulldeveloped insub-SaharanAfricausingacombinationofcompanionplants deliveringsemiochemicals,asplantsecondarymetabolites,for smallholderfarmingcerealproduction,initiallyagainst lepidopterousstemborers.Opportunitiesarebeingdeveloped forotherregionsandfarmingecosystems.Newsemiochemical toolsanddeliverysystems,includingGM,arebeing

incorporatedtoexploitfurtheropportunitiesformainstream arablefarmingsystems.Bydeliveringthepushandpulleffects assecondarymetabolites,forexample,(E )-4,8-dimethyl-1,3,7-nonatrienerepellingpestsandattractingbeneficialinsects, problemsofhighvolatilityandinstabilityareovercomeand compoundsareproducedwhenandwhererequired. Addresses

1

RothamstedResearch,Harpenden,HertfordshireAL52JQ,UK 2

InternationalCentreofInsectPhysiologyandEcology,POBox30772, Nairobi,Kenya

Corresponding author: Pickett, John A ([email protected], [email protected])and

Current Opinion in Biotechnology 2014, 26:125–132

This review comes from a themed issue on Plant biotechnology Edited by Birger Lindberg Møller and R George Ratcliffe ForacompleteoverviewseetheIssueandtheEditorial Availableonline20thJanuary2014

0958-1669# 2013TheAuthors.Publishedby ElsevierLtd.

http://dx.doi.org/10.1016/j.copbio.2013.12.006

Introduction

Allfarmingsystemsrequirecropprotectiontechnologies

forpredictableandeconomicfoodproduction.Pesticides

currentlyserveuswell,withnoconvincingevidencefor

legallyregisteredpesticidescausing problemsof human

health or environmental impact [1]. In terms of risk

analysis,risksassociatedwithuseofpesticideshavebeen extremelylowforsometime[2].However,forsustainable

pest management, seasonal inputs requiring external

production and mechanical application need to be

replacedbyapproachesinvolvingdirectassociationwith

thecropplantsthemselves[3].Currentsynthetic

chemi-cal pesticides have often been designed from natural

productleadstructuresorarethemselvesnaturalproducts

and, although they are in no way more benign than

syntheticpesticides,thereare,innature,genesfor their

biosynthesis which could be exploited for delivery to

agricultureviacroporcompanionplants,orviaindustrial crops.Productionbythelatterisnotsustainablebecause oftheneedforextractionandthenapplicationtothecrop, althoughon-farmextraction,oratleastsomeprocessing,

could beemployedwhere thenecessaryquality control

andsafetycanbeachieved.Manycropplantsincorporate

biosyntheticpathways tonaturalpesticideswhich could

beenhancedbybreeding.Alternatively,pathwayscanbe

added bygeneticengineering, for example,for Bacillus

thuringiensisendotoxinproductionorwithgenesforentire

secondarypathways,forexample,fortoxicsaponinssuch

as the avenacins [4], including from other plants or

organismsentirely.

Pheromones and other semiochemicals have long been

regardedaspresentingopportunitiesforpestmanagement

andmanybiosyntheticpathwayshavebeenelucidated[5].

For semiochemicals, thereisafurther advantagein that

beneficialorganismscanalsobeadvantageously

manipu-lated[6].Thus,semiochemicalsthatrecruitpredatorsand parasitoids(parasitesthatkilltheirhosts),orinotherways

managebeneficialorganisms,canbereleasedbycropor

companion plants, thereby providingnew approachesto

exploitingbiologicalcontrolofpests.Althoughbiological controlissustainablein theexampleofexoticreleaseof controlagents,registrationmaynotbegrantedbecauseof

potential environmental impact, and inundative release

requiresproductionanddelivery.Therefore,managingthe processofconservationbiologicalcontrol,whichexploits

naturalpopulations ofbeneficial organisms,expandsthe

potentialvalueofreleasingsemiochemicalsfromcropsor companionplants[7].Manysemiochemicalsarevolatile,

for example those acting at a distance as attractants or

repellents.Also,inorderthatthesignaldoesnotremainin

the environment after use, these compounds are often

highly unstable chemically, which again promotes the

conceptofreleasefromplants.

From the attributes of a natural product pest control

agents, as described above, follows the concept of

sti-mulo-deterrent or push–pull [8] farming systems

(Figure1).Themainfoodcropisprotectedbynegative Open access under CC BY license.

cuesthatreducepestcolonisationanddevelopment,that is,the‘‘push’’effect.Thisisachievedeitherdirectly,by

modifying the crop, or by companion crops grown

be-tweenthemaincroprows.Ideally,themodifiedcrop,or

thecompanion crop, also creates ameans of exploiting

naturalpopulations of beneficialorganismsby releasing

semiochemicalsthat attract parasitoids or increase their

foraging. The ‘‘pull’’ involves trap plants grown, for

example, as a perimeter to the main crop and which

are attractive to the pest, for example by promoting

egg laying.Ideally,apopulation-reducingeffectwillbe generatedbytrapplants,suchas incorporatinganatural

pesticide,or someinnateplant defence.Push–pullmay

use processes, largely semiochemical based, each of

which, alone, will exert relatively weak pest control.

However,theintegratedeffectmustberobustand

effec-tive. The combination of weaker effects also mitigates

against resistance to the overall system of pest control

because of its multi-genic nature and lack of strong

selectionpressurebyany singlepush–pullcomponent.

Push

–

pull

for

smallholder

cereal

farming

in

sub-Saharan

Africa

Smallholderfarmersindevelopingcountriestraditionally

use companion crops to augment staple crops such as

cereals. Development of the push–pull farming system

for these farmers employed the companion cropping

traditioninestablishinganentrypointforthenew tech-nology.‘‘Push’’and‘‘pull’’plantswereidentifiedinitially

by empirical behavioural testing with lepidopteran

(moth) stem borer adults. Having begun experimental

farmtrialsin1994andmovingon-farmin1995,farmers

veryswiftlyadoptedthemosteffectivecompanioncrops

[9,10](Figure2)andthebenefitssoonbecameapparent

(Figure3).Thesemiochemistryunderpinningtherolesof

thecompanionplantsinthispush–pullsystemwasthen

investigatedbytakingsamplesofvolatilesreleasedfrom

companionplantsandanalysingbygaschromatography,

coupled with electrophysiological recordings from the

mothantennae[11].Inaddition towell-known

attrac-tantsfromthetrapplants(‘‘pull’’),includingisoprenoidal

compounds such as linalool [9] and green leaf alcohols

fromtheoxidationof longchainunsaturatedfattyacids,

othersemiochemicalsarisingthroughtheoxidativeburst

causedbyinsectfeedingofferednegativecuesfor

incom-ing herbivores. These are isoprenoid hydrocarbons, for

example, (E)-ocimene and (1R,4E,9S)-caryophyllene,

and some more powerful negative cues, the

homoter-penes,thatis,homo-isoprenoid,ormorecorrectly,

tetra-nor-isoprenoid hydrocarbons [11] (Figure 4). Most

importantly,theselattercompoundsalsoact asforaging recruitmentcuesforpredatorsandparasitoidsofthepests [11],andmolecular toolsforinvestigatingother activi-tiesarebeingdeveloped[12].Technologytransfer for

this push–pull system requires new approaches, and

althoughsuch transferbenefitsbyatradition of

compa-nioncropping,trainingisrequiredforextensionservices

and farmers, and availability of seed or other planting

material, although, being perennial, these companion

plants are one-off inputs. All the companion plants are

valuable foragefor dairy(cow and goat)husbandry and

potentiatezerograzing,whichisadvantageousinthehigh

population density rural areas in which most of the

populationliveinsub-SaharanAfrica.Thelegume

inter-crop plants, Desmodium spp., also fix nitrogen, with D.

uncinatumbeingabletoaddapproximately110kgN/ha/yr

and contributing approximately160kg/ha/yr equivalent

ofnitrogenfertilizer[13].Desmodiumspp.intercropsalso Figure1

Push-pull: the concept

Natural product pest control agents are, by definition, biosynthesised naturally. The genes for semiochemical biosynthesis expressed in companion plants, or in the crop plants themselves, give a “push” to pests and attract predators and parasitic insects (e.g. parasitoids). At the same time, companion plant genes associated with semiochemicals attractive to pests provide a “pull”. Genes for toxicant biosynthesis can be expressed in the latter in order to reduce pest populations.

“Push”

Produce repellent semiochemicals against the pest, for example (1) from non-host taxa, e.g. organic isothiocyanates, typical of brassicaceous crops, against non-brassicaceous plant feeding pests; (2) feeding stress related semiochemicals that denote pest infestation and also recruit predators and parasitoids.

Crop

Provided with attributes of “push” plants via advanced breeding technologies or GM.

“Pull”

Produce attractant semiochemicals, e.g. associated with host plants and effects heightened by maximising these signals. Produce toxicants enhanced from levels produced in host plants, e.g. benzoxazinoids in certain cereals or from non-host plants, e.g. glucosinolates from brassicaceous plants.

control parasitic striga weeds, for example, Striga her-monthica [13],via release ofallelopathic C-glycosylated

flavonoids [14], which represents another facet of

push–pullin providingweedcontrol[15].Overall,there

is a high take-up and retention in regions where the

technologyistransferred;forexample,inwesternKenya

in2013,nearly60,000farmersareusingthesetechniques [16].Althoughthisrepresentsaverysmallpercentageof themillionsofpeoplewhocouldbenefit,sofartherehave beenveryfewresourcesfortechnologytransfer.Arecent

Current Opinion in Biotechnology

Conventional push–pull field showing maize intercropped with silverleaf desmodium (Desmodiumuncinatum) and with Napier grass (Pennisetum purpureum)plantedasabordercrop(left);climate-adaptedpush–pullfieldshowingsorghumintercroppedwithdroughttolerantgreenleafdesmodium (D.intortum)andBrachiariacvmulatoIIasabordercrop(right).

Figure3

Benefits of push-pull technology

Technological empowerment of farmers Increased household income Increased forage seed production Conservation of biodiversity Sustainable development Gender and social equity

Empowerment of women Improved soil health Improved cattle health Increased crop yields Stemborer and striga control Increased fodder production N-fixation and reduced soil erosion Improved human health Improved manure production Improved dairy production

Current Opinion in Biotechnology

EU-funded research initiative, ADOPT (‘‘Adaptation

and Dissemination Of the ‘Push–pull’ Technology’’),

hassoughtcompanionplantsthatcandealwithdrought,

a rapidly growing problem in sub-Saharan Africa as a

consequence of climate change, and new companion

crops have already been identified and taken up by

farmers[16](Figure2).

The‘‘push’’plantsimitatedamagedcropplants,

particu-larly maize and sorghum which produce the

homoter-penes,andalthoughnormallytoolatetobeofrealvaluein

economic pest management, production of these

com-poundsisinducedbythepest.Recently,wefoundthat

thiscanalsobecausedbyegg-laying,specificallyonthe

openpollinatedvarietiesofmaizenormallygrownbythe

smallholderfarmers [17],but notonhybrids [11].An

egg-relatedelicitorenterstheundamagedplantandthe

signaltravelssystemically,therebyinducingdefenceand causingreleaseofthehomoterpenes.Exploitationofthis

phenomenon (see later) will offer new approaches to

push–pullfarmingsystems.

Biotechnological

development

of

push

–

pull

for

industrialised

farming

New approaches to breeding by alien introgression of

genesfromwidecrosses,includingfromthewild

ances-tors of modern crops [18], as well as incorporation of

heterologousgeneincorporationbyGM[19,20],genome

engineering[21–23]andcreationofsyntheticcropplants

by combining approaches including new crop genomic

information [24], can contribute to push–pull farming

systems. Mixed seed beds are now in use for cereals,

even in industrial agriculture, and push–pull could be

created without separated ‘‘push’’ and ‘‘pull’’ plants,

includingregulatedstaturefacilitatingselective

harvest-ing.The newgenerationof GMandother

biotechnolo-gicallyderivedcrops[3]couldrevolutionisetheprospects

for push–pull in industrialised farming systems by

Figure4 OH OH OH ‘Pull’ ‘Push’ Maize Maize Maize Desmodium Desmodium Napier grass Napier grass OH OH OH OH OH HO HO HO HO O O O O

Current Opinion in Biotechnology

Potentiallyuniversal‘‘push’’semiochemicals,thatishomoterpenessuchas(E)-4,8-dimethyl-1,3,7-nonatriene,biosynthesisedviacytochromesP450 fromthehigherhomologueisoprenoida-unsaturatedsecondaryalcohols,forexample,nerolidol,repelherbivorousinsectsandattracttheirparasitoids [36].Attractantsfrom‘‘pull’’plantsincludeunsaturatedfattyacidproductssuchas(Z)-3-hexen-1-ol.Allelopathiccompounds,forexample,thedi-C -glycosylflavone isoschaftoside, protect the crop from antagonistic organisms such as parasitic weeds [14].

‘‘push’’ trait, thereby obviating the need for labour to

manage theintercrop.

Toxicantsforpopulationreduction

The expression of B.thuringiensis derived genesagainst

certain insectpests hasbeenhighlysuccessful[25],but

we are now able to manipulate secondary metabolite

pathwaysto producepesticides,relatedto thesynthetic

versions, with a much greater range of activities, for

example, cyanogenic glycosides [26], glucosinolates

[27,28,29]andavenacins[30].Thelatter,and alsothe

benzoxazinoids (hydroxamic acids) [31–35], are

bio-synthesised bypathwaysinvolvingaseriesof genes

co-located on plant genomes, potentially facilitating

enhancement or transfer to crop plants by GM [4].

These pathways could be expressed in ‘‘pull’’ plants

for population control. They could also enhance the

‘‘push’’ effect. However, for both, attention must be

directedtowardsobviatinginterferencewiththe‘‘push’’

and ‘‘pull’’mechanisms.

Repellentsforpestsandattractantsforbeneficials Already, in sub-SaharanAfricanpush–pull, thevalueof

the homoterpenes can be seen [11,17]. Laboratory

studies have demonstrated the principle, more widely,

of enhancingproductionby GM[12].Biosynthesisof

boththealcoholprecursors[36]andthehomoterpenes

hasbeendemonstratedwith,forthelatter,Cyp82G1being theenzymeinthemodelplantArabidopsisthaliana[37].

This is now being explored for insect control in rice

(BBSRC International Partnering Award BB/J02028/1

andtheBBSRCChinaUKProgrammeinGlobal

Priori-ties BB/L001683/1).

Pheromones also offer opportunities and, after

demon-stratingtheprincipleinA.thaliana[38],theheterologous expression of genesfor thebiosynthesisof (E)-b

-farne-sene,thealarmpheromoneof manypestaphidspecies,

after success in the laboratory, is being field tested

(BBSRC grant BB/G004781/1, ‘‘A new generation of

insectresistantGMcrops:transgenicwheatsynthesising

the aphidalarmsignal’’) asameansof repellingaphids

andattractingparasitoidstothecrop.Nonetheless,aswell

asovercomingthedemandingissuesofGM,these

soph-isticatedsignalswillneedtobepresentedinthesameway thattheinsectsthemselvesdo,which,fortheaphidalarm

pheromone, is as a pulse of increased concentration.

Indeed,aswellasdemandsofbehaviouralecology,

com-plicated mixturesmay alsobe necessaryto provide the

complete semiochemical cue. However, it is already

proving possible to make relatively simple targeted

changesinindividualcomponentsofmixtures[39],which

could allow an economic GM approach. The latter is

likely to become even more appealing with the

devel-opmentofnewtechnologiesarisingfromgenomeediting

[21–23]. Genes for biosynthesis of the aphid sex

for the highlyvulnerable overwintering population,but

wouldneedtobeisolatedfromtheinsectsthemselvesso

astoavoidthepresenceofotherplant-relatedcompounds

that inhibit the activity of the pheromone. Recent

dis-coveries in plant biosynthesis of compounds related to

aphid sex pheromones [40] will facilitate this quest.

Attractant pheromones of moth (Lepidoptera) pests

mayalsobecomeavailableasaconsequenceofattempts

touseGMplantsas‘‘factories’’forbiosynthesis(Christer

Lo¨fstedt, LundUniversity, personalcommunication).

Inductionofpush–pull

Anumberofbiosyntheticpathwaystoplanttoxicantsand

semiochemicals are subject to induction or priming

[41,42]. Elicitors can be generated by pest, disease or

weed development. Volicitin (N

-(17-hydroxylinolenoyl-L-glutamine))[43–45]andrelated compoundsproduced

in the saliva of chewing insectsinduce both directand

indirectdefence,ofteninvolvingthehomoterpenes,but

require damageto transfer the signalto theplant. The

egg-derivedelicitor (seeabove) [11]should overcome

the problem. Plant-to-plant interactions mediated by

volatile compounds, for example, methyl jasmonate

and methyl salicylate, related to plant hormone stress

signalling, are associated with these effects and can

induce defence. However, there can be deleterious or

erraticeffectsinattemptingtousesuchgeneralpathways [46].cis-Jasmonesignals differentiallyto jasmonate [47] and,withoutphytotoxiceffects,regulatesdefence,often byinductionofhomoterpenes[48]incropsevenwithout

genetic enhancement, for example, in wheat [49], soy

bean[50],cotton[51]andsweetpeppers[52].Inaddition toaeriallytransmittedsignalsthatcouldbeusedtoinduce ‘‘push’’ or ‘‘pull’’ effects, signalling within the rhizo-sphere directly[53,54],or viathemycelial networkof arbuscularmycorrhizalfungi[55],isnowshowing

excit-ing promise. The ‘‘pull’’ effect can be enhanced by

raisingthelevelsofinducibleattractants,providedthere

is nointerference with thepopulation controlling

com-ponents of the push–pull system. However, attractive

plants,withoutpopulationcontrolorwithalateexpressed control,couldbevaluableassentinelplants.Thus,highly susceptibleplants,eitherengineeredornaturally suscept-ible,could,oninitialpestdamage,releasesignalsviathe airorrhizospherethatcould,inturn,switchondefencein

therecipientmaincrop plants,creatingelementsof the

push–pull farmingsystem as afully inducible

phenom-enon activatedwithoutexternalintervention.

Conclusions

Push-pull is notonly a sustainablefarming system,but

canalsoprotectthenewgenerationofGMcropsagainst

development of resistanceby pests.Although

consider-ableworkstill needstobedone forallthenewtoolsof biotechnology to be exploitedin push–pull,agriculture

lostthroughdiversiontootherusesandclimatechange,

and so presents an extremely important target for new

biotechnologicalstudies.

Acknowledgements

RothamstedResearchreceivesgrant-aidedsupportfromtheBiotechnology andBiologicalSciencesResearchCouncil(BBSRC)oftheUnitedKingdom, specificallyincludingBBSRCgrantsBB/G004781/1(Anewgenerationof insectresistantGMcrops:transgenicwheatsynthesisingtheaphidalarm signal),BBH0017/1(Elucidatingthechemicalecologyofbelowgroundplant toplantcommunication),BB/I002278/1(EnhancingdiversityinUKwheat throughapublicsectorpre-breedingprogramme)andBB/J011371/1 (‘Smart’cerealsformanagementofstemborerpestsinstaplecerealsin Africa).TheInternationalCentreofInsectPhysiologyandEcology(icipe) appreciatesthecoresupportfromtheGovernmentsofSweden,Germany, Switzerland,Denmark,Norway,Finland,France,Kenya,andtheUK.The workonpush–pulltechnologywasprimarilyfundedbytheGatsby CharitableFoundation,KilimoTrustandtheEuropeanUnion,with additionalsupportfromtheRockefellerFoundation,Biovision,McKnight Foundation,BillandMelindaGatesFoundationandtheUKGovernment DepartmentforInternationalDevelopment(DFID).

References

and

recommended

reading

Papers of particular interest, published within the period of review, have been highlighted as:

ofspecialinterest of outstanding interest 1.

Pickett JA: Food security: intensification of agriculture is essential,forwhichcurrenttoolsmustbedefendedandnew sustainabletechnologiesinvented.FoodEnergySecurity2013 http://dx.doi.org/10.1002/fes3.32.

Foodproductionmustbeintensifiedonlandthatispresentlyfarmed. Governments,particularlythoseintheEU,mustembraceriskanalysisin whichadvantages,aswellaspotentialhazards,areaccommodated. 2. AmesBN,ProfetM,GoldLS:Nature’schemicalsandsynthetic

chemicals:comparativetoxicology.ProcNatlAcadSciUSA 1990,87:7782-7786.

3. RoyalSocietypolicystatementsandreports:Reapingthebenefits: scienceandthesustainableintensificationofglobalagriculture. 2009.Ref11/09http://royalsociety.org/Reapingthebenefits/. 4.

OsbournA,PapadopoulouKK,QiX,FieldB,WegelE:Findingand analyzingplantmetabolicgeneclusters.MethodEnzymol2012,

517:113-138.

Describes approaches for the identification of secondary metabolic gene clusters in plants through forward and reverse genetics, map-based cloning, and genome mining and gives examples of methods used for the analysis and functional confirmation of new clusters.

5. Keeling CI, Chiu CC, Aw T, Li M, Henderson H, Tittiger C, Weng H-B, Blomquist GJ, Bohlmann J: Frontalin pheromone

biosynthesisinthemountainpinebeetle,Dendroctonus ponderosae,andtheroleofisoprenyldiphosphatesynthases.

ProcNatlAcadSciUSA2013http://dx.doi.org/10.1073/ pnas.1316498110.

6. TakemotoH,PowellW,PickettJ,KainohY,TakabayashiJ: Two-steplearninginvolvedinacquiringolfactorypreferencesfor plantvolatilesbyparasiticwasps.AnimBehav2012,83 :1491-1496.

7.

PickettJA,AradottirGI,BirkettMA,BruceTJA,ChamberlainK, KhanZR,MidegaCAO,SmartLE,WoodcockCM:Aspectsof insectchemicalecology:exploitationofreceptionand detectionastoolsfordeceptionofpestsandbeneficial insects.PhysiolEntomol2012,37:2-9.

Successes in exploiting insect semiochemicals in the interests of better agriculture and animal husbandry are exemplified, and potential new ways of learning more about reception and detection for deception are discussed.

8. Miller JR, Cowles RS: Stimulo-deterrent diversionary cropping: a concept and its possible application to onion maggot control. JChemEcol1990, 16:3197-3212http://dx.doi.org/ 10.1007/BF.00979619.

9. HassanaliA,HerrenH,KhanZR,PickettJA,WoodcockCM:

Integratedpestmanagement:thepush–pullapproachfor controllinginsectpestsandweedsofcereals,anditspotential forotheragriculturalsystemsincludinganimalhusbandry. PhilosTransRSocB2008,363:611-621.

10. KhanZR,MidegaCAO,PittcharJ,BruceTJA,PickettJA:‘Push–

pull’revisited:theprocessofsuccessfuldeploymentofa chemicalecologybasedpestmanagementtool.In Biodiversity andInsectPests:KeyIssuesforSustainableManagement.Edited byGurrGM,WrattenSD,SnyderWE,ReadDMY.NewJersy:John Wiley&SonsLtd.;2012:259-275.

11.

TamiruA,BruceT,WoodcockC,CaulfieldJ,MidegaC,OgolC, MayonP,BirkettM,PickettJ,KhanZ:Maizelandracesrecruit eggandlarvalparasitoidsinresponsetoeggdepositionbya herbivore.EcolLett2011,14:1075-1083.

Natural enemies respond to herbivore-induced plant volatiles (HIPVs), but an often overlooked aspect is that there may be genotypic variation in these ‘indirect’ plant defence traits within plant species. Egg deposition bystemborermoths(Chilopartellus)onmaizelandracevarietiescaused emissionofHIPVsthatattractparasiticwasps.

12.

ThollD,SohrabiR,HuhJH,LeeS:Thebiochemistryof homoterpenes—commonconstituentsoffloraland herbivore-inducedplantvolatilebouquets.Phytochemistry2011, 72:1635-1646http://dx.doi.org/10.1016/j.phytochem.2011.01.019. IdentifiedhomoterpenebiosynthesisgenesinArabidopsisandrelated genesfromotherplantspeciesprovidetoolstoengineerhomoterpene formationandtoaddressquestionsoftheregulationandspecific activ-itiesofhomoterpenesinplant-herbivoreinteractions.

13.

MidegaCAO,PittcharJ,SalifuD,PickettJA,KhanZR:Effectsof mulching,N-fertilizationandintercroppingwithDesmodium uncinatumonStrigahermonthicainfestationinmaize.Crop Prot2013,44:44-49.

ResultsconfirmtheefficacyofD.uncinatuminS.hermonthica suppres-sionleading to better growthand yields ofmaize. Theeffects ofN application, mulching and a combination of both treatments in S. her-monthicacontrol in maize were also observed, although these effects were much weaker.

14.

HamiltonML,KuateSP,Brazier-HicksM,CaulfieldJC,RoseR, EdwardsR,TortoB,PickettJA,HooperAM:Elucidationofthe biosynthesisofthedi-C-glycosylflavoneisoschaftoside,an allelopathiccomponentfromDesmodiumspp.thatinhibits

Strigaspp.development.Phytochemistry2012,84:169-176. Isoschaftoside, an allelopathic di-C-glycosylflavone from Desmodium

spp. root exudates, is biosynthesised through sequential glucosylation and arabinosylation of 2-hydroxynaringenin with UDP-glucose and UDP-arabinose.TheC-glucosyltransferasehasbeenpartiallycharacterised anditsactivitydemonstratedinhighlypurifiedfractions.

15. PickettJA,HamiltonML,HooperAM,KhanZR,MidegaCAO:

Companioncroppingtomanageparasiticplants.AnnuRev Phytopathol2010,48:161-177.

16.

KhanZR,MidegaCAO,PittcharJO,MurageA,BirkettMA, BruceTJA,PickettJA:Achievingfoodsecurityforonemillion sub-SaharanAfricanpoorthroughpush–pullinnovationby 2020.PhilTransRSocB2014.(inpress).

FoodinsecurityisachronicprobleminAfricaandislikelytoworsenwith climatechangeandpopulationgrowth.‘Push–pull’,basedonspecific locallyavailablecompanionplants,hasdoubledyieldsonmanyfarms. Detailsarediscussedwithintheframeworkofimprovingfoodinsecurity whileensuringenvironmentalsustainabilityoffarming.

17.

TamiruA,BruceTJA,MidegaCAO,WoodcockCM,BirkettMA, PickettJA,KhanZR:Ovipositioninducedvolatileemissions fromAfricansmallholderfarmers’maizevarieties.JChemEcol 2012,38:231-234.

Herbivore-induced plant volatiles (HIPVs) were collected from plants exposed to egg deposition by the stemborer Chilopartellus. The parasitic wasp Cotesiasesamiaepreferred samples containing HIPVs from plants with eggs to samples collected from plants without eggs.

18.

KingJ,ArmsteadI,HarperJ,RamseyL,SnapeJ,WaughR, JamesC,ThomasA,GasiorD,KellyRetal.:Exploitationof interspecificdiversityformonocotcropimprovement. Heredity2013,110:475-483.

Use of alien introgression for crop improvement is important for meeting the challenges of global food supply, and the monocots such as the forage grasses and cereals, together with recent technological advances inmolecularbiology,canhelpmeetthesechallenges.

etal.:Thecontributionoftransgenicplantstobetterhealth throughimprovednutrition:opportunitiesandconstraints.

GenesNutr2013,8:29-41 http://dx.doi.org/10.1007/s12263-012-03155.

20. JonesJGD,WitekK,VerweijW,JupeF,CookeD,DorlingS, TomlinsonL,SmokerM,PerkinsS,FosterS:Elevatingcrop diseaseresistancewithclonedgenes.PhilTransRSocB2014. (inpress).

21. LiT,LiuB,SpaldingMH,WeeksDP,YangB:High-efficiency TALEN-basedgeneeditingproducesdisease-resistantrice. NatBiotechnol2012,30:390-392.

22. CurtinSJ,VoytasDF,StuparRM:Genomeengineeringofcrops withdesignernucleases.PlantGenome2012,5:42-50.

23. GajT,GersbachCA,Barbas CFIII: ZFN, TALEN, and CRISPR/ Cas-based methods for genome engineering. Trends Biotechnol2013, 31:397-405.

24. BrenchleyR,SpannaglM,PfeiferM,BarkerGLA,D’AmoreR, AllenAM,McKenzieN,KramerM,KerhornouA,BolserDetal.:

Analysisofthebreadwheatgenomeusingwhole-genome shotgunsequencing.Nature2012,491:705-710.

25. LuY,WuK,JiangY,GuoY,DesneuxN:Widespreadadoptionof Btcottonandinsecticidedecreasepromotesbiocontrol services.Nature2012,487:362-365.

26. MorantAV,JørgensenK,JørgensenC,PaquetteSM, Sa´nchez-Pe´rezR,MøllerBL,BakS:Glucosidasesasdetonatorsofplant chemicaldefense.Phytochemistry2008,69:1795-1813.

27. TextorS,BartramS,KroymannJ,FalkKL,HickA,PickettJA, GershenzonJ:Biosynthesisofmethionine-derived glucosinolatesinArabidopsisthaliana:recombinant expressionandcharacterizationofmethylthioalkylmalate synthase,thecondensingenzymeofthechain-elongation cycle.Planta2004,218:1026-1035.

28. Geu-FloresF,OlsenCE,HalkierBA:Towardsengineering glucosinolatesintonon-cruciferousplants.Planta2009,

229:261-270.

29.

AugustineR,MajeeM,GershenzonJ,BishtNC:Fourgenes encodingMYB28,amajortranscriptionalregulatorofthe aliphaticglucosinolatepathway,aredifferentiallyexpressedin theallopolyploidBrassicajuncea.JExpBot2013,64:4907-4921. Four MYB28genes are differentially expressed and regulated in B.juncea

to play discrete though overlapping roles in controlling aliphatic gluco-sinolate biosynthesis.

30. OwatworakitAetal.:Glycosyltransferasesfromoat(Avena) implicatedintheacylationofavenacins.JBiolChem2012, 288:3696-3704http://dx.doi.org/10.1074/jbc.M112.426155. 31. NomuraT,IshiharaA,ImaishiH,OhkawaH,EndoTR,IwamuraH:

Rearrangementofthegenesforthebiosynthesisof benzoxazinonesintheevolutionofTriticeaespecies.Planta 2003,217:776-782.

32. SueM,YamazakiK,YajimaS,NomuraT,MatsukawaT, IwamuraH,MiyamotoT:Molecularandstructural

characterizationofhexamericb-D-glucosidasesinwheatand

rye.PlantPhysiol2006,141:1237-1247.

33. ElekH,SmartL,MartinJ,AhmadS,Gordon-WeeksR,WelhamS, Na´dasyM,PickettJA,WernerCP:Thepotentialofhydroxamic acidsintetraploidandhexaploidwheatvarietiesasresistance factorsagainstthebird-cherryoataphid,Rhopalosiphum padi.AnnApplBiol2013,162:100-109.

34. GierlA,FreyM:Thehydroxamicacidpathway.NovartisFound Symp1999,223:150-157.

35. FreyM,ChometP,GlawischnigE,StettnerC,Gru¨nS,WinklmairA, EisenreichW,BacherA,MeeleyRB,BriggsSPetal.:Analysisofa chemicalplantdefensemechanismingrasses.Science1997,

277:696-699.

36.

Brillada C, Nishihara M, Shimoda T, Garms S, Boland W, Maffei ME, Arimura G: Metabolic engineering of the C16

homoterpeneTMTTinLotusjaponicasthrough

Phytol2013http://dx.doi.org/10.1111/nph.12442.

Predator responsestothetransgenic plantvolatileTMTT dependon variousbackgroundvolatilesendogenouslyproducedbythetransgenic plants.ThemanipulationofTMTTisanidealplatformforpestcontrolvia the attraction of generalist and specialist predators in different manners. 37. LeeS,BadieyanS,BevanDR,HerdeM,GatzC,ThollD:

Herbivore-inducedandfloralhomoterpenevolatilesare biosynthesizedbyasingleP450enzyme(CYP82G1)in Arabidopsis.ProcNatlAcadSciUSA2010,107:21205-21210.

38. BealeMHetal.:Aphidalarmpheromoneproducedby transgenicplantsaffectsaphidandparasitoidbehaviour.Proc NatlAcadSciUSA2006,103:10509-10513.

39. WebsterB,BruceT,PickettJ,HardieJ:Volatilesfunctioningas hostcuesinablendbecomenonhostcueswhenpresented alonetotheblackbeanaphid.AnimBehav2010,79:451-457.

40. Geu-FloresF,SherdenNH,CourdavaultV,BurlatV,GlennWS, WuC,NimsE,CuiY,O’ConnorSE:Analternativeroutetocyclic terpenesbyreductivecyclizationiniridoidbiosynthesis.

Nature2012,492:138-142http://dx.doi.org/10.1038/nature11692. 41. BruceTJA,PickettJA::Plantdefencesignallinginducedby

bioticattacks.CurrOpinPlantBiol2007,10:387-392.

42. BruceTJA,MatthesMC,NapierJA,PickettJA:Stressful ‘‘memories’’ofplants:evidenceandpossiblemechanisms. PlantSci2007,173:603-608.

43. AlbornHT,TurlingsTCJ,JonesTH,StenhagenG,LoughrinJH, TumlinsonJH:Anelicitorofplantvolatilesfrombeetarmyworm oralsecretion.Science1997,276:945-949.

44. AlbornHT,JonesTH,StenhagenGS,TumlinsonJH:Identification andsynthesisofvolicitinandrelatedcomponentsfrombeet armywormoralsecretions.JChemEcol2000,26:203-220.

45. TurlingsTCJ,AlbornHT,LoughrinJH,TumlinsonJH:Volicitin,an elicitorofmaizevolatilesinoralsecretionofSpodoptera exigua:isolationandbioactivity.JChemEcol2000,26:189-202.

46. SmartL,MartinJ,Limpalae¨rM,BruceTA,PickettJ:Responsesof herbivoreandpredatorymitestotomatoplantsexposedto jasmonicacidseedtreatment.JChemEcol2013,39:1297-1300.

47. MatthesM,BruceT,ChamberlainK,PickettJ,NapierJ:Emerging rolesinplantdefenseforcis-jasmone-inducedcytochrome P450CYP81D11.PlantSignalBehav2011,6:1-3.

48. BruceTJA,MatthesMC,ChamberlainK,WoodcockCM,MohibA, WebsterB,SmartLE,BirkettMA,PickettJA,NapierJA:cis -JasmoneinducesArabidopsisgenesthataffectthechemical ecologyofmultitrophicinteractionswithaphidsandtheir parasitoids.ProcNatlAcadSciUSA2008,105:4553-4558.

49. BruceTJA,MartinJL,PickettJA,PyeBJ,SmartLE,WadhamsLJ: cis-Jasmonetreatmentinducesresistanceinwheatplants againstthegrainaphid,Sitobionavenae(Fabricius) (Homoptera:Aphididae).PestManageSci2003,59:1031-1036.

50. MoraesMCB,LaumannRA,ParejaM,SerenoFTPS,

MichereffMFF,BirkettMA,PickettJA,BorgesM:Attractionof thestinkbugeggparasitoidTelenomuspodisitodefence signalsfromsoybeanactivatedbytreatmentwithcis -jasmone.EntomolExpAppl2009,131:178-188.

51. HegdeMetal.:Aphidantixenosisincottonisactivatedbythe naturalplantdefenceelicitorcis-jasmone.Phytochemistry 2012,78:81-88.

52. DewhirstSY,BirkettMA,Loza-ReyesE,MartinJL,PyeBJ, SmartLE,HardieJ,PickettJA:Activationofdefenceinsweet pepper,Capsicumannuum,bycis-jasmone,anditsimpacton aphidandaphidparasitoidbehaviour.PestManageSci2012,

68:1419-1429.

53. RasmannS,Ko¨llnerTG,DegenhardtJ,HiltpoldI,ToepferS, KuhlmannU,GershenzonJ,TurlingsTCJ:Recruitmentof entomopathogenicnematodesbyinsect-damagedmaize roots.Nature2005,434:732-737.

54.

SobhyIS,ErbM,LouY,TurlingsT:Theprospectofapplying chemicalelicitorsandplantstrengthenerstoenhancethe

biologicalcontrolofcroppests.PhilTransRSocB2014.(in press).

Plantstrengthenerisagenerictermforseveralcommerciallyavailable compoundsormixturesofcompoundsthatcanbeappliedtocultivated plants in order to ‘‘boost their vigour, resilience and performance’’. Studiesintotheconsequencesofboostingplantresistanceagainstpests and diseases on plant volatiles have found a surprising and dramatic increase in the plants’ attractiveness to parasitic wasps.

55.

BabikovaZ,GilbertL,BruceTJA,BirkettM,CaulfieldJC, WoodcockCM,PickettJA,JohnsonD:Undergroundsignals carriedthroughcommonmycelialnetworkswarn

neighbouringplantsofaphidattack.EcolLett2013,16:835-843. Commonmycorrhizalmycelialnetworkscandeterminetheoutcomeof multitrophic interactions by communicating information on herbivore attack between plants, thereby influencing the behaviour of both herbi-vores and their natural enemies.