Volatile communication in plant–aphid interactions

Available online at Volatile communication in plant –aphid interactionsMartin de Vos 1and Georg Jander 2Volatile communication plays an important role in mediating the interactions between plants,aphids,and other organisms in the environment.In response to aphid infestation,many plants initiate indirect defenses through the release of volatiles that attract ladybugs,parasitoid wasps,and other aphid-consuming predators.Aphid-induced volatile release in the model plant Arabidopsis thaliana requires the jasmonatesignaling pathway.Volatile release is also induced by infection with aphid-transmitted viruses.Consistent with mathematical models of optimal transmission,viruses that are acquired rapidly by aphids induce volatile release to attract migratory aphids,but discourage long-term aphid feeding.Although the ecology of these interactions is well-studied,further research is needed to identify the molecular basis of aphid-induced and virus-induced changes in plant volatile release.Addresses 1KeyGene N.V.,P.O.Box 216,6700AE Wageningen,The Netherlands 2Boyce Thompson Institute for Plant Research,1Tower Road,Ithaca,NY 14853,United StatesCorresponding authors:Jander,Georg (gj32@ )Current Opinion in Plant Biology 2010,13:366–371This review comes from a themed issue on Biotic interactionsEdited by Jane E.Parker and Jeffrey G.Ellis Available online 4th June 20101369-5266/$–see front matter#2010Elsevier Ltd.All rights reserved.DOI 10.1016/j.pbi.2010.05.001IntroductionPlants have a tremendous capacity to counteract herbi-vores and pathogens by reprogramming their gene expression and metabolism.Induced responses to her-bivory and even insect oviposition include not only pro-duction of direct defenses such as toxins and spines,but also indirect defenses that involve the recruitment of predators to infested plants.Plant volatile blends elicited by herbivory are quantitatively and qualitatively different from those released in response to mechanical damage alone.Therefore,host plant-specific and herbivore-specific volatile release is a reliable cue that predators and parasitoids can use to find suitable prey.Different signaling pathways are induced by chewing insects,such as caterpillars and piercing-sucking insects,such as aphids and whiteflies.In some cases,this can result in antagon-istic effects,whereby infestation by one herbivore class interferes with the induction of direct or indirect defensesagainst another [1].Aphids,even though they cause relatively little physical damage to the plants upon which they are feeding,nevertheless induce robust plant defense responses.Natural enemies that are attracted by aphid-induced plant volatiles include coccinellid bee-tles (Figure 1),parasitoid wasps,lacewings,and hoverflies [2–5,6 ].In another type of tri-trophic interaction,plant viruses,many of which rely on aphids for their trans-mission,manipulate plant volatile release to recruit aphids and thereby promote virus spread.Plant –aphid –predator interactionsAlthough the aphid-derived elicitors that trigger plant volatile release remain largely unknown,many reports demonstrate that aphid-infested plants release terpenes and other volatile cues to attract predators.Some para-sitoids respond to uninfested plants,but most prefer aphid-elicited cues over ‘clean’plants [5].For instance,infestation of Vicia faba (broad bean),by Acyrthosiphon pisum (pea aphid)elicits attraction of the parasitoid Aphi-dius ervi [7].Wind tunnel and olfactometer behavior assays show that A.ervi females use volatile semiochem-icals from aphid-infested bean plants to locate their hosts,and are relatively unaffected by volatiles released from the aphids themselves [7–9].Additionally,coupled gas chromatography-electroantennography (GC-EAG)allowed the identification of plant-derived volatiles that trigger electrophysiological activity in the antennae of naı¨ve A.ervi females.Specific compounds showing electrophysiological activity,for example 6-methyl-5-hepten-2-one (Figure 2),were increased in V.fabae upon A.pisum feeding and,more importantly,were not released by bean plants during infestation with Aphis fabae (black bean aphid),which is not a host for A.ervi [7].Together,these results show that plant-derived volatiles can be reliable cues for foraging parasitoids.In addition to their innate ability to associate plant volatiles with suitable hosts,most parasitoids,whether specializing in attacking aphids or Lepidoptera,acquire a strong preference for volatile cues from previous success-ful oviposition (e.g.[10]).Experienced A.ervi and Diaer-etiella rapae parasitoids show increased responsiveness toaphid-induced plant volatiles compared to naı¨ve parasi-toids [7,11].Host location through detection of plant volatiles may be impacted by other environmental factors,including attack by other herbivores.In their natural ecosystems,plants often face multiple simultaneous attackers,each of which elicits a specific volatile blend.Infestation with Bemisia tabaci (silverleaf whitefly)inter-feres with (E)-beta-ocimene (Figure 2)induction and thereby indirect defense against Tetranychus urticae(two-spotted spider mite)in Phaseolus limensis (Lima bean)[1].However,in another recent example,Myzus persicae (green peach aphid)feeding on cabbage plants attracted D.rapae through the production of plant vola-tiles,an interaction that was not compromised by volatiles released through simultaneous infestation of the plants with non-host Plutella xylostella (diamondback moth)lar-vae [12].With the rise of Arabidopsis thaliana (mouse ear cress)as a model system,there has been more research on aphid-induced volatiles in the Brassicaceae.The parasitoid D.rapae specifically attacks aphids feeding on Brassicaceae,including both generalists such as M.persicae and special-ists such as Brevicoryne brassicae (cabbage aphid)and Lipaphis erysimi (mustard aphid)[13,14].Glucosinolates and their myrosinase-catalyzed breakdown products are key chemical defenses in Brassicaceae that have been adopted as host-finding cues by both specialist herbivores and parasitoids.A combination of behavioral and GC-EAG studies showed that glucosinolate-derived volatiles,for example,allyl isothiocyanate (Figure 2),attract D.rapae to aphid-infested plants [14–16].Analysis of mutant and transgenic lines showed that attraction of D.rapae to M.persicae -induced A.thaliana requires jasmonate pro-duction via the octadecanoid pathway,but that salicylate signaling negatively effects parasitoid orientation [11,17 ].This is probably due to the known antagonistic effect of salicylate on jasmonate-regulated volatile pro-duction.In addition to recognizing plant-derived volatiles,some natural enemies locate prey by eavesdropping on aphid –aphid communication involving sex and alarm phero-mones.Species-specific ratios of terpenoids,for example,nepetalactone (Figure 2),constitute the major sex phero-mones for many aphids.These volatile compounds attract female parasitoids in the field [18–20]and elicit oriented flights by A .ervi and Aphidius eadyi females in the lab [21].The lacewing predators Chrysopa cognata and Chrysopa oculata are similarly attracted by aphid sex pheromones in olfactometer and field trapping experiments [3,22].How-ever,sex pheromones are only produced in the fall,when aphids reproduce sexually,which would limit their utility as kairomones.By contrast,E -beta-farnesene (EBF;Figure 2),the major component of the aphid alarm pheromone,is produced throughout the year and by all life stages [23].Several studies demonstrate that EBF also attracts predators,alone or in association with plant vola-tiles [4,24,25].Interestingly,EBF is often found in theVolatile communication in plant –aphid interactions de Vos and Jander 367Figure1Coccinella novemnotata (nine-spotted ladybug),an endangered North American species (/),is shown eatingAcyrthosiphon pisum (pea aphid)on Vicia faba (broad bean).Coccinellid beetles and other predators can use plant-derived and aphid-derived volatile cues to locate their prey.Figure2Examples of volatile compounds that help to mediate tri-trophic plant –aphid –predator interactions.blend of aphid-induced plant volatiles,for example in M.persicae -infested Solanum tuberosum (potato)[26,27].Plant-produced EBF could provide protection by repel-ling aphids [28],by attracting predators [25],or perhaps by habituating aphids to the presence of alarm phero-mone by repeated stimulation [29],which could make them more vulnerable to predators.In addition to EBF,other plant-derived volatiles have dual functions,both repelling aphids and attracting predators in a species-specific context.Whereas M.persicae and L.erysimi are attracted to volatiles from untreated plants,volatiles released from A.thaliana sprayed with cis-jasmone repelled the generalist M.persicae ,but did not change the behavior of the specialist L.erysimi [30].The same volatile blend also attracted the generalist parasitoid A.ervi ,but not the specialist D.rapae [30].Phorodon humuli (hop aphid)feeding on Humulus lupulus (hop)induces release of volatile methyl salicylate (Figure 2)a compound that is detected by aphid antennae and repels migratory P.humuli [31,32].Methyl salicylate is also repellent to migratory Rhopalosiphum padi (bird cherry-oat aphid)when they are moving from their winter hosts that release methyl salicylate to several grass species that do not [33,34].However,lacewings and coccinellids use methyl salicylate as an attractive signal to find aphid prey [35,36].Plant –aphid –virus interactionsIn many aphid species,alate (winged)life stages (Figure 3)that can migrate in search of more suitable host plants develop in response to unfavorable growth conditions,crowding,the presence of predators,or exposure to EBF [37,38].Although they are not strong fliers,alate aphids can move considerable distances by drifting in the prevailing winds.Plant viruses,many of which depend on insect vectors for transmission [39],canthus rely on aphid transport not only to other parts of the same plant,but also to more distant,hosts.Two important aphid behaviors can affect the rate of virus transmission:(i)whether aphids feed preferentially from virus-infected tissue,and (ii)whether alate aphids preferentially orient toward virus-infected plants.Mathematical modeling suggests that optimal virus transmission occurs if aphids preferentially orient toward virus-infected plants,but only remain there long enough to acquire the virus and then move to a new,potentially uninfested host [40 ].Therefore,it would be in the best interests of the virus to make the plant attractive for aphid probing,but not necessarily more suitable for long-term aphid feeding.The time required for virus acquisition varies depending on the particular plant –aphid –virus interaction.Non-per-sistent,non-circulative viruses,which attach transiently to the aphid stylets,typically require shorter acquisition times than persistent,circulative viruses,which are taken into the aphid gut,pass via the hemolymph to the salivary glands,and are eventually injected back into a host plant.Visual and olfactory cues from virus-infested plants generally promote settling of alate aphids.However,changes in host plant suitability for aphid feeding vary with the type of virus transmission.A general observation is that persistent viruses,which require relatively long up-take periods,have no effect or make host plants more attractive for aphid feeding.By contrast,non-persistent viruses,which are acquired quickly,sometimes with a single aphid probe of a leaf,can make host plants less suitable for aphid feeding.M.persicae grow better on S.tuberosum and Solanum sarrachoides (hairy nightshade)infested with the persistently transmitted potato leafroll virus than on uninfested plants [41,42].Volatiles from plants infected with potato leafroll virus,are more attrac-tive than controls for both winged and non-winged M.persicae [43,44 ].Similarly,infection with the persist-ently transmitted barley yellow dwarf virus makes Triti-cum aestivum (wheat)volatiles more attractive for R.padi ,but feeding aphids did not preferentially emigrate from virus-infested plants in comparison to controls [45].Although,compared to uninfested plants,alate A.pisum settled preferentially on V.fabae infested with viruses,host plant suitability varied with the transmission mode of the infecting virus [46].Whereas V.fabae infection with the persistent pea enation mosaic virus did not affect growth of A.pisum ,infection with the non-persistent bean yellow mosaic virus reduced aphid growth and survival.Similarly,volatiles from Cucurbita pepo (cucumber)infected with the non-persistent cucumber mosaic virus are attractive for M.persicae and Aphis gossypii (cotton aphid),but aphids grew less well on virus-infested plants and emigrate more readily [47 ].Therefore,by providing a deceptive signal that causes aphids to probe virus-infested plants,but then moving on to look for a more suitable host,rapidly acquired non-circulative viruses may increase their rate of transmission.368Biotic interactionsFigure3Genetically identical winged (alate)and non-winged (apterous)Myzus persicae (green peach aphid)on a Nicotiana tabacum (tobacco)leaf.Winged aphids,which are produced in response to unfavorableconditions,use olfactory and visual cues to find suitable host plants.Future prospectsAlthough changing the volatile profile of crop plants to attract natural enemies of aphids has been proposed as a control measure,there is as yet no implemented,working system.For the long-term ecological success of such an indirect defense response,it is quite important that plant-derived volatiles are reliable signals of herbivory.If volatiles are routinely released in the absence of aphids or other suitable prey,this would lead to predator desen-sitization.Recent sequencing of three Nasonia genomes may make it possible to study such parasitoid wasp responses at the molecular level [6 ].However,more research needs to be done to identify plant gene expres-sion responses to aphid feeding,so that volatile pro-duction can be manipulated in a targeted manner.Although there is genetic evidence for aphid-specific resistance genes in several plant species,aphid elicitors of plant defense and gene expression responses have not yet been identified.The A.pisum genome [48 ]may facilitate the identification of proteinaceous elicitors in aphid saliva.Damage caused by aphid stylet penetration,changes in phloem pressure,and Ca 2+-dependent sieve element clogging are also potential elicitors of local and systemic plant gene expression responses that need to be investigated more thoroughly.For several plant species,global gene expression responses to aphid feeding and aphid-derived elicitors have been assessed with DNA microarrays [49–52].It is quite likely that much of the herbivory-induced plant volatile pro-duction is regulated at the level of transcription.However,signaling pathways leading from aphid-induced gene expression changes to altered volatile production have not yet been elucidated.Future research that combines analysis of both plant volatile responses and gene expres-sion changes may lead to the identification of regulatory networks and specific metabolic pathways that are acti-vated by plants as indirect defenses to attract predators that consume aphids and other phloem-feeding insects.Whereas genetic manipulation of the plant side of plant –insect interactions is now quite feasible,very little is known about the molecular biology of the insect responses to plant volatiles.RNA interference approaches that are being developed for many insect species,in-cluding aphids [53 ],and new insect genome sequences [6,48 ],may make it possible to study volatile response pathways in aphids and their predators in a controlled manner.Volatiles probably play a role in other multi-level interactions involving plants and aphids,but have not yet been investigated in detail.For instance,hyperparasitoids might use volatile cues,that is parasitized aphid-induced plant volatiles,to locate prey infested by parasitoids.Given that different aphid species elicit different plant volatile blends,aphid-tending ants might use these vola-tiles to differentiate between aphids that can and cannot be tended.Although numerous studies have demonstrated the effects of virus infection on plant –aphid interactions,not much is known about the mechanism by which viruses alter the physiology of the plant to make it more or less attractive for aphid feeding.Relatively little research in this field has been done with genetically tractable model plants that would facilitate the identifi-cation of gene expression changes.Publicly available A.thaliana DNA microarray data (e.g.http://www.geneves-tigator.ethz.ch )can provide evidence of virus-induced plant changes that would influence aphid feeding.For instance,infestation of A.thaliana with turnip mosaic virus reduces expression of glucosinolate biosynthesis genes [54 ],which could influence aphid attraction and feeding success.Additional research also needs to be conducted to determine whether virus transmission is actually altered in the manner that is predicted by math-ematical models and insect behavior assays [40 ,47 ].One way in which this could be accomplished more easily is by tracking aphid transmission of viruses expressingVolatile communication in plant –aphid interactions de Vos and Jander 369Figure4Arabidopsis thaliana infected with turnip mosaic virus expressing jellyfish green fluorescent protein (TuMV-GFP)is fed upon by Myzus persicae (green peach aphid),an important vector of TuMV in agricultural settings.In this image,which was made under ultraviolet light,uninfected plant tissue shows red chlorophyll auto-fluorescence and tissue infected with TuMV-GFP fluoresces green.M.persicae are visible as grayish specks on the cauline leaf at the center of the image.Infection with aphid-transmitted viruses such as TuMV can cause volatile release that makes plants more attractive to migratory winged aphids.jellyfish greenfluorescent protein(GFP;Figure4). Finally,the literature on plant–aphid–virus interactions perhaps may be overly virus-centric.The focus of the experiments is generally:‘What does the virus do to promote transmission by aphids?’However,one should also consider a different point of view:‘What must the plant do to limit virus spread by aphids?’Particularly for larger plants such as trees,aphid transmission could accelerate virus spread from one part of the plant to another,and there could be a selective advantage for plants that deter aphid settling and feeding in response to virus infestation.AcknowledgementsWe thank S.Whitham for GFP-expressing turnip mosaic virus,J.Losey for C.novemnotata,M.Mescher for providing data in advance of publication, and M.Haribal for helpful discussions.This work was funded by NSF grant IOS-0718733and USDA grant2009-05201.References and recommended readingPapers of particular interest,published within the annual period of review,have been highlighted as:of special interestof outstanding interest1.Zhang PJ,Zheng SJ,van Loon JJ,Boland W,David A,Mumm R,Dicke M:Whiteflies interfere with indirect plant defenseagainst spider mites in Lima bean.Proc Natl Acad Sci U S A2009,106:21202-21207.2.Verheggen FJ,Mescher MC,Haubruge E,Moraes CM,Schwartzberg EG:Emission of alarm pheromone in aphids:anon-contagious phenomenon.J Chem Ecol2008,34:1146-1148.3.Zhu J,Obrycki JJ,Ochieng SA,Baker TC,Pickett JA,Smiley D:Attraction of two lacewing species to volatiles produced by host plants and aphid prey.Naturwissenschaften2005,92:277-281. 4.Francis F,Lognay G,Haubruge E:Olfactory responses to aphidand host plant volatile releases:(E)-beta-farnesene aneffective kairomone for the predator Adalia bipunctata.J Chem Ecol2004,30:741-755.5.Hatano E,Kunert G,Michaud JP,Weisser WW:Chemical cuesmediating aphid location by natural enemies.Eur J Ent2008, 105:797-806.6. Nasonia Genome Working Group:Functional and evolutionary insights from the genomes of three parasitoid Nasonia species.Science2010,327:343–348.This paper describes the genome sequences of three parasitoid wasps.In addition to providing new insights into volatile responses and other unique aspects of parasitoid biology,these genome sequences will make it possible to develop new methods for utilizing parasitoids in the control of aphids and other pest insects.7.Du Y,Poppy GM,Powell W,Pickett JA,Wadhams LJ,Woodcock CM:Identification of semiochemicals releasedduring aphid feeding that attract parasitoid Aphidius ervi.J Chem Ecol1998,24:1355-1368.8.Du YJ,Poppy GM,Powell W:Relative importance ofsemiochemicals fromfirst and second trophic levels in host foraging behavior of Aphidius ervi.J Chem Ecol1996,22:1591-1605.9.Guerrieri E,Pennacchio F,Tremblay E:Flight behavior of theaphid parasitoid Aphidius ervi(Hymenoptera,Braconidae)in response to plant and host volatiles.Eur J Ent1993,90:415-421.10.Schnee C,Kollner TG,Held M,Turlings TC,Gershenzon J,Degenhardt J:The products of a single maize sesquiterpenesynthase form a volatile defense signal that attracts naturalenemies of maize herbivores.Proc Natl Acad Sci U S A2006, 103:1129-1134.11.Girling RD,Hassall M,Turner JG,Poppy GM:Behaviouralresponses of the aphid parasitoid Diaeretiella rapae tovolatiles from Arabidopsis thaliana induced by Myzuspersicae.Ent Exp Appl2006,120:1-9.12.Agbogba BC,Powell W:Effect of the presence of a nonhostherbivore on the response of the aphid parasitoid Diaeretiella rapae to host-infested cabbage plants.J Chem Ecol2007,33:2229-2235.13.Blande JD,Pickett JA,Poppy GM:A comparison ofsemiochemically mediated interactions involving specialistand generalist Brassica-feeding aphids and the Braconidparasitoid Diaeretiella rapae.J Chem Ecol2007,33:767-779. 14.Bradburne RP,Mithen R:Glucosinolate genetics and theattraction of the aphid parasitoid Diaeretiella rapae toBrassica.Proc Biol Sci2000,267:89-95.15.Pope TW,Kissen R,Grant M,Pickett JA,Rossiter JT,Powell G:Comparative innate responses of the aphid parasitoidDiaeretiella rapae to alkenyl glucosinolate derivedisothiocyanates,nitriles,and epithionitriles.J Chem Ecol2008, 34:1302-1310.16.Kissen R,Pope TW,Grant M,Pickett JA,Rossiter JT,Powell G:Modifying the alkylglucosinolate profile in Arabidopsisthaliana alters the tritrophic interaction with the herbivoreBrevicoryne brassicae and parasitoid Diaeretiella rapae.J Chem Ecol2009,35:958-969.17.Girling RD,Madison R,Hassall M,Poppy GM,Turner JG:Investigations into plant biochemical wound-responsepathways involved in the production of aphid-induced plantvolatiles.J Exp Bot2008,59:3077-3085.Responses of the parasitoid Diaeretiella rapae to volatiles from Arabi-dopsis thaliana mutants with defects in jasmonate,ethylene,and salicy-late signaling were measured.This is one of thefirst publications to address the molecular biology of aphid-induced volatile release in plants.18.Hardie J,Hick AJ,Holler C,Mann J,Merritt L,Nottingham SF,Powell W,Wadhams LJ,Witthinrich J,Wright AF:The responses of Praon spp parasitoids to aphid sex-pheromonecomponents in thefield.Ent Exp Appl1994,71:95-99.19.Hardie J,Nottingham SF,Powell W,Wadhams LJ:Syntheticaphid sex-pheromone lures female parasitoids.Ent Exp Appl 1991,61:97-99.20.Gabrys BJ,Gadomski HJ,Klukowski Z,Pickett JA,Sobota GT,Wadhams LJ,Woodcock CM:Sex pheromone of cabbage aphid Brevicoryne brassicae:identification andfield trapping ofmale aphids and parasitoids.J Chem Ecol1997,23:1881-1890.21.Glinwood RT,Du YJ,Powell W:Responses to aphid sexpheromones by the pea aphid parasitoids Aphidius ervi andAphidius eadyi.Ent Exp Appl1999,92:227-232.22.Boo KS,Chung IB,Han KS,Pickett JA,Wadhams LJ:Responseof the lacewing Chrysopa cognata to pheromones of its aphid prey.J Chem Ecol1998,24:631-643.23.Pickett JA,Wadhams LJ,Woodcock CM,Hardie J:The chemicalecology of aphids.Annu Rev Entomol1992,37:67-90.24.al Abassi S,Birkett MA,Pettersson J,Pickett JA,Wadhams LJ,Woodcock CM:Response of the seven-spot ladybird to anaphid alarm pheromone and an alarm pheromone inhibitor is mediated by paired olfactory cells.J Chem Ecol2000,26:1765-1771.25.Beale MH,Birkett MA,Bruce TJ,Chamberlain K,Field LM,Huttly AK,Martin JL,Parker R,Phillips AL,Pickett JA et al.:Aphid alarm pheromone produced by transgenic plants affects aphid and parasitoid behavior.Proc Natl Acad Sci U S A2006,103:10509-10513.26.Harmel N,Almohamad R,Fauconnier ML,Du Jardin P,Verheggen F,Marlier M,Haubruge E,Francis F:Role of terpenes from aphid-infested potato on searching and ovipositionbehavior of Episyrphus balteatus.Insect Sci2007,14:57-63. 27.Gosset V,Harmel N,Gobel C,Francis F,Haubruge E,Wathelet JP,du Jardin P,Feussner I,Fauconnier ML:Attacks by a piercing-sucking insect(Myzus persicae Sultzer)or a chewing insect(Leptinotarsa decemlineata Say)on potato plants(Solanum370Biotic interactionstuberosum L.)induce differential changes in volatilecompound release and oxylipin synthesis.J Exp Bot2009,60:1231-1240.28.Gibson RW,Pickett JA:Wild potato repels aphids by release ofaphid alarm pheromone.Nature1983,302:608-609.29.Petrescu AS,Mondor EB,Roitberg BD:Subversion of alarmcommunication:do plants habituate aphids to their own alarm signals?Can J Zool2001,79:737-740.30.Bruce TJA,Matthes MC,Chamberlain K,Woodcock CM,Mohib A,Webster B,Smart LE,Birkett MA,Pickett JA,Napier JA:cis-Jasmone induces Arabidopsis genes that affect the chemical ecology of multitrophic interactions with aphids and theirparasitoids.Proc Natl Acad Sci U S A2008,105:4553-4558. 31.Pope TW,Campbell CA,Hardie J,Wadhams LJ:Electroantennogram responses of the three migratory forms of the damson-hop aphid,Phorodon humuli,to aphidpheromones and plant volatiles.J Insect Physiol2004,50:1083-1092.32.Campbell CAM,Pettersson J,Pickett JA,Wadhams LJ,Woodcock CM:Spring migration of damson-hop aphid,Phorodon humili(Homoptera,Aphididae),and summer host plant-derived semiochemicals released on feeding.J Chem Ecol1993,19:1569-1576.33.Pettersson J,Pickett JA,Pye BJ,Quiroz A,Smart LE,Wadhams LJ,Woodcock CM:Winter host component reduces colonization by bird-cherry oat aphid,Rhopalosiphum padi(L) (Homoptera,Aphididae),and other aphids in cerealfields.J Chem Ecol1994,20:2565-2574.34.Glinwood RT,Pettersson J:Change in response ofRhopalosiphum padi spring migrants to the repellent winter host component methyl salicylate.Ent Exp Appl2000,94:325-330.35.James DG,Price TS:Field-testing of methyl salicylate forrecruitment and retention of beneficial insects in grapes and hops.J Chem Ecol2004,30:1613-1628.36.Zhu J,Park KC:Methyl salicylate,a soybean aphid-inducedplant volatile attractive to the predator Coccinellaseptempunctata.J Chem Ecol2005,31:1733-1746.37.Braendle C,Davis GK,Brisson JA,Stern DL:Wing dimorphism inaphids.Heredity2006,97:192-199.38.Kunert G,Schmoock-Ortlepp K,Reissmann U,Creutzburg S,Weisser WW:The influence of natural enemies on winginduction in Aphis fabae and Megoura viciae(Hemiptera:Aphididae).Bull Ent Res2008,98:57-62.39.Ng JCK,Perry KL:Transmission of plant viruses by aphidvectors.Mol Plant Pathol2004,5:505-511.40. Sisterson MS:Effects of insect-vector preference for healthy or infected plants on pathogen spread:insights from a model. J Econ Entomol2008,101:1-8.The author describes mathematical models of aphid-mediated virus transmission,showing how the frequency of infected plants,host plant recognition,and feeding preferences influence the rate of virus spread.41.Srinivasan R,Alvarez JM,Bosque-Perez NA,Eigenbrode SD,Novy RG:Effect of an alternate weed host,hairy nightshade, Solanum sarrachoides,on the biology of the two mostimportant potato leafroll virus(Luteoviridae:Polerovirus)vectors,Myzus persicae and Macrosiphum euphorbiae(Aphididae:Homoptera).Environ Entomol2008,37:592-600.42.Castle SJ,Berger PH:Rates of growth and increase of Myzuspersicae on virus-infected potatoes according to type of virus-vector relationship.Ent Exp Appl1993,69:51-60.43.Ngumbi E,Eigenbrode SD,Bosque-Perez NA,Ding H,Rodriguez A:Myzus persicae is arrested more by blends than by individual compounds elevated in headspace of PLRV-infected potato.J Chem Ecol2007,33:1733-1747.44.Werner BJ,Mowry TM,Bosque-Perez NA,Ding HJ,Eigenbrode SD:Changes in green peach aphid responses topotato leafroll virus-induced volatiles emitted during disease progression.Environ Entomol2009,38:1429-1438.Myzus persicae are attracted to volatiles from virus-infected potatoes in a manner that is dependent on plant age and disease progression.Volatile compounds in the headspace of infected plants may explain differences in aphid behavior.45.Medina-Ortega KJ,Bosque-Perez NA,Ngumbi E,Jimenez-Martinez ES,Eigenbrode SD:Rhopalosiphum padi(Hemiptera: Aphididae)responses to volatile cues from barley yellow dwarf virus-infected wheat.Env Ent2009,38:836-845.46.Hodge S,Powell G:Complex interactions between a plantpathogen and insect parasitoid via the shared vector-host:consequences for host plant infection.Oecologia2008,157:387-397.47.Mauck KE,De Moraes CM,Mescher MC:Deceptive chemicalsignals induced by a plant virus attract insect vectors toinferior hosts.Proc Natl Acad Sci USA2010,107:3600-3605. Cucumber mosaic virus infection of cucumbers not only induces release of aphid-attracting volatiles,but also makes the plants less suitable for aphid feeding.Thereby,viruses are acquired and transmitted rapidly to new host plants.Thesefield observations are consistent with a model for optimal transmission of non-circulative viruses proposed in reference [40 ].48.The International Aphid Genomics Consortium(G.Jander):Genome sequence of the pea aphid Acyrthosiphon pisum.PLoS Biol2010,8(2):e1000313.doi:10.1371/journal.pbio.1000313.Thefirst aphid genome sequence,which is described in this paper,will provide new tools for studying the volatiles that mediate plant–aphid interactions.Analysis of the Acyrthosiphon pisum genome identifies likely receptors and odorant binding proteins that may be involved in host plant recognition and aphid–aphid communication.49.Couldridge C,Newbury HJ,Ford-Lloyd B,Bale J,Pritchard J:Exploring plant responses to aphid feeding using a fullArabidopsis microarray reveals a small number of genes with significantly altered expression.Bull Ent Res2007,57:3183-3193.50.De Vos M,Jander G:Myzus persicae(green peach aphid)salivary components induce defence responses inArabidopsis thaliana.Plant Cell Environ2009,32:1548-1560. 51.Kusnierczyk A,Winge P,Jorstad TS,Troczynska J,Rossiter JT,Bones AM:Towards global understanding of plant defenceagainst aphids—timing and dynamics of early Arabidopsisdefence responses to cabbage aphid(Brevicoryne brassicae) attack.Plant Cell Environ2008,31:1097-1115.52.Smith CM,Liu X,Wang LJ,Chen MS,Starkey S,Bai J:Aphidfeeding activates expression of a transcriptome of oxylipin-based defense signals in wheat involved in resistance toherbivory.J Chem Ecol2010,36:260–276.53.Mutti NS,Louis J,Pappan LK,Pappan K,Begum K,Chen MS,Park Y,Dittmer N,Marshall J,Reese JC et al.:A protein from the salivary glands of the pea aphid,Acyrthosiphon pisum,isessential in feeding on a host plant.Proc Natl Acad Sci U S A 2008,105:9965-9969.This research group developed thefirst RNA interference approach that can be used to silence expression of a gene encoding a secreted aphid salivary protein.The study also demonstrates how an individual aphid salivary protein is essential for successful phloem feeding.54.Yang CL,Guo R,Jie F,Nettleton D,Peng JQ,Carr T,Yeakley JM, Fan JB,Whitham SA:Spatial analysis of Arabidopsis thaliana gene expression in response to turnip mosaic virus infection.Mol Plant Microbe Interact2007,20:358-370.Analysis of virus-induced gene expression changes shows repression of glucosinolate biosynthesis,which may affect aphid host plant choice and feeding.These results suggest the use of Arabidopsis thaliana glucosi-nolate mutants to study aphid responses to virus infection.Volatile communication in plant–aphid interactions de Vos and Jander371。