Resistance Induction and Herbivore Virulence in the Interaction Between

Resistance induction and herbivore virulence in the interaction between Myzus persicae (Sulzer) and a major aphid resistance gene (Rm2) from peach Marie-Hélène Sauge, Jean-Luc Poessel, Thomas Guillemaud, Laurent Lapchin

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Marie-Hélène Sauge, Jean-Luc Poessel, Thomas Guillemaud, Laurent Lapchin. Resistance induction and herbivore virulence in the interaction between Myzus persicae (Sulzer) and a major aphid resistance gene (Rm2) from peach. Arthropod-Plant Interactions, Springer Verlag, 2011, 5 (4), pp.369-377. 10.1007/s11829-011-9141-8. hal-02649450

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Distributed under a Creative Commons Attribution - NonCommercial| 4.0 International License Version preprint Manuscrit d’auteur / Author manuscript Manuscrit d’auteur / Author manuscript Manuscrit d’auteur / Author manuscript Resistance inductionand herbivorevirulence inthe interactionbetween Myzuspersicae (Sulzer) Sauge, M.-H. (Auteurde correspondance), Poëssel, J.-L.,Guillemaud, T.,Lapchin, L.(2011). and amajor aphidresistance gene (Rm2) frompeach. Arthropod Plant Interactions, 5(4),

Running title: Agroparc, F-84914 Avignon cedex9,France; Plant Sauge,INRA, Correspondence to:Marie-Hélène Route desChappes,06903 Sophia-Antipolis Cedex,France Institut NationaldelaRechercheAgronomique, UMR Thomas Guillemaud• LaurentLapchin Domaine SaintMaurice,84143 Montfavet Cedex,France Institut NationaldelaRechercheAgronomique, Gé Jean-Luc Poëssel Agroparc, 84914 Avignon Cedex 9,France Agronomique,Institut NationaldelaRecherche Plan Marie-Hélène Sauge Marie-Hélène Sauge• Jean-LucPoëssel • Thomas Guillemaud • LaurentLapchin Publié dans/publishedin:Arth Version préliminaire dumanuscrit/ Preliminaryversion ofthemanuscript

Resistance inductionandherbivorevi Myzus persicae Resistance and virulencein thepeach- Resistance 369-377. , DOI : 10.1007/s11829-011-9141-8 (Sulzer) andamajoraphidresistancegene( Comment citer cedocument: ropod-Plant Interactions,2011

e-mail:marie-helene peach nétique et Amélioration des Fruits et Légumes, nétique etAméliorationdesFruits Myzus persicae rulence intheinteractionbetween Interactions BiotiquesetSantéVégétale,400 tes etSystèmes decultureHorticoles,Site es et Systèmes de culture Horticoles,Site es etSystèmes de [email protected] interaction

Rm2

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Version preprint Manuscrit d’auteur / Author manuscript Manuscrit d’auteur / Author manuscript Manuscrit d’auteur / Author manuscript Resistance inductionand herbivorevirulence inthe interactionbetween Myzuspersicae (Sulzer) Sauge, M.-H. (Auteurde correspondance), Poëssel, J.-L.,Guillemaud, T.,Lapchin, L.(2011). and amajor aphidresistance gene (Rm2) frompeach. Arthropod Plant Interactions, 5(4), biochemical defenses if they havenegative eff defenses ifthey biochemical in therelationship.In thismetaphor, pl arms race the specialisation onhostplants by isconstrained ( andRaven’s Ehrlich around two major hypotheses. Models ofantagonisticcoevolutio Introduction Abstract Version préliminaire dumanuscrit/ Preliminaryversion ofthemanuscript Key-words depend onfactorsotherthantheme phenomenon andsuggestthat thepotential foraphids aphids toleave plants. detected significantquan responses. However,we colonize theresistanthost,suggestingthat allofth aphid genotypes from collected naturalpopulations resistance • resistance initial attack.Inducedresistancedecayedover feeding timeof 3 h triggeredinducedresistance, wh theduration a response.Similarly, of infestation toleave tendency aphid’s provoke differences inthe in variability the aphid’sability to exploit theresi herbivore density andtime-dependent aspectsof thegreen against peach conferringavoidanceresistance peachaphid qualitative, witheitherafailureorsuccessofhostcolonization. on/off processofrecognition,phenotypicresult ofthe va pathogen recognition that initiatestheinductionof Prunus persica Prunus In gene-for-genehost-enemy interactions, Adaptation • Density dependence • dependence Gene-for-g Adaptation •Density 369-377. , DOI : 10.1007/s11829-011-9141-8

These resultsimprove ourunderstandingof Comment citer cedocument: • Timing ofinduction n between hostplants andtheir enemies havebeenlargelybased re capacity toevade recognition. re capacity

time intheabsenceofadditionalinfestation. ects onthe herbivores (Witt ects diversity of the plant secondary metabolites oftheplantsecondary involveddiversity ants constitutivechemicals, accumulate regarded as emtriggered theinduction of titative variation among clones in the tendency of among inthetendency titative variation clones stant host.Varyingdensities of infestationdid not ich became effectivebetween 24and 48 h afterthe did not affecttheaphid response. Abriefaphid resistance inductionwereexamined, aswell plantdefense asthe responses.Schematically, a plant, and a single aphid was sufficient to elicit toelicit sufficient singleaphidwas a plant,and were tested in the laboratory. Noclonecould inthelaboratory. were tested 1964) theory was that the evolution of insect wasthattheevolutionofinsect 1964) theory to adapt to a majorto adapt a plantresistancegenemay riability inenemy virulenceisexpectedtobe riability monogenic plantresistanceresultsfrom ene plant-insectinteractions•Induced

We focussed on amajorgenefrom We focussed induced resistance as a dynamic inducedresistanceasadynamic

Myzus persicae

effectiveplantdefense stock andGershenzon . Measurements of . Measurements

Thirty Version preprint Manuscrit d’auteur / Author manuscript Manuscrit d’auteur / Author manuscript Manuscrit d’auteur / Author manuscript Resistance inductionand herbivorevirulence inthe interactionbetween Myzuspersicae (Sulzer) Sauge, M.-H. (Auteurde correspondance), Poëssel, J.-L.,Guillemaud, T.,Lapchin, L.(2011). and amajor aphidresistance gene (Rm2) frompeach. Arthropod Plant Interactions, 5(4), 2006). Alstona virulence withrespecttothesegenes(e.g. amongcommonly populationsandhavebeendesigne Dogimontal. 2007).Aphid biotypes et thatcanove R majorgenes,some controlledby is aphids, resistance al. susceptible plantandliving larvae(Harriset response,i.e. binary a as manifested typically (Diptera: havebeen Cecidomyiidae), generally (Say) Boyko 2007). Thegeneticsoftheinteracti andpiercing-sucking between plant interactions resistant crop varieties affects the manner in which herbivorous insects evolve and thus impact andthusimpact evolve herbivorousinsects manner inwhich the affects crop varieties resistant in practical ramifications inso agricultural systems, (Kniskern andRausher2001).Cons local adaptation of enemy to hostthatis difficult to at thepopulation level.In particular, thegene-for-g evolutionary to beusefulunderstandecologicaland gene coevolution,firstdefined altered ordeleted ofstrong that culminates inactivation defe gene. Major ( resistance aspecific unless thehostcarries degree ofcorrespondencebetweenhostandherbi compounds (virulence) acrosspopulations may display al. 2007).Hostdefensechemicals (Després et and turnevolvedbehaviouralor2002). Herbivores havein Version préliminaire dumanuscrit/ Preliminaryversion ofthemanuscript proteins conferring resistance to microbial pathogens (Rossi et al.1998; microbial pathogensKlingler etal.2005; (Rossi proteinsconferringresistanceto The distinction between EhrlichandRaven’sh The gene-for-gene concept proposed by FlorThe gene-for-geneconceptproposedby (1955) st R genes act at the earliest stages of pathogen detection by triggeringasignalingcascade detectionby stages ofpathogen genesactattheearliest 369-377. , DOI : 10.1007/s11829-011-9141-8 Avr genes allows them to evade recognition (Bent and Mackey 2007).Gene-for- (BentandMackey recognition toevade allows them genes Comment citer cedocument: in plant-pathogenassociations,was idering themodeofhost-enemy coevolution canalsohave

on between wheat and the Hessian fly, on betweenwheatandtheHessianfly, nses. Schematically, pathogensadapttoan nses. Schematically, R ) gene that matches a specificpathogenavirulence ( ) genethatmatches vore phenotypes (Berenbaum andZangerl1998). ypothesis andthegene-for-gene concepthasproven either a resistant plant and dead fly larvaeora plantanddeadfly aresistant either insects (KaloshianandWalling2005; Smithand 2003). Inmany interacti reconcile withthearms raceviewofcoevolution far as the type ofgenetic constraintsexertedby far asthetype ene concept may helpexplain thenature ofthe ene conceptmay nd Briggs1977;Porteretal.1997;Burd of whichencodeorshow herbivore ability tometabolizeherbivore ability plantdefensive rcome these forms of resistance have appeared rcome theseformsofresistance have biochemical strategies patterns of variation in resistance and virulence patternsofvariationinresistance recognized to fitthis model. Theinteraction is d on the basis of their qualitative pattern of d onthebasisoftheirqualitative continuous heritablevariationwith ahigh ates that a pathogen isabletoinfectahost ates thata also an inspiration for several aninspirationforseveral also

ons betweenplantsand for avoidingplant toxins tight linkage with plant Mayetiola destructor R gene because genebecause

Avr )

Version preprint Manuscrit d’auteur / Author manuscript Manuscrit d’auteur / Author manuscript Manuscrit d’auteur / Author manuscript Resistance inductionand herbivorevirulence inthe interactionbetween Myzuspersicae (Sulzer) Sauge, M.-H. (Auteurde correspondance), Poëssel, J.-L.,Guillemaud, T.,Lapchin, L.(2011). and amajor aphidresistance gene (Rm2) frompeach. Arthropod Plant Interactions, 5(4), these peach [ these peach forecologicalstudies useful framework a establishes al. cropsintheworld(Saugeet many for athreat which represents gene, named coevolution the Rubira- Thus, weaimtoproduceinformation thatcouldhe the in cultivated fruit trees,since (Sauge critical issue et al.2002). within afewdays representsa The question durability of resistance for thecultivar Rubira,whichconfers strong avoida investigated aphiddensity andtime-dependent asp perception anddefenseinduction processes involvedin thephenotype tendency ofmeasured by resistance,as advantages among naturalpopulations. virulence hasneverbeenperformedtodate,wedo bearing thisgenehasb variety resistant commercial are currentlynoaphid genotypes known toexibit virulencetowards about 2007; Smith2005; BentandMackey 2007) andBoyko the greenpeachaphid resistance quantitativetraitloci(Palloix et al.2009;Brun etal.2010). whenthe monogenic plantresistanceoccurredlessfrequently (Gassmannresistance durability etal.2009).It w Version préliminaire dumanuscrit/ Preliminaryversion ofthemanuscript specifically occurduringgene-for-gene interactions specifically much hasbeendisc 2011). During thelastdecade, Rubira andanchoredtothe“Texa Resistance inRubira isknownto be controlledby Resistance Thereupon, our specific objectives weretwofold. Thereupon, our specificobjectives We previously found within thegenus Rm2 -mediated plant responses to -mediated plant Prunus persica Rm2 , maps, at thebottomendoflinkagegroup 1of anF 369-377. , DOI : 10.1007/s11829-011-9141-8 Myzus persicae M. persicae Comment citer cedocument: (L.) Batsch] genotypes areusedin genotypes (L.)Batsch] management limited. ofresistancegenes intimeand spaceremains interactionapproximates. s” × “Earlygold” reference map s” ×“Earlygold” for (Sulzer)(Hemiptera:Aphidid

M. persicae Prunus (Rosaceae) genetic variation in induced resistance to to (Rosaceae)geneticvariationininducedresistance infestation (Poëssel et al. 2006).Inaddition,et al. there (Poëssel infestation ects ofinduction.Second, we lookedforgenetic as recently demonstratedas recently thatthebreakdown of (StahlandBishop2000; een released so far. Since intensive screening for far.Sinceintensivescreening so een released a major dominant gene(Pascaletal.2002).This nce resistancecausingaphids to leavetheplant not know if there are variants with preadaptive withpreadaptive not knowiftherearevariants overed aboutthebiochemicalinteractionsthat of plant-aphid relationships. Moreover, some of of plant-aphid relationships.of Moreover,some lp determiningmodes towhichofthetwo of We firstwantedtodetermineiftheinduced of aphids to leave plants, matches the enemy enemy matches the of aphidstoleaveplants, . By contrast, only a few data are available afewdata are contrast, only . By R gene-mediated resistance. For that, we Forthat,we resistance. gene-mediated breeding programmes. This is the case Thisisthecase breeding programmes. R ae), apolyphagous aphid species, gene was combined topartial genewascombined

Prunus 2 2006). Thisgeneticsystem Rm2 genetic map derived from map derivedfrom genetic Kaloshian andWalling , probably because no , probably (Lambert and Pascal and Pascal (Lambert

Under temperate climate, climate, Under temperate

cv.Rubira (cloneS2605)isacultivar used 369-377. , DOI : 10.1007/s11829-011-9141-8 Comment citer cedocument: M. persicae parthenogenetic femalefro seedlings weregrowninagreenhou

resistance among natural populations of host-alternates between the peach where sexual reproduction peach where betweenthe host-alternates expression ofvirulence occuramong aphidgenotypes. 2002, 2006)wasaddedtothe set offieldclonesand owth chamber with a 16-h day a16-hday owth chamberlength at19°C. with 2003b). Aphids from each sample Aphids wereassumedeach 2003b). from to riments where the two factors were manipulated thetwofactors were riments where hown). An avirulent laboratory clone(Mp03)used hown). Anavirulentlaboratory southern France, in peach orchards plantedwith France,inpeach southern d from eggs.Webelievedsexually-produced that gns). We asked several questions. Whatisthe several gns). Weasked , France,ina red-leaf relation to (i) theintensity and (ii)the timing of esis that was verified by genotyping asubsetof genotyping esis thatwasverifiedby (secondary hosts). In early spring 2002, thirtyhosts). Inearly (secondary aspeachrootstock. It wasselectedin 1980 m eachsample toinitiatetherearingof 30 Rm2 se, and surveyed to se, andkeep them surveyed

locus, and is usually seed- andisusually locus, peach progenyfrom USA. M. persicae

and and tested Version preprint Manuscrit d’auteur / Author manuscript Manuscrit d’auteur / Author manuscript Manuscrit d’auteur / Author manuscript Resistance inductionand herbivorevirulence inthe interactionbetween Myzuspersicae (Sulzer) Sauge, M.-H. (Auteurde correspondance), Poëssel, J.-L.,Guillemaud, T.,Lapchin, L.(2011). and amajor aphidresistance gene (Rm2) frompeach. Arthropod Plant Interactions, 5(4), aphid feeding (experiment d)? course c)?Finally,whatisthetime well (experiment or canshor Is durationofaphidfeedingthesame, after thebeginning inducingof feedingby aphidsrequ resistance relatedtothe number ofinducingaphi threshold density ofinducing aphids Version préliminaire dumanuscrit/ Preliminaryversion ofthemanuscript To determine whether there was variation intheresponseof To determine whethertherewasvariation Genotypic variationinaphid virulence each treatment. replicates for probability for aninduction bytestaphidsto o Weadoptedashortcountingperi each inspection. 6 times duringthefirst 48 hours aftertheir installa same shootastheoneusedforpreinfestation.The ofpr and preinfestedplant.Inthecase each control ofinduced resistance, 2002). To measurethelevel d, wefixed the number ofinducing aphids at20 to preinfestation at48hours, a sufficientdurationtotr the preinfestationperiod, weremoved allaphids shoot) ofeachplantthegroup; they we preinfested onth not (control).Inducingadultaphidswereplaced produced were not taken into account as a parameter of produced werenottakeninto accountasaparameter at9.00 and counted twiceaday 17.00 hoursuntil adultaphidsoneach 25synchronized plants. Weplaced orchards(pla fromseveral collected we exposedclones natural populations and,if so,whether the level We conductedtheexperimentsonplants thathad been preinfested by 369-377. , DOI : 10.1007/s11829-011-9141-8 Comment citer cedocument: required to elicit induced resistance, and is the level of induced and isthelevelof requiredtoelicitinducedresistance,

ccur oncontrolplants.Weperformed6to10 plant of virulence differed qualitatively or quantitatively, of virulencedifferedqualitatively ds (experiment a)?Whatisthe minimumduration numberaphids remaining of onplantswascounted tion. Thefewoffspring produced wereremovedat ter feeding durations trigger induced resistance as feedingdurationstriggerinducedresistance ter od becausethelongerthis period, the higherthe igger induced b, c,and Inexperimentsresistance. we placed10testadultaphids(cloneMp03)on ensureareasonableaphid (Sauge density et al. of induced resistance in the absence of additional of intheabsence of inducedresistance . Inexperimenta,wefixedtheduration of einfested plants, we installed test aphids on the aphids onthe test weinstalled einfested plants, ired todetectinducedresistance(experimentb)? eir preferred feeding site (the terminal growing eir preferredfeedingsite(theterminal re not restricted from dispersing. At the endof At re notrestrictedfrom dispersing. no more aphids wereleft.Thefewoffspringno more aphids nted with susceptible peach varieties) to Rubira to varieties) peach nted withsusceptible caged plant. Aphids remaining on plants were onplants Aphidsremaining were cagedplant. virulence since they all died onplants virulencesincethey before M. persicae

M. persicae to plant resistance among among toplantresistance (cloneMp03)or

Version preprint Manuscrit d’auteur / Author manuscript Manuscrit d’auteur / Author manuscript Manuscrit d’auteur / Author manuscript Resistance inductionand herbivorevirulence inthe interactionbetween Myzuspersicae (Sulzer) Sauge, M.-H. (Auteurde correspondance), Poëssel, J.-L.,Guillemaud, T.,Lapchin, L.(2011). and amajor aphidresistance gene (Rm2) frompeach. Arthropod Plant Interactions, 5(4), herbivore virulence Thebase wasthe aphidgenotype. plants aftertheperiodof observationhadexpired, were control. Right-censoreddata set tothe hazard was the successively on hostresistancewere experiments covariates) and covariates) and thehazar t(representing time hazard at the baseline coefficient thefirst and checked whereitwas last inspection one reducesthistendency. leaves theplant,giventhat it isstillonit,according to the equation: theinfluenceofcovari aphids. Themodel describes modelWe adoptedaCox’s proportional hazards (Cox etal.1991)orm of parasitoids(e.g.Haccou also appliedinecologi biomedical andis research method astatistical tostudy tim survival analysis, theti by becharacterized avoidance resistancecan usingtheR performed were analyses All statistical Statistical analysis eachclone. replicatesfor performed two thecompleting finalmoult. Weevaluatedthe30field clonesandthereferencecloneMp03. We Version préliminaire dumanuscrit/ Preliminaryversion ofthemanuscript in which increasing effect on the plant-leaving tendency. Acoefficient tendency. ontheplant-leaving increasing effect exponential term (thehazardratio)is great by examining thenullhypothesisby H We estimated thetimeWe estimated takenby anindividual aphi h ( h t ) = ( β t ) is the plant-leaving tendency (hazardfunction) afteratime ) istheplant-leavingtendency by maximizingby apartiallikelihood, and we testedthesignificanteffectofcovariates h o ( β t is the regression coefficient of the covariate ofthecovariate coefficient regression isthe ) exp 369-377. , DOI : 10.1007/s11829-011-9141-8 β

x Comment citer cedocument: ,

β = 0 by a likelihood =0by ratiostatistics. Covariatesinthe er thanone,then the corresponding covariate odelling population dynamics (MaandBechinski2008). cal entomology topredictingtheforagingbehaviour cal entomology inspection where it was missing. We estimated the missing. the Weestimated inspection whereitwas software (RDevelopment ates on the instantaneous probability that probability theaphid ates ontheinstantaneous me at which the aphid leaves the plant, we used me atwhichtheaphidleaves theplant,weused e-to-event variables. It is commonly utilizede-to-event variables.Itiscommonly in d to leave theplantasmean the timebetween d for an individual with the value 0 for allthe d foranindividualwiththevalue0 density and duration of infestation. The baseline anddurationofinfestation.The baseline density i.e. 48h.Thecovariatein theexperiment on line hazard at the mean of all covariates in the inthe ofallcovariates mean atthe line hazard 1972) to quantify the plant-leaving tendency of1972) theplant-leavingtendency toquantify used to take intoaccountaphidsremaining usedto on β leading to a hazard ratio smaller than than toahazardratiosmaller leading x . If a coefficient coefficient Ifa .

t spent ontheplant, spent Core Team 2010). SinceCore Team2010). β is such that the thatthe such is

x has an hasan h o ( t ) is Version preprint Manuscrit d’auteur / Author manuscript Manuscrit d’auteur / Author manuscript Manuscrit d’auteur / Author manuscript Resistance inductionand herbivorevirulence inthe interactionbetween Myzuspersicae (Sulzer) Sauge, M.-H. (Auteurde correspondance), Poëssel, J.-L.,Guillemaud, T.,Lapchin, L.(2011). and amajor aphidresistance gene (Rm2) frompeach. Arthropod Plant Interactions, 5(4), exp ( forsubsequent thehazard aphid significantly increased to elicitinducedresistan amount ofdamageneeded The tendencyof inresponsetoaphidinfestation Plant resistance Results Fleming (1982). P significant effectofthedurationpreinfestati addition, when the timesince the provided induction wasmeasured48hoursafterthe short feedingtimesindicated thatvery (asshortas not possibleto assessifinductionrequired 24hor 48 h minimum todetectinduced since the durationnecessary (Table 3b),wefoundthatinduced resistance became experimentstudi wheretheaphidbehaviour was b 5.1, d.f. =2, lead to an increased level ofinducedresist lead toanincreasedlevel using thelog-rank test,oneofafamily of testprocedureswithparameter of aphids for differencesinthesurvivalcurves considered are not butwhoseeffects the coefficients, additional sourcesofvaria regardedas Cox modelare modelwas settothegenotype Got1.Plantreplicates Version préliminaire dumanuscrit/ Preliminaryversion ofthemanuscript =0.908), showingthat induced resist Varying timing aff Varying ofpreinfestationdifferentially

β ) = 6.31 on average, that is, by 531%) =6.31onaverage,thatis,by (Table P =0.079). M. persicae 369-377. , DOI : 10.1007/s11829-011-9141-8 Comment citer cedocument: to leave plants of Rubira was affected by preinfestation by (Table3).The affected toleaveplantsofRubirawas onset of preinfestation was held constant to 48 hours, there was no onset ofpreinfestationwasheldconstantto48hours, there wasno ance wasnotaphiddensity-dependent.

ance within the tested range (log-ranktest: within thetestedrange ance on thelevelofplantavoidance (log-ranktest: across groupsofpreinfestationoraphidgenotypes 3 hours) weresufficienttoelicitinducedresistance, 3 ce was extremely low. A preinfestation by a single low.Apreinfestationby was extremely ce ed immediately afterremovinginducinged immediately aphids 3a). Highernumbers of tion that must be accounted for the estimation of tion thatmust beaccountedfortheestimation effective between24and48hofaphid feeding, were specified as strata in the model. Strata in a model.a the Stratain in asstrata specified were of particular interest. In a second step we tested second step interest. Ina of particular ected the plant-leaving tendency ofaphids. In ected theplant-leavingtendency of feeding,orsome Experimentc combination. individuals to leave the plant, by afactorof individualsplant, by toleavethe resistance was48hours.Atthisstage,it resistance beginning of preinfestation (Table3c).In

ρ defined by Harringtonand definedby inducing aphids didnot χ 2

= 0.5,d.f.3,

χ 2

= Version preprint Manuscrit d’auteur / Author manuscript Manuscrit d’auteur / Author manuscript Manuscrit d’auteur / Author manuscript Resistance inductionand herbivorevirulence inthe interactionbetween Myzuspersicae (Sulzer) Sauge, M.-H. (Auteurde correspondance), Poëssel, J.-L.,Guillemaud, T.,Lapchin, L.(2011). and amajor aphidresistance gene (Rm2) frompeach. Arthropod Plant Interactions, 5(4), estimated aphid plant-leaving tendency (Kruskal-Wallis ranksum : (Kruskal-Wallis aphidplant-leavingtendency test estimated Car 16(Table 4).Wedid not detectany influenceof thegeographical origin of thegenotypes onthe cloneCar conditions, thehazardratioestimated for preinfestation. Differences amongpreinfestation. Differences groups measured respec 64% wheninducedresistancewas me was when inducedresistance The and themeasureofinduced resistanceincreased. asth hazardratiosdecayed 3d). However,estimated Version préliminaire dumanuscrit/ Preliminaryversion ofthemanuscript among theminplantavoidance (log-ranktest: peach variety,itisunlikely tohaveunde potato, before totestit on Rubira.Anyhow,since possible conditioning host,suchaspepperor effects wouldrequiretorearMp03onasecondary on continuously p clonewasreared this laboratory Mp03 had the lowesthazardratiopossibly reflectsth 2002). Takentogether,theseresultssugg (Sauge etal. ratio thanMp03, the laboratory referenceclonewhich toleavetheplant(Tab looking attheaphidtendency sampledNo aphidgenotype intheorchardcouldestab Genotypic variationinaphid virulence 0.0001). Induced resistancepersistedforatleast48 hours after theendof a48hour preinfestation (Table

Despite the fact that all the field clones were av Despite thefactthatallfieldcloneswere 369-377. , DOI : 10.1007/s11829-011-9141-8 Comment citer cedocument: asured immediately afterremovingasured immediately theaphids, by butonly 241% and

rgone any selective adaptation toRubira. selective adaptation rgone any were highlysignificant(log-ranktest: χ each without host plantalternation.Excluding these Mp03 has always been main been always Mp03 has 2

1 was onaveragefourtimes higherthanforclone le 4), all the clones had a higher estimated hazard hadahigherestimated le 4),alltheclones = 122,d.f. 29, e time elapsed between the end ofpreinfestation betweenthe e timeelapsed e effectsofconditioning (maternal effects),since irulent, we detected highly irulent, wedetectedhighly significant variation hazard to leave the plant was increased by 317% hazard toleavetheplant was increasedby lish coloniesonRubiraplants.Inaddition,when is known to trigger effective induced resistance is knowntotriggereffectiveinducedresistance tively 24 and 48 hours after the end of the 24 ofthe and 48hoursaftertheend tively est that all clones are avirulent. Thefactthat clones are est thatall χ P

2 =0.940, d.f.= 2, <0.0001). Under identical tained onasusceptible χ 2

= 27.8,d.f. =2,

P = 0.62). = P < Version preprint Manuscrit d’auteur / Author manuscript Manuscrit d’auteur / Author manuscript Manuscrit d’auteur / Author manuscript Resistance inductionand herbivorevirulence inthe interactionbetween Myzuspersicae (Sulzer) Sauge, M.-H. (Auteurde correspondance), Poëssel, J.-L.,Guillemaud, T.,Lapchin, L.(2011). and amajor aphidresistance gene (Rm2) frompeach. Arthropod Plant Interactions, 5(4), plant-leaving tendency matchesplant-leaving tendency percep theenemy ex model. Thephenotypic sucha towards accepting Rm2 arenotsuffici thisstudy firstpartof the Data from Discussion Version préliminaire dumanuscrit/ Preliminaryversion ofthemanuscript with the cabbage army moth, moth, with thecabbagearmy Gómez etal.(2010),whereinduciblechangeinleaf gene-mediated resistance.Asimilar behaviouralap of theloss pathogen recognition by the plant. feeding stimuli. Thisqualitative responsesupports neith nothing trait,giventhatitsleveldepends in whiteclover, the inductiondeclined afte ofdefense-related genes could befina morewhose number activated genes, responses wereactivatedassoon6hoursafter resistance derivedfrommajor genes(e.g.,Gaoet otherwell- plantdefenseresponses in dynamics of pest prevails.Thetime of course defensive cardenolides. Fonscolombe) (Hemiptera: Aphididae),aphiddens found that in milkweed ( notremove leaftissue do fact thatphloem-feeders Karban2000;Underwood 2000;(Agrawal and Masseyet ofintensity herbivory was found to influence themagnitude ordefenseinductionof induced resistance with induction contratswithresultsfrom research Irrespective of thegeneticcontextourstud Irrespective The speed of responses to enemy attacks may be attacks toenemy responses The speedof from Rubiraand Trifolium repens 369-377. , DOI : 10.1007/s11829-011-9141-8 M. persicae M. Comment citer cedocument: Asclepias Mamestra brassicae L..Wesuggestthatinducedresist ) species infested by theoleanderaphid, by infested ) species M. persicae follows a gene-for-gene model, but the results are a first step firststep a buttheresultsare model, agene-for-gene follows

-induced resistance showed apatternsimilar-induced resistance tothe er ontheamountnor ontheduration ofthe aphid (L.), was interpreted as a sign of defense activation a signofdefenseactivation as wasinterpreted (L.), lly doubledat36or48hours after infestation.Then, tion anddefenseinductionprocessesinvolvedin arthropods with chewing mouthparts, in arthropods withchewingwhichthe the ideathataphidadaptationmight occurbecause infestation and extended periods ofaphid probing pression of resistance as characterized by theaphid by characterized as pression ofresistance ent toprovethattheinteractionbetweengene al. 2007; Li et al. 2008). In these systems, plant 2007;Liet al.2008).Inthesesystems, al. proach wasadoptedfor example inthe workby ity ity did notleadtoincreasedinduction of plant per se y, the absence of aphid density-dependence in of aphiddensity-dependence y, theabsence r 24or 48 hours. InRubira, brief avery aphid palatability measured by means of choice tests meansofchoice measuredby palatability characterized plant-aphid systems that involve that plant-aphidsystems characterized critical in determining whether the plant or the critical indeterminingwhethertheplant al. 2007).may beduetothe Thisdifference . Forexample ZehnderandHunter(2007) ance inRubiraiscalledanall-or-

Aphis nerii

(Boyer de (Boyer R

Version preprint Manuscrit d’auteur / Author manuscript Manuscrit d’auteur / Author manuscript Manuscrit d’auteur / Author manuscript Resistance inductionand herbivorevirulence inthe interactionbetween Myzuspersicae (Sulzer) Sauge, M.-H. (Auteurde correspondance), Poëssel, J.-L.,Guillemaud, T.,Lapchin, L.(2011). and amajor aphidresistance gene (Rm2) frompeach. Arthropod Plant Interactions, 5(4), because they may influence theevolutionofresistance. may because they maintenance oftheinductionstatusfo traits and beneand possible costs the infestation. Determining d peak inductionat48hours,inducedresistance other againsttheaphid,compared to protection ensures rapidandefficient activation infestation anddefense feeding duration isrequired forproducing the Version préliminaire dumanuscrit/ Preliminaryversion ofthemanuscript exposed alargespatialandtemporal gene conferredby of resistance of in heterogeneous virulentgenotypes frequency virulence, ifitexists,hasremained undetectedin thatmatching couldestablishontheplant. of the It islikely class noprogeny ofavirulence,since class selection pressure exerted by exertedby selection pressure which aphidsusedinthepresentworkweresamp (Weber 1985;Nikolakakis etal.2003) and insecticid et al.2009).Inaddition, to (Guillemaudnecessary et al.2003a),theoretically type may exhibitfeaturesconsistentwith bothmodels experimentations, but it adds weight to the ideath w inconsistent seems Thisassertion hypothesis. notbe qualitative andmayinteraction may also thatcanbedrawnfromtested. Theconclusion th quantitative variation inthe aphid plant-leaving pressure thatpreventsaphidcolonization. aphid populations.Innursery, itis interact with not favour the evolution of virulence.In orchards Field datasuggestthatall Finally, theFinally, important andintriguing finding of this wasthe study identification of significant M. persicae -inducible peach genotypes lacking major gene(Saugeetal.2006).After -inducible lacking resistance peachgenotypes 369-377. , DOI : 10.1007/s11829-011-9141-8 Comment citer cedocument: M. persicae Rm2 M. persicae Rm2 isdifficult. Ontheonehand,aprevious analysis microsatellite remained low very formore than30 asituationthat should years, containsconsiderablegenetic

genotypes tested could be reasonably assigned to a discrete assignedtoadiscrete testedcouldbereasonably genotypes tic variability inFrenchtic variability populations of cultivated as seedling but under strong insecticidal seedling butunderstronginsecticidal cultivatedas r prolongedperiods oftime deservesinvestigations, led (Guillemaud etal.2003b). On theotherhand, is resultthatvirulencein the Rubira- natural populations. Today, predicting theevolution at plant-aphid interactions involving genes of the our sampling scheme becauseofaloworspatially tendency within therange of avirulent genotypes , Rubira isplanted asrootstock andthus doesnot defense signal. Then, a short time lag between defense signal.Then,ashorttime lag ecayed over time in the absence of additional intheabsenceof overtime ecayed allow adaptive genes to evolve (but see Lombaert evolve (butsee allow adaptivegenesto ith theinterpretationoffirstseries e resistance has evolvedin the e resistance populations from evolve accordingtothe of coevolution. There are now at least two cases ofcoevolution.Thereare now atleasttwocases fits associated withthe fits associated activation ofdefensive

variation forhostplantadaptation

chemical coevolution

M. persicae M. persicae R

Version preprint Manuscrit d’auteur / Author manuscript Manuscrit d’auteur / Author manuscript Manuscrit d’auteur / Author manuscript Resistance inductionand herbivorevirulence inthe interactionbetween Myzuspersicae (Sulzer) Sauge, M.-H. (Auteurde correspondance), Poëssel, J.-L.,Guillemaud, T.,Lapchin, L.(2011). and amajor aphidresistance gene (Rm2) frompeach. Arthropod Plant Interactions, 5(4), affected thepopulation growth ofdistinctof thepotato aphid, isolates Environnement, InstitutNational delaRechercheAgronomique. supports from the InstitutFrançaisdelaBiodi sampling andC.Favret forenglishcorrectionofan Acknowledgements and improvedurability theefficiency of resistance. harbouringgenotypes the highest concentrations ininduced defensive compounds, whichmight material2005). Ifsimilar variationexistsinplant (Zangerl and Berenba reported inseveralsystems benefit to breeding for durableresistance.Geneticva attack isalsoneededtogiveev interaction. Adetailedcharacterizationofthebiochemi experimental orchardsisnowre isovercome. trait ‘plantresistance’ transmission’. Thissuggeststhat andnoovercoming of virulence, butnovariability aphid populations acontinuum ofperformanceresponseto non-persistent virusestransmission this sameap by both resistance to the melon aphid, both resistancetothe asavirulent.Inmelon, all (Thomas)of whichwereclassified (Hemiptera: Aphididae), called NBS-LRRfamily of aphids) thathave beenclonedsofar(Rossietal.1998;Dogimont etal.2007). Bothbelong to theso- supporting Thegene this hypothesis. Version préliminaire dumanuscrit/ Preliminaryversion ofthemanuscript the gene Large scale analysis of analysis Large scale Vat frommelon, 369-377. , DOI : 10.1007/s11829-011-9141-8 We acknowledge J.P. Lacroze for technical assistance, S.Simon for aphidWe acknowledgeJ.P.Lacrozefortechnicalassistance, Comment citer cedocument: Cucumis melo Cucumis melo M. persicae R resistance genes.Hebertetal.(2007)found that resistance idence foragene-for-geneinteraction. A. gossypii quired togetmore information aboutthe formalgeneticsofthe Aphis gossypii Mi-1.2

populations collected from peach genotypes carrying genotypescarrying populationscollected from peach L., are the only two genes of resistance to insects (namely (namely toinsects twogenesofresistance L., aretheonly from tomato, is effectively recognized by recognized by effectively is um 1990;um Agrawaletal.2002; Stevensand Lindroth derived from Rubira, breeders could select for peach fromRubira, breederscouldselect derived Glover (Hemiptera: Aphididae), and resistance to Aphididae),andresistanceto Glover(Hemiptera: versité andDépartementSantédes Plantes et Vat earlier draft. Part of this work received financial Part ofthisworkreceived earlier draft. riation ininduction of plant metabolites hasbeen hid species.Lombaertal. (2009)detected et in cal interactions thatoccur in Rubirauponaphidcal interactions resistance were observed for the trait ‘virus forthetrait observed were resistance Lycopersicon peruvianum Vat

from complete avirulencetostrong from complete Thischaracterization couldalso

Vat Macrosiphum euphorbiae melonplants,evenifthe Mi-1.2

(L.) P.Mill., differentially

Vat confers Rm2 and in

Version preprint Manuscrit d’auteur / Author manuscript Manuscrit d’auteur / Author manuscript Manuscrit d’auteur / Author manuscript Resistance inductionand herbivorevirulence inthe interactionbetween Myzuspersicae (Sulzer) Sauge, M.-H. (Auteurde correspondance), Poëssel, J.-L.,Guillemaud, T.,Lapchin, L.(2011). and amajor aphidresistance gene (Rm2) frompeach. Arthropod Plant Interactions, 5(4), Alston FH,BriggsJB(1977) Resistancegenesinapple andbiotypes of Burd JD, Porter DR, Puterka GJ, Haley SD,Burd JD,Porter P DR,PuterkaGJ,Haley Agrawal AA,KarbanR(2000)Specificity ofcons References Version préliminaire dumanuscrit/ Preliminaryversion ofthemanuscript Berenbaum MR, ZangerlAR(1998)ChemicalBerenbaum phe Ehrlich PR, Raven PH (1964)Butterflies andplants: DogimontA, PitratM,Burget-Bigea C,Bendahmane Agrawal AA,ConnerJK,Johnson MT Bent AF, Mackey D(2007)Elicitors,effectors, andthe Bent AF,Mackey Brun H,ChèvreAM,FittBDL,PowersS,Besnard Després L,DavidJP,GalletC(2007) Theevolutionary Cox DR(1972)Regressionmodelsand life- doi:10.1146/annurev.phyto.45.062806.094427 supply of questions. Annu Rev 7458.2000.00677.x influence mites andcaterpillarsoncotton plants 56: 2206-2113. doi:10.1111/j.0014-3820.2002.tb00145.x herbivores:additivegeneticvarian defense against Biol 87: 75-81 American wheataphid(Homoptera: Russian Aphididae) populations. JEconEntomol herbivore. ProcSci USA95:13743-13748 NatlAcad 1866 doi:10.1146/annurev.phyto.45.062806.094427 to resistance Renard M,AndrivonD(2010)Quantitative r Trends EcolEvol22: 298-307. doi:10.1016/j.tree.2007.02.010 no 0070016977 P, CabocheM,Chovelon V (2007)Gene resistantto Leptosphaeria maculans 369-377. , DOI : 10.1007/s11829-011-9141-8

Comment citer cedocument: Phytopathol 45: 399-436. J, Wallsgrove R(2002) Ecological geneticsofaninduced plant in in

Brassica napus. tables. J Roy StatSocB34:187-220. tables. JRoy eairs FB (2006) Biotypiceairs FB variation among North esistance increases the durability ofqualitative esistance increasesthedurability

. Entomol ExpAppl96:39-49. doi:10.1046/j.1570- titutive andinduced resistance:pigment glands notype matchingnotype between aplantanditsinsect AL, ErmelM,HuteauV,MarquerB,EberF, ce and costs of phenotypic plasticity. Evolution and costsofphenotypic plasticity. ce a study incoevolution.a study Evolution 18: 586-608 rd E,Hagen L, LeMenn A, PauquetJ,Rousselle Aphis gossypii ecology of insect resistance toplantchemicals. of insect resistance ecology R genes:thenewparadigmand alifetime New Phytol 185: NewPhytol 285-299.

. United States of America patent . UnitedStatesofAmerica Dysaphis devecta.

99:1862-

AnnAppl Version preprint Manuscrit d’auteur / Author manuscript Manuscrit d’auteur / Author manuscript Manuscrit d’auteur / Author manuscript Resistance inductionand herbivorevirulence inthe interactionbetween Myzuspersicae (Sulzer) Sauge, M.-H. (Auteurde correspondance), Poëssel, J.-L.,Guillemaud, T.,Lapchin, L.(2011). and amajor aphidresistance gene (Rm2) frompeach. Arthropod Plant Interactions, 5(4), Guillemaud T,MieuzetL,Simon JC(2003a)Spatia Gassmann AJ,OnstadDW,Pittendrigh BR (2009)Evol Harris MO, Stuart JJ Mohan M, Nair S, Lamb RJ, Rohfritsch O (2003) Grasses and gallmidges: JJMohanM,NairS, O(2003)Grasses Lamb plant Harris MO,Stuart RJ,Rohfritsch Harrington DP,Fleming (1982)Aclass TR ofranktestproceduresforcensoredsurvivaldata. foragers Information-processing – by Haccou P,DevlasSJ,VanAlphenJJM,VisserME(1991) Flor HH(1955)Host-parasiteinteractioninfl Version préliminaire dumanuscrit/ Preliminaryversion ofthemanuscript Gao LL,AndersonJP,KlinglerNairRM,Ed Hebert SL,JiaL,Goggin FL (2007)Quantitativedi Guillemaud T,BrunA,Anthony N,SaugeMH,BollR,DelormeFournier D,Lapchin R, L, Gómez S,vanDijk W,Stuefer JF(2009)Timing ofinducedresistanceinaclonalplantnetwork. Kaloshian I,WallingLL(2005) Hemipterans asplan Bull Entomol Res93:289-297. doi:10.1079/BER2003241 Biometrika 69:553-566 93-106 Effects ofintra-patchexperienceontheleaving of tendency populations ofthepeach-potatoaphid Vanlerberghe-Masutti F(2003b)Incidence ofinsectic populations ofthepeach-potatoaphid, natural andagriculturalenvironments. PestMa Interact 20:82-93. doi:10.1094/MPMI-20-0082 in Bluegreenaphidresistancein octadecanoid pathway Phytopathology 45: 680-685 Plant Biol12: 512-517.doi:10.1111/j.1438-8677.2009.00234.x doi:10.1038/sj.hdy.6800292 doi:10.1146/annurev.phyto.43.040204.135944 developmenton tomato the plantscarrying doi:10.1146/annurev.ento.48.091801.112559 AnnuRevEntomoldefense andinsectadaptation. 48:549-577. 369-377. , DOI : 10.1007/s11829-011-9141-8 Comment citer cedocument:

Myzus persicae Myzus persicae. Mi ax rust– its geneticsandother implications.

resistancegene.EnvironEntomol 36:458-467

nagement Sci65:1174-1181. doi:10.1002/ps.1844 wards OR,Singh KB (2007)Involvement ofthe

fferences inaphidvirulence andfoliarsymptom l andtemporal inFrench geneticvariability t pathogens.Annu RevPhyt (Hemiptera: Aphididae)from southernFrance. ide resistance alleles in sexually-reproducing resistanceallelesinsexually-reproducing ide utionary of analysis herbivorous insectsin Heredity 91: 143-152. Heredity Medicago truncatula.

Leptopilina heterotoma.

Mol PlantMicrobe opathol 43:491-521. JAnim Ecol60:

Version preprint Manuscrit d’auteur / Author manuscript Manuscrit d’auteur / Author manuscript Manuscrit d’auteur / Author manuscript Resistance inductionand herbivorevirulence inthe interactionbetween Myzuspersicae (Sulzer) Sauge, M.-H. (Auteurde correspondance), Poëssel, J.-L.,Guillemaud, T.,Lapchin, L.(2011). and amajor aphidresistance gene (Rm2) frompeach. Arthropod Plant Interactions, 5(4), Palloix A,Ayme of V,MouryB(2009)Durability Lombaert E,CarlettoJ,PiotteC,FauvergueX, Nikolakakis NN,Margaritopoulos JT,Tsitsipis Performanceof JA(2003) Lambert P,PascalT(2011)Mapping Li Y,ZouJ, Li M,Bilgin DD, Vodkin LO, Ha Klingler J, Creasy R,GaoL,NairRM,CalixAS,SpaffordJacobH,EdwardsOR,SinghKBKlingler J,Creasy (2005) Version préliminaire dumanuscrit/ Preliminaryversion ofthemanuscript Kniskern J,RausherMD(2001)Twomodes of Pascal T, Pfeiffer F, Kervella J, Lacroze JP, Sa J,Lacroze F,Kervella Pascal T,Pfeiffer Ma Z,BechinskiEJ(2008) A survival-analysis- Massey FP, Roland Ennos A, Hartley SE(2007)Herb FP,RolandEnnosA,Hartley Massey 0523.2002.tb02053.x resistance inthepeachcultivar 'Rubira'. potential despitelowgeneticvariability. Entomo Response ofthemelonaphid, doi:10.1079/BER2003230 Aphididae) clonesondifferent host-plants andtheirhost preference.BullEntomol Res93: 235-242. of thesoybean aphid. NewPhytol 0394-2 persicae 137: 1445-1455.doi:10.1146/annurev.phyto.43.040204.135944 antibiosis, andmaps locusflankedby toasingle Aphid resistancein 7458.2009.00904.x doi:10.1111/j.1365-3040.2008.01823.x population dynamics.Model 216: 323-332. Ecol doi:10.1016/j.ecolmodel.2008.04.011 Oecologia 152:677-683. doi:10.1007/s00442-007-0703-5 Phytol Phytol 183: 190-199. doi:10.1111/j.1469-8137.2009.02827.x on thegenetic background:experimentalevidence Sulzer)inthepeachcultivar“Rubira®”. 369-377. , DOI : 10.1007/s11829-011-9141-8

Medicago truncatula

Comment citer cedocument:

Aphis gossypii

179: 185-195. doi:10.1111/j.1469-8137.2008.02443.x Rm2

Plant Breed121:459-461. doi:10.1111/j.1439- gene conferring resistance tothegreenpeachaphid( geneconferringresistance involves antixenosisand , tohost-plantresistance: rtman GL, Clough SJ (2008)Soybeandefenseresponses rtman uge MH (2002) Inheritance of green peach aphid uge MH(2002)Inheritanceofgreenpeachaphid LecoqH,Vanlerberghe-MasuttiF,Lapchin L (2009) host-enemy coevolution. Popul Ecol 43:3-14. based simulation modelfor Russianwheataphid NBS-LRR resistance geneanalogs.PlantPhysiol NBS-LRRresistance l Exp Appl 133:46-56.doi:10.1111/j.1570- plant major resistancegen Tree Genet Genomes. do Genomes. Tree Genet and consequencesforbreedingstrategies.New ivore specificinductionofsilica-baseddefences.

phloem-specific, inducible evidence for highadaptive evidence

Myzus persicae Myzus i: 10.1007/s11295-011- es topathogensdepends

(Hemiptera: Myzus Version preprint Manuscrit d’auteur / Author manuscript Manuscrit d’auteur / Author manuscript Manuscrit d’auteur / Author manuscript Resistance inductionand herbivorevirulence inthe interactionbetween Myzuspersicae (Sulzer) Sauge, M.-H. (Auteurde correspondance), Poëssel, J.-L.,Guillemaud, T.,Lapchin, L.(2011). and amajor aphidresistance gene (Rm2) frompeach. Arthropod Plant Interactions, 5(4), Sauge MH, Lacroze JP, Poëssel JL, PascalT, Sauge MH,LacrozeJP,Poëssel Rossi M,GogginFL, Milligan SB,KaloshianI,Ullman DE,Williamson VM(1998)The nematode Zangerl AR, Berenbaum MR (1990) Zangerl AR,Berenbaum Underwood N (2000)Density dependence ininduced pl Stahl EA,BishopJG(2000) Plant-pathogen arms race Poëssel JL, Sauge MH, Corre MN, Renaud C,Gaudill MH,CorreMN,Renaud Poëssel JL,Sauge Version préliminaire dumanuscrit/ Preliminaryversion ofthemanuscript Smith CM, Boyko EV(2007)Themolecular basesof Smith CM,Boyko T, Kervella Sauge MH,MusF,LacrozeJP,Pascal Stevens MT,Lindroth RL (2005) Induced resistanceintheindeterminate growthofaspen( Weber G (1985) Genetic variability in host plant adaptation of the green peach aphid, in hostplantadaptationofthe greenpeachaphid, Weber G(1985)Geneticvariability Porter DR,BurdJD,Shufran KA,WebsterJA,TeetesGL(1997) Greenbug (Homoptera: Aphididae) R Development CoreTeam(2010) R:ALanguage Wittstock U,GershenzonJ(2002) Constitutive plan 299-304. doi:10.1016/S1369-5266(00)00083-2 tremuloides strength and genetic variation.Oikos 89 resistance and induced resistance and feeding: currentstatus.Entomol ExpAppl Entomol Exp Appl. 38: 49-56 herbivores andpathogens. Curr OpinPlant Biol5:300-307. doi:10.1016/S1369-5266(02)00264-9 in thepeachcultivar'Rubira'. ExpA Entomol 95: 9750-9754 gene resistance 22 April 2010 Accessed peach-potato aphidinsusceptible andresi Loonis M,Lacroze JP,PascalT,Moing A (2006)Metabolic the profiling by ofshootapices infested biotypes: selected by resistantcultivarsorpread selectedby biotypes: Foundation for StatisticalComputing, at http://wwwR-projectorg Vienna, AustriaAvailable ). Oecologia145:298-306. doi:10.1007/s00442-005-0128-y Mi 369-377. , DOI : 10.1007/s11829-011-9141-8 of tomato confers resistance against thepotatoaphid. ProcNatlAcadSciUSA oftomatoconfersresistance susceptibility in the peach- susceptibility Comment citer cedocument: Furanocoumarin induction in wild parsnip – Geneticsand

: 295-300. doi:10.1034/j.1600-0706.2000.890210.x stant peach cultivars. Metabolomicsstant peach 2:288 122: 1-16. doi:10.1111/j.1570-7458.2006.00503.x Kervella J (2002) Induced resistance by by KervellaJ(2002)Induced resistance ppl 102:doi:10.104 29-37.

apted opportunists? JEc J, Poëssel JL (2006) Genotypic PoësselJL(2006) variationin induced J, and Environment forStatistical Computing R Myzus persicae Myzus t toxins andtheir roleindefenseagainst plant resistance and defense responses to aphid plantresistanceanddefenseresponsesto ère M, Maucourt M,DebordeC,Dufour ère M,Maucourt at themolecular level.CurrOpinPlant Biol 3: ant resistancetoherbivore damage: threshold, aphid system. Oikos113: 305-313

6/j.1570-7458.2002.00922.x on Entomol 90:1055-1065 Myzus persicae Myzus persicae

Populus

369-377. , DOI : 10.1007/s11829-011-9141-8 Comment citer cedocument:

ecific variation withinthe genusecific variation J Chem Ecol33:2044-20.doi:10.1007/s10886-007- Asclepias

inresponseto

n ) of n 16 8 6 Myzus persicae the sampled orchards isgiveninGuillemaudet sampled orchards the Longitude Latitude Genotype Longitude Latitude label 4°48É 7°11É 4°57É genotypes collected from peach genotypescollectedfrompeach 43°56Ń 43°47Ń 44°58Ń

Avi 1-6 Car 1-16 Got 1-8

d ( c ( b ( n of Duration a ( Table 2 Version préliminaire dumanuscrit/ Preliminaryversion ofthemanuscript Experiment Number experiment includedcontrol plantsthat were notpreinfested of densitiesvarying (experimenta)andtimingofa representsthenumber ofplantreplicates,with10aphidsper n n n n = 9 to 10) to =9 =10) =10) =6) Experimental designusedtocharacterizeth 369-377. , DOI : 10.1007/s11829-011-9141-8 1 20 20 20 20 20 20 20 20 20 20 20 10 5 aphids inducing Comment citer cedocument: 48 Totaltime inducing frombeginning offeedingby aphidsto

48 48 48 9 6 3 48 24 12 6 48 48 48 feeding [1] feeding [1] testing for induced resistance (h) [1]+[2] (h)[1]+[2] testing forinducedresistance phid preinfestation (experiments b, c and d). Eachphid preinfestation(experimentsb,cand e expression of plantresistanceinresponseto e expression 0 Time betweentheendof 48 24 0 39 42 45 0 0 0 0 0 0 0 induced resistance [2] [2] induced resistance feeding andtestingfor

48 [1]+[2] [1]+[2]

96 72 0 48 48 48 48 24 12 6 48 48 48 Version preprint Manuscrit d’auteur / Author manuscript Manuscrit d’auteur / Author manuscript Manuscrit d’auteur / Author manuscript Resistance inductionand herbivorevirulence inthe interactionbetween Myzuspersicae (Sulzer) Sauge, M.-H. (Auteurde correspondance), Poëssel, J.-L.,Guillemaud, T.,Lapchin, L.(2011). Cox proportionalmodel. hazards Estimated regression coefficients ( Estimated coefficients regression remote the hazard ratiotozero,thestrongerplant-leavingtendencyremote thehazard increasingeffectofthe + indicatesan respectively. hazard (uninfest thebaseline to compared and amajor aphidresistance gene (Rm2) frompeach. Arthropod Plant Interactions, 5(4), d c b a Table 3 Version préliminaire dumanuscrit/ Preliminaryversion ofthemanuscript Experiment Covariates the plant-leavingtendency of Effect ofaphid density (experimenta)andti –48 h +48 h –48 h +24 h –48 h effect Treatment –9 h+39 h –6 h+42h –3 h+45h effect Treatment –48 h –24 h –12 h –6 h effect Treatment –20 aphids –10 aphids –5 aphids –1 aphid effect Treatment 369-377. , DOI : 10.1007/s11829-011-9141-8 Comment citer cedocument: Myzus persicae χ β 2 0.494 1.228 1.427 0.726 0.610 0.432 0.911 0.267 0.322 0.339 1.57 1.78 1.71 1.84 β ), standard errors (SE) and hazard ratios [exp andhazardratios ( ), standarderrors(SE) correspond to a likelihood ratio test. *, **, ***, levels of significance as ***, levelsofsignificance correspond toalikelihood ratiotest.*,**,

ed control) for the coefficients at ed control)forthecoefficientsat 0.209 0.205 0.201 0.162 0.164 0.164 0.207 0.215 0.211 0.218 0.206 0.208 0.206 0.210 SE (

β ) exp ( covariate on the plant-leaving tendency. The more Themore covariate ontheplant-leavingtendency. ming of preinfestation (experiments b,candd) on 1.64* 3.41*** 4.17*** 2.07*** 1.84*** 1.54** 2.45*** 1.31 1.38 0.71 4.80*** 5.95*** 5.53*** 6.31*** β ) n 400 390 300 500

χ 71.9 (3) 24.3 (3) 37.2 (4) 135 (4) 2

(d.f.) P <0.05,0.01and0.001 β )] for the covariates of a )] forthecovariatesofa P <0.0001 <0.0001 <0.0001 <0.0001

tendency leaving Effect on + + + + + + + no effect no effect no effect + + + + Version preprint Manuscrit d’auteur / Author manuscript Manuscrit d’auteur / Author manuscript Manuscrit d’auteur / Author manuscript Resistance inductionand herbivorevirulence inthe interactionbetween Myzuspersicae (Sulzer) Sauge, M.-H. (Auteurde correspondance), Poëssel, J.-L.,Guillemaud, T.,Lapchin, L.(2011). and amajor aphidresistance gene (Rm2) frompeach. Arthropod Plant Interactions, 5(4), tendency as estimated by aCoxproportionalmodel ( asestimated hazards by tendency Estimated regression coefficients ( Estimated coefficients regression = 167,d.f. = 30, Table 4 Version préliminaire dumanuscrit/ Preliminaryversion ofthemanuscript ratios [exp( the baseline hazard (clone Got the baselinehazard(clone to compared likelihood ratio test. *,**,***,levelsofsignificanceas Covariates Covariates –Car 1 –Avi 4 –Car 13 –Car 7 –Car 12 –Car 9 –Got 6 –Got 3 –Car 5 –Avi 1 –Got 8 –Car 10 –Got 2 –Got 5 –Got 4 –Avi 6 –Avi 2 –Avi 3 –Car 4 –Got 7 –Car 2 –Car 15 –Car 3 –Car 11 –Avi 5 –Car 6 –Car 14 –Car 8 –Car 16 –Mp03 Effect of the genotype of Effect ofthegenotype β )] for the covariates of the model. ofthe )] forthecovariates P 1.302 0.942 0.750 0.639 0.509 0.419 0.388 0.375 0.365 0.307 0.296 0.288 0.288 0.242 0.228 0.208 0.197 0.189 0.149 0.122 0.047 0.043 0.008 -0.003 -0.028 -0.053 -0.077 -0.086 -0.094 -0.692 β 369-377. , DOI : 10.1007/s11829-011-9141-8 < 0.0001)

Comment citer cedocument: 1) fortheat coefficients SE ( 0.202 0.202 0.201 0.201 0.201 0.201 0.201 0.201 0.200 0.201 0.200 0.200 0.200 0.201 0.209 0.201 0.200 0.201 0.200 0.201 0.201 0.204 0.201 0.201 0.200 0.202 0.200 0.203 0.202 0.205 β ), standard errors(SE)andhazard ), β Myzus persicae Myzus ) exp (

3.679 *** 2.567 *** 2.119 *** 1.895 ** 1.664 * 1.521 * 1.475 1.456 1.442 1.360 1.345 1.334 1.334 1.275 1.257 1.232 1.218 1.208 1.161 1.131 1.048 1.044 1.009 0.996 0.972 0.948 0.926 0.917 0.909 0.500 *** β χ ) 2 on theplant-leaving correspond toa P <0.05, 0.01 + + + + + + no effect no effect no effect no effect no effect no effect no effect no effect no effect no effect no effect no effect no effect no effect no effect no effect no effect no effect no effect no effect no effect no effect no effect – tendency leaving Effect on n = 1550, = 1550, χ