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Climate Change and Insect Pests: Resistance Is Not Futile? PDF

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Spotlight [32_TD$DIFF] Climate Change and 350millionyears.Plantsdeployanarse- effectors, some plant biotypes nal of physical and chemical defences [41_TD$DIFF][possessing R (resistance) genes[42_TD$DIFF]] can Insect Pests: againstherbivorousinsects,towhichher- produceRproteinsthatrecogniseinsect Resistance Is Not bivores evolve counter-adaptations. In effectors and activate effective down- turn,plantsmaythemselvesevolveadap- stream defence pathways, leading to Futile? tationstocopewithadaptedherbivores. effectortriggeredimmunity(ETI,Figure1[43_TD$DIFF] Scott N. Johnson1,* and Within the last decade, common frame- B) [7]. In essence, PTI is based on non- works have emerged for investigating specific recognition of common PAMPs Tobias Züst2 such plant[37_TD$DIFF]–insect interactions [6] and can be suppressed or hijacked by (Figure 1). Plants generally perceive aphideffectors,whereasETIisprompted Chemical signals produced by attackers using pattern recognition bytherecognitionofspecificcompounds plants when attacked by herbi- receptors(PRRs)uponcontactwithcon- associatedwiththeherbivore’sattempts voresplayacrucialroleinefficient served patterns of molecules associated to manipulateplant defences [7,8]. plantdefence.Arecentstudysug- with the attacker; microbial/pathogen/ gests that herbivore-specific R- herbivore–associatedmolecularpatterns Plant [44_TD$DIFF]Resistance and Climate generesistancemaybeenhanced (MAMPs, PAMPs, HAMPs respectively) Change byelevatedatmosphericCO con- [7] [38_TD$DIFF]{for consistency with Sun et al. [5] Significantly, these specific resistance 2 centrations. Understanding how weadopt(P)athogenversionsoftheacro- mechanisms have not been widely climatechangeaffectsplantresis- nymsfromhereon[39_TD$DIFF]}.ThisleadstoPAMP- studiedinthecontextofclimatechange, triggered immunity (PTI) involving activa- eventhoughtheymaycontributetoexist- tance to herbivorous pests could tion of downstream phytohormone- ing crop resistance to insect pests. be essential for future food dependant signalling pathways as key Breakdown of such resistance could security. regulators of plant resistance to arthro- therefore leave crops more susceptible Withhumanpopulationsexpectedtoreach pod herbivores: the jasmonic acid (JA) toherbivores,impactingproductivityand 11.2 billion by 2100,global food security pathwayactivatesresistanceagainsther- potentiallyfoodsecurity[2].Thestudyof hasbecomeanurgentpriority.Insectpests bivores (especially chewing herbivores), Sunetal.[5]issignificantbecauseitis,to currently reduce crop productivity world- while the salicylic acid (SA) pathway is our knowledge, the first [45_TD$DIFF]to provide a widebyanaverageof14%[1].Asmany involved inresistanceagainstpathogens mechanismbywhiche[CO2]couldaffect pests are anticipated to become more [8]. Many adapted herbivores produce ETI and PTI defences. The study problematic with climate change ([33_TD$DIFF]we effectors (e.g. orally secreted proteins) compared resistance of Medicago trun- include increases in atmospheric carbon that modulate plant defensive pathways catula to the pea aphid (Acyrthosiphon dioxide [34_TD$DIFF]in this) [2], achieving global food andmaysuppressormanipulatePTI[7]. pisum) using two plant genotypes with securitymustinvolveeffectivecropprotec- Aphids are particularly successful in this different resistance strategies. One (cv. tion.Aphidsalreadycausesignificantdam- regard,oftenproducingmultipleeffectors Jester)possessesanR-genewhichcon- agetomanycropplantsataglobalscale intheirsaliva[9].Becauseoftheirunique fers resistance to some Australian A. [3], and comparative meta-analyses mode of feeding, aphids mostly trigger pisum clones, and therefore Jester pre- [35_TD$DIFF](e.g.[4])usuallyshowthataphidsbenefit SA-mediated responses in their host dominantlyexpressesETIresistance;the from elevated concentrations of carbon plant, even though JA-mediated defen- other(A17)doesnotpossesstheR-gene dioxide(e[CO ])comparedtootherherbiv- ceswouldoftenbemoreeffectiveagainst andshouldrelyprimarilyonPTIresistance 2 orous groups (though not universally). A them[3].Aphidsmaythusactivelyinduce [5]. Environmental stress (e.g. drought, recent study by Sun et al. [5], however, theSApathwaytosuppressJA-mediated salinity and temperature) can affect R reported that some plants may resist defences via phytohormonal crosstalk generesistance,withtwostudiesinara- aphidsmuchbetterundere[CO ]because (Figure1[40_TD$DIFF]A).However,itshouldbenoted bidopsis(Arabidopsisthaliana)linkingthis 2 ofincreasedresistance(R)geneactivity. that SA-mediated defences provide to reduced R protein activity and down- potent aphid resistance in some plants, stream signal transduction [46_TD$DIFF](see [5] for Plant [36_TD$DIFF]Resistance to Herbivores – thus an [30_TD$DIFF]upregulation of the SA pathway references).Centraltothisisthefactthat a Co-evolutionary Arms Race may not be universally beneficial for the R protein structure and the initiation of Plantsandherbivorousinsectshavebeen aphid [3]. In response to the aphid’s signaltransductionofETIdefencesrelies lockedinaco-evolutionaryarmsracefor manipulation of plant defences with on a specific subclass of heat-shock TrendsinPlantScience,May2018,Vol.23,No.5 367 (A) (B) PAMPs PAMPs A17 Jester PRR PRR Effectors Effectors SERK SERK= R gene Heat-shock Heat-shock MAPK signalling proteins MAPK signalling proteins CDPK HSP90 CDPK HSP90 MEKK1 MEKK1= R proteins SA JA SA JA ROS = ROS = Ubiqui(cid:415)n proteolysis = Ubiqui(cid:415)n proteolysis Figure 1. [30_TD$DIFF]Simplified Depiction of Defensive Responses of Plants Challenged by Herbivores Involving Various Components of the Signalling Pathway.(A)PAMP(Pathogen-AssociatedMolecularPattern)-triggeredimmunity(PTI):PAMPs(andsomeherbivore-associatedmolecularpatterns,HAMPs)are recognisedbytheplant’sPatternRecognitionReceptors(PRR),whichinitiatemitogen-activatedkinases(MAPK)signallingcascadesthatresultintheupregulationof salicylicacid(SA)-mediateddefence.AphidsmayinjecteffectorsintotheplanttosuppressPTIwheretheyaresusceptibletoSA-mediateddefences.Conversely,where theyaremoresusceptibletojasmonicacid(JA)-mediateddefences,aphidsmayuseeffectorstoactivelystimulatePTI,therebysuppressingJAviaphytohormonal crosstalk(bluntarrows).Upward(yellow)anddownward(red)arrowsindicateincreasedanddecreasedactivityinresponsetoe[CO2]asreportedbySunetal.[5]. The=symbolindicatesnochangeinresponsetoe[CO2].InA17plants,e[CO2]increasedPRRandplantkinaseexpression(somaticembryogenesisreceptor-like kinase,SERK;calmodulin-likedomainproteinkinase,CDPK;mitogen-activatedproteinkinasekinasekinase1,MEKK1),resultingin[30_TD$DIFF]upregulationoftheSApathway andsuppressionoftheJA-pathwaytotheaphid’sbenefit.(B)Effector-triggeredimmunity(ETI):Plantswith(resistance)R-gene-basedresistanceproduceRproteins whicharecapableofinterferingwithandrecognisingaphideffectorsanduponrecognition,activateastrongJA-mediateddefenceresponse.Aclassofheatshock proteins(cytosolicheatshockprotein90,HSP90,anditsco-chaperones)canstabilizeRproteins,whichincreasesefficiencyofR-genemediateddefence.InJester plants,e[CO2]enhancedproductionofheatshockproteins,whichfacilitatedRproteinactivityagainsteffectorsand[31_TD$DIFF]upregulationtheJA-pathwayandubiquitin proteolysis,resultinginreducedaphidabundance.Reactiveoxygenspecies(ROS),anothertraitcommonlyassociatedwithherbivoreresistance,wereinducedby aphidfeedingonbothplantgenotypes,butwereunaffectedbye[CO2]. protein(HSP90).WhileHSP90responds to e[CO ], including the PRR gene SGT1), which increased ETI efficiency 2 negativelytotheabioticfactorsabove,it somatic embryogenesis receptor-like andstronglyactivateddownstreamplant can be upregulated under e[CO ] [10]. kinase (SERK) and downstream mito- responses including JA signalling and 2 Theoverarchinghypothesiswastherefore gen-activatedkinases(MAPKs),resulting ubiquitin-mediated proteolysis. Further that e[CO ] could promote HSP90 gene inanactivationofSAsignallingpathways, supportfortheimportanceofheatshock 2 expression in M. truncatula, resulting in but decreases in JA activity (Figure 1[40_TD$DIFF]A). proteinswasprovidedbythesilencingof increased R gene stability and R gene-[47_TD$DIFF] ThissuggeststhatA.pisumactivelystim- the HSP90 gene in Jester plants; JA dependent defences (i.e. ETI) against A. ulates PTI resistance of A17 plants to activity and ubiquitin-mediated proteoly- pisum [5]. suppress a more potent JA response of sis were impaired and the enhanced the plant. In direct contrast, e[CO ] resistance to aphids observed under 2 The abundance of A. pisum was signifi- decreased performance of A. pisum on e[CO ]wasnegated[5]. 2 cantly higher on A17 plants (R gene Jesterplants(Rgenepresent)compared absent) when grown under e[CO ] com- to aphids grown at a[CO ] (Figure 1[49_TD$DIFF]B). Studiesexploringtheeffectofe[CO ]onR 2 2 2 pared to ambient CO (a[CO ]). Simulta- Increased aphid resistance was linked generesistancetoherbivoresarerareand 2 2 neously, several marker genes of PTI totheupregulationofheatshockproteins have so far reported variable responses. resistancewere[48_TD$DIFF]upregulatedinresponse (HSP90) and co-chaperones (RAR1, For example, Rubus idaeus cultivars 368 TrendsinPlantScience,May2018,Vol.23,No.5 possessingtheA Rgenebecamemore We are now at the stage where we raspberryaphidinsomeraspberrycultivars.J.Appl.Ento- 1 mol.135,237–240 susceptible to the European large rasp- shouldaimtorelateherbivoreresponses 12.Zavala,J.A.etal.(2008)Anthropogenicincreaseincarbon berryaphid(Amphorophoraidaei)undere to e[CO ] more directly to generic plant dioxide compromises plant defense against invasive 2 insects.Proc.Natl.Acad.Sci.U.S.A.105,5129–5133 [CO ],whereasresistancetoA.idaeiwas defence signalling pathways that are 2 unchanged for cultivars possessing the common across plant taxa, such as the A R gene [11]. In a case analogous to PTI/ETI model [6]. While the PTI/ETI 10 R-generesistance,e[CO ]causeddown- model [52_TD$DIFF]is an oversimplification, it has Spotlight 2 regulation of genes associated with proved useful for making conclusions Ligands Switch Model defence signalling hormones ethylene about the specificity of plant recognition for Pollen-Tube Integrity (acc) and JA (lox 7, lox 8) in soybean of its antagonists and consequent (Glycinemax)cultivarspossessingcyste- deploymentofplantdefences[8].Aphids, and Burst ine proteinase inhibitors (CystPI, which in particular, could be a good model for interferewithdigestivefunctionsinmany investigatingtheeffectsofe[CO2]onETI Hong-Ju Li1,* and coleopterans). This resulted in reduced and PTI defences against herbivores [53_TD$DIFF]an Wei-Cai Yang1,* productionofCystPIandenhancedper- increasingnumberofRgenesandeffec- formanceoftheJapanesebeetle(Popillia tor proteins are being identified in this In flowering plants, pollen tubes japonica) and western corn rootworm plant–herbivore system. deliver and release the immotile (Diabrotica virgiferavirgifera)[12]. sperms to the female gametes for 1HawkesburyInstitutefortheEnvironment,Western Concluding [50_TD$DIFF]Remarks SydneyUniversity,LockedBag1797,PenrithNSW2751, fertilization, but mechanisms R gene resistance is highly specific and Australia remain unclear. New results show 2InstituteofPlantSciences,UniversityofBern, can be limited to a single clone of an Altenbergrain21,CH-3013Bern,Switzerland thattheRALFfamilypeptidescon- insect species [7]. Sun et al. [5] readily trolpollen-tubeintegrityandburst *Correspondence: acknowledgethislimitationandhighlight by binding to CrRLK1L family [email protected](S.N.Johnson). thatRgenesareineffectiveagainstsome URL:http://www.scott-johnson.org. receptorsandcellwallleucine-rich European clones of A. pisum. Indeed, https://doi.org/10.1016/j.tplants.2018.03.001 repeat extensins. resistance based on single genes is understrongselectivepressureandher- References 1. Ferry,N.andGatehouse,A.M.R.(2010)Transgeniccrop bivores–particularlyaphids,whichhave plantsforresistancetobioticstress.InTransgenicCrop Duringtheadaptiveevolutionofflowering formidable generation rates – can fre- Plants(Kole,C.etal.,eds),pp.1–65,Springer-Verlag plants,spermlostitsmobilityandapollen 2. Gregory,P.J.etal.(2009)Integratingpestsandpathogens quentlyovercomemonogenicresistance tube, which is germinated from the male intotheclimatechange/foodsecuritydebate.JExp.Bot. [3]. ETI defence, for example, can be 60,2827–2838 gametophyte (pollen), was evolved to overcomebyaphidsthroughdiversifica- 3. Züst,T.andAgrawal,A.A.(2016)Mechanismsandevo- deliverthespermstothefemalegameto- lutionofplantresistancetoaphids.Nat.Plants2,15206 tion, modification, or loss of the effector phyte(embryosac).Thestructureofgame- 4. Robinson,E.A.etal.(2012)Ameta-analyticalreviewofthe gene, or by deploying novel effectors to effectsofelevatedCO2onplant–arthropodinteractions tophytesislargelyreduced,withaseven- highlightstheimportanceofinteractingenvironmentaland suppress defences [7]. Predicting the biologicalvariables.NewPhytol.194,321–336 celledembryosacandathree-celledpollen wider significance and consequences 5. Sun, Y. et al.(2018)Elevated CO2 increasesR gene- grain. The embryo sac typically contains ofe[CO ]onplantresistance,particularly dependent resistance of Medicago truncatula against two synergids,one egg, one centralcell, 2 thepeaaphidbyup-regulatingaheatshockgene.New against aphids, is therefore a risky Phytol.217,1696–1711 andthreeantipodalcells.Thesynergidis endeavour. Nonetheless, we regard the 6. Wu,J.Q.andBaldwin,I.T.(2010)Newinsightsintoplant crucial for pollen-tube attraction and responsestotheattackfrominsectherbivores.Annu.Rev. study by Sun et al. [5] to represent an Genet.44,1–24 reception,aswellaspollen-tubeburstto important step forward in addressing 7. Hogenhout,S.A.andBos,J.I.B.(2011)Effectorproteins releasethespermcells.Theseprocesses how climate change might affect thatmodulateplant-insectinteractions.Curr.Opin.Plant require molecular signaling between the Biol.14,422–428 plant[51_TD$DIFF]–herbivore interactions. In particu- pollentubeandthesynergid[1]. 8. Erb,M.etal.(2012)Roleofphytohormonesininsect- lar, this study presents a mechanistic specificplantreactions.TrendsPlantSci.17,250–259 explanation for how e[CO ] is affecting 9. Will,T.etal.(2013)Howphloem-feedinginsectsfacethe Onthefemaleside,multiplecomponents 2 challengeofphloem-locateddefenses.Front.PlantSci.4,336 ETIandPTIdefencesatamolecularlevel crucial for pollen-tube reception in the 10.Li,P.H.etal.(2008)Arabidopsistranscriptandmetabolite and directly relate this to the perfor- profiles:ecotype-specificresponsestoopen-airelevated synergid have been reported. FERONIA mance and feeding behaviour of the [CO2].PlantCellEnviron.31,1673–1687 (FER),amemberoftheCrRLK1Lsubfam- 11.Martin,P.andJohnson,S.N.(2011)Evidencethatele- model herbivore. vated CO2 reduces resistance to the European large ily, regulates the membrane targeting of TrendsinPlantScience,May2018,Vol.23,No.5 369

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