ContentslistsavailableatScienceDirect
Journal
of
Plant
Physiology
j o u r n a l ho me p a g e : w w w . e l s e v i e r . c o m / l o c a t e / j p l p h
Review
article
The
interactive
effects
of
simultaneous
biotic
and
abiotic
stresses
on
plants:
Mechanistic
understanding
from
drought
and
pathogen
combination
Venkategowda
Ramegowda
a,1,
Muthappa
Senthil-Kumar
b,∗aDepartmentofCropPhysiology,UniversityofAgriculturalSciences,Bangalore,560065,India bNationalInstituteofPlantGenomeResearch(NIPGR),ArunaAsafAliMarg,NewDelhi110067,India
a
r
t
i
c
l
e
i
n
f
o
Articlehistory:Received31August2014 Receivedinrevisedform 29November2014 Accepted29November2014 Availableonline18December2014
Keywords: Drought Pathogen Simultaneousstress Tailoredresponse
a
b
s
t
r
a
c
t
Innature,plantsaresimultaneouslyexposedtoacombinationofbioticandabioticstressesthatlimit cropyields.Onlyrecently,researchershavestartedunderstandingthemolecularbasisofcombinedbiotic andabioticstressinteractions.Evidencessuggestthatundercombinedstressplantsexhibittailored physiologicalandmolecularresponses,inadditiontoseveralsharedresponsesaspartoftheirstress tolerancestrategy.Thesetailoredresponsesaresuggestedtooccuronlyinplantsexposedtosimultaneous stressesandthisinformationcannotbeinferredfromindividualstressstudies.Inthisreviewarticle, weprovideupdateontheresponsesofplantstosimultaneousbioticandabioticstresses,inparticular droughtandpathogen.Simultaneousoccurrenceofdroughtandpathogenduringplantgrowthprovokes complexpathwayscontrolledbydifferentsignalingeventsresultinginpositiveornegativeimpactof onestressovertheother.Here,wesummarizetheeffectofcombineddroughtandpathogeninfection onplantsandhighlightthetailoredstrategiesadaptedbyplants.Besides,weenumeratetheevidences frompathogenderivedelicitorsandABAresponsestudiesforunderstandingsimultaneousdroughtand pathogentolerance.
©2014TheAuthors.PublishedbyElsevierGmbH.ThisisanopenaccessarticleundertheCC BY-NC-NDlicense(http://creativecommons.org/licenses/by-nc-nd/3.0/).
Contents
Introduction... 48
Responseofplantstosimultaneousbioticandabioticstresses... 48
Combineddroughtstressandpathogeninfectionexerteitherpositiveornegativeeffectonplants... 48
Earlyresponseofplantstodroughtstressaffectspathogeninfection... 49
Earlyresponseofplantstopathogenaltersdroughtstresstolerance... 49
Pathogen-derivedelicitorsalterplantresponsetodroughtstress... 50
Plantsexposedtocombineddroughtstressandpathogeninfectionexhibittailoredmolecularresponses... 50
ABAplayspositiveroleinpre-invasivedefense... 52
Conclusionsandoutlook... 52
Conflictofinterest... 53
Acknowledgments... 53
References... 53
∗Correspondingauthor.Tel.:+911126735229.
E-mailaddresses:[email protected](V.Ramegowda),[email protected](M.Senthil-Kumar).
1 Presentaddress:DepartmentofCrop,SoilandEnvironmentalSciences,UniversityofArkansas,Fayetteville,USA.
http://dx.doi.org/10.1016/j.jplph.2014.11.008
0176-1617/©2014TheAuthors.PublishedbyElsevierGmbH.Thisis anopenaccessarticleundertheCCBY-NC-NDlicense(http://creativecommons.org/licenses/ by-nc-nd/3.0/).
48 V.Ramegowda,M.Senthil-Kumar/JournalofPlantPhysiology176(2015)47–54
Introduction
Plants are often exposed to diverse environmental stresses andhaveacquiredspecificmechanismstocombatthesestresses. Overthepastdecade,themolecularmechanismsunderlyingbiotic
and abiotic stress tolerance have been intensely studied with
muchemphasisontolerancemechanismspertainingto
individ-ualstresses(Abuqamaretal.,2009;Mengisteetal.,2003;Suzuki etal.,2005).Besides,existenceofcrosstalkbetweenplants inde-pendentlyexposedtobioticandabioticstressesandtheirpositive (cross-tolerance)ornegativeinfluenceonplantshavebeenshown (Abuqamaretal.,2009;Fujitaetal.,2006;Jakabetal.,2005;Ton etal.,2005)(SupplementaryTableS1). Thesestudieshave pro-videdavenuesforimprovementofplantsforcombatingmultiple individualstresstolerance(SupplementaryTableS2)(Maoetal., 2010;Sreenivasuluet al.,2007).Recently, geneexpressiondata fromindependentbioticandabioticstressexperimentshavebeen exploredto identifysharedstress-responsive genes (Luo et al., 2005; Narsai et al., 2013; Shaik and Ramakrishna,2013, 2014; Sharmaetal.,2013;Tippmannetal.,2006).However,innature, plantsareoftensimultaneouslychallengedbymultiplebioticand abioticstresses.Plantstoleratingtwoormoreindependently occur-ringstresses need not necessarily toleratethese stresses when they occursimultaneously (Atkinson and Urwin, 2012; Collins etal.,2008; Mittler,2006;Mittlerand Blumwald, 2010; Nostar etal.,2013).Recentevidencessuggestthatplantshavethe abil-itytocopewithsimultaneousbioticandabioticstressesthrough exhibitionoftailoredresponses(SupplementaryTableS2)which cannotbeunderstoodbydirectlyextrapolatingtheresultsfrom individualstress studies where each stress is applied indepen-dently(AtkinsonandUrwin,2012;Atkinsonetal.,2013;Bostock etal.,2014;Kissoudisetal.,2014;PraschandSonnewald,2013, 2014;Rasmussenetal., 2013;Riveroetal., 2013;Suzuki etal., 2014).Despitetheneedforunderstandingsimultaneousbioticand abioticstresstoleranceofplants (SupplementaryTableS2), not manystudieswereundertakeninthisdirection.Inthisreview arti-cle,wereportcomprehensiveliteratureinformationoncombined
droughtand pathogeninteraction, and provide future research
prospectsfor mechanisticunderstandingof simultaneousstress tolerance.
SupplementaryTablesS1andS2relatedtothisarticlecanbe found,intheonlineversion,athttp://dx.doi.org/10.1016/j.jplph. 2014.11.008.
Responseofplantstosimultaneousbioticandabiotic
stresses
Theeverchangingclimaticfactorsincreasethechancesof occur-renceof abiotic stresses in future. Evidences also suggest that theclimatechangewillalsoexpandthehostrangeofpathogens withincreasedchancesof virulent strain development(Garrett et al.,2006).Therefore, the occurrence of combined biotic and abioticstressislikelytobehigherinfuture.Althoughthe inter-actionbetweenbioticandabioticfactorsinplantswasanalyzed in the past several years through extrapolation of information fromindividualstressresponses,yet,thephysiologicaland molec-ularresponsesthatoccurinplantsexposedtoa combinationof simultaneousbioticandabioticstressesremainelusive.The avail-able evidences indicate that simultaneous occurrence of biotic andabioticstressescancauseeitheranegative(i.e., susceptibil-ity)orpositive(i.e.,tolerance)effectonplantsdependingonthe stressandpathogenunderstudy(Tippmannetal.,2006).Reports oncombinedpathogenandhightemperaturestressindicatethat hightemperature increasesthe diseasesusceptibility of plants. In tobacco(Nicotianatabacum)and pepper (Capsicumannuum),
hightemperaturesuppresseditsresistancetoTobaccomosaicvirus
(TMV)andTomatospottedwiltvirus(TSWV),respectively(Király etal.,2008;Mouryetal.,1998).Theincreaseinspotblotch(caused by Cochliobolus sativus) severity observed in wheat genotypes wascorrelatedwithanincrease inaveragenighttime tempera-turesinanexperimentconductedover sixyears(Sharmaetal., 2007).InArabidopsisandN.benthamiana,bothbasalandthe resis-tance(R)-gene-mediateddefenseresponsesagainstPseudomonas syringaewereinhibitedunderhightemperature(Wangetal.,2009). Hypersensitiveresponse(HR)inducedbyR-genesagainstPotato
virus X (PVX)and TMVwas also delayed in plants exposed to
hightemperaturestress(Wangetal.,2009).Thesestudies indi-catethatbothbasalandtheR-gene-mediateddefenseresponses
aresuppressedduringcombinedhightemperatureandpathogen
infection,andthistrendisnotseeninplantsexposedtoindividual stresses.
Contrasttotheabovementionedstudiesonincreased suscep-tibility,severalotherstudiesdocumentedresistanceresponsesof plantsduringcombinedbioticandabioticstresses.Occurrenceof hightemperaturestressincombination withPucciniastriiformis
(causalagentofstriperust)infectionenhanceddiseaseresistance inspringwheat(Triticumaestivum)(Carteretal.,2009).Salinity stressalsoincreasedresistanceofbarley(Hordeumvulgare)plants toBlumeriagraminis(causalagentofpowderymildew)ina con-centrationdependentmanner(Wieseetal.,2004).Salinitystress canexertbothosmoticandiontoxicityeffectpotentially
restric-tingthepathogengrowth.Exposureof rice plantstocombined
droughtstressandplant-parasiticnematodeinfectionameliorated theseverityofdroughtstress(AtkinsonandUrwin,2012).Taken together,thesestudiesindicatethatduringsimultaneousbioticand abioticstresses,plantsexhibitacomplexanddifferentialresponse leadingtoresistanceorsusceptibilityofplants.
Combineddroughtstressandpathogeninfectionexert
eitherpositiveornegativeeffectonplants
Among severalbiotic and abiotic stress combinations,plant interactionwithsimultaneousdroughtstressandpathogenisone ofthewell-studiedcombinations(Carteretal.,2009;Királyetal., 2008;Mayek-Perezetal.,2002;McElroneetal.,2003;Ramegowda etal.,2013a;Sharmaetal.,2007;Wangetal.,2009;Xuetal.,2008). Unlikeotherbioticandabioticstresscombinations,theoccurrence ofpathogen-droughtstresscombinationisnot instantaneousas droughtstressdevelopsgradually.Inthefieldsituation,duringthe courseofdroughtstressdevelopment,pathogenscaninfectplants ordroughtstresscanoccuronalreadypathogeninfectedplants
resultinginplants havingtodealwithcombinedpathogenand
droughtstress.Theoutcomeofthisinteractionvariesdependingon theseverityofeachstress(Achuoetal.,2006;McElroneandForseth, 2004;Olsonetal.,1990;Xuetal.,2008).Thefollowingscenario explainshowseverityofonestressinfluencestheplantresponses tocombinedstress(Fig.1;topmiddlepanel).Plantsexposedtomild droughtstressactivatethebasaldefense(SupplementaryTableS2) responsewhichenablesplanttodefendthepathogeninfection.On thecontrary,severedroughtcausesleakageofcellularnutrients intoapoplastwhichfacilitatessuccessfulpathogeninfection.Oneof thepossiblereasonsforcombinedtoleranceistheinherentcapacity ofplantstotailortheexistingmechanisms.Ontheotherhand,the susceptibilitycouldbeduetoinabilitytotailortolerance
mech-anismsandmostimportantly,potentialexacerbationofdamage
causedbyonestress.Thisscenariogetsfurthercomplicatedwhen severalstressesoccuratthesametime.Abscisicacid(ABA),the primaryregulatorofdroughtstressresponseisalsoknowntoalter pathogenresponseofplants.Inthefollowingsections,we com-prehendtheavailableliteratureinformation andenumeratethe
Fig.1. Potentialphenotypicresponseofplantsexposedtocombinationofdroughtstressandpathogeninfection.Topleft:Pathogeninfectiononalreadydroughtstressed plantscaneitherresultinplantresistancetopathogenthroughdrought-inducedactivationofbasaldefenseorcanresultinsusceptibilityduetoweakenedbasaldefense. Drought-inducedpathogenresistanceispresumablyduetoenhancedinductionofantimicrobialandPR-proteinsactivatedbydrought.Thesecompoundscanprotectplants duringearlystagesofpathogeninfection.ThesusceptibilitycouldbeattributedtohighlevelsofABAindroughtstressedplantswhichcaninterferewithpathogen-induced plantdefensesignalingandtherebyreducetheexpressionofdefense-relatedgenes.Topmiddle:Exposureofplantstosimultaneousdroughtstressandpathogeninfection canresultintolerancetobothstressesduetoinherentabilityofplantstoinduceuniquetailoredstrategies.Oncontrary,itcanalsomakeplantsmoresusceptibletoboththe stressesduetoweakenedfitnessofplantsduetoexacerbationofdamagecausedbyonestressonother.Topright:Exposureofpathogeninfectedplantstodroughtstress canresultintheirtolerancetodroughtstressthroughpathogen-inducedsalicylicacid(SA)-dependentROSsignaling.Conversely,itcanalsoresultinsusceptibilityofthe plantstodroughtstressduetoSAorjasmonicacid(JA)-mediatedreductioninresponsivenessofplantstoabscisicacid(ABA).Bottomleft:IncreaseinABAconcentration beforepathogentreatmentcaneitherpreventpathogeninvasionthroughstomatalclosureorABAcanmakeplantsmoresusceptibletopathogenbysuppressingJAorSA orethylene-mediatedsignaling.Dottedlinearrowanddottedlineboxindicatespossibleacclimation(seeGlossary)ornoacclimationresponseofplants,respectively;solid lineboxesindicatepossiblemolecularandbiochemicalresponseofplantstostresscombination.
possibleresponsesofplantstothecombinationofsimultaneous droughtstressandpathogeninfection.
Earlyresponseofplantstodroughtstressaffectspathogen infection
Under drought stress, plants could become vulnerable to
pathogens (Fig. 1; top left panel). Infection of Xylella fastidiosa
(causalagentofbacterialleafscorch)onParthenocissus quinque-foliaplantsgrownunderlowsoilmoisturelevelsresultedinsevere scorchsymptomsinleavesinadditiontoreducedtotalleafarea, shootlength,leaf water potentialand stomatalconductance as
compared topathogen alone infected plants grown under
nor-mal soil moisture (McElrone et al., 2001, 2003; McElrone and
Forseth,2004).Similarly,simultaneousexposureofcommonbean (Phaseolusvulgaris)plantstodroughtstressandafungalpathogen,
Macrophominaphaseolina(causalagentofcharcoalrotandseedling blight)resultedinhighertranspirationrateandleaftemperatureas comparedtoplantssubjectedtoonlydroughtstress(Mayek-Perez etal.,2002).Hybridpoplar(Populusnigra×P.maximowiczii)grown underdroughtstressandinfectedbySeptoriamusiva(causalagent ofleafspotandcankerdiseases)developedlargercankers(Maxwell etal.,1997).Also,redpines(Pinusresinosa)grownundermoderate droughtstressweresusceptibletovariousisolatesofSphaeropsis sapinea(causalagentofblight)(Blodgettetal.,1997).Itappears thatthesepathogensattackplantsgrowingunderstressful condi-tionswhentheirbasalprotectionmechanismisweakenedcausing furtherdamagetotheplants(Kendigetal.,2000).
Conversely,droughtstressedplantswereshowntoresistcertain
pathogenswhichrequireconsistentwetorhumidenvironmental
conditions(Fig.1;topleftpanel).Intomato,droughtstressreduced
fungal pathogen, Botrytis cinerea (causal agent of gray mold)
infection by50% and also suppressedspread of anotherfungal
pathogen,Oidiumneolycopersici(causalagentofpowderymildew) (Achuoetal.,2006),duetoconcomitantincreaseinendogenous
ABA levels. Drought acclimated N. benthamiana plants showed
lessdiseasesymptomsuponinfectionwiththefungalpathogen,
Sclerotiniasclerotiorum(causalagentofwhitemold),andthe bac-terialpathogenP.syringaepv. tomato(causalagentof bacterial speck)comparedtowell-wateredplantsinfectedwithpathogens (Ramegowdaetal.,2013a).Consistently,increasedreactiveoxygen species(ROS)levelsandinductionofPR-proteinencodinggenes
were observed in theseplants indicating ROS-mediated
oxida-tiveburstandPR-proteinshavecontributedfordiseaseresistance incombinedstressedplants(Ramegowdaetal.,2013a).Here,it appearsthatearlyexposureofplantstodroughtstressresultsin onsetofdroughtstressresponsessuchasincreasedABAandROS levelswhichplayantagonisticroleinsuppressingorminimizing theeffectofpathogeninfection(Fujitaetal.,2006;Mauch-Mani andMauch,2005).
Earlyresponseofplantstopathogenaltersdroughtstress tolerance
Pathogen-infectedplantscanexhibiteitherincreased suscepti-bilitytodroughtstressasaconsequenceofweakenedbasaldefense
50 V.Ramegowda,M.Senthil-Kumar/JournalofPlantPhysiology176(2015)47–54
orenhanced droughttoleranceasa resultof pathogen-induced
priming(SupplementaryTableS2)(Fig.1;toprightpanel)(Conrath etal.,2002;Tonetal.,2005;TonandMauch-Mani,2004;van Hul-tenetal.,2006).Forexample,Maizedwarfmosaicvirus(MDMV) infected sweet corn plants (Zea mays var. saccharata) simulta-neouslyexposedtodroughtstressshowedmorereductioninear weight,leafareaandplantheightcomparedtonon-infectedplants (Olsonetal.,1990).MDMV-inducedyellowingofleavescouldbe
one of the reasons for reduced growth and yield of this virus
infected plants under combined stress. Simultaneous exposure
ofArabidopsisplantstodrought,andTurnipmosaicvirus(TuMV) resultedinhigherreductioninplantweightandleafnumberunder stresscombinationcompared toindividualstresses(Praschand Sonnewald,2013).Hereearlyinfectionofthesepathogenscauses chloroticlocallesions,mosaicandmottling.Consistently photosyn-theticcapacityisreducedtoshieldfromsubsequentdroughtstress
inducedROSdamage.
Incontrast, anotherstudyoncombined stressprovided evi-dencesforpathogen-induceddroughttolerance(Fig.1;topright panel).N. benthamianaplants infected withBrome mosaic virus
(BMV),Cucumbermosaic virus(CMV)and TMVshoweddelayed
appearance of leaf wilting and stem dehydration under
com-binedvirusanddroughtstresscomparedtoonlydroughtstressed plants (Xu etal., 2008).BMV and CMV-infectedplants showed increasedaccumulationofosmoprotectantslikeglucose,fructose andsucrose.Inaddition,virusinfectedplantsalsoshowedlower transpirationrateduetopartialstomatalclosureresultingin bet-terwaterretentioninleaftissues.Conceivably,themetabolicand
physiological changes due to virusinfection combateddrought
stresseffectsandtherebyimpartedcombinedstresstolerancein thisstudy.
Pathogen-derivedelicitorsalterplantresponsetodroughtstress
Some bacterial pathogen-derived elicitors (Supplementary
TableS2)havethepotentialtoaffectdroughttoleranceinplants.
These can be used to mimic pathogen infection and to study
simultaneousdroughtandpathogeneffectsonplants.Exogenous applicationofpurifiedErwiniaamylovoraharpinproteinondrought stressedArabidopsisleavesconferreddroughttolerance.The tol-eranceisduetoconcomitantincreaseinendogenousABAlevels triggeringstomatalclosuretherebyreducingthetranspirationrate (Dongetal.,2005).Purifiedflg22(flagellin22),abiologicallyactive 22-aminoacidpeptidederivedfromconservedN-terminalregion of flagellin, and a bacterial lipopolysaccharide (LPS), conferred
drought tolerance in Arabidopsis plants through ABA-mediated
stomatal closure (Melotto et al., 2006). Similarly, Pseudomonas chlororaphissecretedvolatilemetabolite2R,3R-butanediolinduced droughttoleranceinArabidopsisthroughearlyclosureofstomata (Choetal.,2008).Pathogen-derivedmoleculeshavethepotential
toinducesomeimmuneresponsessimilartopathogeninfection
andtheycanhelpinpreciselycoincidingsimultaneousstress treat-ments(BonasandLahaye,2002;Montesanoetal.,2003;Rasmussen etal.,2013).Taken together,thesestudieshighlightthe impor-tanceofbacteria-derivedmoleculesinunderstandingtheeffectof simultaneousdroughtandpathogenonplants.
Plantsexposedtocombineddroughtstressandpathogen
infectionexhibittailoredmolecularresponses
Sofar,onlyonestudydocumentedtheglobaltranscriptomeand metabolomechangesinplantssimultaneouslyexposedtodrought
stressand pathogeninfection.Transcriptomicand metabolomic
analysesofArabidopsisplantssimultaneouslyexposedtodrought stress,heatandTuMVinfectionshowedseveraltailoredresponses
Fig.2.Transcriptomeanalysisinplantsexposedtodroughtstressalone,virusalone anddroughtstressandviruscombination–acasestudy.(a)Numberofgenes differ-entiallyexpressedinindividualstresses(droughtstressorvirusinfection)andstress combination(droughtstressplusvirusinfection)areshown.Amongthe differen-tiallyexpressedgenes,severalgeneswerespecifictoeachstress.Indroughtstress andviruscombination,outof1370differentiallyexpressedgenes776werespecific tostresscombination.Numbersinparenthesesaretotalnumberofdifferentially expressedgenesunderthatstresscondition.(b)Specificregulatorygeneswithmore than2-foldup-regulationduringdroughtstressplusvirusinfectionareshown.Data usedforanalysisweretakenfrompreviousliterature(PraschandSonnewald,2013) andreanalyzedusingBioConductorpackageinRstatisticalprogram(Gentleman etal.,2004)toconverttheprobeIDsintoAGIgeneIDs.Genesymbolsnotwell definedinliteraturearemarkedingray.
(PraschandSonnewald,2013).Virusalonetreatmentenhancedthe expressionofdefensegenes,whichwasabolishedinplantsexposed toa combinationofvirus,heatand droughtstress.Further,this triplestresscombinationsuppressedtheR-gene-mediateddefense responseandincreasedtheendoplasmicreticulumboundunfolded
proteinresponse(UPR)pathway,whichwerenotobservedunder
individualstresses.Reanalysisofthetranscriptomedatafromvirus anddroughtstressexperimentsusingBioConductorpackageinR (Gentlemanetal.,2004)revealedthatthenumberofgenes differen-tiallyexpressedunderindividualdroughtstressandvirusinfection was434and539,respectively,butwhenbothstresseswereapplied simultaneously1370genesweredifferentiallyexpressed(Fig.2A). Amongthedifferentiallyexpressedgenesin respectivestresses,
156 genes were unique to drought stress and 99 genes were
uniquetovirusinfection.Interestingly,776differentiallyexpressed geneswereuniquetosimultaneousdroughtstressandvirus infec-tionandarenotrepresentedeitherunderdroughtstressorvirus
infection alone. Many of the stress combination specific genes
highlightedhereencodetranscriptionfactorsandotherregulatory genes(Fig.2B).Individualstressresponseofsomeofthesegenes hasbeenwellstudied.Inparticular,theroleofWRKY transcrip-tionfactorsinmediatingplantbioticandabioticstressresponse throughsalicylicacid(SA),jasmonicacid(JA)orethylenesignaling havebeenwellreported.AtWRKY30hasbeenshowntobeinduced underoxidativestressandpathogenattackanditsoverexpression
Fig.3.Modelforexpectedmolecularresponsesofplantsexposedtoacombinationofdroughtstressandpathogeninfection.Thisrepresentationcomparesthetranscriptome profileofplantsunderrespectiveindividualstresses.Venndiagramisshowntoindicatepossiblegeneregulationscenarios.Inadditiontoseveralsharedgenes,certainnumber ofgenescanbespecificallyregulatedundereachstresscondition.D–genesuniquetodroughtstress;P–genesuniquetopathogen;C–genesuniquetodroughtstressand pathogencombination(tailoredresponse);DP–genessharedbetweendroughtstressandpathogen;DC–genessharedbetweendroughtstressandcombinationofdrought andpathogen;PC–genessharedbetweenpathogenandcombinationofdroughtandpathogen;andDPC–genessharedbetweendroughtstress,pathogenandcombination ofdroughtandpathogen.Genesspecificallyinducedunderstresscombination“C”reflectsthetailoredmolecularmechanismsregulatedinplantssimultaneouslyexposedto droughtandpathogen.Individualstressresponsesofsomeoftheseuniquegenesinducedunderstresscombinationsuggestthatinitialsignalingismediatedbyphytohormones andreactiveoxygenspecies(ROS).ThetoleranceofdroughtstressacclimatedNicotianabenthamianaplantstoPseudomonassyringaepv.tabaciandSclerotiniasclerotiorum
wascorrelatedwithhighlevelsofROS(Ramegowdaetal.,2013a).Thesesignalingmoleculescaninitiatespecificsignaltransductioncascadeinvolvingreceptorlikekinases andreceptorlikeproteinsresultingintheactivationofspecifictranscriptionfactors.Basedontheindividualstressresponsestudies,itcanbepresumedthattheregulatory eventsafterrecognitionsofcombineddroughtandvirusinfectioninvolvessalicylicacid,jasmonicacidandethylenemediatedregualtionofWRKYtranscriptionfactorsand abscisicacidmediatedregulationofAP2/ERFtranscriptionfactors.Thesetranscriptionfactorscanfurtheractivateorsuppressfunctionalgenestherebybringingintolerance orsusceptibilityofplantstosimultaneousdroughtstressandpathogeninfection.CRK–cysteine-richreceptorlikekinases;RLK–receptor-likeproteinkinases;WRKY–WRKY domaincontainingtranscriptionfactors;AP2/ERF–APETALA2/ethyleneresponsefactors;dottedarrowsindicatepossiblesignalingresponse.
inArabidopsisimprovedoxidativeandsalinitystressesduringseed germination(Besseauet al., 2012). Anotherstudy alsoshowed
the role of AtWRKY30 in SA dependent negative regulation of
leafsenescence(Scarpecietal.,2013).Simultaneousknock-outof
AtWRKY18and AtWRKY40geneexpressionresultedinimproved
resistance of Arabidopsis plants to biotrophic powdery mildew
fungusGolovinomycesorontiwhichwasaccompaniedbyaltered
SAandJAsignaling,EDS1genesexpressionandaccumulationof phytoalexincamalexin(Schönetal.,2013).AtWRKY50hasbeen showntomediatebothSA-andlow-oleicacid-dependent repres-sionofJAsignalinginArabidopsis.MutationinAtWRKY50resulted inbothJA-induciblePDF1.2(defensin)expressionandbasal resis-tancetoB.cinerea(Gaoetal.,2011).AtWRKY62hasbeenshown toactdownstream of cytosolicNPR1 which isessential forthe SA-mediatedsuppressionofJA-responsivegeneexpression(Mao etal.,2007).OverexpressionofAtWRKY75inducedoxidativeburst inArabidopsisplants,suppressedthehyphalgrowthofS. sclerotio-rum,andconsequentlyinhibitedfungalinfection.Geneexpression profilingindicatedthatAtWRKY75istranscriptionalregulatorof
SA- and JA or ethylene-dependent defense signaling pathways
(Chen et al., 2013). Furthermore, individual stress response of AP2/ERFtranscriptionfactorsinmediatingbioticandabioticstress
responsethroughABAwasstudied.AtERF11hasbeenshownto
negatively regulateABA-mediated controlof ethylenesynthesis therebyavertingthenegativeeffectofethyleneonplantgrowth anddevelopment(Lietal.,2011).OverexpressionofAtERF13in Ara-bidopsisconferredABAhypersensitivityduringpost-germination growthsuggestingitsroleinABAmediatedstressresponse(Lee et al.,2010).AnotherAP2/ERFtranscription factor,RAP2.6 con-ferredresistanceagainstbeetcystnematodeHeteroderaschachtii
in Arabidopsisroots by enhanced callose depositionin syncytia (Alietal.,2013)andshowedhypersensitivitytoexogenousABA andabioticstressesduringseedgerminationandearlyseedling growthinArabidopsis(Zhuetal.,2010).Inadditionto transcrip-tion factors, individual stress response of upstream regulatory genes such as receptor-like kinases, receptor-like proteins and
protein phosphatases has been reported. CRK7, a cysteine-rich
receptorlikekinase,hasbeenshowntomediateoxidativesignaling induced by apoplastic ROS (Idänheimo et al., 2014). Arabidop-sis receptor-like protein, AtRLP23, wasshown tobe associated
withthe receptor-like kinaseAtSOBIR1 which in turnrequired
forAtRLP30-mediatedresistancetoS.sclerotiorum(Bietal.,2014; Zhang et al.,2013).Roleof AtRLP41 inABA response hasbeen
demonstratedusingknock-outlineswhichshowedenhanced
sen-sitivity to exogenous ABA application (Ellendorff et al., 2008; Wangetal.,2008).PIA1,(PP2CInducedbyAvrRpm1)wasshown
52 V.Ramegowda,M.Senthil-Kumar/JournalofPlantPhysiology176(2015)47–54
tobeinducedbyinfectionofP.syringae expressingtheeffector
AvrRpm1andsubsequentlyactivatedNB-LRR diseaseresistance
protein RPM1 in plant (Widjaja et al., 2010). Taken together
thesereportsshowthat phytohormones ABA,SA,JAand
ethyl-eneplaypivotalroleinmediatingresponseofplantstocombined droughtandpathogeninfection.Wehypothesizethatunder com-binedstresses theearlysignalingeventslikely operatethrough ABA,SA,JAorethylene,howeverthemodulationofstresssignal, crosstalkandsubsequentdownstreameventsarelatertailored.As observedunderdroughtandvirusstresscombination,wespeculate thatplantscandisplaysimilartailoredmolecularresponseswhen exposedtoacombinationofdroughtandbacteriaorfungus.The plausiblesignalingeventsundercombineddroughtandpathogen infectionaregiveninFig.3.
ABAplayspositiveroleinpre-invasivedefense
Apartfromitsroleindroughtandlowtemperaturestress tol-erance(Shinozakietal.,2003),ABAalsomediatesplantdefense responses(Melottoetal.,2006).High ABAconcentration,either duetodrought-inducedaccumulationorexogenousapplicationat thetimeof pathogeninfectionisknowntoaffectplantdisease resistance(Mohr andCahill,2003).ABA canplayboth negative andpositiveroleinplantresponsetopathogeninfection(Fig.1; lowerpanel).HigherlevelsofABAinplantscanrepressdefense geneexpressionbysuppressingthesignalingmediatedbySA,JAor ethylene(Andersonetal.,2004).ExogenousapplicationofABAon
ArabidopsisplantsincreasedthevirulenceofP.syringaepv.tomato ontheseplants(deTorres-Zabalaetal.,2007).Similarly,application ofABAsuppressedthetranscriptionofdefensegeneslikePDF1.2 (plantdefensin1.2),CHI(basicchitinase),HEL(hevein-likeprotein), andLEC(lectin-likeprotein)resultinginsusceptibilityof Arabidop-sisplantstothefungus,Fusariumoxysporum(causalagentofwilt), andtothebacteria,Erwiniachrysanthemi(causalagentofbacterial wilt)infection(Asselberghetal.,2008;Fujitaetal.,2006).The nega-tiveeffectofABAindiseaseresistancehasalsobeendemonstrated usingmutantsdefectiveinABAbiosynthesisandperception.For example,B.cinereainfectionontomatomutants,flaccaandsitiens, deficientinABAbiosynthesisresultedinreducedpathogengrowth (Audenaert et al.,2002).Similarly, Peronospora parasitica infec-tiononArabidopsisABA-deficientmutant,aba1-1,inducedHR-like defenseresponseatthesiteofinoculationandsuchresponsewas notshownbywildtypeplants(MohrandCahill,2003).
ABAexert positive responses predominantly in pre-invasive defense against pathogens by increasingthe penetration resis-tancethroughrapidclosureofstomataasshownbyapplication ofpathogen-derivedelicitorssuchasflg22andLPS(Melottoetal., 2006).Arabidopsis ABA-deficientmutant, aba3-1,failed toclose stomatauponapplicationofpathogen-derived elicitors
suggest-ingthe involvement of ABA-mediatedsignaling in pre-invasive
defense.ABAalsoexertspositiveresponseinearlypost-invasive defense.ExogenousapplicationofABAcontributedtothe resis-tanceofArabidopsisplantsagainstthefungalpathogens,Pythium irregulare(causalagentofdamping-off),andAlternariabrassicicola
(causalagentofdarkleafspot)(Adieetal.,2007),andbarleyplants againstthefungusBlumeriagraminisf.sp.hordei(causalagentof powderymildew)(Wieseetal.,2004).Conceivably,theenhanced resistanceobservedinthesestudiesisduetoreducedpathogen spreadachievedbyABA-mediatedcallosebiosynthesisor inhibi-tionofitsdegradation(Jacobsetal.,2003;Rezzonicoetal.,1998).
Conclusionsandoutlook
Theresponseofplantstoacombinationofbioticandabiotic stresses is complex involving interaction of various signaling
pathways.Plantresponsetostresscombinationisaffectedbythe typeofabioticstressandthepathogeninvolved.Bothsusceptible
and tolerantresponseswereobserved in plantssimultaneously
exposedtodroughtandpathogen.However,itisnotclearwhy
someinteractionsresultedintolerancewhileothersleadto sus-ceptibility.Mostofthestudiesreportedherewereconductedatthe fieldlevel.Plantstage,severityanddurationofeachstress,effectof stresscombinationatthecellularlevelandwhetherthegivenstress combinationsweresimultaneousorsequentialarenotwell estab-lishedinmostofthesestudies.Thoughtheextentofcropdamage causedbystresscombinationsisknownforalongtime(Mittler, 2006;MittlerandBlumwald,2010),thesestresscombinationsare rarelystudiedatthelaboratorylevel. Substantialinformation is availableonthephysiological,molecular,andmetabolicchanges inplantsexposedtoindividualstresses.Thesestudieshave delin-eatedtheeffectofeachstressatcellularaswellasplantlevelby exposingplantstodifferentstressintensitiesatdifferentgrowth stagesundercontrolledlaboratoryconditionsandtheresultshave
been translated to field situation (Atkinson and Urwin, 2012;
Mittler,2006;Suzukietal.,2014).However,thisknowledgeis lim-itingundercombinationofstresses.Thereislacunaindelineating thecontributionofindividualstressesandstresscombinationand alsochallengesin accuratecombinedstressimposition(Lawlor, 2013).Thereforestresscombinationneedtobehandledasa differ-entstateofstressandstudiedatthelaboratoryleveltoadequately exploretheinteractions.Inaddition,italsorequiresarepositoryof combinedstressinteractionsusingpastliteratureandallowusers toknowwhatpathogencausespositiveornegativeinteractionon droughtonwhatplantspeciesatwhatstresslevel.
Responseofplantstoacombinationofdroughtandpathogen stronglydependsonthecropinvolved,developmentalstageand intensity and duration of each stress. Therefore, precise stress impositionatspecificgrowthstageofplantsisneededforbetter understandingofthecombinedstresseffects.Asmentionedbefore, occurrenceofdroughtstressunderfieldsituationisnot instan-taneous,ratherdevelopsoveraperiodoftimedependingonthe
vaporpressuredeficitofthegrowingenvironment.Mostofthe
studiesreportedherewereconductedatthefieldlevel.Though
droughtandpathogeninfectionhad coincidedatsomestagein
thesestudies, thestress imposition wassequential rather than
simultaneous. Thesestudies suggest thatsimultaneous drought
andpathogenapplicationisdifficultevenunderthelaboratory con-ditionsusingsoildryingmethods.Analternativemethodwould
beexploitationofprimingresponseofphytohormonesor
chem-icalswhichmimicdroughtandpathogeninfection.Thiswillhelp
bettermanagementofsimultaneousdroughtandpathogen
combi-nationunderlaboratoryconditions.Forexample,combinedstress canbeappliedaccuratelybyusingABAtomimicdroughtstressand pathogen-derivedelicitorstomimicpathogeninfection.Similarly, exogenousJAorSAcanbeusedtoinducesomedefenseresponses relatedtopathogeninfection(Anticoetal.,2012;Singhetal.,2004).
An increasing number of studies suggest that plants have
evolved tailored strategies to combat simultaneous stresses
(Pandeyetal.,2014).Thoughthefinalcellularresponseofplants isexpectedtobespecifictostresscombinations,theperception
andsignaltransductioneventscouldbeoperatedthroughsome
knownsignalingcomponents.Thesesignalingcomponentsinclude hormonesignals,receptorsandtranscriptionfactors.However,our
knowledge onrole of these signalingcomponents understress
combinationislimited,therefore,furtherstudiesarerequiredto
understandthesemechanisms.Transcriptome,metabolome and
proteomicapproachescanbeusedtorevealsignalingeventsunder combinationofdroughtandpathogeninfection.Ahighthroughput functionalgenomicapproachsuchasvirus-inducedgene silenc-inginassociationwithhighthroughputstresseffectquantification
(Ramegowdaetal.,2013b;Senthil-KumarandMysore,2011).Key playersidentifiedfromtheseapproachescanbeusedtodevelop cropplantstoleranttosimultaneousstresses.
Conflictofinterest
Theauthorshavenoconflictofinteresttodeclare.
Acknowledgments
ProjectsatMS-KlabaresupportedbyNationalInstituteofPlant
GenomeResearchcorefundingandDBT-Ramalingaswamire-entry
fellowship grant (BT/RLF/re-entry/23/2012). Authors thank Mr.
Chirag Gupta for bioinformatics help. Authors also thank Mr.
MehanathanMuthamilarasanandDr.ClemenciaM.Rojasfor criti-calreadingofthemanuscript.
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