Guard Cell Signal Transduction Netword advances in

ANRV410-PP61-24ARI31March201019:9GuardCellSignalTransductionNetwork:AdvancesinUnderstandingAbscisicAcid,CO2,andCa2+SignalingTae-HounKim,1MaikB¨ohmer,1HonghongHu,NoriyukiNishimura,andJulianI.SchroederUniversityofCalifornia,SanDiego,DivisionofBiologicalSciences,SectionofCellandDevelopmentalBiology,LaJolla,California92093-0116;email:[e-mail],[e-mail],[e-mail],[e-mail],[e-mail].2010.61:561–91FirstpublishedonlineasaReviewinAdvanceonFebruary26,2010TheAnnualReviewofPlantBiologyisonlineatplant.annualreviews.orgThisarticle’sdoi:10.1146/annurev-arplant-042809-112226Copyrightc2010byAnnualReviews.Allrightsreserved1543-5008/10/0602-0561$20.001Theseauthorscontributedequally.KeyWordsstomata,ionchannel,ABA,calcium,drought,carbondioxideAbstractStomatalporesareformedbypairsofspecializedepidermalguardcellsandserveasmajorgatewaysforbothCO2influxintoplantsfromtheat-mosphereandtranspirationalwaterlossofplants.Becausetheyregulatestomatalporeaperturesviaintegrationofbothendogenoushormonalstimuliandenvironmentalsignals,guardcellshavebeenhighlyde-velopedasamodelsystemtodissectthedynamicsandmechanismsofplant-cellsignaling.ThestresshormoneABAandelevatedlevelsofCO2activatecomplexsignalingpathwaysinguardcellsthataremediatedbykinases/phosphatases,secondarymessengers,andionchannelregula-tion.Recentresearchinguardcellshasledtoanewhypothesisforhowplantsachievespecificityinintracellularcalciumsignaling:CO2andABAenhance(prime)thecalciumsensitivityofdownstreamcalcium-signalingmechanisms.Recentprogressinidentificationofearlystom-atalsignalingcomponentsarereviewedhere,includingABAreceptorsandCO2-bindingresponseproteins,aswellassystemsapproachesthatadvanceourunderstandingofguardcell-signalingmechanisms.561Annu.Rev.PlantBiol.2010.61:561-591.Downloadedfromarjournals.annualreviews.orgbyChinaAgriculturalUniversityon07/12/10.Forpersonaluseonly.ANRV410-PP61-24ARI31March201019:9ContentsINTRODUCTION..................562IONCHANNELSINGUARDCELLS..................563AnOverviewofGuardCellIonChannelsandTheirFunctions...563UpdatesonIonChannelsandRegulationduringStomatalClosure.........................564RecentUpdatesonIonChannelsandRegulationduringStomatalOpening........................565ABA-RegulationofIonChannelActivitiesbyProteinTrafficking.....................566CO2SIGNALINGINGUARDCELLS..................566SiteofCO2Signaling..............566ArabidopsisMutantsintheCO2SignalingNetwork..............567MechanismsofCO2SignalinginGuardCells..................568GUARDCELLABASIGNALTRANSDUCTION...............569ABAReceptorsandEarlySignalingComponents..........569CalciuminGuardCellSignaling...572Calcium-DependentandCalcium-IndependentSignaling..........573CalciumSignalTransducers:CDPKsandCIPK/CBLs........573Calcium-SensitivityPrimingHypothesis.............575Calcium-ProgrammedStomatalResponse..............576NEWLYIDENTIFIEDCOMPONENTSANDMECHANISMSINABASIGNALTRANSDUCTION.....576RegulationofABAMetabolism.....576TranscriptionFactorsInvolvedinABASignaling..................577Rolesof26SProteasome-DependentProteinDegradationinABASignaling.......................578EpigeneticRegulationinABASignaling...............579InteractionwithJasmonicAcidSignaling..................579NEWAPPROACHESANDPERSPECTIVESONTHESTUDYOFGUARDCELLSIGNALING.....................579INTRODUCTIONPlantsneedtoassimilateCO2forphotosynthe-siswhilesimultaneouslypreventingexcessivelossofwater.Becausetheplantcuticleisimper-meabletobothwaterandCO2,transpirationalwaterlossandCO2influxinplantsaretightlyregulatedbytheopeningandclosingofstom-atalporesinaerialtissues.Thestomatalporeisformedbytwospecializedguardcells,whichinsomeplantspeciesaresurroundedbysub-sidiarycells(12).Thetransportofionsandwa-terthroughchannelproteinsacrosstheplasmaandvacuolarmembraneschangesturgorandguardcellvolume,therebyregulatingstomatalaperture(138,148,161).Guardcellscontinuouslysenseinformationfromtheleafenvironment,includingabioticandbioticstimuli,aswellaslong-distancesig-nalsfromroots.Guardcellsintegrateallofthesesignalsandconvertthemintoappropri-ateturgorpressurechanges.Severalimportantenvironmentalfactorsinducestomatalopen-inginC3andC4plants,includingblueandredlight.StomatesalsoopeninresponsetohighhumidityandlowCO2inordertomain-tainCO2intake.Stomatalclosure,ontheotherhand,ispromotedbydarknessinC3andC4plants.Inordertopreservewater,CAM-plantsdonotclosetheirstomatesinresponsetodarkness.Instead,theyaccumulateCO2dur-ingthenighttimebyconvertingitintoorganic562Kimetal.Annu.Rev.PlantBiol.2010.61:561-591.Downloadedfromarjournals.annualreviews.orgbyChinaAgriculturalUniversityon07/12/10.Forpersonaluseonly.ANRV410-PP61-24ARI31March201019:9moleculessuchasmalate.ElevatedCO2leadstostomatalclosurebecauselessopeningisre-quiredforefficientCO2influx.Stomataarealsoclosedinresponsetodrought,aswellaselevatedozone,thusprotectingtheinsideofleavesfromozone-inducedoxidativedamagetoplants(62,72,170).Droughtcausesproduc-tionoftheplanthormoneabscisicacid(ABA),whichpromotesstomatalclosureandtherebyreducestrans