Guard Cell Signal Transduction Network Advances in

ANRV410-PP61-13ARI21January201017:22REVIEWSINADVANCEGuardCellSignalTransductionNetwork:AdvancesinUnderstandingAbscisicAcid,CO2,andCa2+SignalingTae-HounKim,1MaikB¨ohmer,1HonghongHu,NoriyukiNishimura,andJulianI.SchroederUniversityofCalifornia,SanDiego,DivisionofBiologicalSciences,SectionofCellandDevelopmentalBiology,LaJolla,California,92093-0116;email:[e-mail],[e-mail],[e-mail],[e-mail],[e-mail].2010.61:13.1–13.31TheAnnualReviewofPlantBiologyisonlineatplant.annualreviews.orgThisarticle’sdoi:10.1146/annurev-arplant-042809-112226Copyrightc2010byAnnualReviews.Allrightsreserved1543-5008/10/0602-0001$20.001Theseauthorscontributedequally.KeyWordsstomata,ionchannel,ABA,calcium,drought,carbondioxideAbstractStomatalporesareformedbypairsofspecializedepidermalguardcellsandserveasmajorgatewaysforbothCO2influxintoplantsfromtheat-mosphereandtranspirationalwaterlossofplants.Becausetheyregulatestomatalporeaperturesviaintegrationofbothendogenoushormonalstimuliandenvironmentalsignals,guardcellshavebeenhighlyde-velopedasamodelsystemtodissectthedynamicsandmechanismsofplant-cellsignaling.ThestresshormoneABAandelevatedlevelsofCO2activatecomplexsignalingpathwaysinguardcellsthataremediatedbykinase/phosphatase,secondarymessengers,andionchannelregula-tion.Recentresearchinguardcellshasledtoanewhypothesisforhowplantsachievespecificityinintracellularcalciumsignaling:CO2andABAenhance(prime)thecalciumsensitivityofdownstreamcalcium-signalingmechanisms.Recentprogressinidentificationofearlystom-atalsignalingcomponentsarereviewedhere,includingABAreceptors,CO2-bindingproteins,aswellassystemsapproachesthatadvanceourunderstandingofguardcell-signalingmechanisms.13.1ReviewinAdvancefirstpostedonlineonFebruary26,2010.(Changesmaystilloccurbeforefinalpublicationonlineandinprint.)Changesmaystilloccurbeforefinalpublicationonlineandinprint.Annu.Rev.PlantBiol.2010.61.Downloadedfromarjournals.annualreviews.orgbyYaleUniversitySTERLINGCHEMISTRYLIBRARYon02/28/10.Forpersonaluseonly.ANRV410-PP61-13ARI21January201017:22ContentsINTRODUCTION..................13.2IONCHANNELSINGUARDCELLS..................13.3AnOverviewofGuardCellIonChannelsandTheirFunctions...13.3UpdatesonIonChannelsandRegulationduringStomatalClosure.........................13.4RecentUpdatesonIonChannelsandRegulationduringStomatalOpening........................13.5ABA-RegulationofIonChannelActivitiesbyProteinTrafficking.....................13.6CO2SIGNALINGINGUARDCELLS..................13.6SiteofCO2Signaling..............13.6ArabidopsisMutantsintheCO2SignalingNetwork..............13.7MechanismsofCO2SignalinginGuardCells..................13.8GUARDCELLABASIGNALTRANSDUCTION...............13.9ABAReceptorsandEarlySignalingComponents..........13.9CalciuminGuardCellSignaling...13.12Calcium-DependentandCalcium-IndependentSignaling..........13.13CalciumSignalTransducers:CDPKsandCIPK/CBLs........13.13Calcium-SensitivityPrimingHypothesis.............13.15Calcium-ProgrammedStomatalResponse..............13.16NEWLYIDENTIFIEDCOMPONENTSANDMECHANISMSINABASIGNALTRANSDUCTION.....13.16RegulationofABAMetabolism.....13.16TranscriptionFactorsInvolvedinABASignaling..................13.17Rolesof26SProteasome-DependentProteinDegradationinABASignaling.......................13.18EpigeneticRegulationinABASignaling...............13.19InteractionwithJasmoniciAcidSignaling..................13.19NEWAPPROACHESANDPERSPECTIVESONTHESTUDYOFGUARDCELLSIGNALING.....................13.19INTRODUCTIONPlantsneedtoassimilateCO2forphotosynthe-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,however,ispromotedbydarknessinC3andC4plants.Inordertopreservewater,CAM-plantsdonotclosetheirstomatesinresponsetodark-ness.Instead,theyaccumulateCO2duringthenighttimebyconvertingitintoorganic13.2Kimetal.REVIEWSINADVANCEChangesmaystilloccurbeforefinalpublicationonlineandinprint.Annu.Rev.PlantBiol.2010.61.Downloadedfromarjournals.annualreviews.orgbyYaleUniversitySTERLINGCHEMISTRYLIBRARYon02/28/10.Forpersonaluseonly.ANRV410-PP61-13ARI21January201017:22moleculessuchasmalate.ElevatedCO2leadstostomatalclosurebecauselessopeningisre-quiredforefficientCO2influx.Stomataarealsocl