Brassinosteroid Signal Transduction from Receptor

ANRV410-PP61-23ARI29January201014:43REVIEWSINADVANCEBrassinosteroidSignalTransductionfromReceptorKinasestoTranscriptionFactorsTae-WukKimandZhi-YongWangDepartmentofPlantBiology,CarnegieInstitutionforScience,Stanford,California94305;email:[e-mail].2010.61:23.1–23.24TheAnnualReviewofPlantBiologyisonlineatplant.annualreviews.orgThisarticle’sdoi:10.1146/annurev.arplant.043008.092057Copyrightc2010byAnnualReviews.Allrightsreserved1543-5008/10/0602-0001$20.00KeyWordsArabidopsis,GSK3kinase,planthormone,receptorkinase,signaltransduction,steroidhormoneAbstractBrassinosteroids(BRs)aregrowth-promotingsteroidhormonesinplants.GeneticstudiesinArabidopsisillustratedtheessentialrolesofBRsinawiderangeofdevelopmentalprocessesandhelpedidentifymanygenesinvolvedinBRbiosynthesisandsignaltransduction.Recently,proteomicstudiesidentifiedmissinglinks.Together,theseapproachesestablishedtheBRsignaltransductioncascade,whichincludesBRper-ceptionbytheBRI1receptorkinaseatthecellsurface,activationofBRI1/BAK1kinasecomplexbytransphosphorylation,subsequentphos-phorylationoftheBSKkinases,activationoftheBSU1phosphatase,dephosphorylationandinactivationoftheBIN2kinase,andaccumu-lationofunphosphorylatedBZRtranscriptionfactorsinthenucleus.Massspectrometricanalysesareprovidingdetailedinformationonthephosphorylationeventsinvolvedineachstepofsignalrelay.Thus,theBRsignalingpathwayprovidesaparadigmforunderstandingrecep-torkianse–mediatedsignaltransductionaswellastoolsforthegeneticimprovementoftheproductivityofcropplants.23.1ReviewinAdvancefirstpostedonlineonFebruary5,2010.(Changesmaystilloccurbeforefinalpublicationonlineandinprint.)Changesmaystilloccurbeforefinalpublicationonlineandinprint.Annu.Rev.PlantBiol.2010.61.Downloadedfromarjournals.annualreviews.orgbyUniversidaddeConcepcionon02/21/10.Forpersonaluseonly.ANRV410-PP61-23ARI29January201014:43ContentsINTRODUCTION..................23.2RECEPTORACTIVATION.........23.4BRI1PerceivesBRsattheCellSurface.........................23.4BrassinosteroidsIncreasetheAffinityofBRI1forItsCoreceptorHetero-OligomerizationBR-InducedReceptorKinaseDimerizationandOligomerization............23.4TeamPlayandMultitaskingoftheReceptorKinases.........23.6RegulationbyAuto-andTransphosphorylation...........23.7EndocytosisofBRI1andBAK1.....23.10RegulationbyBKI1................23.10SIGNALINGOUTPUTFROMTHERECEPTORKINASES.....23.11BZR1ANDBZR2/BES1:KEYTRANSCRIPTIONFACTORSFORBR-REGULATEDGENEEXPRESION.....................23.12REGULATIONOFBZR1ANDBZR2/BES1BYBIN2-MEDIATEDPHOSPHORYLATION...........23.14REGULATIONOFBIN2BYBSU1-MEDIATEDTYROSINEDEPHOSPHORYLATIONANDPROTEASOME-MEDIATEDDEGRADATION.................23.16CONCLUDINGREMARKS.........23.19INTRODUCTIONSteroidshavelongbeenknownashormonesinmetazoans(85).Theirhormonalactivityinplantswasonlydiscoveredabout30yearsago,whenagrowth-promotingactivityinpollenextractofoilseedrape(Brassicanapus)wasat-tributedtoasteroidcompoundnamedbrassi-nolide(BL)(24).Sincethen,steroidswithsimilarstructureandactivitiesasBLhavebeenidentifiedinavarietyofplantsandarecollectivelycalledbrassinosteroids(BRs)(13).Whilehormonetreatmentsdemonstratedmanyphysiologicalanddevelopmentalre-sponsesinducedbyexogenousBR,theessen-tialfunctionofBRsinplantdevelopmentwasnotwidelyappreciateduntilBR-deficientandBR-insensitivemutantswereidentifiedinarel-ativeofB.napus,themodelorganismArabidop-sisthaliana(12,49,81).Thesemutantsdisplaymanygrowthdefects,includingdwarfism,darkgreenleaves,delayedflowering,malesterility,andphotomorphogenesisincompletedarkness.NowBRsareconsideredessentialhormonesthatregulateawiderangeofdevelopmentalandphysiologicalprocesses,suchascellelongation,vasculardifferentiation,rootgrowth,responsestolight,resistancetostresses,andsenescence.ArabidopsismutantsidentifiednotonlyBRbiosyntheticenzymesbutalsosignalingpro-teinsthatperceiveandtransducetheBRsignal.ForwardgeneticscreensinArabidopsisidenti-fiedmultipleallelesoftwolocithatcauseBRinsensitivity,bri1andbin2.BRINSENSITIVE1(BRI1)encodesoneofover200membersoftheleucine-richrepeat-receptor-likekinase(LRR-RLK)familyinArabidopsis(79),andBRINSENSITIVE2(BIN2)encodesoneofthe10glycogensynthasekinase3(GSK3)-likekinasesofArabidopsis(50).SensitizedgeneticscreensusingtheBRbiosyntheticinhibitorbrassina-zole(BRZ)orweakallelesofbri1asgeneticbackgroundidentifiedadditionalcomponentsofthepathway,includingtheBRASSINA-ZOLERESISTANT1(BZR1)andbri1-EMS-SUPPRESSOR1(BES1)transcriptionfactors(93,97),BRI1-ASSOCIATEDRECEPTORKINASE1(BAK1)(52,60),andbri1-SUPPRESSOR1(BSU1)phosphatase(57)(Figure1).BES1is89%identicaltoBZR1andwasalsonamedBZR2(93).BAK1wasalsoiden-tifiedbyyeasttwo-hybridscreeningasaBRI1-interactingprotein(60).AdditionalcomponentsoftheBRsig-naltransductionpathwayhavebeeniden-tifiedasproteinsthatinteractwiththesegeneticallydefinedcomponents.TheBRI1-interactingproteinsincludeBAK1(60),BRI1KINASEINHIBITOR1(BKI1)(89),andTRANSTHYRETIN-LIKE(TTL)(61).The23.2Kim·WangREVIEWSINADVANCEChangesmaystilloccurbeforefinalpublicationonlineandinprint.Annu.Rev.PlantBiol.2010.61.Downloadedfromarjournal