Calcium at the Crossroads of Signaling.docx

Calcium at the Crossroads of Signaling.docx

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CalciumattheCrossroadsofSignaling

ThePlantCell,S401–S417,Supplement2002,www.plantcell.org©2002AmericanSocietyofPlantBiologists

CalciumattheCrossroadsofSignaling

DaleSanders,a,1JérômePelloux,aColinBrownlee,bandJeffreyF.Harperc

aBiology

bMarine

Department,UniversityofYork,YorkYO105YW,UnitedKingdom

BiologicalAssociation,TheLaboratory,CitadelHill,PlymouthPL12PB,UnitedKingdom

cScrippsResearchInstitute,10550NorthTorreyPinesRoad,LaJolla,California92037

INTRODUCTION

CalciumSignals:

ACentralParadigmin

Stimulus–ResponseCoupling

Cellsmustrespondtoanarrayofenvironmentalanddevel-

opmentalcues.Thesignalingnetworksthathaveevolvedto

generateappropriatecellularresponsesarevariedandare

normallycomposedofelementsthatincludeasequenceof

receptors,nonproteinmessengers,enzymesandtranscrip-

tionfactors.Receptorsarenormallyhighlyspecificforthe

physiologicalstimulus,andthereforearedisparateintheir

identities.Likewiseenzymesandtranscriptionfactorstend

towardspecificity,andthisfactisreflectedinabundanceat

thegenomelevel.TheArabidopsisgenome,forexample,

potentiallyencodesintheregionof1000proteinkinases,

300proteinphosphatases,and1500transcriptionfactors.

Bycontrast,nonproteinmessengersarerelativelyfew.They

includecyclicnucleotides（Newtonetal.,1999）,hydrogen

ions（Guernetal.,1991）,activeoxygenspecies（Van

Breusegemetal.,2001）,lipids（NgandHetherington,2001;

NurnbergerandScheel,2001;Munne-BoschandAlegre,

2002）,and,aboveall,calcium.

Changesincytosolicfreecalcium（[Ca2]c）areapparent

duringthetransductionofaverywidevarietyofabioticand

bioticsignals.Thespectrumofstimulithatevokesrapid

changesin[Ca2]chasbeencatalogedinanumberofre-

centreviews（Sandersetal.,1999;Knight,2000;Aniland

Rao,2001;KnightandKnight,2001;RuddandFranklin-

Tong,2001）.Abioticstimuliincludelight—withred,blue,

andUV/Birradiationeachactingviadifferentreceptorsand

leadingtodistinctdevelopmentalresponses（Shacklocket

al.,1992;Baumetal.,1999;Frohnmeyeretal.,1999）,low

andhightemperature,touch,hyperosmoticstress,andoxi-

dativestress.Bioticstimuliincludethehormonesabscissic

acid（ABA）andgibberellin,fungalelicitors,andnodulation

（Nod）factors.

1Towhomcorrespondenceshouldbeaddressed.E-mailds10@

york.ac.uk;fax44-1904-434317.

Article,publicationdate,andcitationinformationcanbefoundat

www.plantcell.org/cgi/doi/10.1105/tpc.002899.

TheSpecificityQuestion

Anall-pervadingquestionduringthelastdecadeofcalcium

signalingresearchhasrevolvedaroundtheissueofspecificity

（McAinshandHetherington,1998）.Howcanasimplenon-

proteinmessengerbeinvolvedinsomanysignaltransduc-

tionpathwaysandyetstillconveystimulusspecificitywithina

varietyofpathways?

Ostensiblythereareanumberreason-

ablenonexclusiveanswerstothisquestion.First,theCa2

signalitselfmightbeanecessarybutinsufficienttriggerfor

theresponse,witheffectivesignaltransductionoccurring

onlyshouldanothersignalchangeinparallel.Second,speci-

ficitymightbeencodedbythespatialpropertiesoftheCa2

signal,eitherbecausethesignaliscompartmentallylocalized

（forexample,tothenucleus,ratherthanthecytosol）orbe-

causethesourceoftheCa2signal（fromoutsidethecellor

fromintracellularstores）canselectivelytriggerresponseele-

ments.Third,thedynamicpropertiesoftheCa2signalmight

determinetheefficacywithwhichtheresponseiselicited.

Fourth,ofcourse,theappropriateresponseelementsmust

bepresentintheparticularcelltypeinwhichtheCa2signal

arises.SinceCa2signalingwaslastreviewedinthisjournal

（Sandersetal.,1999）,remarkableadvanceshavebeenmade

inaddressingthiscentralproblemofspecificity,inmany

casesthankstotheinsightsprovidedbygeneticapproaches.

Thus,whilealludingbrieflytotheearlierliterature,thepresent

reviewwillfocusondevelopmentsinourunderstandingthat

haveoccurredoverthepastfouryears.

ELEMENTSENCODINGCALCIUMSIGNALS

Calciumsignalsaregeneratedthroughtheopeningofion

channelsthatallowthedownhillflowofCa2fromacom-

partmentinwhichtheionispresentatrelativelyhighelec-

trochemicalpotential（eitheroutsidethecell,orfroman

intracellularstore）tooneinwhichCa2isatlowerpotential.

Therehas,inthepast,beenatendencytorefertosuch

channelsas“Ca2channels,”althoughweprefertheterm

“Ca2-permeablechannels”becausethisreflectsthelikely

importanceofnonselectivecationchannelsingenerating

plantCa2signals.MaintenanceoflowCa2electrochemical

activityintheCa2-responsivecompartmentisachievedby

S402

ThePlantCell

theATP-orprotonmotiveforce–drivenremovalofCa2on

pumpsorcarriers（transporters）,respectively.Asshownin

Figure1,theinterplaybetweeninfluxthroughchannelsand

effluxfrompumpsandcarrierswilldeterminetheformofa

Ca2spikethatispotentiallyspecifictorelevantdecoders.

Figure2showsthelocationofchannels,pumps,andcarri-

ersinvolvedinCa2transportforageneralizedArabidopsis

cell,asthebasisforthediscussionbelow.

Calcium-PermeableIonChannels

Theimportanceofthecellularlocationofionchannelsinde-

terminingstimulusspecificityisemphasizedbyastudyof

Ca2-mediatedstomatalclosureintobacco（Woodetal.,

2000）.RemovalofextracellularCa2withthechelatorEGTA

orblockageofentrywithanumberofionchannelblockers

suggestedthatlowtemperature–inducedclosureinvolves

primarilyentryofCa2acrosstheplasmamembrane,while

intracellularmobilizationappearstodominateifstomatal

closureisinitiatedwithABAormechanicalstimulation.

Calcium-permeablechannelshavebeeninvestigated

withelectrophysiological,biochemical,andmolecularap-

proaches,andthesearenowbeginningtoyieldcomple-

mentaryinsightsintothenatureandcontrolofchannelsthat

underliethegenerationofCa2signals.

cium-permeablechannelsthatareactivatedbymembrane

depolarization（reviewedbyWhite,2000）.Ithasbeenspecu-

latedthatthisformofvoltagegatingmightendowsuch

channelswithapivotalroleatanearlystageinsignaltrans-

duction（Wardetal.,1995）.Thus,perceptionofarangeof

stimuliresultsinmembranedepolarization,possiblyasare-

sultoftheactivationofanionchannels,andtheresultant

openingofdepolarization-activatedCa2-permeablechan-

nelscouldleadtoelevationof[Ca2]c.

Whiledepolarization-activationofCa2-permeablechan-

nelsisarecurringthemeinanumberofbiologicalsystems,

recentsimultaneousandindependentstudieshavefollowed

pioneeringworkbyGellietal.（1997）andGelliandBlumwald

（1997）ontomatocellsuspensions,reportingthepresence

inplantplasmamembranesofCa2-permeablechannels

thatareactivatedbymembranehyperpolarization.Such

channelshaveahighselectivityforCa2overKandCl

（GelliandBlumwald,1997;Hamiltonetal.,2000;Véryand

Davies,2000）.Ithasbeenknownforsometimethatin

guardcells,membranehyperpolarizationisdirectlyasso-

ciatedwiththeelevationof[Ca2]cthatfollowsABAappli-

cation（GrabovandBlatt,1998）.Theobservationthat

hyperpolarization-activatedCa2-permeablechannelsinthe

plasmamembraneofguardcellsareopenedbyABAeven

inexcisedmembranepatchesimpliesaveryclosephysical

couplingbetweenthechannelsandthesitesofABAper-

ception（Hamiltonetal.,2000）.Channelopeningmightalso

besubjecttonegativefeedbackcontroltopreventexces-

PlasmaMembrane

siveCa2

entry,sinceactivitydecreasesaroundten-fold

Electrophysiologicalstudiesduringthepastdecadehave

revealedthepresenceinplantplasmamembranesofcal-

Figure1.DecodingCalciumSignalsLeadstoaSpecificResponse

attheCellularLevel.

Variousfeedbackmechanismsfromthecalciumsensor（or“de-

coder”）arepossible.Thesecouldincludetheregulationofcalcium

spikesviathecontrolofcalciumpermeablechannelgating（e.g.,

throughEFbindinghands,orviaCa2/CaMbinding）orviacontrolof

pumpactivity.

overtherangeof[Ca2]cfrom0.2to2M.Inroothairs,

channelactivityispresentatthetipsofgrowingcells,but

notdetectableinsubapicalregionsoratthetipsofmature

cells（VéryandDavies,2000）,anobservationconsistent

withthenotionthatthesechannelsplayapivotalroleinthe

generationofthetip-to-baseCa2gradientthatisessential

formaintainingpolarizationintip-growingsystems（includ-

ingpollentubesandrhizoidcells）.Intriguingly,theroothair

channelsare,incontrasttotheircounterpartsinguardcells,

activatedbyelevationof[Ca2]c,suggestingthattheymight

playaself-sustainingroleinmaintainingthetip-to-base

Ca2gradient.Hyperpolarization-activatedCa2-permeable

channelshavealsobeenreportedinthegrowingrootapex

ofArabidopsisroots,butnotinothermorematurecells

（Kiegleetal.,2000a）,possiblysuggestingaroleforthese

channelsincelldivisionandelongation.

ABA-inducedstomatalclosureinvolvestheproductionof

reactiveoxygenspecies,notablyhydrogenperoxide（Peiet

al.,2000;Zhangetal.,2001）,andhyperpolarization-acti-

vatedCa2-permeablechannelsplayacriticalroleinthis

reponse.InArabidopsisguardcells,hydrogenperoxide

stimulateshyperpolarization-activatedCa2-permeablechan-

nels,andtherebyanincreasein[Ca2]c（Peietal.,2000）.

ThisprocessrequirescytosolicNAD（P）H,sugge