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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;
Vé
ryand
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(Vé
ryandDavies,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