83Calculumacentralregulatorofplantgrowthanddevelop

HISTORICALPERSPECTIVEESSAYCalcium:ACentralRegulatorofPlantGrowthandDevelopmentTodaynoonequestionstheassertionthatCa21isacrucialregulatorofgrowthanddevelopmentinplants.Themyriadpro-cessesinwhichthisionparticipatesislargeandgrowingandinvolvesnearlyallaspectsofplantdevelopment(recentreviewsinHarperetal.,2004;HetheringtonandBrownlee,2004;Hirschi,2004;ReddyandReddy,2004;BothwellandNg,2005).Despitethiswealthofresearch,thecon-ceptofCa21asanintracellularregulatorisrelativelyrecentandwithintheprofessionallifespanofmanypeoplewhoarestillactiveandworkingonthistopictoday.TheaimofthisessayistoidentifythoselinesofthoughtandresearchthatledtotheideathatCa21isasecondmessengerinplantcellgrowthanddevelopment.Thisessaythusfocusesprimarilyonworkstartinginthemidsixtiesandextendingtothemideighties.IdonotprovideanexhaustivereviewofthehistoryofCa21research,nordoIattempttotreatmodernaspectsofCa21research.However,IdostrivetoidentifytherootsofmodernCa21researchandtocharttheoriginofthecurrentrevolution.EARLYSTUDIESONPLANTCALCIUMCa21isanessentialelement;however,itsroleiselusive.WhenexaminingtotalCa21inplants,theconcentrationisquitelarge(mM),butitsrequirementisthatofamicro-nutrient(mM).Ca21isnotusuallylimitinginfieldconditions,stillthereareseveraldefectsthatcanbeassociatedwithlowlevelsofthision,includingpoorrootdevelopment,leafnecrosisandcurling,blossomendrot,bitterpit,fruitcracking,poorfruitstorage,andwatersoaking(Simon,1978;WhiteandBroadley,2003).Theunderlyingcausesfortheseeffectsarenotentirelyclear;nevertheless,twoareaswithinthecellhavebeenrecognizedasbeingimportanttargets.Firstisthecellwall,whereCa21playsakeyroleincross-linkingacidicpectinresidues.Thesecondisthecellularmembranesystem,wherelow[Ca21]eincreasesthepermeabilityoftheplasmamembrane.Thesearebrieflydiscussedbelow.Ca21andtheCellWallSincethe19thcentury,ithasbeenappre-ciatedthatCa21playsacrucialroleindeterminingthestructuralrigidityofthecellwall(reviewedinWynJonesandLunt,1967;Burstrom,1968).Duringcellwallformation,theacidicpectinresidues(e.g.,galacturonicacid)aresecretedasmethylesters,andonlylaterdeesterifiedbypectinmethylesterase,liberatingcarboxylgroups,whichbindCa21.Itfollowsthatlow[Ca21]eshouldmakethecellwallmorepliableandeasilyruptured,whereashighconcentra-tionsshouldrigidifythewallandmakeitlessplastic.Ithadbecomeapparentinthemidtolatefiftiesthatmodifyingthe[Ca21]eproducedapronouncedeffectoncellgrowth.Thus,elevatingthe[Ca21]eledtoaninhibitioninshootorcoleoptilegrowth,whereasreducingitsconcentrationpro-motedcellandtissueelongation(Bennet-Clark,1956;TagawaandBonner,1957).StrongsupportfortheCa21/pectatein-teractioncamefromaquantitativeexami-nationofthecationexchangecapacityofthecoleoptilecellwall,whichwasshowntobeduetothenumberoffreepecticcarboxylgroups(Jansenetal.,1960).StillfurthersupportcamefromstudiesusingthecationchelatorEDTA,whichhadbeenemployedtomacerateplanttissueswith-outdestroyingthecellstructure(Letham,1958).TheexplanationcenteredaroundtheideathatEDTA,bychelatingCa21,ledtoamarkedweakeningorlossofpectatesinthemiddlelamella,thusremovingtheagentthatcementedcellstogether.TheimportanceoftheCa21/pectateinteractionasaregulatorofgrowthen-couragedresearcherstoincludearoleforauxininthisscheme,particularlybecauseitwasbecomingevidentthatCa21andauxinhadantagonisticactions.Thus,auxinpro-motedshootgrowthandinhibitedrootgrowth,whereasCa21inhibitedshootgrowthandpromotedrootgrowth.Workingwithoatcoleoptiles,Bennet-Clark(1956)proposedthattheremightbeadirectantagonismbetweenindoleaceticacid(IAA)andCa21.NotingthatCa21,andthelanthanidepraseodymium,inhibitedIAA-inducedelongation,whereasEDTAre-versedtheinhibitoryactivityofCa21,andevenpromotedgrowth,Bennet-Clark(1956)suggestedthatIAAactsasaCa21/Mg21chelator.ThismodelproposedthatIAAremovesCa21andleadstoalossofCa21pectates,whicharereplacedbypectatefreeacidsormethylesters.Thelatter,becausetheyarenotcross-linked,wouldrenderthewallplasticandabletoelongate(Bennet-Clark,1956).ThisideawaschallengedbyCleland(1960),whodemonstratedthatIAAdoesnotenhancethelossofCa21fromthecellwall,nordoesitcausearedistributionofCa21betweenpectinandproto-pectin.Somewhatlater,BurlingandJackson(1965)usedatomicabsorptionspectroscopytoshowthatCa21accumulatedinthecellwallsofelongatingcoleoptilesandthatthisaccu-mulationwasunaffectedbyauxin.FurtherstudiesbyBakerandRay(1965)andRayandBaker(1965)establishedthesepara-tioninactionbetweenCa21andIAA,providingclearevidencethattheinhibitionofcellelongationbyCa21doesnotpreventIAAfromstimulatingcellwallsynthesis.InthepresenceofCa21,andthustheinhi-bitionofcellenlargement,theydemon-stratedageneralpromotionofsynthesisofmatrixpolysaccharidesinthepresenceofIAA(RayandBaker,1965).AcompellinginteractionbetweenCa21,thecallwall,andcellgrowthwasalsofoundinpollentubes.Itwasshownin1963thatCa21mustbepresentinthemediumtosupportpollentubegrowthinvitro(BrewbakerandKwack,1963).Using45Ca21,Kwack(1967)showedthatThePlantCell,Vol.17,2142–2155,August2005,