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JournalofExperimentalBotany,Vol.51,No.345,pp.659–668,April2000 REVIEWARTICLEChlorophyllfluorescence—apracticalguideKateMaxwellandGilesN.JohnsonEnvironmentalandMolecularPlantPhysiologyLaboratory,DepartmentofAgriculturalandEnvironmentalScience,TheUniversity,NewcastleuponTyneNE17RU,UKUniversityofManchester,SchoolofBiologicalSciences,3.614StopfordBuilding,OxfordRoad,ManchesterM139PT,UK chlorophyllmoleculesinaleafcanundergooneofthreefates:itcanbeusedtodrivephotosynthesis(photo-Introductionchemistry),excessenergycanbedissipatedasheatoritcanbere-emittedaslight—chlorophylluorescence.Inrecentyears,thetechniqueofchlorophylluorescence MaxwellandJohnsonthatofabsorption.Therefore,uorescenceyieldcanbeicalquenching.Atthesametime,thereisaincreaseintheeciencywithwhichenergyisconvertedtoheat.Thisedbyexposingaleaftolightofdenedwave-lengthandmeasuringtheamountoflightre-emittedatlatterprocessistermednon-photochemicalquenching).Inatypicalplant,changesinthesetwoprocesseslongerwavelengths.Itisimportanttonote,however,thatthismeasurementcanonlyeverberelative,sincelightiswillbecompletewithinabout1520minandanapproxi-matesteady-stateisattained,althoughthetimetakentoinevitablylost.Hence,allanalysismustincludesomeformofnormalisation,withawidevarietyofdierentreachthisstatecanvarysignicantlybetweenplantspecies(Johnsonetal.,1990).uorescenceparametersbeingcalculated(seebelow).Onemodicationtobasicmeasuringdevicesthathasbeeninstrumentalinrevolutionizingtheapplicationofuorescence,hasbeentheuseofaDeconvolutingfluorescencesignalsmeasuringsystem(QuickandHorton,1984).Insuchsystems,thelightsourceusedtomeasureuores-Inordertogainusefulinformationaboutthephoto-syntheticperformanceofaplantfrommeasurementsofcenceismodulated(switchedonandoathighfrequency)andthedetectoristunedtodetectonlyuorescencechlorophylluorescenceyield,itisnecessarytobeabletodistinguishbetweenthephotochemicalandnon-excitedbythemeasuringlight.Therefore,therelativeyieldofuorescencecannowbemeasuredinthepresencephotochemicalcontributionstoquenching.Theusualapproachistoswitchooneofthetwocontributors,ofbackgroundillumination,and,mostsignicantly,inthepresenceoffullsunlightintheeld.Mostmodernspecicallyphotochemistry,sothattheuorescenceyieldinthepresenceoftheotheralonecanbeestimated.uorometersusesuchmodulatedmeasuringsystemsandanyoneconsideringinvestinginauorescencesystemisthiscanbeachievedbytheadditionofchemicals,suchastheherbicideDiuron(DCMU),thatinhibitPSII,stronglyadvisedtoselectamodulatedreducingphotochemistrytozero.Thismethodis,how-ever,bothimpracticalandundesirableinamorephysio-Whydoesfluorescenceyieldchange?TheKautskylogicalcontext.Instead,amethodhasbeendeveloped,effectandbeyondlightdoublingtechnique,thatallowsthecontributionofphotochemicalquenchingtobetransientlyreducedtoChangesintheyieldofchlorophylluorescencewereobservedasearlyas1960byKautskyandco-workerszero(BradburyandBaker,1981;QuickandHorton,1984).Inthisapproach,ahighintensity,shortdur-(Kautskyetal.,1960).Theyfoundthat,upontransferringphotosyntheticmaterialfromthedarkintothelight,anationashoflightisgiven.TheeectistransientlytocloseallPSIIreactioncentres.Providedtheashisincreaseintheyieldofchlorophylluorescenceoccurredoveratimeperiodofaround1s.Thisrisehassub-shortenough,no(oranegligible)increaseinnon-photochemicalquenchingoccursandnolong-termchangesequentlybeenexplainedasaconsequenceofreductionofelectronacceptorsinthephotosyntheticpathway,intheeciencyofphotosynthesisisinduced.Duringtheash,theuorescenceyieldreachesavalueequivalenttodownstreamofPSII,notablyplastoquinoneandinpar-ticular,Q.OncePSIIabsorbslightandQhasacceptedthatwhichwouldbeattainedintheabsenceofanyphotochemicalquenching,themaximumanelectron,itisnotabletoacceptanotheruntilithaspassedtherstontoasubsequentelectroncarrier(Q).Comparisonofthisvaluewiththesteady-stateyieldofuorescenceinthelight()andtheyieldofDuringthisperiod,thereactioncentreissaidtobe.Atanypointintime,thepresenceofaproportionintheabsenceofanactinic(photosynthetic)light(givesinformationabouttheeciencyofphotochemicalofclosedreactioncentresleadstoanoverallreductionintheeciencyofphotochemistryandsotoacorrespondingquenchingandbyextension,theperformanceofPSII.Aswellaschangesoccurringintheeciencyofphoto-increaseintheyieldofWhenaleafistransferredfromdarknessintolight,chemistry,theeciencyofheatdissipation(i.e.non-photochemicalquenching)canchangedependingonvari-PSIIreactioncentresareprogressivelyclosed.Thisgivesrise(duringtherstsecondorsoofillumination)toanousinternalandexternalfactors.Suchchangesareectedaschangesinthelevelof.Unlikephotochem-increaseintheyieldofchlorophylluorescence.Followingonfromthis,however,theuorescenceleveltypicallyistry,itisnotpossibletoinhibitheatdissipationtotally,soitisnotpossibletomeasuretheyieldofchlorophyllstartstofallagain,overatime-scaleofafewminutes.Thisphenomenon,termeduorescencequenching,isuorescenceintheabsenceofnon-photochemicalquench-ing.Hence,allestimationsofnon-photochemicalquench-explainedintwoways.Firstly,thereisanincreaseintherateatwhichelectronsaretransportedawayfromPSII;ingarestrictlyrelativetosomedark-adaptedpoint(termedhere).Forthisreason,itisnecessarytothisisduemainlytothelight-inducedactivationofenzymesinvolvedincarbonmetabolismandtheopeningdesignexperimentsinsuchawaythatadark-adapted,non-stressedreferencepointcanbeestimated.Thisofstomata.Suchquenchingisreferredtoas MaxwellandJohnsonAnotherwidelyuseduorescenceparameter,measuringquenching.Assuch,itdoesnotnecessarilyapplyunderotherconditions,especiallywheretheplantisexposedtophotochemistry,isphotochemicalquenching.Thisiscalculatedas:stressandwheresignicantamountsofphotoinhibitionmayoccur.Forthisreason,theapplicationofthis)(3)approachisprobablybestavoidedundereldconditions.AnalternativeexpressionthatissometimesusedandAlthough,superciallyverysimilarto,thesignianceofthisparameterissomewhatdierent.Whilstthatisessentiallyidenticalto(KrauseandWeis,1991).Althoughperhapsnotsuchanintuitiveistheproportionofabsorbedenergybeingusedingivesanindicationoftheproportionparameter(itdoesnotgiveadirectmeasureofeciency),ithastheadvantageofbeingmoresensitivetochangesofPSIIreactioncentresthatareopen.Analternativeexpressionofthisis1,theproportionofcentresthatineciencyathighvaluesandso,insomecircumstances,maybeabetterwayofexpressingdata.areclosedandissometimestermedtheexcitationpres-onPSII(DPMaxwelletal.,1994).canbeinterrelatedbyathirdparameter,(GentyNon-photochemicalprocessesetal.,1989).Thisisameasureoftheintrinsic(ormaximum)eciencyofPSII(i.e.thequantumeciencyTheproblemofneedingtodark-adaptleavesalsoapplieswhenquantifyingnon-photochemicalquenching.Here,ifallPSIIcentreswereopen).isgivenbytheequation:however,theproblemsareexacerbatedbytheneedtomeasureavalueof.Thisvaluewouldtypicallybemeasured,inthelaboratory,afterbetweenafullnightand24hofdark-adaptation.Thereisalsothecanbeeither).So,whilstrelatestoachievedeprovideimplicitassumptioninsuchexperimentsthattheplantshavenotbeenexposedtoanystresspriortothestartofinformationabouttheunderlyingprocesseswhichhavealteredeciency.Achangeinisduetoclosureoftheexperiment.Theaimofsuchproceduresistoattainareferencelevelofinwhichphotochemicalereactioncentres,resultingfromasaturationofphoto-synthesisbylight.Achangeinisduetoachangeisatitsmaximumandheatdissipationisataminimum.eldexperiments,itispossibletomeasurethepre-intheeciencyofnon-photochemicalquenching.Dark-adaptedvaluesofectthepotentialquantumdawnvalueofandusethisasareferencepoint,however,thismaybesensitivetotheprehistoryoftheciencyofPSIIandareusedasasensitiveindicatorofplantphotosyntheticperformance,withoptimalvaluesofplant.Changesinthedawnmay,however,giveimportantinformationconcerningtheeectontheplantaround0.83measuredformostplantspecies(BjoandDemmig,1987;Johnsonetal.,1993).Valueslowerofenvironmentalstress(seebelow).Themoststraightforwardwayofquantifyingnon-thanthiswillbeseenwhentheplanthasbeenexposedtostress,indicatinginparticularthephenomenonofphotochemicalquenchingisbymeasuringtheratioofachangeintothenalvalueofAdicultyintheestimationofistheneedtoestimatethevalueofatthetimeofmeasure-ment.Inthelaboratory,thisisachievedbydarkeningthe(BilgerandBjorkman,1990).(sometimesreferredtoas)islinearlyrelatedtoheatdissipationandliesleafand,usually,byapplyingfar-redillumination(wave-680nm)forafewsecondsbeforeandimmedi-onascale0nity.Inatypicalplant,valuesmightbeexpectedintherange0.53.5atsaturatinglightintensities,atelyaftertheendofillumination.ThelatterisimportanttoensurethatallPSIIreactioncentresopenrapidlyafterhowever,thisvariesmarkedlybetweenspeciesandontheprevioushistoryoftheplant.Anoldertermforquantify-theendofillumination.Commercialportablemetersusuallyincorporateafar-redlightsource,however,ingnon-photochemicalquenching,thatrequiresmeas-urementof,isstillsometimesused(vanKootenandthetechnicalproblemsofdarkeningtheleafintheremain.TheseareusuallyovercomebytransientlySnel,1990).Thisparameterfallsonascaleof01andis,therefore,veryinsensitivetochangesinquenchingatcoveringtheleafwithablackclothwhilstsimultaneouslyprovidingfar-redlight.Amethodforestimating,highervalues.Itisimportanttonotethatmeasurechangesinheatdissipationrelativetothedark-withoutmakingdirectmeasurementshasrecentlybeenproposed(OxboroughandBaker,1997).Thismethodadaptedstate.Thesameincreaseinheatdissipationwillappearasasmallerincreaseinquenchinginthecasewasdevelopedspecicallyforuseinuorescenceimagingtechniqueswhereestimationofisparticularlyproblem-wherethereferencepointhashigherquenching.Thismeansthatdirectcomparisonsbetweenleaveswithdiatic.Whilstthismethodseemstoworkwellunderspecilaboratoryconditions,itmakesassumptionsabouttheenthistoriesorleavesofdierentspeciescanbeambigu-ous.Generally,ifthedark-adaptedvalueofnatureoftheprocessescontributingto MaxwellandJohnsonanalysingthekineticsoftheuorescenceriseresultingtransportandCOxationcancorrelateverywell(Gentyetal.,1989;EdwardsandBaker,1993).Thatcorrelationfromthetransferofaleaffromdarktolight.Onecantadvantageofthisapproachisthatitallowscan(anddoes)breakdownundereldconditions(Fryeretal.,1998).Discrepanciescanbecausedbychangesininformationtobeattainedusingsimple(cheaper)non-uorometers.Workby,inparticular,StrassertherelativeratesofCOxationandcompetingprocessessuchasphotorespiration,nitrogenmetabolismandelec-andco-workers(Stirbetetal.,1998)hassuggestedthederivationofanumberofdierentparameters,basedontrondonationtooxygen(theMehlerreaction).Suchdiscrepanciesmaybeinthemselvesinteresting(seebelow),thedetailsofthekineticsofuorescencerise.Thisanalysisremains,however,controversialandisprobablybestbutmeanthataccuratedeterminationofCOxationisnotpossiblewithuorescencealone.Furthercomplicationavoideduntilithasbeenplacedonarmertheoreticalfooting.mayariseduetoheterogeneitybetweensamples.CalculationofelectrontransportusingassumesthatthelightabsorbedperPSIIisconstant.ForWhatcanchlorophyllfluorescencedoforyou?leavesgrowingindierentmicroclimates,thiswilltypic-Thediscussionabovehascoveredtheoreticalandtech-allynotbetrue.Thiscanbepartiallyovercomeifnicalconsiderationsaboutchlorophylluorescenceana-absorbancecanbemeasureddirectly,usinganintegratinglysis.Therestofthisreviewisintendedtoexaminethesphere,however,theproblemofdierencesinphoto-questionofhowthistheorycanbeappliedtoobtainsystemstoichiometryremain.Thus,uorescencecanneverusefulinformationineldandlaboratoryecophysiologybeusedtomakecomparativemeasurementsofphotosyn-studies.Ashasbeenstatedalready,chlorophyllthesisbetweendierentleavesorplants.FortheabovecencegivesinformationaboutthestateofPhotosystemreasons,measurementsofgasexchange,usinginfraredII.ItcantellyoutheextenttowhichPSIIisusingthegasanalysers,remainattheheartofstudiesinplantenergyabsorbedbychlorophyllandtheextenttowhichitisbeingdamagedbyexcesslight.ThismaysoundlikeProvidedtheabovereservationsareborneinmind,fairlyobscureinformation,ofrelevanceonlytothosecanprovideusefulinformationconcerningphotosyn-withaspecialistinterestinPSII,however,itisofmuchtheticperformanceintheeld.Inparticular,widerimportancetothephysiologyofaplant.Thecangiveagood,rapidandminimallyinvasivemeasure-ofelectronsthroughPSIIisindicative,undermanycondi-mentofchangesinaparticularsample(orinsamplestions,oftheoverallrateofphotosynthesis.Itgivesusthethatcanbeconsideredtobehomogenous)throughtime.potentialtoestimatephotosyntheticperformance,underForexample,uorescencehasbeenused(Murchieetalconditionsinwhichothermethodswouldfail,inamanner1999)tofollowtheelectrontransportrateinparticularthatisalmostinstantaneous.PSIIisalsoacceptedtobeleavesoftworicecultivarsthroughoutthedayatdithemostvulnerablepartofthephotosyntheticapparatusdevelopmentalstages.Individualleavesweremarkedandtolight-induceddamage.DamagetoPSIIwilloftenbesubsequentmeasurementsmadeonthesameleaves,sorstmanifestationofstressinaleaf.Althoughensuringcomparabilitybetweenmeasurements.Asimilarrescenceisapowerfultechnique,itisalsolimited.Itisapproachwasusedinfollowingdiurnalchangesinelec-easytomeasurebut,ifexperimentsarenotdesignedtrontransportinloblollypinetreesexposedtoelevatedcorrectly,itcanalsobeimpossibletointerpret.Themost,usingfree-airCOenrichment(FACE)(Hymuspowerfulandelegantapplicationsofuorescencedonotetal.,1999).Theseauthorsobservedthat,whilst,inusethistechniquealone,butcombineitwithothersummer,elevationofCOresultsinanincreaseinelectrontechniques,inparticular,gasexchangemeasurements,totransport,inwinter,electrontransportisinhibited.AobtainafullpictureoftheresponseofplantstotheirrelativelygreaterincreaseinwasobservedduringecksinaterrestrialCAMbromeliad,ascomparedtosympatricCspecieswithinaPanamanianrainforestPSIIquantumyieldasaproxymeasureofphotosynthesis(SkillmanandWinter,1997).Thisreectsthegreaterenergeticdemandofdecarboxylationofnocturnallyaccu-Oneofthemainattractionsofchlorophyllisthatittogiveameasureofphotosynthesis.mulatedorganicacidintheCAMplant,relativetothecostsofCphotosynthesis(includingphotorespiration),Thisis,however,agreatsimplicationandfailuretoappreciatethispointcanleadtheuserintodiculties.whichsupportslightuseunderpotentiallydamagingincidentPFD.Asinthepreviousexample,acomparisonFluorescencecanbeusedtomeasurethePSIIphotochemistry.Asindicatedabove,thiscanbeismaderelativetomeasurementsinthesameleaf,sothaterencesinabsorbancearelikelytobeinsigniconvertedintoarelativerateoflinearelectrontransportbymultiplyingbythelightintensity.PhotosynthesisisAnotherapplicationwhereuorescencemaybeusefulisinexaminingtheacclimationofplantstodiusuallythoughtofasbeingthegrossrateofcarbonxation.Underlaboratoryconditions,PSIIelectronmicroenvironments.Bymeasuringthelightdependency ChlorophyllfluorescenceforbeginnersitispossibletomakesimpleandrapidestimatestheextentofphotorespirationmaybeestimatedinvivoInparticular,thisprotocolhasbeenusedtoexploretheofthelightsaturationbehaviourofdierentplantsundereldconditions.Thisdoesnotallowacomparisonofthesignicanceofphotorespirationasaphotoprotectivemaintenancemechanismduringdroughtstress(Cornicabsoluteratesofphotosynthesisbetweensites,butcanbeusefulwhenstudyingsamples,suchaslichensandbryo-andBriantais,1991;Valentinietal.,1995;Niinemetsetal.,1999).phytes,whosestructuremakesthemdiculttostudywithconventionalgasexchange.MeyerandGentyusedhighresolutionimagesoftodeneleafinternalCOconcentration()followingProblemsmayarisewhenmeasurementsofelectrontransportratearemadeintheopen(especiallyintheABAtreatmentinleavesofRosarubiginosa(MeyerandGenty,1998).Measurementsofmadeconventionallylaboratory),whenuctuatinglevelsofCO(oftengener-atedbytheexperimentersexhalations)precludein-depthusinggasexchangetechniquesduringdroughtmaybeover-estimatedasaconsequenceofbothpatchystomatalanalysisoftherelationshipbetweenthelightanddarkreactionsofphotosynthesis.Therefore,specializedleafresponseandanunder-estimationofcuticulartranspir-ation.Thisuseofchlorophylluorescencehassuggestedcuvettesorgas-tightleafchamberswhichincorporateportswhichhousethebreopticcable(s)shouldbeusedthattheprimaryeectofdroughtstressisoneofstomatalclosurewitharesultingdecreasingininternalCOwherepracticable.Thesystemshouldlimitself-shadingwhilstmaximizinguorescenceyield,withthebrecom-trationwhichmaylimitcarboxylation(MeyerandGenty,1998,1999;Saetal.,1999).Thetech-monlypositionedatanangleof45totheleaf.Importantinformationmaybeobtainedifitispossibleniquedoesnotrequireuorescenceimagingequipmentandhasbeenperformedwithcombinedmeasurementsoftocontrolthegassupplytoaleaf.TheHansatechleafdiscelectrodechamberhasbeenusedtovaryambientgasexchangeanduoromtery.Saguezandco-workersusedtheempiricalrelationshipbetweentheandO(LovelockandWinter,1996)andtoassessthecapacityforelectronuxthroughthephotorespiratoryratioofassimilationrateandincontrolleavessubsequentlytomodelindroughtedleavesandMehler-ascorbateperoxidasepathway(pseudocyclicelectrontransport)andtherelationshipwithphotoinhibi-(Saetal.,1999).However,themethodo-logyrequiresthatthisrelationshipdoesnotchangefollow-tionandleafsenescenceinanevergreen()anddeciduous()tropicaltreespecies.Inaingtheimpositionofstress,thatalternativeelectron(i.e.totheMehler-peroxidasereaction)isnegligibleanderentapproachwhichexempliesthenovelkindofsystemswhichcanbeused,diusionlimitationsacrossthatrespiratoryratesdonotdiersignicantlybetweentreatments.ItisalsonecessarythatcanbeaccuratelythelichenthalluswasinvestigatedinLobariascrobiculataThethalluswassealedinacustom-builtgas-tightPetrideterminedbygasexchangeincontrolleaves,whichmayprecludespecieswithaninherentlylowstomatalordishandushedwithnitrogen,withCOthroughdierentareasandthicknessofthethalluscuticularconductance.Fluorescenceanalysiscanalsobeappliedtounder-assessedbytrackingtherecoveryofunderlowlightwhenairwasreintroducedtothesystem(Maetal.,standingtheeectsoflowandhightemperatures.Forexample,comparisonsoftheyieldofCOxation(1997).weremadetoprovideevidencethat,whenexposedtolowtemperatures,maizeincreaseselectronRelatingelectrontransporttocarbonfixationtransporttoalternativeelectronsinks,probablygenerat-Despitethefactthatuorescenceemanatesfromonlytheingactiveoxygenspecies(Fryeretal.,1998).Earlyintopfewlayersofchlorenchyma,whereasgasexchangeisthegrowingseason,theratioofwashigherintegratedacrossthethicknessoftheleaf,simultaneousthanthatseeninunstressed,fullydevelopedleaves,measurementshaveemergedasapowerfultoolforinvesti-suggestingthatelectronswerebeingusedinpathwaysgatingtherelationshipbetweenlightuseeciency,COotherthanCOxation.Thisincreasewasaccompaniedxationandphotoinhibition.Arelativelysimpleandbyanincreaseinthecapacityofantioxidationsystems,widelyusedtechniqueinvolvesexploringtheempiricalimplyingthattheleavesweresueringfromoxidativerelationshipbetweenelectrontransportandCOstressatthistime.invivo.SimultaneousmeasurementsaremadeofCOassimilationandundernon-photorespiratorycon-Measuringstressandstresstoleranceditions(elevatedCOor12%O)atdierentlightintensities.AlinearplotofthequantumyieldofCOuorescencemeasurementsmaysometimespro-videausefulmeasureofthephotosyntheticperformancexation()andPSIIphotochemistry()allowstheelectronrequirementpermoleculeCOxedtobeofplants,itsrealstrengthliesinitsabilitytogiveinformationthatisnotreadilyavailableinotherways.ed(Epronetal.,1995).Assumingthatthisrela-tionshipholdsundernon-photorespiratoryconditions,Inparticular,uorescencecangiveinsightsintotheability 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