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Photosystem IIGovindjee, UniversityofIllinoisatUrbana-Champaign,Urbana,Illinois,USAJan F Kern,LawrenceBerkeleyNationalLaboratory,Berkeley,California,USAJohannes Messinger, UmeaUniversity,Umea,SwedenJohn Whitmarsh, NationalInstitutesofHealth,Bethesda,Maryland,USABasedinpartonthepreviousversionofthisEncyclopediaofLifeSciences(ELS)article,PhotosystemIIbyJohnWhitmarshandGovindjee.PhotosystemII(PSII)isaspecializedproteincomplexthatuseslightenergytodrivethetran
sferofelectronsfromwatertoplastoquinone,resultingintheproductionofoxygenandthereleaseofreducedplastoquinoneintothephotosyntheticmembrane.ThekeycomponentsofthePSIIcomplexincludeaperipheralantennasystemthatemployschlorophyllandotherpigmentmoleculestoabsorblight,areactioncentreatthecoreofthecomplexthatisthesiteoftheinitialelectrontransferreactions,anMn4OxCaclusterthatcatalyseswateroxidationandabindingpocketforthereductionofplastoquinone.PSIIisthesolesourceofoxygenproductioninalloxygenicphotosyntheticorganisms,whichincludeplants,algaeandcyanobacteria.Intheseorganisms,PSIIoperatesinserieswithotherproteincomplexes,includingthePSIreactioncentre,toproducethereducedformofnicote-namideadeninedinucleotidephosphate(NADPH)andadenosinetriphosphate(ATP),whichisusedintheCalvinBensoncycletoproducecarbohydratesfromcarbondioxide.Introduction
Oxygenicphotosynthesisisthephysical-chemicalprocessbywhichplants,algaeandcertainbacteriauselightenergytobuildcarbohydratesfromcarbondioxideandwater,resultinginthereleaseofmolecularoxygenintotheatmosphere.Theproductionofoxygendependsonpho-tosystemII(PSII),auniqueproteincomplexthatremovesELS subject area: BiochemistryHow to cite:Govindjee;Kern,JanF;Messinger,Johannes;andWhitmarsh,John(February2010)PhotosystemII.In:EncyclopediaofLifeSciences(ELS).JohnWiley&Sons,Ltd:Chichester.DOI:10.1002/9780470015902.a0000669.pub2Advanced articleArticle Contents.Introduction
.Organization, Composition and Structure
.Light Capture: The Antenna System
.Primary Photochemistry: The Reaction Centre
.Oxidation of Water: The Source of Atmospheric Oxygen
.Reduction of Plastoquinone: TheTwo-electron Gate.Concluding RemarksOnline posting date: 15th February 2010
electronsfromwater
andtransfersthemtoplastoquinone(PQ).Anancientformofphotosynthesisoccursin
certaintypesof
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bacteriathatuselightenergytooxidize
moleculesotherthanwater(Hunteretal.,2009).Fossilevidenceindicatesthat
PSII-containingorganismsemergedmorethanthreebillionyearsago,resultingintheconversion
oftheearthsatmospherefromamildlyreducinganaerobicstatetotheoxygen-richairsurroundingustoday(DesMarais,2000;KastingandSiefert,2002).The
releaseofoxygen
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intotheatmospherebyPSIIenabledthe
evolutionofoxidativerespiration,whichhashadaprofoundimpactonthe
diversityoflifeonourplanet.Seealso:Earth:ChangesThroughTime;Evolution
ofPhotosynthesis;Photosynthesis
Oxygenicphotosynthesisdependsontworeactioncentrecomplexes,PSIIandPSI,thatarelinkedbythecytochromebfcomplexand
mobileelectroncarriers
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(WhitmarshandGovindjee,1999;Figure 1).PSII,the
cytochromebfcomplexandPSIareembeddedinthephotosyntheticmembrane(Figure 1a;
seelegendfordetails)andoperateinseriestotransferelectronsfromwater
tonicotinamideadeninedinucleotidephosphate(NADP+)(seeFigure 1b legendfordetails).TheenergyneededtotransferelectronsfromwatertoNADP+isprovidedbylight,whichis
capturedbythe
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PSIIandthePSIantennasystems.In
plantsandalgaethephotosyntheticmembranesarelocatedinsidechloroplasts,whichare
subcellularorganelles.Inoxygeniccyanobacteria,thephotosyntheticmembranesarelocatedinsidetheplasma
membrane.Seealso:Chlorophyll:StructureandFunction;PhotosystemI;PlantChloroplastsandOtherPlastids
Chloroplastsoriginatedfromoxygenicbacteriathatwereengulfedby
aeukaryoticnonphotosynthetic
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organism.Inbothchloroplastsandcyanobacteria,photosynthetic
membranesformvesiclesthatdefineaninnerandouterwaterspace.Light-driven
electrontransferthroughthePSIIandPSIreactioncentresprovidesenergyforthe
creationofaprotonelectrochemicalpotentialacrossthemembrane.TheenergystoredintheprotonelectrochemicalgradientisusedbyATPsynthasetoproduceATP.
Inadditionto
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oxygen,theproductsofthelight-driven
electronandprotontransportreactionsareNADPHandATP,whichprovidethe
freeenergyneeded
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Stroma2 H+ 2 H+hNADP+NADPHH+
3 H+Lumen2 H2O O24 H+4 H+hYDP680PheoLHCIIQA QBPQCyt
b559PQPCCyt fCyt b6FeSP700PCFNRFdFeSLHClLHClA0A1CF1
CF0PQH2PQH2PQH2YZMn4Stroma2 H+ 2 H+hNADP+NADPHH+3 H+Lumen2 H2O O24 H+4 H+hYDP680PheoLHCIIQA QBPQCytb559
PQPCCyt fCyt b6
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FeSP700PCFNRFdFeSLHClLHClA0
A1CF1CF0PQH2PQH2PQH2YZMn4Photosystem IIATP 3 H+ ADP + Pi
4 nm
Cytochrome b6f
(a) Photosystem II Photosystem I ATP synthase.1.6.1.2.0.8.0.4
Photosystem II~10 ps200 ps100.600 .s
200 .sCyt b6f~1 ps40.200 ps15.200 ns< 1.125 .s2 NADPH~1 ms2 NADP+h200.500 nsComplexPhotosystem I< 1 ms1.20 ms1 msh.2 H2O 50 .s.1.5 ms20 ns.35 .sO2+4 H+P680P680*P700*A0A1 Fx FABFd
FNRPheoQA QBPQ
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FeS Cyt fPC P700Mn4OxCaYzEm(volts)
0.0
0.4
0.8
1.2
(b) 1.6Figure 1 (a)Schematicrepresentation
ofproteincomplexesandcofactorsinvolvedinthelinearelectrontransportandthe
protontransportofphotosynthesisinhigherplants(fordifferenceswithotheroxygenicorganisms,seelaterdiscussionandthetext).(b)TheZschemeshowingthe
energeticsofoxygenic
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photosyntheticelectrontransport.Theverticalscaleshows
theequilibriummidpointredoxpotential(Em)oftheelectrontransportcomponents.Approximate
electrontransfertimesareshownforseveralreactions.Lookingatthecomponentsfrom
thebottomleftofthediagrams:Mn4OxCa(orMn4),tetranuclearmanganeseoxygencalciumcluster,wherex54;Yz,tyrosine-161ontheD1protein;P680,primaryelectrondonorof
photosystemII;P680 ,
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excitedelectronicstateofP680(fordetails,
seetextandFigure 3c);Pheo,pheophytin;QA,atightlyboundplastoquinone;QB,
aplastoquinonethatbindsandunbindsfromphotosystemII;PQ,apoolof
mobileplastoquinonemolecules;themiddleboxrepresentsaproteincomplexcontainingtwomoleculesofcytochromeb6(Cytb6;onlyoneisshown),anironsulfurprotein
(FeS;knownas
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RieskeFeSprotein)andacytochromef
(Cytf);PC,plastocyanin(cyanobacteriaoftenemployCytc6);P700,reactioncentre
chlorophyllaofphotosystemI;P700,excitedelectronicstateofP700;A0,a
specialchlorophyllamolecule;A1,vitaminK;FX,FA,FB,ironsulfurcentres;Fd,ferredoxin;FNR,ferredoxinNADPreductaseandNADP+,nicotinamideadeninedinucleotidephosphate.Figure 1a shows,inaddition,LHC-Iand
LHC-II,light-harvestingcomplexes
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ofphotosystemsIandII,respectively(see
Figure 2b forcyanobacteria),andtheATPsynthasewithcouplingfactors(CF0andCF1).
ThisfigurewasdrawnfortheauthorsbyDmitriyShevela(inthelaboratory
ofJM).
forthereductionofcarbondioxideandthesynthesisandRenger,2008).Thesechemicalreactionsaredrivenbyofcarbohydrates,the
finalproductof
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oxygenicphoto-theprimaryphotochemicalreactionofPSII,
whichresultssynthesis.Seealso:AlgalChloroplasts;Photophosphory-inseparatingapositiveand
anegativechargewithinthelation;Photosynthesis:TheCalvinCycle;Photosyntheticreactioncentre.
TheprimaryphotochemicalreactionisCarbonMetabolism;RubiscogovernedbyEinsteinslawofphotochemistryone
PSIIuseslightenergytodrivetwo
chemicalreactions:absorbed
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photondrivesthetransferofoneelectron.
Fourtheoxidationofwaterandthereductionofplastoquinonephotochemicalreactions
arerequiredtoremovefour(WydrzynskiandSatoh,2005;Lubitzetal.,2008;
Rengerelectronsfromtwowatermolecules,whichresultsinthe
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Photosystem II Photosystem IIhhh.productionofone
moleculeofoxygenandthereleaseoffourprotonsintotheinner
waterphase(thelumen)ofthephotosyntheticmembrane(Figure 2).Thefourelectronsextracted
fromthewatermoleculesaretransferredtotheplastoquinone-bindingsitewhere,inconcertwithfour
StromaHCO3.Fe2+PheoD1ChlD1 ChlD2P680YDYZ
PheoD2QAD2 D1
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CP47CP43QBLumenLHC-IILHC-IICytb559PQPQ PQ
PQPQPsbO PsbPclusterPsbQMn4OxCa2 H2O
Thylakoid membrane
protons
takenupfromtheouterwaterphase(thestroma/cytoplasm;seelaterdiscussion),
twomoleculesofplasto
quinonearereduced:
2H2O.2PQ.4H..4hn! O2.2PQH2.4H.
outin
O2 + 4 H+
(a)h.
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Herewedescribethestructure
andfunctionofPSIIwithoutdiscussingtheexperimentalresultsthatunderlieour
knowledge.Thereferencesattheendofthearticleprovideanentryto
theliteraturedescribingprogressoverthepasthalfcenturyinunderstandingthisubiquitousenzyme,whoseemergencethreebillionyearsagocanbeviewedasa
seminaleventin
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theevolution.
Organization, Composition andStructure
PSIIislocatedinthephotosyntheticmembrane,withtheoxygen-evolvingsitenear
theinnerwaterphase(lumen),andtheplastoquinone-bindingsiteneartheouterwater
phase(stromaineukaryotesandcytoplasmincyanobacteria;Figure 2a andb),anorientationthatenablestheoxidationreductionchemistryofthereactioncentretocontributetothe
protonelectrochemicaldifference
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acrossthethylakoidmembrane(seethelegend
ofFigure 2).Inchloroplasts,thearchitectureofthephotosyntheticmembraneiscomplicated,
withregionsofstackedmembranes(granamembranes)andregionsofnonstackedmembrane(stromal
membranes).PSIIandPSIareunevenlydistributedbetweenthetworegions,withmostofthePSIIcomplexeslocatedinthestackedmembranes,andvirtuallyall
Cytoplasm
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D2 D1HCO3.Fe2+QBQAPheoD1 PheoD2ChlD2ChlD1P680
YDYZPhycobilisomeLumen2 H2OThylakoid membraneCytb559PQPQ PQPQPQCP43 CP47PsbO PsbU
clusterPsbVMn4OxCa(b)O2 + 4 H+
Figure 2 (a)Schematicrepresentationofcomponentsofphotosystem
IIin
higherplantsandgreenalgae.(b)SchematicrepresentationofcomponentsofphotosystemIIincyanobacteria.D1andD2arethereaction
centreproteinsof
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photosystemII(PSII).PSIIuseslightenergy
toremoveelectronsfromwater,resultinginthereleaseofoxygenand
protons(seetheLumensideofthediagram).Theelectronsfromwaterare
transferredviaredoxcofactorsintheproteincomplextoformreducedplastoquinone.Mn4OxCaisthemanganeseoxygencalciumclusterinvolvedinremovingelectronsfromwater;P680is
apairof
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chlorophylls(PD1andPD2)ofPSII;ChlD1
istheprimaryelectrondonorandPheoD1,pheophytinonD1,isthe
primaryelectronacceptor;QA(onD2),boundplastoquinone;QB(onD1),plastoquinonethat
bindsandunbindsfromPSII;Yz(onD1)andYD(onD2)areredoxactivetyrosineresiduesinPSIIwithdifferentfunctionsandPQ,mobile
plastoquinonemoleculesin
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themembrane.CP43andCP47arechlorophyllprotein
complexesof43and47kDathatformtheinner(alsocalled
core)antennasystemofPSII;LHC-II(light-harvestingcomplexII;Figure 2a)denotesallother
PSIIantennaineukaryotes;PsbO(33kDa),PsbQ(16kDa)andPsbP(23kDa)areextrinsicproteinsthatstabilizeandoptimizethewater-splittingcomplexand
itsreactivity(Figure 2a);
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Cytb559isadimericproteinthat
containstheredoxactivecytochromeb559thatmaybeinvolvedinphotoprotectionof
PSII
ofthePSIcomplexeslocatedinthenonstackedmembranes.It
isnotclearwhyPSIIandPSIarespatiallyseparatedinchloroplasts,butlocationofPSIIinthestackedmembranesallowsforveryclosepacking
ofthemembranes
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becauseoftherelativelylimitedextensionof
PSIIintotheouterwaterphase(thestroma)comparedtoPSI.In
chloroplasts,thePSIIcomplexisdenselypackedinthephotosyntheticmembrane,withaverage
centre-to-centre
.
distancesof150250A.Onesquarecentimeterofatypicalleafcontainsapproximately30trillionPSIIcomplexes.Inprokaryotes,the
photosyntheticmembranesdo
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notform
(thisproteinis
alsoessentialfortheassemblyofPSII).Bicarbonate(HCO3;hydrogencarbonate)
showninthefigureasboundtononhaemeiron;itmaybebound
intheformofcarbonate(CO322).Incyanobacteria(Figure 2b),themajorantennaisthephycobilisomethatisextrinsictothemembraneandconnectedtothe
CP47proteinof
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PSIIviaananchorprotein;also,instead
ofPsbPandPsbQasextrinsicpolypeptidesontheluminalside,these
organismshavePsbU(12kDa)andPsbV(Cytc550)proteins.Thisfigurewas
drawnbyDmitriyShevela(inthelaboratoryofJM).
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Photosystem II Photosystem IICytoplasmD2 D1 CP43Mn4OxCaPsbOPsbV
50 .40 .10 .CP47ThylakoidmembraneLumenCyt b559PsbUQAQBCyt b559
Bicarbonate8.8Fe9.0 QBQAPheoD1ChlZD1CarD1YzMn4OxCa Cl.PD1PD2ChlD2ChlD1 ChlZD213.1 .
10.5 .10.4 .13.6 .5.4 .CarD2PheoD2Cyt b559YDFeD2D1CP43CP47(a)(b)(c)ENCYCLOPEDIAOFLIFESCIENCES&2010,JohnWiley&
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Photosystem II
Figure 3 Structureofthephotosystem
II(PSII)complexfromthethermophiliccyanobacteriumThermosynechocuuselongatus(Guskovetal.,
2009).(a)Aviewofonemonomerofthecomplex;theviewdirection
isalongthemembraneplane.Dimensions,inangstroms,areindicatedontherightside.Proteinsubunitsareshownascartoonandcolouredinyellow(D1),
orange(D2),red
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(CP47),magenta(CP43),cyan(Cytb559),green
(PsbO),blue(PsbU),salmon(PsbV)andgrey(remainingsmallsubunits).Cofactorsare
shownassticksingreen(chlorophylls),orange(carotenoids)andblue(haeme).Thelocation
ofthecatalyticsiteofwateroxidation,theMn4OxCacluster(x44),ishighlightedattheluminalside.(b)ThemembraneintrinsicpartofPSII;this
viewisonto
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themembraneplanefromthecytoplasmicside;
thecolouringisasinpanel(a).ThereactioncentredomainD1
andD2andtheantennasubunitsCP43andCP47arehighlightedbyellipses,
andthepositionoftheCytb559,thenonhaemeiron(bluesphere)andofQAandQBarelabelled.(c)Redoxactivecofactorsinthe
reactioncentre.At
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therightside,thecentre-to-centredistances,in
angstroms,betweenthecofactorsareindicatedstarting(frombottomtotop)from
Ca(yellowsphere)oftheMn4OxCacluster,totheOHofthetyrosine,
labelledasYz,chlorophyllPD1(ofP680),ChlD1(green),pheophytinPheoD1(yellow)andplastoquinoneQA(magenta)andthedistancesbetweenQA,Fe(bluesphere)and
QBaregiven
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directlyinthefigureinangstroms.Bicarbonate
(moreappropriatelycalledhydrogencarbonate)isshowntobeboundtothe
nonhaemeiron.(Wedonotexcludethepossibilitythattheboundspeciesmay
alsobecarbonate).Thefigurewasgeneratedbyusingthecoordinates(pdbcode:3BZ1,3BZ2)ofthe2.9A.resolutioncrystalstructure.Thisfigurewas
drawnbyone
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ofus(JFK).
stackedmembranes
andthePSIIandPSIcomplexesappeartobeintermixed.
ThereisaremarkablesimilarityinthestructureandfunctionofPSIIin
higherplants,algaeandbacteria.Furthermore,thePSII,PSIand(anoxygenic)bacterialreactioncentresshareseveralstructuralfeatures,indicatingancientevolutionarylinks(Sadekaretal.,
2006).Incontrast,
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thestructuresofthelight-capturingantennasystems
invariousphotosyntheticsystemsarequitedifferent,indicatingmultipleorigins.Seealso:
EvolutionofPhotosynthesis
PSIIiscomposedofacentralreactioncentre
coresurroundedbyalight-harvestingantennasystem(Figure2a andb).ThereactioncentrecoreincludesD1andD2polypeptidesthatbindthecofactorsofthephotochemical
chargeseparationand
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electrontransfercarriersthatoxidizewaterand
reduceplastoquinone(Figure 1,Figure 2 andFigure 3).Theantennasystemconsistsofproteincomplexes
thatcontainlight-absorbingmolecules(chlorophyllorphycobilinsandotheraccessorypigments;seelater
discussion)whichoperateinconcerttocapturephotonsandtransfertheexcitationenergytoreactioncentreswhereprimarychargeseparationoccurs.Inmosteukaryoticorganisms
(e.g.higherplants
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andgreenalgae),thelight-harvestingcomplexes
areorganizedasaninnerantennasystemlocatedclosetothereaction
centre,andaperipheralantennasystemcomposedofpigmentproteinsknownaslight-harvesting
complexII(LHC-II;Lhcb16)(Figure 2a).Inothereukaryoticorganisms(e.g.redalgae)andinmanyprokaryoticorganisms(e.g.mostcyanobacteria),thelight-harvestingcomplexes,
whichareknown
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asphycobilisomes,areextrinsictothephotosynthetic
membraneandusephycobilinsratherthanchlorophyllstocapturelight(Figure 2b).The
PSIIreactioncentrecomplex,excludingtheperipherallight-harvestingcomplexes,iscomposedofmore
than20differentpolypeptides,mostofwhichareintegralmembranepolypeptides(Figure 3a andb).Theonlyknownmembraneperipheralproteinsarelocatedinthelumen.In
additiontothe
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differencesbetweentheantenna,thephotosystemsII
ofhigherplantsandcyanobacteriadifferwithrespecttothecompositionof
thesemembraneperipheralproteins(seeFigure 2a andb)asplantPSIIhavePsbO(33
kDa),PsbP(23kDa)andPsbQ(16kDa)andcyanobacterialPSIIPsbO(33kDa),PsbU(12kDa)andPsbV(Cytc550)(seelaterdiscussion).Table 1 lists
thegenesencoding
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thePSIIpolypeptides,togetherwiththe
polypeptidemolecularweightsandtheirputativefunctions.Seealso:ChloroplastGenome
PSIIcontainsatleasteightdifferenttypesofredoxcomponentsthat
havebeenobservedtoundergolight-inducedelectrontransfer.Thesecomponentsincludechlorophyll,pheophytin,plastoquinone,tyrosine,manganese,iron,cytochromeb559andcarotenoid(Figure 3).However,only
thefollowingredox
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componentsareknowntobeinvolvedin
theelectrontransferfromwatertotheplastoquinone:thewater-oxidizingmanganeseoxygencalcium
cluster(Mn4OxCa,wherex4isthenumberofbridgingoxygens),atyrosine
(Yz),achlorophylldimer(PD1andPD2),whichisalsoreferredtoasP680,historicallythoughttobetheprimaryelectrondonor,butseethe
discussiononthe
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primarychargeseparationeventbelow),amonomeric
chlorophyll(ChlD1),apheophytin(PheoD1)andtwoplastoquinonemolecules(QAandQB)(Figure 2).
Theprimaryelectrondonormoleculeinvolvedinthefirstchargeseparationreactionis
ChlD1(Figure 3c;seethesectiononPrimaryphotochemistry:Thereactioncentre).
Afterdecadesofeffortbymanyresearchers,thethree-dimensionalstructureof
thePSIIinner
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corefroma.
thermophiliccyanobacterium
wasdeterminedto3.8AresolutionbyHTWitt,WSaengerandcoworkers
(Zounietal.,2001).FollowingtheworkofWittandcoworkers,
.
morehighlyresolvedPSIIstructures(3.72.9Aresolution)havebeendetermined(KamiyaandShen,2003;Ferreiraetal.,2004;Lolletal.,2005;Guskov
etal.,2009).
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ThePSII
.
reaction
centrecoreis100Aacross(intheplaneof.
the
membrane)andextendsapproximately10Aintothe.
stromalaqueousphaseand
approximately55Aintothelumen(Figure 3a).AtthecentreofPSIIaretheD1andD2polypeptides,whichformtwobranchesthatprovidetheprimary
scaffoldingforthe
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electroncarriers(Figure 3aandc).TheMn4OxCa
clusterisligatedbyaminoacidsfromtheD1polypeptideandthe
innerantenna(alsocalledcoreantenna)proteinCP43(Figure 4;Table 1).Inadditionto
thesecomponents,thePSIIreactioncentrecoreandthetwoinner(orcore)antennaproteins(CP43andCP47)bind29moleculesofchlorophylla,12
carotenoids,onenonhaeme
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iron,oneormorechlorideionsand
onecarbonate
222
(CO3)orhydrogencarbonate(HCO3
)ion(Figure 3bandc).AllPSIIcomplexescontaincytochromeb559,ahaeme
proteincomposedoftwopolypeptideslocatedattheperipheryofthecomplex,aswellasatleast12smallmembraneintrinsicproteins(Figure 3;Table 1).In
plants,the
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Photosystem II Photosystem IITable1PhotosystemIIgenes,
proteinsandputativeroles(excludingantennalight-harvestingcomplexII)
Mass
IntegralorGeneaProtein(kDa)bperipheralcCommentspsbA(c)D139I
(5)D1(andD2)formthereactioncentrecorethatbindsmostofthePSIIelectrontransportcomponents;QBbindstoD1psbB(c)
CP4756I
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(6)BindsantennachlorophyllapsbC
(c)CP4347I(6)Bindsantennachlorophylla,providesaligand
totheMn4OxCacomplexpsbD(c)D239I(5)D2(and
D1)formthereactioncentrecorethatbindsmostofthePSIIelectrontransportcomponents;QAbindstoD2psbE(c)aSubunit9.3
I(1)Binds
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b-haeme;maybeinvolvedinphotoprotectionCyt
b559psbF(c)bSubunit4.5I(1)Bindsb-haeme;may
beinvolvedinphotoprotectionCytb559psbH(c)PsbH7.8I(1)
Canbephosphorylatedinplants,involvedinrepairofD1,optimizeselectronflowinprokaryotespsbI(c)PsbI4.2I(1)Stabilizationandassembly
ofthecomplex
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psbJ(c)PsbJ4.2I(1)
InfluencesplastoquinoneexchangeandelectronflowonacceptorsidepsbK(c)
PsbK4.3I(1)StabilizationofthecomplexpsbL(c)PsbL4.5
I(1)Influencesplastoquinonebindingandelectronflowonacceptorside,stabilizesdimerizationpsbM(c)PsbM4I(1)Mediatesinteractionbetweenthemonomers
inthedimeric
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complexpsbO(n)PsbO27P
(0)Involvedinoptimizingoxygenevolution,bindspossibleregulatory(MSP)calciumpsb
P(n)PsbP20P(0)Involvedinoxygenevolution;eukaryotespecific(in
prokaryotesaPsbP-likeproteinisfoundinsubstoichiometricamounts)psbQ(n)PsbQ17P(0)Involvedinoxygenevolution;eukaryotespecific,aslightlydifferent
formofPsbQ
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isalsopresentinprokaryotes,optimizingoxygen
evolutionactivitypsbR(n)PsbR10I(1)Neededforstable
assemblyofPsbPinthecomplex,influencesdonorandacceptorsideelectrontransfer;
eukaryotespecificpsbS(n)PsbS21I(4)InvolvedinnonphotochemicalquenchingpsbT(c)PsbT3.8P(1)StabilizesQA-bindingsite,supportsdimerization
psbTn(n)
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PsbTn3.2P(0)Unknownfunction;eukaryote
specificpsbUPsbU10P(0)Maybeinvolvedincalciumand
chlorinedeliverytotheOEC;prokaryotespecific;butalsofoundinbrownand
redalgaepsbVCytc55012P(0)Bindsc-haeme,optimizesoxygenevolutionactivity;prokaryotespecific;butalsofoundinbrownandredalgae
psbW(n)
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PsbW6I(1)InvolvedinPSII
dimerization;eukaryotespecificpsbX(c)PsbX4I(1)Unknownfunction
psbY(c)PsbY4.7I(1)UnknownfunctionpsbZ(c)PsbZ
11I(2)Connectiontoexternalantennasubunitsinplantsycf12(c)Ycf125I(1)Unknownfunction(Psb30)
Notes:Cyt,cytochrome;I,
integral;MSP,manganese-stabilizing
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protein;OEC,oxygenevolvingcomplex;P,peripheral
andPS,photosystem.WeacknowledgethehelpofKimberlyWegner,JohannaRoose,
HimadriPakrasiandJulianEaton-Ryeinthepreparationofthistable.aForeukaryotic
organisms,theletterinparenthesesindicateswhethernuclear(n)orchloroplast(c)geneisencoded.bMasscalculatedfromaminoacidsequence.cNumberofahelices
isgivenin
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parentheses.
luminalsideofthe
complexisshieldedbythreemembrane-areanalogoustothe16kDaand
23kDaproteinsfoundextrinsicproteinsknownasthe33kDaorPsbO
protein,theineukaryoticcells.Anotabledifferencebetweencyano16kDaorPsbQproteinandthe23kDaorPsbPprotein.Inbacteriaandplants
isthepresence
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ofcytochromec550cyanobacteria,twoadditionalextrinsic
proteins,PsbUand(PsbV)incyanobacteria.AlthoughthecytochromePsbV,arepresent
attheluminalside,asaretwolesstightlyundergoeslight-activatedredoxreactions,
itsroleinPSIIis(ortransiently)boundproteins,PsbPandPsbQ,whichunknown.
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Asp170D2CP436.5Asp170 Asp170Glu189
Glu189His332His332His332Glu189Chl PD1Yz(Tyr161)(a)(b) (c)Photosystem IIAsp170
D2CP436.5Asp170 Asp170Glu189Glu189His332His332His332Glu189Chl PD1Yz(Tyr161)
(a)(b) (c)Photosystem IIFigure 4 ThecatalyticsiteofwateroxidationinphotosystemII(PSII);aminoacidsareshownwiththeir3-lettercodes.(a)Structuralmodelfor
themetalions
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andaminoacidligandsoftheMn4OxCa
cluster,theredoxactivetyrosineYz(Tyr161)andthechlorophyllPD1,as
derivedfromthe2.9A.resolutioncrystalstructure(Guskovetal.,2009);the
viewisalongthemembranewithlumenatthebottomandcytoplasmatthetop.Theproteinsurroundingisshownincartoonmodeinlight
yellow(D1),orange
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(D2)andmagenta(CP43).Mn(purple),Ca2+
(orange)andCl2(green)ionsareshownasspheres,ligatingaminoacids
assticks.Thenitrogenandoxygenatomsoftheaminoacidligandsare
colouredinblueandred,respectively;thecarbonatomsarecoloureddependingonthesubunittheaminoacidbelongsto:yellowforD1,orangefor
D2andmagenta
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forCP43.(b)ModelfortheMn4OxCa
clusterinthedarkstableS1stateofthewateroxidizingcomplex,
obtainedfromorientationdependentX-rayspectroscopyonPSIIsinglecrystals(Yanoetal.,
2006)embeddedintheligandenvironmentderivedfromthecrystalstructure.Thecolouringandtheviewdirectionisasinpanel(a),bridgingoxygensare
shownassmall
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redspheres.(c)Theoreticalmodelforthe
Mn4OxCaclusteranditsfirstligandsphereintheS1statederived
fromdensityfunctionalcalculations(Siegbahn,2008);thecolouringandtheviewdirectionis
asinpanel(a);thebridgingoxygensareshownassmallredspheres.Thismodelalsoincludessomewater/hydroxidegroups(hydrogensshowningrey)as
ligandstothe
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manganeseandcalciumions.Thisfigurewas
drawnbyoneofus(JFK).
Thepathwayandrate
ofelectrontransferwithinthePSIIcomplexmustberigorouslycontrolledforefficient
operationintheelectrontransportchain.Oneofthekeyfactorscontrollingelectrontransferfromoneredoxsitetoanotheristhedistancebetweenthe
components(Moseret
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al.,1992),whichisdeterminedbythe
orientationandpositionoftheredoxcomponentsestablishedbytheproteinscaffolding
ofthecomplex.Theimportanceofdistanceincontrollingelectrontransferisdemonstrated
bytheremarkablehomologybetween(anoxygenic)bacterial
reactioncentresandplant,algalandcyanobacterialPSIIreactioncentres(Sadekaretal.,2006).Anotherfactor
incontrollingelectron
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transferisproteindynamics,whichappearsto
playanimportantroleinthestabilizationoftheprimarychargeseparation
andmanyotherreactionswithinPSII.Notethatthecentralcoreformedby
theD1andD2polypeptidesformsasymmetricalstructure,whichprovidestwopotentialelectrontransportpathwaysthroughthereactioncentre.However,onlyonepathwayis
active(Figure 2).Although
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theelectrontransferpathwaysin
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Photosystem II
Table2Distributionof
chlorophyllsandcarotenoidsinphotosystemIIfromhigherplants
Protein
NumberofchlorophyllmoleculesNumberofcarotenoidmoleculesReactioncentreproteins(D1/D2)6
Chla2InnerantennaproteinsCP4716Chla5CP4313Chla3(+2boundbysmallsubunits)CP24+CP26+CP2918Chla+9
Chlb6
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OuterantennaproteinsOnetightlybound+onemedium-bound
48Chla+36Chlb24LHC-IIbtrimerLooselyboundLHC-IIb+otherLHCs
Approximately100Chl(a+b)Approximately30CarPhotosystemII(reactioncentre+antennaApproximately250
Chl(a+b)Approximately70Carsystem)
thereactioncentrearetightlycontrolled,thereappeartobemultiplepathwaysforprotontransferfromthe
outerwaterphase
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totheQBsite,andforthe
releaseofprotonsfromtheMn4OxCaclusterintotheinnerwaterphase
(thelumen).
Light Capture: The Antenna System
Oxygenicphotosynthesisisdrivenbyvisiblelight
thatisabsorbedbychlorophyll/phycobilinsandotherpigments
(e.g.carotenoids)boundtothelight-harvestingproteinsthatsurroundthePSIIandPSIreactioncentres
inthephotosynthetic
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membrane.Themajorlight-absorbingpigmentinplants
andmanyalgaeischlorophyll,whichisacyclictetrapyrroleinwhich
thenitrogensofthepyrrolesarecoordinatedtoacentralmagnesiumion.Chlorophyll
isagreenpigmentthatstronglyabsorbsblueandredlight.Plantsandmanytypesofalgaecontaintwotypesofchlorophyll,aandb,
whichdifferby
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asinglegroupononeofthe
pyrrolerings.Incontrasttoplants,cyanobacteriaandredalgaeemployphycobilins
(thatareopen-chaintetrapyrrolesboundcovalentlytoproteins)asthemajorlight-absorbingpigments,
whichtransferexcitationenergytochlorophylla.Inmanyplantsandalgae,theantennasystemservingasinglePSIIreactioncentrecontains200250chlorophyll
and6070carotenoid
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molecules(Table 2).Carotenoids,whicharelinearpolyenes
thatabsorbblueandgreenlight,serveadualroleinphotosynthesis.
Theyareimportantlight-harvestingpigments,significantlyenhancingthespectrumofvisiblelightabsorbed
bytheantennasystem.Inaddition,carotenoidsserveacriticalroleinprotectingthephotosyntheticapparatusfromdamageassociatedwithlightcapture.Theseprotectiveprocesses
includedownregulation,which
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protectsmembranecomponentsunderconditionsofexcess
light,andquenchingofexcitedtripletstatesofchlorophyllthatcaninduce
oxidativedamage(Demmig-Adamsetal.,2006;Franketal.,1999).Thestructureof
oneofthelight-harvestingproteincomplexes(LHC-II)associatedwitheukaryoticPSIIhasbeendeterminedbyelectroncrystallography(Ku.hlbrandt
etal.,1994)and
byX-raycrystallography
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(seereviewbyBarrosandKu.hlbrandt,
2009).TheLHC-IIcomplexformsatrimer,witheachsubunitbindingeight
moleculesofchlorophylla,sixmoleculesofchlorophyllbandfourmoleculesof
carotenoids.Seealso:Chlorophyll-bindingProteins
Photosynthesisisinitiatedbyabsorptionofaphotonbyanantennamolecule,whichinducesarapid(10215s)
transitionfromthe
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electronicgroundstatetoanexcitedelectronic
state.Theexcitedstatedecaysrapidly(10213s)byvibrationalrelaxationto
thefirstexcitedsingletstate.Thefateoftheseshort-livedexcitedstatesis
guidedbythestructureandcompositionofthelight-harvestingproteinpigmentcomplexes.Becauseoftheproximityofotherantennamoleculeswiththesameorsimilar
electronicenergylevels,
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theexcitedsingletstateenergyhasa
highprobabilityofbeingtransferredtoaneighbouringmoleculebyaprocess
knownasFo.rsterResonanceEnergyTransfer(FRET)(Lakowicz,1999).Transferofexcitation
energybetweenantennamoleculesdependsontheinteractionbetweenthetransitiondipolemomentsofthedonorandacceptormolecules.Theprobabilityoftransferfallsoff
quicklyasthe
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distancebetweenthepigmentsincreases(inmany
cases,therateisproportionaltoR26,whereRisthedistance
betweenthetransitiondipoles),anddependsstronglyontheoverlapoftheemission
spectrumofthedonormoleculeandtheabsorptionspectrumoftheacceptormolecule,aswellastherelativeorientationofthedonorandacceptorpigments.
Aschematicrepresentation
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ofexcitationenergymigrationovertheantenna
systemisshowninFigure 5.Becausethefirstexcitedsingletstateof
chlorophyllaisenergeticallylowerthanthatofchlorophyllborthecarotenoids,
excitationenergyisrapidlylocalizedonthechlorophyllamolecules.Asaconsequence,excitationenergythatescapestheantennasystemasfluorescencecomesalmostentirely
fromchlorophylla.
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Photosyntheticantennasystemshaveevolved
tobehighlyefficientatguidingexcitedstateenergytoareaction
centretopromoteprimaryphotochemistry,ratherthanallowingtheenergytobelost
asheatorfluorescence.However,ifareactioncentreisunable
Notes:Car,carotenoid;Chl,chlorophyll;CP,chlorophyll-bindingprotein;LHC,light-harvestingcomplex.
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Photosystem II
Antenna system with an open reaction centre
Fluorescence (F0)
Light
(a)Antenna system with a closed reaction centre
Fluorescence (Fmax)
Light
(b)
Figure 5 Schematicrepresentationshowingexcitationenergytransfer(smallredarrows)fromonechlorophyllmolecule
toanotherinagenericLHC-typeantennasystemofhigherplants.Greendiscsrepresentchlorophyllsaandb,andyellowdiscsrepresentcarotenoids;thedarker
greendiscin
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themiddleofpanel(a)representsan
openreactioncentreandthelightergreendiscinthemiddleof
panel(b)representsaclosedreactioncentre.Whenthereactioncentreisopen
(a),mostenergyisusedforchargeseparation,andthesystememitsminimalchlorophyllafluorescence(labelledasF0);whenthereactioncentreisclosed
(b),chlorophylla
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fluorescenceismaximal(Fmax).Thisfigurewas
drawnbyDmitriyShevela(inthelaboratoryofoneofus,JM).
toundergoprimarychargeseparation(closed),thentheprobabilityofthe
excitationenergygoingintofluorescenceorheatishigher(cf.Figure 5a andb).Measurementsofphotosynthesisunderoptimalconditionsshowthatover90%ofabsorbedphotons
canbetrapped
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byareactioncentreandpromotecharge
separation.However,environmentalconditionsmayimposelimitationsonphotosynthesisthatsignificantlylimit
therateofelectrontransport,whichsignificantlyincreasesthefractionofabsorbedlight
energythatgoesintofluorescenceandheat.Measurementsofchlorophyllfluorescenceprovideaneffectiveandnoninvasivemethodformonitoringphotosyntheticperformanceunderremarkablywiderange
ofconditionsand
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environments(PapageorgiouandGovindjee,2004).
Primary Photochemistry: The ReactionCentre
Thereisconvincingevidencethattheprimaryphotochemicalreaction
inPSIIresultsinchargeseparationbetweenPD1andPheoD1within8ps
(Greenfieldetal.,
+2+
1997),creatingPD1/PheoD1(alsodenotedasP680/Pheo2).However,thereisuncertaintyconcerninghowthis
charge-separatedstateis
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formed,whichisdueinpartto
theproximityofthefourchlorophyll(ChlD1,PD1,PD2andChlD2)andtwopheophytin
(PheoD1andPheoD2)molecules(Figure 3c).Becausetheelectronicenergylevelsofcorechromophore
moleculesarenearlysimilar,excitationenergywithinthereactioncentreequilibratesrapidly(within1ps)betweenthecorechlorophyllandpheophytinmoleculesbeforechargeseparation
occurs.Itappears
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thatthisensembleofmoleculesformsthe
excitedstateoftheprimarydonorandthatchargeseparationcanoccur
betweendifferentchromophoresinthereactioncentre(Grootetal.,2005).(Thus,several
authors(see,e.g.RengerandRenger,2008)haveadoptedanalternatedefinitionforP680fortheentireensembleofpigmentmolecules;however,wepreferto
keeptheoriginal
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definitionofP680.)Afewpicosecondsafter
theformationoftheexcitedstate,theprimaryphotochemicalreactionofPSII
begins,mostlikelybyelectrontransferfromthemonomericChlD1tothePheoD1,
whichisfollowedbyasecondelectrontransfer
+2
leadingtotheformationofPD1/PheoD1(Dineretal.,2001;Holzwarthet
al.,2006;Di
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Donatoetal.,2008).
The
highefficiencyofreactioncentrephotochemistrydependsonpreventingrecombinationofthe
primarychargeseparation,whichisaccomplishedbytherapid(intherange
2
of200ps)transferoftheelectronfromPheoD1toQA(Figure
2
1b,Figure 2a andb andFigure 3c).FromQA,the
electronistransferred
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toanotherplastoquinonemoleculeboundatthe
QBsite.Aftertwophotochemicalturnovers,QBbecomesfullyreducedandprotonated,
formingPQH2,whichdebindsfromPSIIandentersthehydrophobiccoreofthe
photosyntheticmembrane.Concurrentwithelectrontransfertoplastoquinone,thetyrosineresidue(Yz)ontheD1polypeptidetransfersanelectronto(PD1PD2)+.Electronsforthereduction
ofoxidizedYz
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(Yz.)areextractedfromtheMn4OxCa
cluster,whichisthecoreofthewater-oxidizingcomplex.(ThenotationYz
.denotesaneutralradicalduetoprotontransfertothenearbyhistidine
residue.)TherateofelectrontransferfromYztoP680+rangesfrom20nsto35ms,dependingontheredoxstatesofthecomponents
involvedinwater
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oxidation(Figure 1b andFigure 3c).
Oxidation of Water: The Source ofAtmospheric Oxygen
In1969,PierreJoliotandcoworkersmeasuredoxygenreleaseduringsuccessive
single-turnoverlightflashesindark-adaptedalgae(Joliotetal.,1969).Theyfoundthat
the
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Photosystem II Photosystem IIyieldofoxygenplottedas
afunctionoftheflashnumberremovesasingleelectronfromthe
water-oxidizingcomexhibitedaperiodicityoffour(Figure 6a).Thisclassicplex,whichadvancesPSII
tothenexthigherSstateuntilexperimentdemonstratedthateachPSIIcomplexoperatestherearefouroxidizingequivalentsinthecomplex,leadingindependentlyand
thatfourphotochemical
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reactionstotheoxidationoftwomolecules
ofwater.Identifyingthearerequiredforthereleaseofoneoxygen
molecule(Joliotchemicalstepsleadingtowateroxidationhasproventobeand
Kok,1975).Theperiodicityoffourwasreadilyachallengingproblem.ItappearsthatnostableOOexplainedbythechemistryofwateroxidation,but
theintermediateis
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formeduptotheS3state(Messinger
etal.,observationthatthemaximumoxygenyieldoccurredon1995;Hillier
andWydrzynski,2000;HillierandMessinger,thethirdratherthanfourthflash,and
thattheperiodi-2005),andthattheformationofmolecularoxygenoccurscitydisappearedafterseveralcyclesindicatedanunex-duringtheS3!S4!S0transition,eitherthroughtwo
pectedlevelof
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complexityinthemechanismofwatersequential
two-electronsteps,orthroughoneconcertedoxidation.four-electronoxidationevent(seelater
discussionand
OnthebasisofJoliotsobservationsandtheirown
HillierandMessinger,2005;McEvoyandBrudvig,2006;experiments,Koketal.(1970)showedthattheperiodBrudvig,2008;MessingerandRenger,2008).Thecomplete
fouroscillationis
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independentofthenumberofactivewater-oxidation
cycleresultsintheproductionofonePSIIcentresanddevelopedan
elegantmodelofwateroxygenmolecule,thereleaseoffourprotonsintothe
inneroxidationinwhichtheoxygen-evolvingcomplexcanexistwaterphase(theluminalphase)andthesequentialtransferinoneofthefiveoxidationstates,
labelledS0,S1,S2,S3and
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offourelectronsthroughthereactioncentre
totheplasS4(Figure6b).InKoksmodel,eachphotochemicalreactiontoquinonepool.
Seealso:OxygenProduction
Mn3+Mn3+
Mn4+Mn4+
.eto Yz
eto Y .
z
S1
1
4
H+ +
Mn3+Mn3+ Mn3+Mn4+
S2
Mn3+Mn4+ S0 Mn4+Mn4+
H+ H+
O2 2 .
eto Y
z
H+
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2 H2O
+
+
S4 3S3
3 7 1115 19
Flash number
.
(a) (b) eto Yz(I) S4 (II) S3Yz (III) S3H
H+ H+
Y
Hz
O Ca
HOOH OO
Mn4+ OO
O+ O
O Ca Mn4+
Mn3+
O (Mn4+)3 Mn3+(Mn4+)2OOMn4+ O (Mn4+)2Mn3+
(Mn4+)3
O
0.750.500.25Oxygen yield per flash(c)Figure 6 Theoxygencycle(alsocalledtheoxygen
clock)ofphotosystem
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II(PSII).(a)OxygenyieldfromPSII
asafunctionofflashnumber(oxygencycle)(seeJoliotandKok,
1975).(b)Oneofthecurrentmodelsofthestepsinoxygenevolution
inPSII.SeetextandJoliotandKok(1975)fordetails.(c)SimplifiedschemesforthreecurrentlydiscussedpathwaysfortheOObondformationat
theMn4OxCacluster
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inphotosystemII.Thethreedisplayedmechanisms
differinthewayhowthesubstratewatermolecules(termwaterincludes
herealldeprotonatedandpartiallyoxidizedwater-derivedligands)arebound,andtheOO
bondformationisinitiated:(I)viaanucleophilicattackmechanism(S4isshown);(II)aradicalmechanism(S3Yz.isshown)or(III)anoxidative
couplingoftwo
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hydroxogroupswithinanequilibriuminthe
S3state.Inthelatterexamplethecomplexedoxowouldrepresenta
minorfractionofthecentres,butonlythisfractionwouldbeoxidizedby
Yz..Forfurtherdetailsseetextandthereferencesstatedtherein.ThisfigurewasdrawnbyDmitriyShevela(inthelaboratoryofoneof
us,JM).
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Photosystem II Photosystem IIToaccountfortheobservation
thatthemaximumoxygenyieldoccursonthethird,ratherthanthe
fourthflash(Figure 6a),Koketal.(1970)proposedthatmostofthewater-oxidizing
complexesareintheS1stateindark-adaptedPSIIreactioncentres.Asaconsequence,theS4stateisreachedafterthreeflashesresultingin
thereleaseof
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oxygen.Toaccountforthesmallyield
ofoxygenonthesecondandfourthflash,andthelossof
periodicityastheflashnumberincreased,Koketal.(1970)assumedthatin
somePSIIcomplexesashortsaturatinglightflashmayfailtoadvancetheS-state(misses),whereasinothercomplexestheflashmaypromoteatwo-state
advance(doublehits).
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TheKokmodelsuccessfullyexplainedtheflash
dependenceofoxygenevolutionandcontinuestoguideresearchintothemechanism
ofwateroxidationandoxygenreleasebyPSII(MessingerandRenger,2008).
Thecoreoftheoxygen-evolvingcomplexisaninorganicclusteroffourmanganeseionsandonecalciumionheldtogetherbyseveralm-oxobridges.
TheMn4OxCacluster
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(x4)islocatedontheluminal
sideoftheD1proteinandhasoneligandfromtheCP43
protein(Figure 4).TheMn4OxCaclusterissurroundedbyaproteinmicro-environmentthat
includesD1andD2proteins,theluminalextensionsoftheCP43andCP47proteinsandseveralextrinsicpolypeptides(Figure 2 andFigure 3).Althoughtheproteinsphereserves
toshieldthe
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water-oxidizingcomplexfromtheinneraqueousphase,
channelsexistfortheentryofsubstratewaterandthereleaseof
molecularoxygenandprotons.Recentlyachloride-bindingsitehasbeenidenti
.
fiedapproximately67AfromtheMn4OxCacluster(Figure 4;Guskovetal.,2009).Althoughchloridehasbeenshowntoinfluencewater-oxidation,therelativelydistant
locationfromthe
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clustermakesitdifficulttoproposea
mechanism.Onepossibilityisthatchlorideplaysaroleinstabilizingthe
protonnetworksurroundingtheMn4OxCacluster(OlesonandAndreasson,2003).
As
aforementioned,thestructureofthePSIIreaction.
centreisnowavailableat3.52.9Aresolution(Ferreiraetal.,2004;Lolletal.,2005;Guskov
etal.,2009),
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andreasonablydetailedmodelsfortheMn4OxCa
clusterhavebeenproposedbasedonthesestructuresandonpolarizedExtended
X-rayAbsorptionFineStructure(EXAFS)spectroscopy(Yanoetal.,2006).Incombinationwith
experimentaldatathatincludesFourier-TransformInfraRed(FTIR)andElectronParamagneticResonance(EPR)spectroscopy,aswellasmassspectrometryanddetailedtheoreticalcalculations,the
goalofunderstanding
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themolecularmechanismofwateroxidationappears
tobewithinreach(Siegbahn,2008;Sprovieroetal.,2008;Zeinet
al.,2008).Figure 4b andcshowtwooftheproposedgeometricarrangementsofthe
manganeseandcalciumions.Thebindingsitesforsubstratewaterarespeculative,withatleastonewatermoleculeboundintheS0andS1states,
andtwowater
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moleculesboundintheS2andS3
states.Thereisevidencethatcalciumisinvolvedinbindingonesubstrate
watermoleculeandthatmanganeseisinvolvedinbindingatleastoneof
thetwowatermolecules.
Oneofthechallengesinmodellingwateroxidationisaccountingforthepatternofprotonreleaseintothelumen
duringtheS0!S1,S1!S2,S2!S3
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andS3!(S4)!S0transitions(Figure 6b).Theproblemis
thattheprotonsappearinginthelumencouldcomefromaminoacids
nearthewateroxidationsiteratherthandirectlyfromthecatalyticstepsinvolved
inwateroxidation(seeSuzukietal.,2009andreferencestherein).
AstheMn4OxCaclustertransitionsfromoneS-statetoanother,theearly
oxidationstatesmust
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bestabilizedlongenoughtoenablethe
relativelyslowwater-oxidationchemistry( 1ms)tooccurduringtheS3!S4!S0
transition.TheformaloxidationstateofS0includes3Mn3+and1Mn4+
(Kuliketal.,2007;Figure 6b).(Intheliterature,analternativenotationMn(III)3Mn(IV)isalsousedtodescribetheformaloxidationstateofMninthe
OEC.)Assignmentof
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theseoxidationstatestospecificmanganeseions
withintheclusterhasprovendifficult.Furthermore,chargedelocalizationoverthemanganese
ionsandtheoxygenbridgesandligandsoftheclusterresultinginpartial
chargeshasbeenproposedforsomeS-states.
DuringtheS0!S1transition,anMn3+toMn4+oxidationoccursthatiscoupledtoastructural
changeofthe
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Mn4OxCacluster.Thestructuralchangeappearsto
includeadecreaseinoneoftheMnMndistancesfrom2.85to
.
2.75Aduetodeprotonationofonem-OHbridge(Kulik
etal.,2007).IntheS1!S2transition,anotherMn3+toMn4+
oxidationoccurs,butwithoutanysignificantstructuralchangeandnosignificantproton
releaseisobserved.
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Thus,intheS2statetheMn4OxCa
clusterhasanadditionalpositivecharge.TheS2!S3transitioninvolvestherelease
ofaproton,whichisfollowedbytheoxidationoftheMn4OxCacluster
bytyrosineYz..Thenatureofthisoxidationiscontroversial
ithasbeenproposedtobeMn3+toMn4+oxidation,oran
oxidationofa
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moxobridge.TheS2!S3transitioninvolvesa
significantstructuralchangethathasyettobefullycharacterized.
DuringtheS3!S4!S0transition,theOObondisformedandtwoprotonsare
released.TheformationoftheOObond,acriticalstepinwateroxidation,requiresactivationofthetwosubstratewatermolecules.Threepossibilitieshavebeen
proposed(Figure 6c):(I)
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Oneofthesubstratewatermolecules(bound
toMn)isdeprotonatedandbecomeselectrophilicduringtheS-statecycleby
successiveoxidationoftheligatingMnion.Thisspeciesisdescribedinthe
S4stateasMn4+=O.,Mn5+=Oor
Mn4+:O+
andisthoughttobeattackedbythesecond(nucleophilic)substratewatermolecule,whichis
activatedandpositioned
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bybindingtoalowervalentmanganese
and/orcalciumandmaybepartiallydeprotonated.(II)Duringoxidationofthe
Mn4OxCacluster,oneoftheoxygenbridgesoranoxygenligand(originatingfrom
substratewater)becomespartiallyoxidizedforminganoxygenradical,whichcanformtheOObondinaradical-likemechanismwithasecondoxygenspecies
thatmaybecoordinated
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tomanganeseand/orcalcium.(III)Inthe
S3state,asmallfractionoftheMn4OxCaclustersmaycontainthe
OObondintheformofacomplexedperoxide,which
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OFLIFESCIENCES&2010,JohnWiley&Sons,Ltd.www.els.net
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Photosystem II
ispostulatedtobe
thespeciesthatisoxidizedbyYz.inthenexttransition.
InthismodeltherateoftheS3!S4transitiondependsontheequilibrium
constantbetweentheopenandclosedformsoftheS3Yz.state(forreviewsseeHillierandMessinger,2005;McEvoyandBrudvig,2006;Brudvig,2008;
MessingerandRenger,
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2008;Lubitzetal.,2008).Seealso:
OxygenProduction
Reduction of Plastoquinone: TheTwo-electron Gate
Plastoquinoneplaysakeyrole
inphotosynthesisbylinkingelectrontransporttoprotontransferacrossthephotosyntheticmembrane.
InthePSIIcomplex,twoplastoquinonemoleculesworkintandem,withonemoleculepermanentlyboundattheQAsite,andanothermoleculeboundatthe
QBsite.Once
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plastoquinoneattheQBsitehasbeen
fullyreducedbytheadditionoftwoelectronsandtwoprotons,the
reducedform(PQH2)isreleasedintothephotosyntheticmembrane.Thereductionofplastoquinone
attheQBsiteisknownasthetwo-electrongate,becausetwoelectrons,andthereforetwophotochemicalreactionsarerequiredfortheformationandrelease
ofPQH2(Bouges-Bocquet,
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1973;VelthuysandAmesz,1974;Figure7).The
QBsiteofPSIIisofparticularinterestbecausesomeherbicidesused
inagriculture(e.g.Atrazine)inhibitphotosynthesisbybindingatorneartheQB
site(Oettmeier,1999).
Thepathwayofelectronsfromtheprimaryelectrondonor(ChlD1)toQBisshowninFigure 2.Inthefirstreac
2
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tion,anelectronistransferredfromQA
toQBwithin100
2
200ms,producingthe
stateQA/QB(Figure7b).Inthesecond
22
reactionanelectron
istransferredfromQAtoQBwithin400600ms,producingthestateQA/QB22,whichtakesupprotonsfromtheouterwaterphase,producingPQH2.Although
thepathwayof
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protonsthroughPSIIinvolvesspecificaminoacids,
Figure 7b showsaproton(H+)nearQBwithoutspecifyingitssource.Thereis
evidencethatbicarbonate/carbonateionsplayaroleinprotonationby
Chlorophyll
afluorescence,.F
0.75
0.50
0.25
13579
(a)Number of preilluminating flashesbindingneartheQBsite(VanRensenetal.,
1999;cf.Rose
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etal.,2008),whichissupportedby
structuraldata(Ferreiraetal.,2004;Lolletal.,2005)showingthat
abicarbonate/carbonateisboundtothenonhaemeironandiswithin
.
3.2AofLysine264(onproteinD2;seeCoxetal.,2009forevidence).Onfullreduction,PQH2debindsfromtheQB
site,migratesthrough
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ahydrophobicquinoneexchangecavitywithinthe
proteincomplex,andentersthehydrophobiccoreofthephotosyntheticmembrane(Guskov
etal.,2009).ThereductioncycleisrepeatedbybindingofaPQ
moleculefromthequinoneexchangecavity.Photosystem II contributes to thetransmembrane proton electrochemicalpotential difference that drives ATP synthesis
TheproductionofATPinphotosynthesisdependsontheconversionofredox-freeenergyintoa
transmembraneprotonelectrochemical
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potentialdifference,whichismadeupof
apHdifference(DpH)andanelectricalpotentialdifference(DC)acrossthe
photosyntheticmembrane(Mitchell,1961;reviewedinRenger,2008).PSIIcontributestotheproton
potentialenergybythereleaseofprotonsintotheinnerwaterphaseassociatedwithoxidationofwater,andbytheuptakeofprotonsfromthe
outerwaterphase
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associatedwiththereductionofPQ.Reduction
ofplastoquinoneattheQBsitebyPSIIisfollowedbyuptake
ofprotonsfromtheouterwaterphase.Thisreactionisthefirststep
inaproton-transportingmechanismthatiscompletedbytheoxidationofPQH2bythecytochromeb6fcomplex.AsPQH2isoxidized,twoelectronsfromit
arepassedon
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tothecytochromeb6fcomplexandthe
protonsarereleasedintothelumen.InadditiontotheDpHthat
isbuiltupinthisway,anelectricalpotentialdifference(DC)isalso
createdacrossthethylakoidmembraneduetothedirectionalelectrontransferthroughthePSIIreactioncentrefromwater(luminalside)toplastoquinone(stromal/cytoplasmicside).See
also:Photophosphorylation;Photosynthesis:
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LightReactions
QAQB(H+)
H+
I
QAQB Q.AQB(H+)
PQH2
100.200 .sPQ
QAQBH2 QAQ.B(H+)
2
H+2.
QAQB (H+) Q.AQ.B(H+)(b)300.600 .s
Figure 7 Thetwo-electrongateontheelectronacceptorsideofphotosystemII(PSII).(a)ChlorophyllafluorescencefromPSII,asafunctionofflashnumber,
aftertheoxygen
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cycleisinhibitedandwaterisreplaced
byanartificialelectrondonor(VelthuysandAmesz,1974);datashowclearly
thetwo-flashdependence.(b)Stepsinthetwo-electronreductionofplastoquinoneatthe
QBsiteofPSII(seeFigure 2 andtextfordetails).ThisfigurewasdrawnbyDmitriyShevela(inthelaboratoryofoneofus,JM).
ENCYCLOPEDIAOF
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Sons,Ltd.www.els.net
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Photosystem II
Downregulation: Energy can be divertedaway from the photosystem II reaction centrein excess light
Environmentalconditionsoftenimposeseverelimitationsonboththerateandefficiency
ofphotosynthesis.Acommonstresssituationforaphotosyntheticorganismistheabsorption
ofmorelightthanitcanuseforcarbonreduction.Theexcesslightcandriveinopportuneelectrontransferreactions,whichcancausebothlong-andshort-
termdamageto
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PSII,impairingphotosyntheticproductivity.Photosyntheticorganismshave
evolveddifferentstrategiestoavoidinjuryduetoexcesslight.Oneof
thedominantprotectivemechanismsinplantsandalgaeisknownasdownregulationor
nonphotochemicalquenching,whichisadynamicregulationofexcitationenergytransferpathwayswithintheantennasystemthatdivertsexcitationenergyintoheatbeforeitreaches
thereactioncentre
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(Demmig-Adamsetal.,2006).Thisprocessinvolves
xanthophylls,aspecialclassofcarotenoids.Underexcesslightitisnot
unusualforhalfoftheabsorbedquantatobeconvertedintoheat.
Secondary electron transfer reactions inphotosystem II protect against photodamage
Despitetheprotectionprovidedbydownregulation,PSIIissusceptibletodamagebyinopportuneredoxreactionsassociatedwiththepowerfuloxidantsrequired
fortheoxidation
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ofwater,andreductantsrequiredforthe
reductionofplastoquinone.Toavoidsuchdamage,PSIIcontainsredoxcomponentsthat
protectbyacceptingordonatingelectronsatopportunetimes.Forexample,cytochromeb559
appearstodeactivateararelyformed,buthighlydamaging,redoxstateofPSII(WhitmarshandPakrasi,1996;Kaminskayaetal.,2007).Inaddition,somecarotenoid
andchlorophyllmolecules
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ontheD1/D2reactioncentrehavebeen
showntoactasalternativeelectrondonorstoP680+[(PD1,PD2)+]incases
whenthewater-oxidizingcomplexisinactive.
Some photosystem II centres are inactive
Althoughmost
PSIIreactioncentrecomplexesworkefficientlytooxidizewaterandreduceplastoquinone,anumberofinvivoassayshaveshownthatasignificantproportionof
thesecentresare
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unabletotransferelectronstotheplastoquinone
poolatphysiologicallysignificantrates.Experimentsusinghigherplants,algaeandcyanobacteria
indicatethatinactivePSIIcomplexesareacommonfeatureofoxygenicorganisms.It
hasbeenestimatedthatinactivecentresmayreducethequantumefficiencyofphotosynthesisbyasmuchas10%.Theseinactivecentresmaybeaconsequence
ofthesignificant
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turn-overofdamagedPSIIcentreswhichrequires
partialdisassemblyofthecomplex,replacementofthesubunitD1andreassembly
ofanactivecomplex.TheD1subunitofPSIIispronetolight-induced
damage,exhibitingahalf-lifetimein
plantsasshortas30min(seeVassandAro,2008forreviewonassembly).Manyof
theintermediatestates
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occurringduringthedisassemblyandreassemblyprocess
haveimpairedoxygen-evolvingactivity,whichmaynecessitatecontrolprocessestoavoidthe
productionofdeleteriousproductssuchashydrogenperoxide.
Concluding Remarks
As
thesourceofatmosphericoxygen,PSIIhasplayedaseminalroleintheevolutionoflifeonourplanet.PSIIisachlorophyllproteincomplexfound
inalloxygenic
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photosyntheticorganisms,whichincludecyanobacteria,algaeand
plants.Itiscomposedofanantennasystemforcapturinglight,and
areactioncentrecorethatusesthelightenergytodriveelectronand
protontransferreactions.Theantennasystemconsistsofproteincomplexesthatbindchlorophyllandothermoleculesthatconvertlightenergyintoexcitationenergy.Atthe
centreofPSII
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isareactioncentrethatcontainselectron
carriersthattransferelectronsfromwatertoplastoquinone.Thesecarriersincludean
oxygenbridgedclusteroffourmanganeseionsandonecalciumion(Mn4OxCacluster)
thatisthesiteofwateroxidation,atyrosine(Yz),anarrayoffourchlorophyllmolecules(ChlD1,PD1(wecanalsocallitChlPD1)PD2(wecan
alsocallit
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ChlPD2),ChlD2),twopheophytinmolecules(PheoD1and
PheoD2),apermanentlyboundplastoquinone(QA)andaplastoquinonethatbindsreversibly
toPSIIattheQBsite.WithinaPSIIcomplex,fourconsecutivephotochemical
reactionsleadtotheoxidationoftwowatermolecules,whichresultsinthereleaseofoneoxygenmolecule,fourprotonsandthereleaseoftwo
reducedplastoquinonemolecules.
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Nowthatwehavewell-resolvedPSIIstructures,
detailedspectroscopicinformationonthestructureandfunctionoftheMn4OxCacluster,
andpowerfultheoreticalmethods,thegoalofunderstandingthemolecularmechanismofwater
oxidationappearstobewithinreach.Adeepunderstandingofthisfundamentalbiologicalprocesscanacceleratethedevelopmentofartificialcatalystsforsolarhydrogenand
oxygenproductionfrom
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water(Lubitzetal.,2008).
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