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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


68/184

manganeseandcalciumions.Thisfigurewas

drawnbyoneofus(JFK).

Thepathwayandrate

ofelectrontransferwithinthePSIIcomplexmustberigorouslycontrolledforefficient

operationintheelectrontransportchain.Oneofthekeyfactorscontrollingelectrontransferfromoneredoxsitetoanotheristhedistancebetweenthe

components(Moseret


69/184

al.,1992),whichisdeterminedbythe

orientationandpositionoftheredoxcomponentsestablishedbytheproteinscaffolding

ofthecomplex.Theimportanceofdistanceincontrollingelectrontransferisdemonstrated

bytheremarkablehomologybetween(anoxygenic)bacterial

reactioncentresandplant,algalandcyanobacterialPSIIreactioncentres(Sadekaretal.,2006).Anotherfactor

incontrollingelectron


70/184

transferisproteindynamics,whichappearsto

playanimportantroleinthestabilizationoftheprimarychargeseparation

andmanyotherreactionswithinPSII.Notethatthecentralcoreformedby

theD1andD2polypeptidesformsasymmetricalstructure,whichprovidestwopotentialelectrontransportpathwaysthroughthereactioncentre.However,onlyonepathwayis

active(Figure 2).Although


71/184

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


74/184

totheQBsite,andforthe

releaseofprotonsfromtheMn4OxCaclusterintotheinnerwaterphase

(thelumen).

Light Capture: The Antenna System

Oxygenicphotosynthesisisdrivenbyvisiblelight

thatisabsorbedbychlorophyll/phycobilinsandotherpigments

(e.g.carotenoids)boundtothelight-harvestingproteinsthatsurroundthePSIIandPSIreactioncentres

inthephotosynthetic


75/184

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


79/184

(seereviewbyBarrosandKu.hlbrandt,

2009).TheLHC-IIcomplexformsatrimer,witheachsubunitbindingeight

moleculesofchlorophylla,sixmoleculesofchlorophyllbandfourmoleculesof

carotenoids.Seealso:Chlorophyll-bindingProteins

Photosynthesisisinitiatedbyabsorptionofaphotonbyanantennamolecule,whichinducesarapid(10215s)

transitionfromthe


80/184

electronicgroundstatetoanexcitedelectronic

state.Theexcitedstatedecaysrapidly(10213s)byvibrationalrelaxationto

thefirstexcitedsingletstate.Thefateoftheseshort-livedexcitedstatesis

guidedbythestructureandcompositionofthelight-harvestingproteinpigmentcomplexes.Becauseoftheproximityofotherantennamoleculeswiththesameorsimilar

electronicenergylevels,


81/184

theexcitedsingletstateenergyhasa

highprobabilityofbeingtransferredtoaneighbouringmoleculebyaprocess

knownasFo.rsterResonanceEnergyTransfer(FRET)(Lakowicz,1999).Transferofexcitation

energybetweenantennamoleculesdependsontheinteractionbetweenthetransitiondipolemomentsofthedonorandacceptormolecules.Theprobabilityoftransferfallsoff

quicklyasthe


82/184

distancebetweenthepigmentsincreases(inmany

cases,therateisproportionaltoR26,whereRisthedistance

betweenthetransitiondipoles),anddependsstronglyontheoverlapoftheemission

spectrumofthedonormoleculeandtheabsorptionspectrumoftheacceptormolecule,aswellastherelativeorientationofthedonorandacceptorpigments.

Aschematicrepresentation


83/184

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.

ENCYCLOPEDIAOF


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LIFESCIENCES&2010,JohnWiley&



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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


87/184

themiddleofpanel(a)representsan

openreactioncentreandthelightergreendiscinthemiddleof

panel(b)representsaclosedreactioncentre.Whenthereactioncentreisopen

(a),mostenergyisusedforchargeseparation,andthesystememitsminimalchlorophyllafluorescence(labelledasF0);whenthereactioncentreisclosed

(b),chlorophylla


88/184

fluorescenceismaximal(Fmax).Thisfigurewas

drawnbyDmitriyShevela(inthelaboratoryofoneofus,JM).

toundergoprimarychargeseparation(closed),thentheprobabilityofthe

excitationenergygoingintofluorescenceorheatishigher(cf.Figure 5a andb).Measurementsofphotosynthesisunderoptimalconditionsshowthatover90%ofabsorbedphotons

canbetrapped


89/184

byareactioncentreandpromotecharge

separation.However,environmentalconditionsmayimposelimitationsonphotosynthesisthatsignificantlylimit

therateofelectrontransport,whichsignificantlyincreasesthefractionofabsorbedlight

energythatgoesintofluorescenceandheat.Measurementsofchlorophyllfluorescenceprovideaneffectiveandnoninvasivemethodformonitoringphotosyntheticperformanceunderremarkablywiderange

ofconditionsand


90/184

environments(PapageorgiouandGovindjee,2004).

Primary Photochemistry: The ReactionCentre

Thereisconvincingevidencethattheprimaryphotochemicalreaction

inPSIIresultsinchargeseparationbetweenPD1andPheoD1within8ps

(Greenfieldetal.,

+2+

1997),creatingPD1/PheoD1(alsodenotedasP680/Pheo2).However,thereisuncertaintyconcerninghowthis

charge-separatedstateis


91/184

formed,whichisdueinpartto

theproximityofthefourchlorophyll(ChlD1,PD1,PD2andChlD2)andtwopheophytin

(PheoD1andPheoD2)molecules(Figure 3c).Becausetheelectronicenergylevelsofcorechromophore

moleculesarenearlysimilar,excitationenergywithinthereactioncentreequilibratesrapidly(within1ps)betweenthecorechlorophyllandpheophytinmoleculesbeforechargeseparation

occurs.Itappears


92/184

thatthisensembleofmoleculesformsthe

excitedstateoftheprimarydonorandthatchargeseparationcanoccur

betweendifferentchromophoresinthereactioncentre(Grootetal.,2005).(Thus,several

authors(see,e.g.RengerandRenger,2008)haveadoptedanalternatedefinitionforP680fortheentireensembleofpigmentmolecules;however,wepreferto

keeptheoriginal


93/184

definitionofP680.)Afewpicosecondsafter

theformationoftheexcitedstate,theprimaryphotochemicalreactionofPSII

begins,mostlikelybyelectrontransferfromthemonomericChlD1tothePheoD1,

whichisfollowedbyasecondelectrontransfer

+2

leadingtotheformationofPD1/PheoD1(Dineretal.,2001;Holzwarthet

al.,2006;Di


94/184

Donatoetal.,2008).

The

highefficiencyofreactioncentrephotochemistrydependsonpreventingrecombinationofthe

primarychargeseparation,whichisaccomplishedbytherapid(intherange

2

of200ps)transferoftheelectronfromPheoD1toQA(Figure

2

1b,Figure 2a andb andFigure 3c).FromQA,the

electronistransferred


95/184

toanotherplastoquinonemoleculeboundatthe

QBsite.Aftertwophotochemicalturnovers,QBbecomesfullyreducedandprotonated,

formingPQH2,whichdebindsfromPSIIandentersthehydrophobiccoreofthe

photosyntheticmembrane.Concurrentwithelectrontransfertoplastoquinone,thetyrosineresidue(Yz)ontheD1polypeptidetransfersanelectronto(PD1PD2)+.Electronsforthereduction

ofoxidizedYz


96/184

(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



98/184

Photosystem II Photosystem IIyieldofoxygenplottedas

afunctionoftheflashnumberremovesasingleelectronfromthe

water-oxidizingcomexhibitedaperiodicityoffour(Figure 6a).Thisclassicplex,whichadvancesPSII

tothenexthigherSstateuntilexperimentdemonstratedthateachPSIIcomplexoperatestherearefouroxidizingequivalentsinthecomplex,leadingindependentlyand

thatfourphotochemical


99/184

reactionstotheoxidationoftwomolecules

ofwater.Identifyingthearerequiredforthereleaseofoneoxygen

molecule(Joliotchemicalstepsleadingtowateroxidationhasproventobeand

Kok,1975).Theperiodicityoffourwasreadilyachallengingproblem.ItappearsthatnostableOOexplainedbythechemistryofwateroxidation,but

theintermediateis


100/184

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


102/184

independentofthenumberofactivewater-oxidation

cycleresultsintheproductionofonePSIIcentresanddevelopedan

elegantmodelofwateroxygenmolecule,thereleaseoffourprotonsintothe

inneroxidationinwhichtheoxygen-evolvingcomplexcanexistwaterphase(theluminalphase)andthesequentialtransferinoneofthefiveoxidationstates,

labelledS0,S1,S2,S3and


103/184

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).


108/184




109/184

Photosystem II Photosystem IIToaccountfortheobservation

thatthemaximumoxygenyieldoccursonthethird,ratherthanthe

fourthflash(Figure 6a),Koketal.(1970)proposedthatmostofthewater-oxidizing

complexesareintheS1stateindark-adaptedPSIIreactioncentres.Asaconsequence,theS4stateisreachedafterthreeflashesresultingin

thereleaseof


110/184

oxygen.Toaccountforthesmallyield

ofoxygenonthesecondandfourthflash,andthelossof

periodicityastheflashnumberincreased,Koketal.(1970)assumedthatin

somePSIIcomplexesashortsaturatinglightflashmayfailtoadvancetheS-state(misses),whereasinothercomplexestheflashmaypromoteatwo-state

advance(doublehits).


111/184

TheKokmodelsuccessfullyexplainedtheflash

dependenceofoxygenevolutionandcontinuestoguideresearchintothemechanism

ofwateroxidationandoxygenreleasebyPSII(MessingerandRenger,2008).

Thecoreoftheoxygen-evolvingcomplexisaninorganicclusteroffourmanganeseionsandonecalciumionheldtogetherbyseveralm-oxobridges.

TheMn4OxCacluster


112/184

(x4)islocatedontheluminal

sideoftheD1proteinandhasoneligandfromtheCP43

protein(Figure 4).TheMn4OxCaclusterissurroundedbyaproteinmicro-environmentthat

includesD1andD2proteins,theluminalextensionsoftheCP43andCP47proteinsandseveralextrinsicpolypeptides(Figure 2 andFigure 3).Althoughtheproteinsphereserves

toshieldthe


113/184

water-oxidizingcomplexfromtheinneraqueousphase,

channelsexistfortheentryofsubstratewaterandthereleaseof

molecularoxygenandprotons.Recentlyachloride-bindingsitehasbeenidenti

.

fiedapproximately67AfromtheMn4OxCacluster(Figure 4;Guskovetal.,2009).Althoughchloridehasbeenshowntoinfluencewater-oxidation,therelativelydistant

locationfromthe


114/184

clustermakesitdifficulttoproposea

mechanism.Onepossibilityisthatchlorideplaysaroleinstabilizingthe

protonnetworksurroundingtheMn4OxCacluster(OlesonandAndreasson,2003).

As

aforementioned,thestructureofthePSIIreaction.

centreisnowavailableat3.52.9Aresolution(Ferreiraetal.,2004;Lolletal.,2005;Guskov

etal.,2009),


115/184

andreasonablydetailedmodelsfortheMn4OxCa

clusterhavebeenproposedbasedonthesestructuresandonpolarizedExtended

X-rayAbsorptionFineStructure(EXAFS)spectroscopy(Yanoetal.,2006).Incombinationwith

experimentaldatathatincludesFourier-TransformInfraRed(FTIR)andElectronParamagneticResonance(EPR)spectroscopy,aswellasmassspectrometryanddetailedtheoreticalcalculations,the

goalofunderstanding


116/184

themolecularmechanismofwateroxidationappears

tobewithinreach(Siegbahn,2008;Sprovieroetal.,2008;Zeinet

al.,2008).Figure 4b andcshowtwooftheproposedgeometricarrangementsofthe

manganeseandcalciumions.Thebindingsitesforsubstratewaterarespeculative,withatleastonewatermoleculeboundintheS0andS1states,

andtwowater


117/184

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


119/184

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


121/184

Mn4OxCacluster.Thestructuralchangeappearsto

includeadecreaseinoneoftheMnMndistancesfrom2.85to

.

2.75Aduetodeprotonationofonem-OHbridge(Kulik

etal.,2007).IntheS1!S2transition,anotherMn3+toMn4+

oxidationoccurs,butwithoutanysignificantstructuralchangeandnosignificantproton

releaseisobserved.


122/184

Thus,intheS2statetheMn4OxCa

clusterhasanadditionalpositivecharge.TheS2!S3transitioninvolvestherelease

ofaproton,whichisfollowedbytheoxidationoftheMn4OxCacluster

bytyrosineYz..Thenatureofthisoxidationiscontroversial

ithasbeenproposedtobeMn3+toMn4+oxidation,oran

oxidationofa


123/184

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


125/184

bybindingtoalowervalentmanganese

and/orcalciumandmaybepartiallydeprotonated.(II)Duringoxidationofthe

Mn4OxCacluster,oneoftheoxygenbridgesoranoxygenligand(originatingfrom

substratewater)becomespartiallyoxidizedforminganoxygenradical,whichcanformtheOObondinaradical-likemechanismwithasecondoxygenspecies

thatmaybecoordinated


126/184

tomanganeseand/orcalcium.(III)Inthe

S3state,asmallfractionoftheMn4OxCaclustersmaycontainthe

OObondintheformofacomplexedperoxide,which

ENCYCLOPEDIA

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,


128/184

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


131/184

tion,anelectronistransferredfromQA

toQBwithin100

2

200ms,producingthe

stateQA/QB(Figure7b).Inthesecond

22

reactionanelectron

istransferredfromQAtoQBwithin400600ms,producingthestateQA/QB22,whichtakesupprotonsfromtheouterwaterphase,producingPQH2.Although

thepathwayof


132/184

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


133/184

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


135/184

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).

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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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