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The Calcium and Chloride Cofactors

  • Chapter
Photosystem II

Part of the book series: Advances in Photosynthesis and Respiration ((AIPH,volume 22))

Summary

Single atoms of Ca2+ and Cl− are closely associated with the tetranuclear Mn cluster of Photosystem II (PS II). Extraction of either cofactor blocks advancement of the S-state cycle beyond S2. In the case of Cl− depletion, this modification has been proposed to result from replacement of the anion as a Mn ligand. This would cause a decrease of the potential, and thereby localization of the Mn(IV) state on the Mn to which Cl− was bound. The implications of this hypothesis, and of the notion that the ligand replacing Cl− in the modified S2 state is most likely hydroxyl (OH−), are discussed and found to provide a plausible explanation for apparently conflicting reports in the literature. The location of Ca2+ with respect to the Mn cluster is less certain. Although the metal is positioned so as to interfere with the attack of a small ligand, such as hydroxylamine (NH2OH), on the Mn cluster, the distance between Ca2+ and atoms of the Mn cluster is not resolved at the present time. Calcium can be shown to reinforce the stability of Mn ligation by PS II. However, its role in water oxidation must extend beyond structural effects to account for the block in electron transfer at S2 observed in Ca2+-depleted PS II, and the upward shift in the minimum temperature at which the transition from S1 to S2 occurs. The inactivation of PS II caused by replacement of Ca2+ with lanthanides suggests that it functions as a site for binding of water molecules destined for oxidation at the Mn site in PS II.

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References

  • Ädelroth P, Lindberg K and Andréasson LE (1995) Studies of Ca2+ binding in spinach Photosystem II using 45Ca2+. Biochemistry 34: 9021–9027

    PubMed  Google Scholar 

  • Ananyev GM and Dismukes GC (1997) Calcium induces binding and formation of a spin-coupled dimanganese(II,II) center in the apo-water oxidation complex of Photosystem II as precursor to the functional tetra-Mn/Ca cluster. Biochemistry 36: 11342–11350

    Article  CAS  PubMed  Google Scholar 

  • Ananyev GM, Murphy A, Abe Y and Dismukes GC (1999) Remarkable affinity and selectivity for Cs+ and uranyl (UO22+) binding to the manganese site of the apo-water oxidation complex of Photosystem II. Biochemistry 38: 7200–7209

    Article  CAS  PubMed  Google Scholar 

  • Andréasson LE, Vass I and Styring S (1995) Ca2+ depletion modifies the electron-transfer on both donor and acceptor sides in Photosystem II from spinach. Biochim Biophys Acta 1230: 155–164

    Google Scholar 

  • Arnon DI and Whatley FR (1949) Is chloride a coenzyme of photosynthesis? Science 110: 554–556

    CAS  PubMed  Google Scholar 

  • Baumgarten M, Philo JS and Dismukes GC (1990) Mechanism of photoinhibition of photosynthetic water oxidation by chloride depletion and fluoride substitution: Oxidation of a protein residue. Biochemistry 29: 10814–10822

    Article  CAS  PubMed  Google Scholar 

  • Becker DW and Brand JJ (1982) An in vivo requirement for calcium in Photosystem II of Anacystis nidulans. Biochem Biophys Res Commun 109: 1134–1139

    CAS  PubMed  Google Scholar 

  • Blubaugh DJ and Cheniae GM (1992) Photoassembly of the PS2 Mn/Ca cluster. Photosynth Res 34: 147–147

    Google Scholar 

  • Booth PJ, Rutherford AW and Boussac A (1996) Location of the calcium binding site in Photosystem II: A Mn2+ substitution study. Biochim Biophys Acta 1277: 127–134

    Google Scholar 

  • Boussac A and Rutherford AW (1988a) Ca2+ Binding to the oxygen evolving enzyme varies with the redox state of the Mn cluster. FEBS Lett 236: 432–136

    Article  CAS  Google Scholar 

  • Boussac A and Rutherford AW (1988b) Nature of the inhibition of the oxygen-evolving enzyme of Photosystem II induced by NaCl washing and reversed by the addition of Ca2+ or Sr2+. Biochemistry 27: 3476–3483

    Article  CAS  Google Scholar 

  • Boussac A and Rutherford AW (1992) The origin of the split S3 EPR signal in Ca2+-depleted Photosystem II-histidine versus tyrosine. Biochemistry 31: 7441–7445

    CAS  PubMed  Google Scholar 

  • Boussac A, Zimmermann JL and Rutherford AW (1989) EPR signals from modified charge accumulation states of the oxygen evolving enzyme in Ca2+-deficient Photosystem II. Biochemistry 28: 8984–8989

    Article  CAS  PubMed  Google Scholar 

  • Boussac A, Zimmermann JL, Rutherford AW and Lavergne J (1990) Histidine oxidation in the oxygen-evolving Photosystem II enzyme. Nature 347: 303–306

    Article  CAS  Google Scholar 

  • Bove JM, Bove C, Whatley FR and Arnon DI (1963) Chloride requirement for oxygen evolution in photosynthesis. Z Naturforsch 18b: 683–688

    CAS  Google Scholar 

  • Brayer GD, Luo YG and Withers SG (1995) The structure of human pancreatic alpha-amylase at 1.8 Å resolution and comparisons with related enzymes. Protein Sci 4: 1730–1742

    CAS  PubMed  Google Scholar 

  • Britt RD (1996) Oxygen evolution. In: Ort DR and Yocum CF (eds) Oxygenic Photosynthesis: The Light Reactions, pp 137–164. Kluwer Academic Publishers, Dordrecht

    Google Scholar 

  • Büchel C, Barber J, Ananyev G, Eshaghi S, Watt R and Dismukes GC (1999) Photoassembly of the manganese cluster and oxygen evolution from monomeric and dimeric CP47 reaction center Photosystem II complexes. Proc Natl Acad Sci USA 96: 14288–14293

    PubMed  Google Scholar 

  • Cammarata KV and Cheniae GM (1987) Studies on 17, 24 Kd depleted Photosystem II membranes. 1 Evidences for high and low affinity calcium sites in 17, 24 kD depleted PS II membranes from wheat versus spinach. Plant Physiol 84: 587–595

    CAS  Google Scholar 

  • Campbell KA, Gregor W, Pham DP, Peloquin JM, Debus RJ and Britt RD (1998) The 23 and 17 kDa extrinsic proteins of Photosystem II modulate the magnetic properties of the S-l-state manganese cluster. Biochemistry 37: 5039–5045

    Article  CAS  PubMed  Google Scholar 

  • Casey JL and Sauer K (1984) EPR detection of a cryogenically photogenerated intermediate in photosynthetic oxygen evolution. Biochim Biophys Acta 767: 21–28

    CAS  Google Scholar 

  • Chen CG and Cheniae GM (1993) The photoassembly of active O2-evolving Mn clusters by 17/23 kDa-less NH2OH-PS II is modulated by Ca2+. Plant Physiol 102: 144

    Google Scholar 

  • Chen CG and Cheniae GM (1995) High affinity binding of the Ca2+ essential for O2 evolution is dependent on the existence of the Mn-cluster but it independent of the extrinsic proteins. In Mathis P (ed) Photosynthesis: From Light to Biosphere, Vol II, pp 329–332. Kluwer Academic Publishers, Dordrecht

    Google Scholar 

  • Chen CG, Kazimir J and Cheniae GM (1995) Calcium modulates the photoassembly of Photosystem II (Mn)(4)-clusters by preventing ligation of nonfunctional high-valency states of manganese. Biochemistry 34: 13511–13526

    CAS  PubMed  Google Scholar 

  • Chen WJ and Ta Y (2001) The EXAFS study on the local structure of lanthanum in spinach PS II. Biol Trace Elem Res 82: 231–237

    Article  CAS  PubMed  Google Scholar 

  • Chu HA, Nguyen AP and Debus RJ (1995a) Amino acid residues that influence the binding of manganese or calcium to Photosystem II. 1 The lumenal interhelical domains of the D1 polypeptide. Biochemistry 34: 5839–5858

    CAS  PubMed  Google Scholar 

  • Chu HA, Nguyen AP and Debus RJ (1995b) Amino acid residues that influence the binding of manganese or calcium to Photosystem II. 2 The carboxy-terminal domain of the D1 polypeptide. Biochemistry 34: 5859–5882

    CAS  PubMed  Google Scholar 

  • Cinco RM, Robblee JH, Rompel A, Fernandez C, Yachandra VK, Sauer K and Klein MP (1998) Strontium EXAFS reveals the proximity of calcium to the manganese cluster of oxygen-evolving Photosystem II. J Phys Chem B 102: 8248–8256

    Article  CAS  Google Scholar 

  • Cinco RM, Holman KLM, Robblee JH, Yano J, Pizarro SA, Bellacchio E, Sauer K and Yachandra VK (2002) Calcium EXAFS establishes the Mn-Ca cluster in the oxygen-evolving complex of Photosystem II. Biochemistry 41: 12928–12933

    Article  CAS  PubMed  Google Scholar 

  • Clarke SM and Eaton-Rye JJ (1999) Mutation of Phe-363 in the Photosystem II protein CP47 impairs photoautotrophic growth, alters the chloride requirement, and prevents photosynthesis in the absence of either PS II-O or PS II-V in Synechocystis sp. PCC 6803. Biochemistry 38: 2707–2715

    CAS  PubMed  Google Scholar 

  • Clemens KL, Force DA and Britt RD (2002) Acetate binding at the Photosystem II oxygen evolving complex: An S2-state multiline signal ESEEM study. J Am Chem Soc 124: 10921–10933

    Article  CAS  PubMed  Google Scholar 

  • Debus RJ (1992) The manganese and calcium ions of photosynthetic oxygen evolution. Biochim Biophys Acta 1102: 269–352

    CAS  PubMed  Google Scholar 

  • Debus RJ (2001) Amino acid residues that modulate the properties of tyrosine YZ and the manganese cluster in the water oxidizing complex of Photosystem II. Biochim Biophys Acta 1503: 164–186

    CAS  PubMed  Google Scholar 

  • Dekker JP, Ghanotakis DF, Plijter JJ, van Gorkom HJ and Babcock GT (1984) Kinetics of the oxygen-evolving complex in salt-washed Photosystem II preparations. Biochim Biophys Acta 767: 515–523

    CAS  Google Scholar 

  • Fabian M, Skultety L, Brunel C and Palmer G (2001) Cyanide stimulated dissociation from the catalytic center of oxidized cytochrome c oxidase. Biochemistry 40: 6061–6069

    CAS  PubMed  Google Scholar 

  • Feller G, LeBussy O, Houssier C and Gerday C (1996) Structural and functional aspects of chloride binding to Alteromonas haloplanctis α-amylase. J Biol Chem 271: 23836–23841

    CAS  PubMed  Google Scholar 

  • Ferreira K, Iverson TM, Mughlouni K, Barber J and Iwata S (2004) Architecture of the photosynthetic oxygen-evolving center. Science 303: 1831–1838

    Article  CAS  PubMed  Google Scholar 

  • Ghanotakis DF, Babcock GT and Yocum CF (1984a) Calcium reconstitutes high rates of oxygen evolution in polypeptide depleted Photosystem II preparations. FEBS Lett 167: 127–130

    Article  CAS  Google Scholar 

  • Ghanotakis DF, Topper JN, Babcock GT and Yocum CF (1984b) Water-soluble 17-Kda and 23-kDa polypeptides restore oxygen evolution activity by creating a high-affinity binding site for Ca2+ on the oxidizing side of Photosystem II. FEBS Lett 170: 169–173

    Article  CAS  Google Scholar 

  • Ghanotakis DF, Demetriou DM and Yocum CF (1987) Isolation and characterization of an oxygen-evolving Photosystem II reaction center core preparation and a 28 kDa Chl-a binding protein. Biochim Biophys Acta 891: 15–21

    CAS  Google Scholar 

  • Gilchrist ML, Ball JA, Randall DW and Britt RD (1995) Proximity of the manganese cluster of Photosystem II to the redox active tyrosine YZ. Proc Natl Acad Sci USA 92: 9545–9549

    CAS  PubMed  Google Scholar 

  • Grove GN and Brudvig GW (1998) Calcium binding studies of Photosystem II using a calcium-selective electrode. Biochemistry 37: 1532–1539

    Article  CAS  PubMed  Google Scholar 

  • Haddy A, Dunham WR, Sands RH and Aasa R (1992) Multifrequency EPR investigations into the S2-state signal at g = 4.1 of the O2 evolving complex. Biochim Biophys Acta 1099: 25–34

    CAS  PubMed  Google Scholar 

  • Haddy A, Hatchell JA, Kimel RA and Thomas R (1999) Azide as a competitor of chloride in oxygen evolution by Photosystem II. Biochemistry 38: 6104–6110

    Article  CAS  PubMed  Google Scholar 

  • Han K and Katoh S (1993) Different localization of 2 Ca2+ in spinach oxygen-evolving Photosystem II membranes—Evidence for involvement of only one Ca2+ in oxygen revolution. Plant Cell Physiol. 34: 585–593

    CAS  Google Scholar 

  • Han KC and Katoh S (1995) Different binding affinity sites of Ca2+ for reactivation of oxygen evolution in NaCl-washed Photosystem II membranes represent differently modified states of a single binding site. Biochim Biophys Acta 1232: 230–236

    Google Scholar 

  • Hasegawa K, Kimura Y and Ono T (2002) Chloride cofactor in the photosynthetic oxygen-evolving complex studied by Fourier transform infrared spectroscopy. Biochemistry 41: 13839–13850

    CAS  PubMed  Google Scholar 

  • Haumann M, Drevenstedt W, Hundelt M and Junge W (1996) Chloride depletion of Photosystem II of green plants exposes amino acid redox cofactor of water oxidation. Biochim Biophys Acta 1273: 237–250

    Google Scholar 

  • Hendry G, and Wydrzynski T (2003) 18O2 isotope exchange measurements reveal that calcium is involved in the binding of one substrate water molecule to the oxygen-evolving complex in Photosystem II. Biochemistry 42: 6209–6217.

    Article  CAS  PubMed  Google Scholar 

  • Homann PH (1985) The association of functional anions with the oxygen-evolving center of chloroplasts. Biochim Biophys Acta 809: 311–319

    CAS  Google Scholar 

  • Homann PH (1988a) Chloride relations of photosystem-II membrane preparations depleted of, and resupplied with, their 17-kDa and 23-kDa extrinsic polypeptides. Photosynth Res 15: 205–220

    Article  CAS  Google Scholar 

  • Homann PH (1988b) The chloride and calcium requirements of photosynthetic water oxidation: Effects of pH. Biochim Biophys Acta 934: 1–13

    CAS  Google Scholar 

  • Itoh S, Yerkes CT, Koike H, Robinson HH and Crofts AR (1984) Effects of chloride depletion on electron donation from the water-oxidizing complex to the Photosystem II reaction center as measured by the microsecond rise of chlorophyll fluorescence in isolated pea chloroplasts. Biochim Biophys Acta 766: 612–622

    CAS  Google Scholar 

  • Izawa S, Heath RL and Hind G (1969) Role of chloride ion in photosynthesis.3. Effect of artificial electron donors upon electron transport. Biochim Biophys Acta 180: 388–398

    CAS  PubMed  Google Scholar 

  • Kimura Y, Hasegawa K and Ono T (2002) Characteristic changes of the S2/S1 difference FTIR spectrum induced by Ca2+ depletion and metal cation substitution in the photosynthetic oxygen-evolving complex. Biochemistry 41: 5844–5853

    Article  CAS  PubMed  Google Scholar 

  • Kamiya N and Shen J-R (2003) Crystal structure of oxygen-evolving Photosystem II from Thermosynechococcus vulcanus at 3.7-Å resolution. Proc Natl Acad Sci USA 100: 98–103

    Article  CAS  PubMed  Google Scholar 

  • Kelley PM and Izawa S (1978) The role of chloride in Photosystem II. I. Effects of chloride ion on Photosystem II electron transport and on hydroxylamine inhibition. Biochim Biophys Acta 502: 198–210

    CAS  PubMed  Google Scholar 

  • Kimura, Y and Ono, TA (2001) Chelator-induced disappearance of carboxylate stretching vibrational modes in S2/S1 FTIR spectrum in oxygen-evolving complex of Photosystem II. Biochemistry 40: 14061–14068

    Article  CAS  PubMed  Google Scholar 

  • Kretsinger RH and Nelson DJ (1976) Calcium in biological systems. Coord Chem Rev 18: 29–124

    Article  CAS  Google Scholar 

  • Krieger A and Rutherford AW (1997) Comparison of chloride-depleted and calcium-depleted PS II: The midpoint potential of QA and susceptibility to photodamage. Biochim Biophys Acta 1319: 91–98

    CAS  Google Scholar 

  • Krieger A, Weis E and Demeter S (1993) Low-pH-induced Ca2+ ion release in the water-splitting system is accompanied by a shift in the midpoint redox potential of the primary quinone acceptor QA. Biochim Biophys Acta 1144: 411–418

    CAS  Google Scholar 

  • Latimer MJ, Derose VJ, Mukerji I, Yachandra VK, Sauer K and Klein, MP (1995) Evidence for the proximity of calcium to the manganese cluster of Photosystem II—determination by X-ray absorption spectroscopy. Biochemistry 34: 10898–10909

    Article  CAS  PubMed  Google Scholar 

  • Lewit-Bentley A and Rety S (2000) EF-hand calcium-binding proteins. Curr Opin Struct Biol 10: 637–643

    Article  CAS  PubMed  Google Scholar 

  • Li X and Weinman SA (2002) Chloride channels and hepatocellular function: Prospects for molecular identification. Annu Rev Physiol 64: 609–633.

    Article  CAS  PubMed  Google Scholar 

  • Lindberg K and Andréasson L-E (1996) A one-site, two-state model for the binding of anions in Photosystem II. Biochemistry 35: 14259–14267

    Article  CAS  PubMed  Google Scholar 

  • Lindberg K, Wydrzynski T, Vänngård T and Andréasson L-E (1990) Slow release of chloride from 36Cl-labeled Photosystem II membranes. FEBS Lett 264: 153–155

    Article  CAS  Google Scholar 

  • Lindberg K, Vänngård T and Andréasson L-E (1993) Studies of the slowly exchanging chloride in Photosystem II of higher plants. Photosynth Res 38: 401–108

    Article  CAS  Google Scholar 

  • Lübbers K, Drevenstedt W and Junge W (1993) Chloride depletion of photosynthetic water oxidase. FEBS Lett 336: 304–308

    Article  PubMed  Google Scholar 

  • Martin RB and Richardson FS (1979) Lanthanides as probes for calcium in biological systems. Q Rev Biophys 12: 181–209

    CAS  PubMed  Google Scholar 

  • Matysik J, Alia, Nachtegaal G, van Gorkom HJ, Hoff AJ and de Groot HJM (2000) Exploring the calcium-binding site in Photosystem II membranes by solid-state Cd113 NMR. Biochemistry 39: 6751–6755

    Article  CAS  PubMed  Google Scholar 

  • Mei R and Yocum CF (1991) Calcium retards NH2OH inhibition of O2 evolution activity by stabilization of Mn2+ binding to Photosystem II. Biochemistry 30: 7836–7842

    Article  CAS  PubMed  Google Scholar 

  • Mei R and Yocum CF (1992) Comparative properties of hydroquinone and hydroxylamine reduction of the Ca2+-stabilized O2-evolving complex of Photosystem II — Reductant-dependent Mn2+ formation and activity inhibition. Biochemistry 31: 8449–8454

    CAS  PubMed  Google Scholar 

  • Mei R and Yocum C (1993) Characterization of inhibitory effects of NH2OH and its N-methyl derivatives on the O2-evolving complex of Photosystem II. Photosynth Res 38: 449–453

    Article  CAS  Google Scholar 

  • Metzler D (2001) Biochemistry: The Chemical Reactions of Living Cells, Vol 1. Harcourt Academic Press, San Diego

    Google Scholar 

  • Miller AF and Brudvig GW (1989) Manganese and calcium requirements for reconstitution of oxygen-evolution activity in manganese-depleted Photosystem II membranes. Biochemistry 28: 8181–8190

    CAS  PubMed  Google Scholar 

  • Miller AF and Brudvig GW (1990) Electron transfer events leading to reconstitution of oxygen evolution activity in manganese-depleted Photosystem II membranes. Biochemistry 29: 1385–1392

    CAS  PubMed  Google Scholar 

  • Miyao M and Murata N (1984) Calcium ions can be substituted for the 24-kDa polypeptide in photosynthetic oxygen evolution. FEBS Lett 168: 118–120

    Article  CAS  Google Scholar 

  • Miyao, M and Murata, N (1985) The Cl− effect on photosynthetic oxygen evolution—interaction of Cl− with 18-kDa, 24-kDa and 33-kDa proteins. FEBS Lett 180: 303–308

    Article  CAS  Google Scholar 

  • Miyao M and Murata N (1986) Light-dependent inactivation of photosynthetic oxygen evolution during NaCl treatment of Photosystem II particles—the role of the 24-kDa protein. Photosynth Res 10: 489–496

    Article  CAS  Google Scholar 

  • Morgan TR, Shand JA, Clarke SM and Eaton-Rye JJ (1998) Specific requirements for cytochrome c-550 and the manganese-stabilizing protein in photoautotrophic strains of Synechocystis sp. PCC 6803 with mutations in the domain Gly-351 to Thr-436 of the chlorophyll-binding protein CP47. Biochemistry 37: 14437–14449

    CAS  PubMed  Google Scholar 

  • Noguchi T, Ono T and Inoue Y (1995) Direct detection of a carboxylate bridge between Mn and Ca2+ in the photosynthetic oxygen-evolving center by means of Fourier-transform infrared spectroscopy. Biochim Biophys Acta 1228: 189–200

    Google Scholar 

  • Ono T and Inoue Y (1988) Discrete extraction of the Ca atom functional for O2 evolution in higher plant Photosystem II by a simple low pH treatment. FEBS Lett 227: 147–152

    Article  CAS  Google Scholar 

  • Ono T and Inoue Y (1990a) Abnormal redox reactions in photosynthetic O2-evolving centers in NaCl/EDTA-washed PS II— a dark-stable EPR multiline signal and an unknown positive charge accumulator. Biochim Biophys Acta 1020: 269–277

    CAS  Google Scholar 

  • Ono TA and Inoue Y (1990b) A marked upshift in threshold temperature for the S1 to S2 transition induced by low pH treatment of PS II membranes. Biochim Biophys Acta 1015: 373–377

    CAS  Google Scholar 

  • Ono T, Zimmermann JL, Inoue Y and Rutherford AW (1986) EPR evidence for a modified S-transition in chloride-depleted Photosystem II. Biochim Biophys Acta 851: 193–201

    CAS  Google Scholar 

  • Ono T, Rompel A, Mino H and Chiba N (2001) Ca2+ function in photosynthetic oxygen evolution studied by alkali metal cations substitution. Biophys J 81: 1831–1840

    CAS  PubMed  Google Scholar 

  • Pecoraro VL, Baldwin MJ, Caudle MT, Hsieh WY and Law NA (1998) A proposal for water oxidation in Photosystem II. Pure Appl Chem 70: 925–929

    CAS  Google Scholar 

  • Peloquin JM, Campbell KA, Randall DW, Evanchik MA, Pecoraro VL, Armstrong WA and Britt RD (2000) 55Mn ENDOR of the S2 state mutliline signal of Photosystem II: Implications on the structure of the tetranuclear Mn cluster. J Am Chem Soc 122: 10926–10942

    Article  CAS  Google Scholar 

  • Putnam-Evans C and Bricker TM (1994) Site-directed mutagenesis of the CP47 protein of Photosystem II—alteration of the basic residue 448R to 448G prevents the assembly of functional Photosystem II centers under chloride-limiting conditions. Biochemistry 33: 10770–10776

    Article  CAS  PubMed  Google Scholar 

  • Putnam-Evans C and Bricker TM (1997) Site-directed mutagenesis of the basic residues K-321 to (321)G in the CP 47 protein of Photosystem II alters the chloride requirement for growth and oxygen-evolving activity in Synechocystis 6803. Plant Mol Biol 34: 455–463

    Article  CAS  PubMed  Google Scholar 

  • Qian M, Dao LA, Debus RJ and Burnap RL (1999) Impact of mutations within the putative Ca2+-binding lumenal interhelical a–b loop of the Photosystem II D1 protein on the kinetics of photoactivation and H2O oxidation in Synechocystis sp PCC6803. Biochemistry 38: 6070–6081

    Article  CAS  PubMed  Google Scholar 

  • Rashid A and Homann PH (1992) Properties of iodide-activated photosynthetic water-oxidizing complexes. Biochim Biophys Acta 1101: 303–310

    CAS  Google Scholar 

  • Riggs PJ, Mei R, Yocum CF and Penner-Hahn JE (1992) Reduced derivatives of the manganese cluster in the photosynthetic oxygen-evolving complex. J Am Chem Soc 114: 10650–10651

    CAS  Google Scholar 

  • Riggs-Gelasco PJ, Mei R, Ghanotakis DF, Yocum CF and Penner-Hahn JE (1996a) X-ray absorption spectroscopy of calcium-substituted derivatives of the oxygen-evolving complex of Photosystem II. J Am Chem Soc 118: 2400–2410

    CAS  Google Scholar 

  • Riggs-Gelasco PJ, Mei R, Yocum CF and Penner-Hahn JE (1996b) Reduced derivatives of the Mn cluster in the oxygen-evolving complex of Photosystem II: An EXAFS study. J Am Chem Soc 118: 2387–2399

    CAS  Google Scholar 

  • Rutherford AW (1989) Photosystem II, the water-splitting enzyme. Trends Biochem Sci 14: 227–232

    Article  CAS  PubMed  Google Scholar 

  • Rutherford AW, Zimmermann JL and Boussac A (1992) Oxygen evolution. In: Barber J (ed) The Photosystems: Structure, Function and Molecular Biology, pp 179–229. Elsevier Science Publishers, New York

    Google Scholar 

  • Sandusky PO and Yocum CF (1984) The chloride requirement for photosynthetic oxygen evolution; analysis of the effects of chloride and other anions on amine inhibition of the oxygen-evolving complex. Biochim Biophys Acta 766: 603–611

    CAS  Google Scholar 

  • Sandusky PO and Yocum CF (1986) The chloride requirement for photosynthetic oxygen evolution: factors affecting nucleophilic displacement of chloride from the oxygen-evolving complex. Biochim Biophys Acta 849: 85–93

    CAS  Google Scholar 

  • Sandusky PO, Selvius DeRoo CL, Hicks DB, Yocum CF, Ghanotakis DF and Babcock GT (1983) Electron transport activity and polypeptide composition in the isolated Photosystem II complex. In: Inoue Y, Crofts AR, Govindjee, Murata N, Renger G and Satoh K (eds) The Oxygen Evolving System of Photosynthesis, pp 189–199. Academic Press, Tokyo

    Google Scholar 

  • Shen JR and Inoue Y (1991) Low pH-induced dissociation of 3 extrinsic proteins fro O2 evolving Photosystem II. Plant Cell Physiol. 32: 453–57.

    CAS  Google Scholar 

  • Shen JR, Satoh K and Katoh S (1988a) Isolation of an oxygen-evolving Photosystem II preparation containing only one atom of calcium from a chlorophyll b deficient mutant of rice. Biochim Biophys Acta 936: 386–394

    CAS  Google Scholar 

  • Shen JR, Satoh K and Katoh S (1988b) Calcium content of oxygen-evolving Photosystem II preparations from higher plants—Effects of NaCl treatment. Biochim Biophys Acta 933: 358–364

    CAS  Google Scholar 

  • Sinclair J (1984) The influence of anions on oxygen evolution by isolated chloroplasts. Biochim Biophys Acta 764: 247–252

    CAS  Google Scholar 

  • Sivaraja M, Tso J and Dismukes GC (1989) A calcium-specific site influences the structure and activity of the manganese cluster responsible for photosynthetic water oxidation. Biochemistry 28: 9459–9464

    Article  CAS  PubMed  Google Scholar 

  • Strynadka NCJ and James MNG (1989) Crystal-structures of the helix-loop-helix calcium-binding proteins. Annu Rev Biochem 58: 951–998

    Article  CAS  PubMed  Google Scholar 

  • Szalai VA and Brudvig GW (1996) Reversible binding of nitric oxide to tyrosyl radicals in Photosystem II. Nitric oxide quenches formation of the S3 EPR signal species in acetate-inhibited Photosystem II. Biochemistry 35: 15080–15087

    CAS  PubMed  Google Scholar 

  • Tamura N and Cheniae GM (1986) Requirements for the photoligation of Mn2+ in PS II membranes and the expression of water-oxidizing activity of the polynuclear Mn-catalyst. FEBS Lett 200: 231–236

    Article  CAS  Google Scholar 

  • Tamura N and Cheniae GM (1988) Photoactivation of the water oxidizing complex: The mechanism and general consequences to photosystem 2. In: Stevens ES and Bryant DA (eds) Light-Energy Transduction in Photosynthesis: Higher Plant and Bacterial Models, pp 227–242. American Society for Plant Physiology, Rockville

    Google Scholar 

  • Tamura N, Inoue Y and Cheniae GM (1989) Photoactivation of the water-oxidizing complex in Photosystem II membranes depleted of Mn, Ca and extrinsic proteins. 2 Studies on the functions of Ca2+. Biochim Biophys Acta 976: 173–181

    CAS  Google Scholar 

  • Tang XS, Randall DW, Force DA, Diner BA and Britt RD (1996) Manganese-tyrosine interaction in the Photosystem II oxygen-evolving complex. J Am Chem Soc 118: 7638–7639

    Article  CAS  Google Scholar 

  • Theg SN and Homann PH (1982) Light-, pH-, and uncoupler-dependent association of chloride with chloroplast thylakoids. Biochim Biophys Acta 679: 221–234

    CAS  Google Scholar 

  • Theg SN, Jursinic PA and Homann PH (1984) Studies on the mechanism of chloride action in photosynthetic water oxidation. Biochim Biophys Acta 766: 636–646

    CAS  Google Scholar 

  • Tichy M and Vermaas W (1998) Functional analysis of combinatorial mutants altered in a conserved region in loop E of the CP47 protein in Synechocystis sp. PCC 6803. Biochemistry 37: 1523–1531

    Article  CAS  PubMed  Google Scholar 

  • Tommos C, Hoganson CW, Di Valentin M, Lydakis-Simantiris N, Dorlet P, Westphal K, Chu HA, McCracken J and Babcock GT (1998) Manganese and tyrosyl radical function in photosynthetic oxygen evolution. Curr Opin Chem Biol 2: 244–252

    Article  CAS  PubMed  Google Scholar 

  • Vander Meulen KA, Hobson A and Yocum CF (2002) Calcium depletion modifies the structure of the Photosystem II O2-evolving complex. Biochemistry 41: 958–966

    CAS  PubMed  Google Scholar 

  • Van Vliet P and Rutherford AW (1996) Properties of chloride-depleted oxygen-evolving complex of Photosystem II studied by electron paramagnetic resonance. Biochemistry 35: 1829–1839

    PubMed  Google Scholar 

  • Vass I, Ono TA and Inoue Y (1987) Stability and oscillation properties of thermoluminescent charge pairs in the O2-evolving system depleted of Cl− or the 33 kDa extrinsic protein. Biochim Biophys Acta 892: 224–235

    CAS  Google Scholar 

  • Velthuys BR (1975) Binding of the inhibitor NH3 to the oxygen evolving apparatus of spinach chloroplasts. Biochim Biophys Acta 396: 392–401

    CAS  PubMed  Google Scholar 

  • Vrettos JS, Limburg J and Brudvig GW (2001a) Mechanism of photosynthetic water oxidation: Combining biophysical studies of Photosystem II with inorganic model chemistry. Biochim Biophys Acta 1503: 229–245

    CAS  PubMed  Google Scholar 

  • Vrettos JS, Stone DA and Brudvig GW (2001b) Quantifying the ion selectivity of the Ca2+ site in Photosystem II: Evidence for direct involvement of Ca2+ in O2 formation. Biochemistry 40: 7937–7945

    Article  CAS  PubMed  Google Scholar 

  • Waggoner CM, Pecoraro V and Yocum CF (1989) Monovalent cations (Na+, K+, Cs+) inhibit calcium activation of photosynthetic oxygen evolution. FEBS Lett 244: 237–240

    Article  CAS  Google Scholar 

  • Wales R, Newman BJ, Pappin D and Gray JC (1989) The extrinsic 33 kDa polypeptide of the oxygen-evolving complex of Photosystem II is a putative calcium-binding protein and is encoded by a multi-gene family in pea. Plant Mol Biol 12: 439–451

    Article  CAS  Google Scholar 

  • Webber AN and Gray JC (1989) Detection of calcium binding by Photosystem II polypeptides immobilized onto nitrocellulose membrane. FEBS Lett 249: 79–82

    Article  CAS  Google Scholar 

  • Westphal KL, Lydakis-Simantiris N, Cukier RI and Babcock GT (2000) Effects of Sr2+ substitution on the reduction rates of YZ in PS II membranes—Evidence for concerted hydrogen-atom transfer in oxygen evolution. Biochemistry 39: 16220–16229

    Article  CAS  PubMed  Google Scholar 

  • Wincencjusz H, van Gorkom HJ and Yocum CF (1997) The photosynthetic oxygen evolving complex requires chloride for its redox state S2 → S3 and S3 → S0 transitions but not for S0 → S1 or S1 → S2 transitions. Biochemistry 36: 3663–3670

    Article  CAS  PubMed  Google Scholar 

  • Wincencjusz H, Yocum CF and van Gorkom HJ (1998) S-state dependence of chloride binding affinity and exchange dynamics in the intact and polypeptide-depleted O2 evolving complex of Photosystem II. Biochemistry 37: 8595–8604

    Article  CAS  PubMed  Google Scholar 

  • Wincencjusz H, Yocum CF and van Gorkom HJ (1999) Activating anions that replace Cl− in the O2-evolving complex of Photosystem II slow the kinetics of the terminal step in water oxidation and destabilize the S2 and S3 states. Biochemistry 38: 3719–3725

    Article  CAS  PubMed  Google Scholar 

  • Wydrzynski T, Baumgart F, Macmillan F and Renger G (1990) Is there a direct cofactor requirement in the oxygen-evolving reactions of Photosystem II? Photosynth Res 25: 59–72

    Article  CAS  Google Scholar 

  • Yachandra VK, DeRose VJ, Latimer MJ, Mukerji I, Sauer K and Klein MP (1993) Where plants make oxygen: A structural model for the photosynthetic oxygen-evolving manganese cluster. Science 260: 675–679

    CAS  PubMed  Google Scholar 

  • Yocum CF (1991) Calcium activation of photosynthetic water oxidation. Biochim Biophys Acta 1059: 1–15

    CAS  Google Scholar 

  • Zheng M and Dismukes GC (1996) Orbital configuration of the valence electrons, ligand field symmetry, and manganese oxidation states of the photosynthetic water oxidizing complex: Analysis of the S2 state multiline EPR signals. Inorg Chem 35: 3307–3319

    CAS  PubMed  Google Scholar 

  • Zouni A, Witt HT, Kern J, Fromme P, Krauss N, Saenger W and Orth P (2001) Crystal structure of Photosystem II from Synechococcus elongatus at 3.8 Ångstrom resolution. Nature 409: 739–743

    Article  CAS  PubMed  Google Scholar 

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Author information

Authors and Affiliations

  1. Department of Biophysics, Huygens Laboratory, Leiden University, P.O. Box 9504, 2300 RA, Leiden, The Netherlands

    Hans J. van Gorkom

  2. Department of Molecular, Cellular and Developmental Biology, University of Michigan, Ann Arbor, MI, 48109-1048, USA

    Charles F. Yocum

  3. Department of Chemistry, University of Michigan, Ann Arbor, MI, 48109-1048, USA

    Charles F. Yocum

Authors
  1. Hans J. van Gorkom
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  2. Charles F. Yocum
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Editors and Affiliations

  1. The Australian National University, Canberra, Australia

    Thomas J. Wydrzynski

  2. Okayama University, Okayama, Japan

    Kimiyuki Satoh

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van Gorkom, H.J., Yocum, C.F. (2005). The Calcium and Chloride Cofactors. In: Wydrzynski, T.J., Satoh, K., Freeman, J.A. (eds) Photosystem II. Advances in Photosynthesis and Respiration, vol 22. Springer, Dordrecht. https://doi.org/10.1007/1-4020-4254-X_14

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