Photosystem II pp 753-775 | Cite as

Understanding Photosystem II Function by Artificial Photosynthesis

  • Ann Magnuson
  • Stenbjörn Styring
  • Leif Hammarström
Part of the Advances in Photosynthesis and Respiration book series (AIPH, volume 22)


Inspired by the Photosystem II reaction center and the water oxidation chemistry that it performs, we aim to develop artificial photosynthesis for fuel production. Besides the original work we do in this direction, we also acquire knowledge feedback from our novel compounds. Our man-made systems create new perspectives on electron and proton transfer, bioinorganic chemistry, excitation energy transfer and other issues that are central to photosynthesis research. In this chapter we describe some of the highlights in our research and the conclusions they have generated.


Manganese PLASTOQUI None 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Abrahamsson MLA, Baudin HB, Tran A, Philouze C, Berg KE, Raymond-Johansson MK, Sun L, Åkermark B, Styring S and Hammarström L (2002) Ruthenium-manganese complexes for artificial photosynthesis: Factors controlling intramolecular electron transfer and excited-state quenching reactions. Inorg Chem 41: 1534–1544PubMedCrossRefGoogle Scholar
  2. Ahlbrink R, Haumann M, Cherepanov D, Bögershausen O, Mulkidjanian A and Junge W (1998) Function of TyrosineZ in water oxidation by Photosystem II: Electrostatical promoter instead of hydrogen abstractor. Biochemistry 37: 1131–1142PubMedCrossRefGoogle Scholar
  3. Åhrling KA, Peterson S and Styring S (1997) An oscillating manganese electron paramagnetic resonance signal from the S0 state of the oxygen evolving complex in Photosystem II. Biochemistry 36: 13148–13152PubMedGoogle Scholar
  4. Andréasson L-E, Vass I and Styring S (1995) Ca2+ depletion modifies the electron transfer on both the donor and acceptor side of Photosystem II from spinach. Biochim Biophys Acta 1230: 155–164Google Scholar
  5. Aro E-M, Virgin I and Andersson B (1993) Photoinhibition of Photosystem II. Inactivation, protein damage and turnover. Biochim Biophys Acta 1143: 113–134PubMedGoogle Scholar
  6. Babcock GT, Espe M, Hoganson C, Lydakis-Simantiris N, McCracken J, Shi W, Styring S, Tommos C and Warncke K (1997) Tyrosyl radicals in enzyme catalysis: Some properties and a focus on photosynthetic water oxidation. Acta Chemica Scandinavica 51: 533–540PubMedGoogle Scholar
  7. Balzani V and Carassiti V (1970) Photochemistry of Coordination Compounds. Academic Press, LondonGoogle Scholar
  8. Barber J and Andersson B (1992) Light can be both good and bad to photosynthesis. Trends Biochem Sci 17: 61–66PubMedCrossRefGoogle Scholar
  9. Berg KE, Tran A, Raymond MK, Abrahamsson M, Wolny J, Redon S, Andersson M, Sun L, Styring S, Hammarström L, Toftlund H and Åkermark B (2001) Covalently linked Ruthenium(II)-Manganese (II) complexes: Distance dependence of quenching and electron transfer. Eur J Inorg Chem 4: 1019–1029Google Scholar
  10. Berglund-Baudin H, Sun L, Davydov R, Sundahl M, Styring S, Åkermark B, Almgren M and Hammarström L (1998) Intramolecular electron transfer from manganese (II) coordinatively linked to a photogenerated Ru(III)-polypyridine complex: A kinetic analysis. J Phys Chem A 102: 2512–2518CrossRefGoogle Scholar
  11. Bernat G, Morvaridi F, Feyziyev Y and Styring S (2002) pH-dependence of the four individual transitions in the catalytic S-cycle during photosynthetic oxygen evolution. Biochemistry 41: 5830–5843PubMedCrossRefGoogle Scholar
  12. Boerner RJ and Barry BAB (1994) EPR evidence that the M+ radical which is observed in three site directed mutants of Photosystem II is a tyrosine radical. J Biol Chem 269: 134–137PubMedGoogle Scholar
  13. Britt RD (1996) Oxygen evolution. In: Ort D and Yocum C (eds) Oxygenic Photosynthesis: The Light Reactions, pp 137–164. Kluwer Academic Publishers, DordrechtGoogle Scholar
  14. Carrell, TG, Tyryshkin AM and Dismukes GC (2002) An evaluation of structural models for the photosynthetic water-oxidizing complex derived from spectroscopic and X-ray diffraction signatures. J Biol Inorg Chem 7: 2–22PubMedCrossRefGoogle Scholar
  15. Chen P and Meyer TJ (1996) Electron transfer in frozen media. Inorg Chem 35: 5520–5524PubMedGoogle Scholar
  16. Damrauer NH, Boussie TR, Devenney M and McCusker JK (1997) Effects of intraligand electron delocalization, steric tuning, and excited-state vibronic coupling on the photophysics of aryl-substituted bipyridyl complexes of Ru(II). J Am Chem Soc 119: 8253–8268CrossRefGoogle Scholar
  17. Dau H, Iuzzolino L and Dittmer J (2001) The tetra-manganese complex of Photosystem II during its redox cycle — X-ray absorption results and mechanistic implications. Biochim Biophys Acta 1503: 24–39PubMedGoogle Scholar
  18. Diner BA (2001) Amino acid residues involved in the coordination and assembly of the manganese cluster of Photosystem II. Proton-coupled electron transfer of the redox-active tyrosines and its relationship to water oxidation. Biochim Biophys Acta 1503:147–163PubMedGoogle Scholar
  19. Diner BA and Babcock GT (1996) Structure, dynamics and energy conversion efficiency in Photosystem II. In: Ort D and Yocum C (eds) Oxygenic Photosynthesis: The Light Reactions, pp 213–247. Kluwer Academic Publishers, DordrechtGoogle Scholar
  20. Diner BA, Force DA, Randall DW and Britt RD (1998) Hydrogen bonding, solvent exchange, and coupled proton and electron transfer in the oxidation and reduction of redox-active tyrosine YZ in Mn-depleted core complexes of Photosystem II. Biochemistry 37: 17931–17943PubMedCrossRefGoogle Scholar
  21. Diril H, Chang H-R, Zhang X, Larsen SK, Potenza JA, Pierpont CG, Schugar HJ, Isied SS and Hendrickson DN (1987) Binuclear mixed-valence MnIIMnIII complexes: Insight about the resolution of hyperfine structure in the EPR spectrum. J Am Chem Soc 109: 6207–6208CrossRefGoogle Scholar
  22. Dismukes GC and Siderer Y (1981) Intermediates of a polynuclear manganese center involved in the photosynthetic oxidation of water. Proc Natl Acad Sci USA 78: 274–178Google Scholar
  23. Ferreira KN, Iverson TM, Maghlaoui K, Barber J and Iwata S (2004) Architecture of the photosynthetic oxygen-evolving center. Science 303: 1831–1838PubMedCrossRefGoogle Scholar
  24. Frey M (2002) Hydrogenases: Hydrogen-activating enzymes. Chem Bio Chem 3: 153–160PubMedGoogle Scholar
  25. Gaines GL, O’Neil MP, Svec WA, Niemczyk MP and Wasielewski MR (1991) Photo-induced electron transfer in the solid state—Rate vs. free energy dependence in fixed-distance porphyrin acceptor molecules. J Am Chem Soc 113: 719–721CrossRefGoogle Scholar
  26. Geijer P, Morvaridi F and Styring S (2001) The S3 state of the oxygen evolving system in Photosystem II is converted to the S2YZ state at alkaline pH. Biochemistry 40: 10881–10891PubMedCrossRefGoogle Scholar
  27. Hammarström L, Barigelletti F, Flamigni L, Indelli MT, Armaroli N, Calogero G, Guardigli M, Sour A, Collin J-P and Sauvage J-P (1997) A study on delocalization of MLCT excited states by rigid bridging ligands in homometallic binuclear complexes of Ruthenium. J Phys Chem A 101: 9061–9069Google Scholar
  28. Hammarström L, Sun L, Magnuson A, Frapart Y, Berglund-Baudin H, Åkermark B and Styring S (1999) Mimicking Photosystem II reactions in artificial photosynthesis. Zeitschrift Phys Chem 123:157–163Google Scholar
  29. Hammarström L, Sun L, Åkermark B and Styring S (2001) A biomimetic approach to artificial photosynthesis: Ru(II)-poly-pyridine photosensitisers linked to tyrosine and manganese electron donors. Spectrochimica Acta A 37: 2145–2160Google Scholar
  30. Haumann M, Mulkidjanian A and Junge W (1999) Tyrosine-Z in oxygen-evolving Photosystem II: A hydrogen-bonded tyrosinate. Biochemistry 38: 1258–1267PubMedCrossRefGoogle Scholar
  31. Hays A-MA, Vassiliev IR, Golbeck JH and Debus RJ (1998) Role of D1-His190 in proton-coupled electron transfer reactions in Photosystem II: A chemical complementation study. Biochemistry 37: 11352–11365PubMedCrossRefGoogle Scholar
  32. Hays A-MA, Vassiliev IR, Golbeck JH and Debus RJ (1999) Role of D1-His190 in the proton-coupled oxidation of tyrosine YZ in manganese-depleted Photosystem II. Biochemistry 38: 11851–11865PubMedCrossRefGoogle Scholar
  33. Hogansson CW and Babcock GT (1997) A metalloradical mechanism for the generation of oxygen from water in photosynthesis. Science 277: 1953–1956Google Scholar
  34. Hoganson CW, Lydakis-Simantiris N, Tang X-S, Tommos C, Warncke K, Babcock GT, Diner BA, McCracken J and Styring S (1995) A hydrogen-atom abstraction model for the function of YZ in photosynthetic oxygen evolution. Photosynth Res 46: 177–184CrossRefGoogle Scholar
  35. Horner O, Anxolabehere-Mallart E, Chariot MF, Tchertanov L, Guilhem J, Mattioli TA, Boussac A and Girerd JJ (1999) A new manganese dinuclear complex with phenolate ligands and a single unsupported oxo bridge. Storage of two positive charges within less than 500 mV. Relevance to photosynthesis. Inorganic Chemistry 38: 1222–1232PubMedCrossRefGoogle Scholar
  36. Huang P, Magnuson A, Lomoth R, Abrahamsson M, Tamm M, Sun L, van Rotterdam B, Park J, Hammarström L, Åkermark B and Styring S (2002) Three-step oxidation of a MnII,IIdimer to MnIII,IV by photogenerated RuIII: Towards a functional mimic of the water oxidizing center in Photosystem II. J Inorg Biochemistry 91: 159–172Google Scholar
  37. Huang P, Högblom J, Anderlund MF, Sun L, Magnuson A and Styring S (2004) Light-induced multistep oxidation of dinuclear manganese complexes for artificial photosynthesis. J Inorg Biochemistry 98: 733–745Google Scholar
  38. Ioannidis N and Petrouleas V (2000) Electron paramagnetic resonance signals from the S3 state of the oxygen evolving complex: A broadened radical signal induced by low-temperature near-infrared light illumination. Biochemistry 39: 5246–5254PubMedCrossRefGoogle Scholar
  39. Iuzzolino L, Dittmer J, Dorner W, Meyer-Kaucke W and Dau H (1998) X-ray absorption spectroscopy on layered Photosystem II membrane particles suggests manganese-centered oxidation of the oxygen-evolving complex for the S0–S1; S1–S2, and S2–S3 transitions of the water oxidation cycle. Biochemistry 37: 17112–17119PubMedCrossRefGoogle Scholar
  40. Jegerschöld C and Styring S (1991) Fast oxygen-independent degradation of the D1 reaction center protein in Photosystem II. FEBS Lett 280: 87–90PubMedCrossRefGoogle Scholar
  41. Jegerschöld C and Styring S (1992) Photoinhibition of Cl-depleted thylakoid membranes. Effects of illumination under anaerobic conditions. In: Barber J, Medrane H and Guerrero MG (eds) Trends in Photosynthesis Research, pp 59–69. Intercept Ltd, AndoverGoogle Scholar
  42. Jegerschöld C and Styring S (1996) Spectroscopic characterization of intermediate steps involved in donor-side photoinhibition of Photosystem II. Biochemistry 35: 7794–7801PubMedGoogle Scholar
  43. Jegerschöld C, Virgin I and Styring S (1990) Light-dependent degradation of the D1 protein in Photosystem-II is accelerated after inhibition of the water splitting reaction. Biochemistry 29: 6179–6186PubMedGoogle Scholar
  44. Juris A, Balzani V, Barigelletti F, Campagna S, Belser P and von Zelewsky A (1988) Ru(II) polypyridine complexes: Photophysics, photochemistry, electrochemistry and chemiluminescence. Coord Chem Rev 84: 85–277CrossRefGoogle Scholar
  45. 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: 98–103PubMedCrossRefGoogle Scholar
  46. Krieger A, Rutherford AW and Johnson GN (1995) On the determination of redox midpoint potential of the primary quinone electron acceptor, QA, in Photosystem II. Biochim Biophys Acta 1229: 193–201Google Scholar
  47. Kuzek D and Pace RJ (2001) Probing the Mn oxidation states in the OEC. Insights from spectroscopic, computational and kinetic data. Biochim Biophys Acta 1503: 123–137PubMedGoogle Scholar
  48. Lavergne J and Junge W (1993) Proton release during the redox cycle of the water oxidase Photosynth Res 38: 279–296CrossRefGoogle Scholar
  49. Liang WC, Roelofs TA, Cinco RM, Rompel A, Latimer MJ, Yu WO, Sauer K, Klein MP and Yachandra VK (2000) Structural change of the Mn cluster during the S2 → S3 state transition of the oxygen-evolving complex of Photosystem II. Does it reflect the onset of water/substrate oxidation? Determination by Mn X-ray absorption spectroscopy. J Am Chem Soc 122: 3399–3412Google Scholar
  50. Lomoth R, Huang P, Zheng J, Sun L, Hammarström L, Åkermark B and Styring S (2002) Synthesis and characterization of a dinuclear manganese(III,III) complex with three phenolate ligands. Eur J Inorg Chem 2965–2974Google Scholar
  51. Ma C and Barry BAB (1996) Electron paramagnetic resonance characterization of tyrosine radical M+, in site-directed mutants of Photosystem II. Biophys J 71: 1961–1972PubMedGoogle Scholar
  52. Magnuson A, Berglund H, Korall P, Hammarström L, Åkermark B, Styring S and Sun L (1997) Mimicking electron transfer reactions in Photosystem II: Synthesis and photochemical characterization of a ruthenium(II) tris-bipyridyl complex with a covalently linked tyrosine. J Am Chem Soc 119: 10720–10725CrossRefGoogle Scholar
  53. Magnuson A, Frapart Y, Abrahamsson M, Horner O, Åkermark B, Sun L, Girerd J-J, Hammarström L and Styring S (1999) A biomimetic model system for the water oxidizing triad in Photosystem II. J Am Chem Soc 121: 89–96CrossRefGoogle Scholar
  54. Mamedov F, Sayre RT and Styring S (1998) Involvement of histidine 190 on the D1 protein in electron/proton transfer reactions on the donor side of Photosystem II. Biochemistry 37: 14245–14256PubMedCrossRefGoogle Scholar
  55. Marcus RA and Sutin N (1985) Electron transfers in chemistry and biology. Biochim Biophys Acta 811: 265–322Google Scholar
  56. Matsukawa T, Mino H, Yoneda D and Kawamori A (1999) Dual-mode EPR study of new signals from the S3-state of oxygen-evolving complex in Photosystem II. Biochemistry 38: 4072–4077PubMedCrossRefGoogle Scholar
  57. Messinger J, Robblee JH, Yu WO, Sauer K, Yachandra VK and Klein MP (1997) The S0 state of the oxygen-evolving complex in Photosystem II is paramagnetic: Detection of an EPR multiline signal. J Am Chem Soc 119: 11349–11350CrossRefGoogle Scholar
  58. Mino H, Kawamori A, Matsukawa T and Ono T (1998) Light-induced high-spin signals from the oxygen evolving center in Ca2+-depleted Photosystem II studied by dual mode electron paramagnetic resonance spectroscopy. Biochemistry 37: 2794–2799PubMedCrossRefGoogle Scholar
  59. Nugent JH (ed) (2001) Special Issue: Photosynthetic Water Oxidation. Biochim Biophys Acta 1503: 1–259Google Scholar
  60. Nugent JHA, Rich AM and Evans MCW (2001) Photosynthetic water oxidation: Towards a mechanism. Biochim Biophys Acta 1503: 138–146PubMedGoogle Scholar
  61. Nugent JHA, Muhiuddin IP and Evans MCW (2002) Electron transfer from the water oxidizing complex at cryogenic temperatures: The S1 to S2 Step. Biochemistry 41: 4117–4126PubMedCrossRefGoogle Scholar
  62. Pecoraro V (ed) (1992) Manganese Redox Systems. Wiley, New YorkGoogle Scholar
  63. Pecoraro VL, Baldwin MJ, Caudle MT, Hsieh W-Y and Law NA (1998) A proposal for water oxidation in Photosystem II. Pure Appl Chem 70: 925–929Google Scholar
  64. Peloquin JM and Britt RD (2001) EPR/ENDOR characterization of the physical and electronic structure of the OEC Mn cluster. Biochim Biophys Acta 1503: 96–110PubMedGoogle Scholar
  65. Porter GB and Schäfer HL (1964) Zur Frage der Lumineszenz bei Ubergangsmetallverbindungen. Ber Bunsen-Ges Phys Chem 68: 316–331Google Scholar
  66. Prasil O, Adir N and Ohad I (1992) Dynamics of Photosystem II: Mechanism of photoinhibition and recovery process. In: Barber J (ed) Current Topics in Photosynthesis Vol 11, pp 220–250. Elsevier Science Publishers, AmsterdamGoogle Scholar
  67. Rappaport F and Lavergne J (2001) Coupling of electron and proton transfer in the photosynthetic water oxidase. Biochim Biophys Acta 1503: 246–259PubMedGoogle Scholar
  68. Renger G (2001) Photosynthetic water oxidation to molecular oxygen: Apparatus and mechanism. Biochim Biophys Acta 1503:210–228PubMedGoogle Scholar
  69. Robblee JH, Cinco RM and Yachandra VK (2001) X-ray spectroscopy-based structure of the Mn cluster and mechanism of photosynthetic oxygen evolution. Biochim Biophys Acta 1503: 7–23PubMedGoogle Scholar
  70. Rova M, Franzén L-G, Fredriksson P-O and Styring S (1993) Photosystem II in a mutant of Chlamydomonas reinhardtii I lacking the 23 kDa psbP protein is sensitive to photoinhibition in the absence of chloride. Photosynth Res 39: 75–83Google Scholar
  71. Rova M, MacEwen B, Fredriksson PO and Styring S (1996) Photoactivation and photoinhibition are competing in a mutant of Chlamydomonas reinhardtii lacking the 23kDa subunit of Photosystem II. J Biol Chem 271: 28918–28924PubMedGoogle Scholar
  72. Rova M, Mamedov F, Magnuson A, Fredriksson P-O and Styring S (1998) Coupled activation of the donor and the acceptor Side of Photosystem II during photoactivation of the oxygen evolving cluster. Biochemistry 37: 11039–11045PubMedCrossRefGoogle Scholar
  73. Siegbahn PEM and Crabtree RH (1999) Manganese oxyl radical intermediates and O-O bond formation in photosynthetic oxygen evolution and a proposed role for the calcium cofactor in Photosystem II. J Am Chem Soc 121: 117–127CrossRefGoogle Scholar
  74. Sjödin M, Styring S, Åkermark B, Sun L and Hammarström L (2000) Proton coupled electron transfer from tyrosine in a tyrosine-ruthenium-tris-bipyridine complex: Comparison with tyrosineZ oxidation in Photosystem II. J Am Chem Soc 122: 3932–3936Google Scholar
  75. Sjödin M, Styring S, Åkermark B, Sun L and Hammarström L (2002) The mechanism for proton coupled electron transfer from tyrosine in a model complex and comparisons with tyrosine Z oxidation in Photosystem II. Phil Trans B 357: 1471–1478Google Scholar
  76. Sjödin M, Ghanem R, Polivka T, Pan J, Styring S, Sun L, Sundström V and Hammarström L (2004) Tuning proton coupled electron transfer from tyrosine: A competition between concerted and step-wise mechanisms. Phys Chem Chem Phys 6: 4851–4858CrossRefGoogle Scholar
  77. Steinberg-Yfrach G, Rigaud J-L, Durantini EN, Moore AL, Gust D and Moore TA (1998) Light-driven production of ATP catalysed by F0F1-ATP synthase in an artificial photosynthetic membrane. Nature 392: 479–482PubMedGoogle Scholar
  78. Styring S and Jegerschöld C (1994) Light induced reactions impairing the electron transfer through Photosystem II. In: Baker NR and Bowyer JR (eds) Photoinhibition of Photosynthesis, pp 51–73. BIOS Scientific, OxfordGoogle Scholar
  79. Styring S, Virgin I, Ehrenberg A and Andersson B (1990) Strong light photoinhibition of electron transport in Photosystem II. Impairment of the function of the first quinone acceptor QA. Biochim Biophys Acta 1015: 269–278Google Scholar
  80. Sun L, Berglund H, Davydov R, Norrby T, Hammarström L, Korall P, Börje A, Philouze C, Berg K, Tran A, Andersson M, Stenhagen G, Mårtensson J, Almgren M, Styring S and Åkermark B (1997) Binucelar ruthenium-manganese complexes as simple artificial models for Photosystem II in green plants J Am Chem Soc 119: 6996–7004Google Scholar
  81. Sun L, Åkermark B, Hammarström L and Styring S (1999) Intramolecular electron transfer from manganese to photogenerated Ru(bpy)33+. A functional mimic of the photoevents on the donor side of Photosystem II. Trends Inorg Chem 6: 151–155Google Scholar
  82. Sun L, Raymond MK, Magnuson A, LeGourriérec D, Tamm M, Abrahamsson M, Kenéz PH, Mårtensson J, Stenhagen G, Hammarström L, Styring S and Åkermark B (2000) Towards an artificial model for Photosystem II: A manganese (II,II) dimer covalently linked to ruthenium(II)tris-bipyridine via a tyrosine derivative. J Inorg Biochemistry 78: 15–22Google Scholar
  83. Sun L, Hammarström L, Åkermark B and Styring S (2001) Towards artificial photosynthesis: Ruthenium-manganese chemistry for energy production. Chem Soc Rev 30: 36–49CrossRefGoogle Scholar
  84. Sutin N (1982) Nuclear, electronic, and frequency factors in electron-transfer reactions. Acc Chem Res 15: 275–282CrossRefGoogle Scholar
  85. Svensson B, Vass I and Styring S (1991) Sequence analysis of the D1 and D2 reaction center proteins of Photosystem II. Z Naturforsch 46c: 62–73Google Scholar
  86. Svensson B, Etchebest C, Tuffery P, van Kan P, Smith J and Styring S (1996) A model for the Photosystem II reaction centre core including the structure of the primary donor P680. Biochemistry 35: 14486–14502PubMedCrossRefGoogle Scholar
  87. Tommos CT and Babcock GT (2000) Proton and hydrogen currents in photosynthetic water oxidation. Biochim Biophys Acta 1458: 199–219PubMedGoogle Scholar
  88. Tommos C, Tang X-S, Warncke K, Hoganson CW, Styring S, McCracken J, Diner BA and Babcock GT (1995) Spin-density distribution, and hydrogen bonding of the redox-active tyrosine YZ in Photosystem II from multiple electron magnetic-resonance spectroscopies: Implications for photosynthetic oxygen evolution. J Am Chem Soc 117: 10325–10335CrossRefGoogle Scholar
  89. Treadway JA, Loeb B, Lopez R, Anderson PA, Keene FR and Meyer TJ (1996) Effect of delocalization and rigidity in the acceptor ligand on MLCT excited-state decay. Inorg Chem 35:2242–2246PubMedCrossRefGoogle Scholar
  90. van Wijk KJ, Nilsson LO and Styring S (1994) Synthesis of reaction center proteins and reactivation of redox components during repair of Photosystem II after light induced inactivation. J Biol Chem 269: 28382–28392PubMedGoogle Scholar
  91. Vass I and Styring S (1991) pH-dependent charge-equilibria between tyrosine D and the S-states in Photosystem II. Estimation of relative midpoint potentials. Biochemistry 30: 830–839PubMedCrossRefGoogle Scholar
  92. Vrettos JS, Limburg J and Brudvig GW (2001) Mechanism of photosynthetic water oxidation: combining biophysical studies of Photosystem II with inorganic model chemistry. Biochim Biophys Acta 1503: 229–245PubMedGoogle Scholar
  93. Wasielewski MR, Johnson DG, Svec WA, Kersey KM and Minjsek DW (1988) Achieving high quantum yield charge separation in porphyrin-containing donor-acceptor molecules at 10 K. J Am Chem Soc 110: 7219–7221CrossRefGoogle Scholar
  94. Yachandra VK, Sauer K and Klein MP (1996) Manganese cluster in Photosystem II: Where plants oxidize water to dioxygen. Chem Rev 96: 2927–2950PubMedCrossRefGoogle Scholar
  95. Yamauchi T, Mino H, Matsukawa T, Kawamori A and Ono T (1997) Parallel polarization electron paramagnetic resonance studies of the S-l-state manganese cluster in the photosynthetic oxygen-evolving system. Biochemistry 36: 7520–7526PubMedCrossRefGoogle Scholar
  96. Zhang C and Styring S (2003) Formation of split electron paramagnetic resonance signals in Photosystem II suggests that TyrosineZ can by photooxidized at 5 K in the S0 and S1 states of the oxygen-evolving complex. Biochemistry 42: 8066–8076PubMedGoogle Scholar
  97. Zouni A, Witt H-T, Kern J, Fromme P, Krauss N, Saenger W and Orth P (2001) Crystal structure of Photosystem II from Synechococcus elongatus at 3.8Å resolution. Nature 409: 739–743PubMedCrossRefGoogle Scholar

Copyright information

© Springer 2005

Authors and Affiliations

  • Ann Magnuson
    • 1
  • Stenbjörn Styring
    • 1
  • Leif Hammarström
    • 2
  1. 1.Molecular BiomimeticsUppsala UniversityUppsalaSweden
  2. 2.Department of Physical ChemistryUppsala UniversityUppsalaSweden

Personalised recommendations