Apparatus and mechanism of photosynthetic oxygen evolution: a personal perspective

  • Gernot Renger
Part of the Advances in Photosynthesis and Respiration book series (AIPH, volume 20)


This historical minireview describes basic lines of progress in our understanding of the functional pattern of photosynthetic water oxidation and the structure of the Photosystem II core complex. After a short introduction into the state of the art about 35 years ago, results are reviewed that led to identification of the essential cofactors of this process and the kinetics of their reactions. Special emphasis is paid on the flash induced oxygen measurements performed by Pierre Joliot (in Paris, France) and Bessel Kok (Baltimore, MD) and their coworkers that led to the scheme, known as the Kok-cycle. These findings not only unraveled the reaction pattern of oxidation steps leading from water to molecular oxygen but also provided the essential fingerprint as prerequisite for studying individual redox reactions. Starting with the S. Singer and G. Nicolson model of membrane organization, attempts were made to gain information on the structure of the Photsystem II complex that eventually led to the current stage of knowledge based on the recently published X-ray crystal structure of 3.8 Å resolution in Berlin (Germany). With respect to the mechanism of water oxidation, the impact of Gerald T. Babcock’s hydrogen abstractor model and all the considerations of electron/proton transfer coupling are outlined. According to my own model cosiderations, the protein matrix is not only a ‘cofactor holder’ but actively participates by fine tuning via hydrogen bond networks, playing most likely an essential role in water substrate coordination and in oxygen-oxygen bond formation as the key step of the overall process.

Key words

Gerald T. Babcock Bernadette Bouges-Bocquet George Cheniae hydrogen atom abstraction Pierre Joliot Melvin Klein Bessel Kok mechanism Photosystem II Gernot Renger Ken Sauer structure water cleavage 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Adir N, Zer H, Shochat S and Ohad I (2003) Photoinhibition — a historical perspective Photosynth Res 76: 343–370PubMedCrossRefGoogle Scholar
  2. Allen FA and Franck J (1955) Photosynthetic evolution of oxygen by flashes of light. Arch Biochem Biophys 58: 124–143PubMedCrossRefGoogle Scholar
  3. Ananyev GM, Zaltsman L, Vasko C and Dismukes GC (2001) The inorganic biochemistry of photosynthetic oxygen evolution/ water oxidation. Biochim Biophys Acta 1503: 52–68PubMedCrossRefGoogle Scholar
  4. Anderson JM (2001) Does functional Photosystem II complex have an oxygen channel? FEBS Lett 488: 1–4PubMedCrossRefGoogle Scholar
  5. Anderson JM (2002) Changing concepts about the distribution of Photosystems I and II between grana-appressed and stroma-exposed thylakoid membranes. Photosynth Res 73: 157–164PubMedCrossRefGoogle Scholar
  6. Anderson JM and Boardman NK (1966) Fractionation of the photochemical systems of photosynthesis. I. Chlorophyll contents and photochemical activities of particles isolated from spinach chloroplasts. Biochim Biophys Acta 112: 403–412Google Scholar
  7. Astashkin AV, Mino H, Kawamori A and Ono T (1997) Pulsed EPR study of the S’3 signal in the Ca2+-depleted Photosystem II. Chem Phys Lett 272: 506–516CrossRefGoogle Scholar
  8. Babcock GT (1995) The oxygen-evolving complex in Photosystem II as a metallo-radical enzyme. In: Mathis P (ed) Photosynthesis: from Light to Biosphere, pp 209–215. Kluwer Adademic Publishers, Dordrecht, The NetherlandsGoogle Scholar
  9. Babcock GT and Sauer K (1973) Electron paramagnetic resonance signal II in spinach chloroplasts. I. Kinetic analysis for untreated chloroplasts. Biochim Biophys Acta 325: 483–503PubMedCrossRefGoogle Scholar
  10. Babcock GT and Sauer K (1975a) A rapid light-induced transient in electron paramagnetic resonance signal II activated upon inhibition of photosynthetic oxygen evolution. Biochim Biophys Acta 376: 315–328PubMedCrossRefGoogle Scholar
  11. Babcock GT and Sauer K (1975b) The rapid component of electron paramagnetic resonance signal II: a candidate for the physiological donor to Photosystem II in spinach chloroplasts. Biochim Biophys Acta 376: 329–344PubMedCrossRefGoogle Scholar
  12. Babcock GT, Blankenship RE and Sauer K (1976) Reaction kinetics for positive charge accumulation on the water side of chloroplast Photosystem II. FEBS Lett 61: 286–289PubMedCrossRefGoogle Scholar
  13. Babcock GT, Barry BA, Debus RJ, Hoganson CW, Atamian m, McIntosh L, Sithole I and Yocum CF (1989) Water oxidation in Photosystem II: from radical chemistry to multielectron chemistry. Biochemistry 28: 9557–9565PubMedCrossRefGoogle Scholar
  14. Bader KP, Renger G and Schmid GH (1993) A mass spectroscopic analysis of the water-splitting reaction. Photosynth Res 38: 355–361CrossRefGoogle Scholar
  15. Barry B and Babcock GT (1987) Tyrosine radicals are involved in the photosynthetic oxygen-evolving system. Proc Natl Acad Sci USA 84: 7099–7103PubMedCrossRefGoogle Scholar
  16. Berthold DA, Babcock GT and Yocum CF (1981) A highly resolved, oxygen evolving Photosystem II preparation from spinach thylakoid membranes. EPR and electron transport properties. FEBS Lett 134: 231–234CrossRefGoogle Scholar
  17. Bernarding J, Eckert H-J, Eichler HJ, Napiwotzki A and Renger G (1994) Kinetic studies on the stabilisation of the primary radical pair P680+Pheo in different Photosystem II preparations from higher plants. Photochem Photobiol 59: 566–573Google Scholar
  18. Blankenship RE, Babcock GT, Warden JT and Sauer K (1975) Observation of a new EPR transient in chloroplasts that may reflect the electron donor to Photosystem II at room temperature. FEBS Lett 51: 287–293PubMedCrossRefGoogle Scholar
  19. Bogorad L (2003) Photosynthesis research: advances through molecular biology — the beginnings, 1975–1980s and on.... Photosynth Res 76: 13–33PubMedCrossRefGoogle Scholar
  20. Boska M, Sauer K, Buttner W and Babcock GT (1983) Similarity of EPR signal II, rise and P-680+ decay kinetics in tris-washed chloroplast Photosystem II preparations as a function of pH. Biochim Biophys Acta 722: 327–330CrossRefGoogle Scholar
  21. Bouges-Bocquet B (1973) Electron transfer between the two photosystems in spinach chloroplasts. Biochim Biophys Acta 314:250–256PubMedCrossRefGoogle Scholar
  22. Bouges-Bocquet B (1980) Kinetic models for the electron donors of Photosystem II of photosynthesis. Biochim Biophys Acta 594:85–103PubMedGoogle Scholar
  23. Brettel K, Schlodder E and Witt HT (1984) Nanosecond reduction kinetics of photooxidized chlorophyll-aII (P-680) in single flashes as a probe for the electron pathway, H+-release and charge accumulation in the O2-evolving complex. Biochim Biophys Acta 766: 403–415CrossRefGoogle Scholar
  24. Britt RD, Sauer K and Yachandra VK (2001) Remembering Melvin P. Klein (1921–2000). Biochim Biophys Acta 1503: 2–6PubMedCrossRefGoogle Scholar
  25. Broad W and Wade N (1982) Betrayers of the Truth. Fraud and Deceit in the Hall of Science. Simon and Schuster, New York.Google Scholar
  26. Brok M, Ebskamp FCR and Hoff, AJ (1985) The structure of the secondary donor of Photosystem II investigated by EPR at 9 and 35 GHz. Biochim Biophys Acta 809: 421–428CrossRefGoogle Scholar
  27. Cheniae GM and Martin IF (1969) Photoreactivation of manganese catalyst in photosynthetic oxygen evolution. Plant Physiol 44:351–360PubMedGoogle Scholar
  28. Cheniae GM and Martin IF (1970) Sites of function of manganese within photosystem II. Roles in O2-evolution and system II. Biochim Biophys Acta 197: 219–239PubMedCrossRefGoogle Scholar
  29. Christen G and Renger G (1999) The role of hydrogen bonds for the multiphasic P680+. reduction by YZ in Photosystem II with intact oxygen evolution capacity. Analysis of kinetic H/D isotope exchange effects. Biochemistry 38: 2068–2077PubMedCrossRefGoogle Scholar
  30. Christen G, Reifarth F and Renger G (1998) On the origin of the ‘35 µs kinetics’ of P680+. reduction in Photosystem II with an intact water oxidising complex. FEBS Lett 429: 49–52PubMedCrossRefGoogle Scholar
  31. Christen G, Seeliger A and Renger G (1999) P680+. reduction kinetics and redox transition probability of the water oxidising complex as a function of pH and H/D isotope exchange in spinach thylakoids. Biochemistry 38: 6082–6092PubMedCrossRefGoogle Scholar
  32. Clark LC Jr, World R, Granger D and Taylor Z (1953) Continuous recording of blood oxygen tensions by polarography. J Appl Physiol 6: 189–193PubMedGoogle Scholar
  33. Clayton RK (2002) Research on photosynthetic reaction centers from 1932–1987. Photosynth Res 73: 63–71PubMedCrossRefGoogle Scholar
  34. Cogdell R (1996) Philip Thornber (1934–1996). Photosynth Res 50:1–3CrossRefGoogle Scholar
  35. Commoner B, Heise JJ and Townsend J (1956) Light-induced paramagnetism in chloroplasts. Proc Natl Acad Sci USA 42:710–718PubMedCrossRefGoogle Scholar
  36. Conjeaud H and Mathis P (1980) The effect of pH on the reduction kinetics of P-680 in tris-treated chloroplasts. Biochim Biophys Acta 590: 353–359PubMedCrossRefGoogle Scholar
  37. Conjeaud H, Mathis P and Paillotin G (1979) Primary and secondary electron donors in Photosystem II of chloroplasts. Rates of electron transfer and location in the membrane. Biochim Biophys Acta 546: 280–291PubMedCrossRefGoogle Scholar
  38. Debus RJ (1992) The manganese and calcium ions in photosynthetic O2 evolution. Biochim Biophys Acta 1102: 269–352PubMedCrossRefGoogle Scholar
  39. 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: 164–186PubMedCrossRefGoogle Scholar
  40. Debus RJ, Barry BA, Babcock GT and McIntosh L (1988a) Directed mutagenesis indicates that the donor to P680+ in Photosystem II is tyrosine-161 of the D1 polypeptide. Biochemistry 27: 9071–9074PubMedCrossRefGoogle Scholar
  41. Debus RJ, Barry BA, Babcock GT and McIntosh L (1988b) Site-directed mutagenesis identifies a tyrosine radical involved in the photosynthetic oxygen-evolving system. Proc Natl Acad Sci USA 85: 427–430PubMedCrossRefGoogle Scholar
  42. Deisenhofer J, Epp O, Miki K, Huber R and Michel H (1984) X-Ray structure analysis of a membrane protein complex; electron density map at 3 Å resolution and a model of the chromophores of the photosynthetic reaction center from Rhodopseudomonas viridis. J Mol Biol 180: 385–398PubMedCrossRefGoogle Scholar
  43. Dekker JP, van Gorkom HJ, Wessink J and Ouwehand L (1984a) Absorbance difference spectra of the successive redox states of the oxygen-evolving apparatus of photosynthesis. Biochim Biophys Acta 767: 1–9CrossRefGoogle Scholar
  44. Dekker JP, Brok M and van Gorkom HJ (1984b) Absorbance changes of Z+, the component responsible for EPR signal II fast in tris-treated Photosystem II particles. In: Sybesma C (ed) Advances in Photosynthesis Research, Vol I, pp 171–174. Martinus Nijhoff/Dr W Junk Publishers, The Hague/Boston/LancasterGoogle Scholar
  45. Diner BA (2001) Amino acid residues involved in the coordination and assembly of the manganese cluster of Photosystem II. Proton-coupled electron transport of the redox-active tyrosines and its relationship to water oxidation. Biochim Biophys Acta 1503: 147–163PubMedCrossRefGoogle Scholar
  46. Diner BA, Schlodder E, Nixon PJ, Coleman WJ, Rappaport F, Lavergne J, Vermaas WFJ and Chisholm DA (2001) Site-directed Mutations at D1-His198 and D2-His197 of Photosystem II in Synechocystis PCC 6803: sites of primary charge separation and cation and triplet stabilization. Biochemistry 40: 9265–9281PubMedCrossRefGoogle Scholar
  47. Dismukes GC and Siderer Y (1981) Intermediates of a polynuclear manganese center involved in photosynthetic oxidation of water. Proc Natl Acad Sci USA 78: 274–278PubMedCrossRefGoogle Scholar
  48. Döring G, Renger G, Vater J and Witt HT (1969) Properties of the photoactive chlorophyll-a in photosynthesis. Z Naturforsch 24 b: 1139–1143Google Scholar
  49. Dorlet P, DiValentin M, Babcock GT and McCracken JL (1998) Interaction of YZ. with its environment in acetate-treated Photosystem II membranes and reaction center cores. J Phys Chem B 102: 8239–8247CrossRefGoogle Scholar
  50. Eckert HJ and Renger G (1988) Temperature dependence of P680+ reduction in O2-evolving PS II membrane fragments at different redox states Si of the water oxidizing system. FEBS Lett 236:425–431CrossRefGoogle Scholar
  51. Eckert HJ, Renger G and Witt HT (1984) Reduction kinetics of the photooxidized chlorophyll-aII in the ns-range. FEBS Lett 167:316–320CrossRefGoogle Scholar
  52. Eckert HJ, Wiese N, Bernarding J, Eichler HJ and Renger G (1988) Analysis of the electron transfer from Pheoin to QA in PS II membrane fragments from spinach by time-resolved 325 nm absorption changes in the picosecond domain. FEBS Lett 240:153–158PubMedCrossRefGoogle Scholar
  53. Franzen LG, Styring S, Etienne AL, Hansson Ö and Vernotte C (1986) Spectroscopic and functional characterization of a highly oxygen-evolving Photosystem II reaction center complex from spinach. Photobiochem Photobiophys 13: 15–28Google Scholar
  54. Frasch WD and Sayre RT (2002) Remembering George Cheniae, who never compromised his high standards of science. Photosynth Res 70: 245–247CrossRefGoogle Scholar
  55. Gerken S, Brettel K, Schlodder E and Witt HT (1988) Optical characterization of the immediate electron donor to chlorophyll a+II in O2-evolving Photosystem II complexes. Tyrosine as possible electron carrier between chlorophyll aII and the water-oxidizing manganese complex. FEBS Lett 237: 69–75CrossRefGoogle Scholar
  56. Ghanotakis DF, O’Malley PJ, Babcock GT and Yocum CF (1983) Structure and inhibition of components on the oxidizing side of Photosystem II. In: Inoue Y, Crofts AR, Govindjee, Murata N, Renger G and Satoh K (eds) Studies on the Mechanism of Photosynthetic Oxygen Formation, pp 95–101. Academic Press Japan, TokyoGoogle Scholar
  57. Ghanotakis DF, Waggoner CM, Bowlby NR, Demetriou DM, Babcock GT and Yocum CF (1987) Comparative structural and catalytic properties of oxygen-evolving Photsystem II preparations. Photosynth Res 14: 191–199CrossRefGoogle Scholar
  58. Gläser M, Wolff Ch and Renger G (1976) Indirect evidence for a very fast recovery kinetics of chlorophyll-aII in spinach chloroplasts. Z Naturforsch 31c: 712–721Google Scholar
  59. Gleiter HM, Haag E, Shen JR, Eaton Rye JJ, Inoue Y, Vermaas WFJ and Renger G (1994) Functional characterization of mutant strains of the cyanobacterium Synechocystis sp. PCC 6803 lacking short domains within the large, lumen-exposed loop of the chlorophyll-protein CP47 in Photosystem II. Biochemistry 33: 12063–12071PubMedCrossRefGoogle Scholar
  60. Gleiter HM, Haag E, Shen JR, Eaton-Rye JJ, Seeliger AG, Inoue Y, Vermaas WFJ and Renger G (1995) Involvement of the CP47 protein in stabilization and photoactivation of a functional water oxidizing complex in the cyanobacterium Synechocystis sp. PCC 6803. Biochemistry 34: 15721–15731CrossRefGoogle Scholar
  61. Govindjee (2000) Milestones in photosynthesis research. In: Yunus M, Pathre U and Mohanty P (eds) Probing Photosynthesis, pp 9–39. Taylor & Francis, New YorkGoogle Scholar
  62. Greenfield SR, Seibert M, Govindjee and Wasielewski MR (1997) Direct measurements of the effective rate constant for primary charge separation in isolated Photosystem II reaction centers. J Phys Chem B 101: 2251–2255CrossRefGoogle Scholar
  63. Haag E, Irrgang KD, Boekema EJ and Renger G (1990) Functional and structural analysis of PS II core complexes from spinach with high oxygen evolution capacity. Eur J Biochem 189: 47–53PubMedCrossRefGoogle Scholar
  64. Haag E, Eaton-Rye J, Renger G and Vermaas WFJ (1993) Functionally important domains of the large hydrophilic loop of CP 47 as probed by oligonucleotide-directed mutagenesis in Synechocystis sp. PCC 6803. Biochemistry 32: 4444–4454PubMedCrossRefGoogle Scholar
  65. Hales BJ and Gupta AD (1981) Supposition of the origin of signal II from random and orientated chloroplasts. Biochim Biophys Acta 637: 303–311CrossRefGoogle Scholar
  66. Haveman J and Mathis P (1976) Flash-induced absorption changes of the primary donor of Photosystem II at 820 nm in chloroplasts inhibited by low pH or tris-treatment. Biochim Biophys Acta 440: 346–355PubMedCrossRefGoogle Scholar
  67. Hays AMA, Vasiliev 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: 11852–11865CrossRefGoogle Scholar
  68. Hillier W and Wydrzynski T (2000) Oxygen ligand exchange at metal sites — implications for the O2 evolving mechanism of Photosystem II. Biochim Biophys Acta 1503: 197–209Google Scholar
  69. Hoganson CW and Babcock GT (1997) A metalloradical mechanism for the generation of oxygen from water in photosynthesis. Science 277: 1953–1956PubMedCrossRefGoogle Scholar
  70. Homann PH (2002) Chloride and calcium in Photosystem II: from effects to enigma. Photosynth Res 73: 169–175PubMedCrossRefGoogle Scholar
  71. Ikeuchi M, Yuasa M and Inoue Y (1985) Simple and discrete isolation of an O2-evolving PS II reaction center complex retaining Mn and the extrinsic 33 kDa protein. FEBS Lett 185: 316–322CrossRefGoogle Scholar
  72. Irrgang KD, Renger G and Vater J (1986) Identification of Chlbinding proteins in a PS II preparation from spinach. FEBS Lett 204: 67–75CrossRefGoogle Scholar
  73. Joliot P (1965) Cinétiques de réactions liées à l’émission d’oxygène photosynthétique (in French). Biochim Biophys Acta 102, 116–134PubMedGoogle Scholar
  74. Joliot P (2003) Period-four oscillations of the flash-induced oxygen formation in photosynthesis. Photosynth Res 76: 65–72PubMedCrossRefGoogle Scholar
  75. Joliot P and Kok B (1975) Oxygen evolution in photosynthesis. In: Govindjee (ed) Bioenergetics of Photosynthesis, pp 387–412. Academic Press, New YorkGoogle Scholar
  76. Joliot P, Hofnung M and Chabaud R (1966) Etude de l’émission d’oxygène par des algues soumises à un éclairement modulé sinusoïdalement. J Chim Phys 10: 1423–1441Google Scholar
  77. Joliot P, Barbieri G and Chabaud R (1969) Un nouveau modèle des centres photochimiques du système II. Photochem Photobiol 10: 309–329Google Scholar
  78. Junge W (1975) Physical aspects of the electron transport and photophosphorylation in green plants. Ber Deutsch Bot Ges 88: 283–301Google Scholar
  79. Karge M, Irrgang KD, Sellin S, Feinäugle R, Liu B, Eckert HJ, Eichler HJ and Renger G (1996) Effects of hydrogen/deuterium exchange on photosynthetic water cleavage in PS II core complexes from spinach. FEBS Lett 378: 140–144PubMedCrossRefGoogle Scholar
  80. Karge M, Irrgang KD and Renger G (1997) Analysis of the reaction coordinate of photosynthetic water oxidation by kinetic measurements of 355 nm absorption changes at different temperatures in PS II preparations suspended in H2O or D2O. Biochemistry 36: 8904–8913PubMedCrossRefGoogle Scholar
  81. Keren N, Ohad I, Rutherford AW, Drepper F and Krieger-Liszkay A (2000) Inhibition of Photosystem II activity by saturating single turnover flashes in calcium-depleted and active Photosystem II. Photosynth Res 63: 209–216PubMedCrossRefGoogle Scholar
  82. Kessler E (1957) Stoffwechselphysiologische Untersuchungen an Hydrogenase enthaltenden Grünalgen. I. über die Rolle des Mangans bei Photoreduktion und Photosynthese (in German). Planta 49: 435–454CrossRefGoogle Scholar
  83. Klimov VV (2003) Discovery of pheophytin function in the photosynthetic energy conversion as the primary electron acceptor of Photosystem II. Photosynth Res 76: 247–253PubMedCrossRefGoogle Scholar
  84. Klimov VV, Klevanik AV, Shuvalov VA and Krasnovsky AA (1977) Reduction of pheophytin in the primary light reaction of Photosystem II. FEBS Lett 82: 183–186PubMedCrossRefGoogle Scholar
  85. Kohl DH, Wright JR and Weissman (1969) Electron spin resonance studies of free radicals derived from plastoquinone, α-and γ-tocopherol and their relation to free radicals observed in photosynthetic materials. Biochim Biophys Acta 180: 536–544PubMedCrossRefGoogle Scholar
  86. Koike H, Hanssum B, Inoue Y and Renger G (1987) Temperature dependence of S-state transition in a thermophilic cyanobacterium, Synechococcus vulcanus Copeland, measured by absorption changes in UV region. Biochim Biophys Acta 893: 524–533CrossRefGoogle Scholar
  87. Kok B, Forbush B and McGloin M (1970) Cooperation of charges in photosynthetic O2 evolution — I. A linear four step mechanism. Photochem Photobiol 11: 457–475PubMedGoogle Scholar
  88. Kouchkovsky Y (2002) The laboratory of photosynthesis and its successors at Gif-sur-Yvette, France. Photosynth Res 73: 295–303PubMedCrossRefGoogle Scholar
  89. Krasnovsky AA (1992) Excited chlorophyll and related problems. Photosynth Res 33: 177–193CrossRefGoogle Scholar
  90. Kühn P, Iwanowski N, Eckert HJ, Irrgang KD, Eichler HJ and Renger G (2001) Reaction coordinate of P680+• reduction by YZ in PS II core complexes from spinach. In: Proceedings of the 12th International Congress on Photosynthesis, Brisbane, Australia, S13-024. CSIRO Publishing, Collingwood, Australia (www. Scholar
  91. Lakshmi KV, Eaton SS, Eaton GR and Brudvig GW (1999) Orientation of the tetranuclear manganese cluster and tyrosine Z in the O2-evolving complex of Photosystem II: an EPR study of the S2YZ state in oriented Acetate-inhibited Photosystem II membranes. Biochemistry 38: 12758–12767PubMedCrossRefGoogle Scholar
  92. Lavergne J (1991) Improved UV visible spectra of the S-transitions in the photosynthetic oxygen evolving system. Biochim Biophys Acta 1060: 175–188Google Scholar
  93. Lavergne J and Junge W (1993) Proton release during the redox cycle of the water oxidase. Photosynth Res 38: 269–276CrossRefGoogle Scholar
  94. Markwell JP, Thornber JP and Boggs RT (1979) Higher plant chloroplasts: evidence that all of the chlorophyll exists as chlorophyll-protein complexes. Proc Natl Acad Sci USA 76: 1233–1235PubMedCrossRefGoogle Scholar
  95. Matoo AK, Pick U, Hoffman-Falk H and Edelman M (1981) Rapidly metabolized 32.000 dalton polypeptide of the chloroplast is the proteinaecous shield regulating Photosystem II electron transport and mediating diuron herbicide sensitivity. Proc Natl Acad Sci USA 78: 1572–1576CrossRefGoogle Scholar
  96. Menke W (1940) Untersuchungen über den Feinbau des Protoplasmas mit dem Universal-Elektronenmikroskop. Protoplasma 35: 115–130 [in German]Google Scholar
  97. Menke W (1990) Retrospective of a botanist. Photosynth Res 25: 77–82CrossRefGoogle Scholar
  98. Messinger J and Renger G (1993) Generation, oxidation by YDOX and possible electronic configuration of the redox states S0, S−1 and S−2 of the water oxidase in isolated spinach thylakoids. Biochemistry 32: 9379–9386PubMedCrossRefGoogle Scholar
  99. Messinger J, Badger M and Wydrzynski T (1995) Detection of one slowly exchanging substrate water molecule in the S3 state of Photosystem II. Proc Natl Acad Sci USA 92: 3209–3213PubMedCrossRefGoogle Scholar
  100. Messinger J, Seaton GR, Wydrzynski T, Wacker U and Renger G (1997) S−3 state of the water oxidase in Photosystem II. Biochemistry 36: 6862–6873PubMedCrossRefGoogle Scholar
  101. Messinger J, Robblee JH, Bergmann U, Fernandez C, Glatzel P, Visser H, Cinco RM, McFarlane KL, Bellacchio E., Pizarro SA, Cramer SP, Sauer K, Klein MP and Yanchandra VK (2001a) Absence of Mn-Centered oxidation in the S2 → S3 transition: implications for the mechanism of photosynthetic water oxidation. J Am Chem Soc 123: 7804–7820PubMedCrossRefGoogle Scholar
  102. Messinger J, Robblee JH, Bergmann U, Fernandez C, Glatzel P, Isgandarova S, Hanssum B, Renger G, Cramer SP, Sauer K and Yachandra VK (2001b) Manganese oxidation states in Photosystem II. In: Proceedings of the 12th International Congress on Photosynthesis, Brisbane, Australia, S10-019. CSIRO Publishing, Collingwood, Australia ( Scholar
  103. Metz JG, Nixon PJ, Rögner M, Brudvig GW and Diner BA (1989) Directed alteration of the D1 polypeptide of Photosystem II: evidence that tyrosine-161 is the redox component, Z, connecting the oxygen-evolving complex to the primary electron doner, P680. Biochemistry 28: 6960–6969PubMedCrossRefGoogle Scholar
  104. Michel H and Deisenhofer J (1988) Relevance of the photosynthetic reaction center from purple bacteria to the structure of Photosystem II. Biochemistry 27: 1–7CrossRefGoogle Scholar
  105. Nanba O and Satoh K (1987) Isolation of a Photosystem II reaction center consisting of D-1 and D-2 polypeptides and cytochrome b-559. Proc Natl Acad Sci USA 84: 109–112PubMedCrossRefGoogle Scholar
  106. Nield J, Orlova EV, Morris EP, Gowen B, van Heel M and Barber J (2000) 3-D map of the plant Photosystem II supercomplex obtained by cryoelectron microscopy and single particle analysis. Nature Struct Biol 7: 44–47PubMedCrossRefGoogle Scholar
  107. Nuijs AM, van Gorkom HJ, Plijter JJ and Duysens LNM (1986) Primary-charge separation and excitation of chlorophyll a in Photosystem II particles from spinach as studied by picosecond absorbance-difference spectroscopy. Biochim Biophys Acta 848: 167–175CrossRefGoogle Scholar
  108. Ogawa T (2003) Physical separation of chlorophyll-protein complexes. Photosynth Res 76: 227–232PubMedCrossRefGoogle Scholar
  109. Ogawa T, Obata F and Shibata K (1966) Two pigment proteins in spinach chloroplasts. Biochim Biophys Acta 112: 223–234PubMedGoogle Scholar
  110. Ono T (2001) Metallo-radical hypothesis for photoassembly of (Mn)4-cluster of photosynthetic oxygen evolving complex. Biochim Biophys Acta 1503: 40–51PubMedCrossRefGoogle Scholar
  111. Peloquin JM and Britt RD (2001) EPR/ENDOR characterization of the physical and electronic structure of the OEC Mn cluster. Biochim Biophys Acta 1503: 96–111PubMedCrossRefGoogle Scholar
  112. Pfister K, Steinback KE, Gardner G and Arntzen CJ (1981) Photoaffinity labelling on a herbicide receptor protein in chloroplast membranes. Proc Natl Acad Sci USA 78: 981–985PubMedCrossRefGoogle Scholar
  113. Pirson A (1937) Ernährungs-und stoffwechselphysiologische Untersuchungen an Fontinalis chlorella. Z Bot 31: 193–267 [in German]Google Scholar
  114. Pirson A (1994) 60 years in algal physiology and photosynthesis. Photosynth Res 40: 209–221CrossRefGoogle Scholar
  115. Prokhorenko VI and Holzwarth AR (2000) Primary processes and structure of the Photosystem II reaction center: a photon echo study. J Phys Chem B 104: 11563–11578CrossRefGoogle Scholar
  116. Rabinowitch E and Govindjee (1965) The role of chlorophyll in photosynthesis. Sci Am 213: 74–83PubMedCrossRefGoogle Scholar
  117. Radmer R and Cheniae GM (1977) Mechanism of O2 evolution. In: Barber J (ed) Primary Processes of Photosynthesis, Vol 2, pp 303–348. Elsevier, AmsterdamGoogle Scholar
  118. Radmer R and Ollinger O (1986) Do the higher oxidation states of the photosynthetic O2-evolving system contain bound H2O? FEBS Lett 195: 285–289PubMedCrossRefGoogle Scholar
  119. Razeghifard MR and Pace RJ (1997) Electron paramagnetic resonance kinetic studies of the S states in spinach PS II membranes. Biochim Biophys Acta 1322: 141–150CrossRefGoogle Scholar
  120. Reed DW and Clayton RK (1968) Isolation of a reaction center fraction from Rhodopseudomonas spheroides. Biochem Biophys Res Commun 30: 471–475PubMedCrossRefGoogle Scholar
  121. Renger G (1969a) Untersuchungen über das System der Wasserspaltung in der Photosynthese. PhD Thesis, Technical University, BerlinGoogle Scholar
  122. Renger G (1969b) Reaction of CCCP in photosynthesis on an intermediate between chlorophyll aII and water. Naturwissenschaften 56: 370PubMedCrossRefGoogle Scholar
  123. Renger G (1972) The action of 2-anilinothiophenes as accelerators of the deactivation reactions in the water splitting enzyme system of photosynthesis. Biochim Biophys Acta 256: 428–439PubMedCrossRefGoogle Scholar
  124. Renger G (1976) Studies on the structural and functional organization of system II of photosynthesis. The use of trypsin as a structurally selective inhibitor at the outer surface of the thylakoid membrane. Biochim Biophys Acta 440: 287–300PubMedCrossRefGoogle Scholar
  125. Renger G (1979) A rapid vectorial back reaction at the reaction centers of Photosystem II in tris-washed chloroplasts induced by repetitive flash excitation. Biochim Biophys Acta 547: 103–116PubMedCrossRefGoogle Scholar
  126. Renger G (1987a) Mechanistic aspects of photosynthetic water cleavage. Photosynthetica 21: 203–224Google Scholar
  127. Renger G (1987b) Biological exploitation of solar energy by photosynthetic water cleavage. Angew Chem (Int Ed English) 26: 643–660CrossRefGoogle Scholar
  128. Renger G (1993) Water cleavage by solar radiation — an inspiring challenge of photosynthesis research. Photosynth Res 38: 229–247CrossRefGoogle Scholar
  129. Renger G (1999) Molecular mechanism of water oxidation. In: Singhal GS, Renger G, Govindjee, Irrgang KD, Sopory SK (eds) Concepts in Photobiology: Photosynthesis and Photomorphogenesis, pp 292–329. Kluwer Academic Publishers, Dordrecht, The Netherlands/Narosa Publishing, New Delhi, IndiaGoogle Scholar
  130. Renger G (2001a) Photosynthetic water oxidation to molecular oxygen: apparatus and mechanism. Biochim Biophys Acta 1503: 210–228PubMedCrossRefGoogle Scholar
  131. Renger G (2001b) Coupling of electron and proton movement in photosynthetic water oxidation. In: Proceedings of the 12th International Congress on Photosynthesis, Brisbane, Australia, S10-005, CSIRO Publishing, Collingwood, Australia ( Scholar
  132. Renger G and Govindjee (1985) The mechanism of photosynthetic water oxidation. Photosynth Res 6: 33–55CrossRefGoogle Scholar
  133. Renger G and Govindjee (eds) (1993) How plants and cyanobacteria make oxygen: 25 years of period four oscillations. Photosynth Res 38(3) (special issue): 211–469Google Scholar
  134. Renger G and Hanssum B (1992) Studies on the reaction coordinates of the water oxidase in PS II membrane fragments from spinach. FEBS Lett 299: 28–32PubMedCrossRefGoogle Scholar
  135. Renger G and Völker M (1982) Studies on the proton release of the donor side of system II. Correlation between oxidation and deprotonization of donor D1 in Tris-washed inside-out thylakoids. FEBS Lett 149: 203–207CrossRefGoogle Scholar
  136. Renger G and Weiss W (1982) The detection of intrinsic 320 nm absorption changes reflecting the turnover of the water splitting enzyme system Y, which leads to oxygen formation in trypsinized chloroplats. FEBS Lett 137: 217–221CrossRefGoogle Scholar
  137. Renger G and Weiss W (1983) Spectral characterization in the ultraviolet region of the precursor of photosynthetically evolved oxygen in isolated trypsinized chloroplasts. Biochim Biophys Acta 722: 1–11CrossRefGoogle Scholar
  138. Renger G and Weiss W (1986) Functional and structural aspects of photosynthetic water oxidation. Biochem Soc Trans 14: 17–20PubMedGoogle Scholar
  139. Renger G and Wolff Ch (1976) The existence of a high photochemical turnover rate at the reaction centers of system II in Tris-washed chloroplasts. Biochim Biophys Acta 423: 610–614PubMedCrossRefGoogle Scholar
  140. Renger G, Bouges-Bocquet G and Delosme R (1973) Studies on the ADRY-agent induced mechanism of the discharge of the holes trapped in the photosynthetic water splitting enzyme system. Biochim Biophys Acta 292: 796–807PubMedCrossRefGoogle Scholar
  141. Renger G, Eckert HJ and Weiss W (1983) The oxygen evolving system in photosynthesis. In: Inoue Y, Crofts AR, Govindjee, Murata N, Renger G and Satoh K (eds) Studies on the Mechanism of Photosynthetic Oxygen Formation, pp 73–82. Academic Press Japan, TokyoGoogle Scholar
  142. Renger G, Völker M and Weiss W (1984) Studies on the nature of the water oxidizing enzyme. I. The effect of trypsin on the system II reaction pattern in inside-out thylakoids. Biochim Biophys Acta 766: 582–591CrossRefGoogle Scholar
  143. Renger G, Eckert HJ and Völker M (1989) Studies on the electron transfer from Tyr-161 of polypeptide D-1 to P680+ in PS II membrane fragments from spinach. Photosynth Res 22: 247–256CrossRefGoogle Scholar
  144. Renger G, Bittner T and Messinger J (1994) Structure-function relationship in photosynthetic water oxidation. Biochem Soc Trans 22: 318–322PubMedGoogle Scholar
  145. Renger G, Eckert HJ, Bergmann A, Bernarding J, Liu B, Napiwotzki A, Reifarth F, and Eichler JH (1995) Fluorescence and spectroscopic studies on exciton trapping and electron transfer in Photosystem II of higher plants. Aust J Plant Physiol 22: 167–181CrossRefGoogle Scholar
  146. Renger G, Christen G, Karge M, Eckert HJ and Irrgang KD (1998) Application of the Marcus theory for analysis of the temperature dependence of the reactions leading to photosynthetic water oxidation — results and implications. J Bioinorg Chem 3: 360–366Google Scholar
  147. Rhee KH, Morris EP, Barber J and Kühlbrandt W (1998) Three-dimensional structure of the plant Photosystem II reaction centre at 8 Å resolution. Nature 396: 283–286PubMedCrossRefGoogle Scholar
  148. Robblee JH, Cinco RM and Yachandra VK (2001) The tetramanganese complex of Photosystem II during its redox cycle — X-ray absorption results and mechanistic implications. Biochim Biophys Acta 1503: 7–23PubMedCrossRefGoogle Scholar
  149. Rochaix JD, Dron M, Rahire M and Maloe P (1984) Sequence homology between the 32K dalton and the D2 chloroplast membrane polypeptides of Chlamydomonas reinhardtii. Plant Mol Biol 3: 363–370CrossRefGoogle Scholar
  150. Satoh K (2003) The identification of the Photosystem II reaction center: a personal story. Photosynth Res 76: 233–240PubMedCrossRefGoogle Scholar
  151. Schilstra MJ, Rappaport F, Nugent JHA, Barnett CJ and Klug DR (1998) Proton/hydrogen transfer affects the S-state-dependent microsecond phases of P680+ reduction during water splitting. Biochemistry 37: 3974–3981PubMedCrossRefGoogle Scholar
  152. Schröder H, Siggel U and Rumberg B (1975) The stoichiometry on non-cyclic photophosphorylation, In: Avron M (ed) Proceeding of the 3rd International Congress on Photosynthesis, Rehovot/Israel, pp 1031–1039. Elsevier Scientific Publishing, AmsterdamGoogle Scholar
  153. Siggel U, Renger G, Stiehl HH and Rumberg B (1972a) Evidence for electronic and ionic interaction between electron transport chains in chloroplasts. Biochim Biophys Acta 256: 328–335PubMedCrossRefGoogle Scholar
  154. Siggel U, Renger G and Rumberg B (1972b) Different types of cooperation between electron transport chains in chloroplasts, In: Forti G, Avron M and Melandri A (eds) Proceedings of the International Congress on Photosynthesis Research, Stresa 1971 Vol 1, pp 753–762. Dr W Junk, The HagueGoogle Scholar
  155. Singer SJ and Nicolson GL (1972) The fluid mosaic model of the structure of cell membranes. Science 175: 720–731PubMedGoogle Scholar
  156. Spector M and Winget GD (1980) Purification of a manganese-containing protein involved in photosynthetic oxygen evolution and its use in reconstituting an active membrane. Proc Natl Acad Sci USA 77: 957–959PubMedCrossRefGoogle Scholar
  157. Staehelin LA (2003) Chloroplast structure: from chlorophyll granules to supra-molecular architecture of thylakoid membranes. Photosynth Res 76: 185–196PubMedCrossRefGoogle Scholar
  158. Stemler A (2002) The bicarbonate effect, oxygen evolution and the shadow of Otto Warburg. Photosynth Res 73: 177–183PubMedCrossRefGoogle Scholar
  159. Stiehl HH and Witt HT (1969) Quantitative treatment of the function of plastoquinone in photosynthesis. Z Naturforsch 24b: 1588–1598Google Scholar
  160. Strasser RJ and Sironval C (1972) Induction of Photosystem II activity in flashed leaves. FEBS Lett 28: 56–60CrossRefGoogle Scholar
  161. Tamura N and Cheniae G (1987) Photoactivation of the water-oxidizing complex in Photosystem II membranes depleted of Mn and extrinsic proteins. Biochim Biophys Acta 890: 179–197CrossRefGoogle Scholar
  162. Tamura N, Inoue Y and Cheniae G (1989) Photoactivation of the water-oxidizing complex in Photosystem II membranes depleted of Mn, Ca and extrinsic proteins. II. Studies on the functions of Ca2+. Biochim Biophys Acta 976: 173–181Google Scholar
  163. Tommos C and Babcock GT (1998) Oxygen production in nature: a light-driven metalloradical enzyme process. Acc Chem Res 31: 18–25CrossRefGoogle Scholar
  164. Trebst A and Depka B (1985) The architecture of Photosystem II in plant photosynthesis. Which peptide subunits carry the reaction center of PS II? In: Michel-Beyerle ME (ed) Antennas and Reaction Centers in Photosynthetic Bacteria, pp 216–224. Springer-Verlag, BerlinGoogle Scholar
  165. van Best JA and Mathis P (1978) Kinetics of reduction of the oxidized primary electron donor of Photosystem II in spinach chloroplasts and in chlorella cells in the microsecond and nano-second time ranges following flash excitation. Biochim Biophys Acta 503: 178–188PubMedCrossRefGoogle Scholar
  166. van Leeuwen PJ, Heimann C and van Gorkom HJ (1993) Absorbance difference spectra of the S-state transitions in Photosystem II core particles. Photosynth Res 38: 323–330CrossRefGoogle Scholar
  167. van Rensen JJS (2002) Role of bicarbonate at the acceptor side of Photosystem II. Photosynth Res 73: 185–192PubMedCrossRefGoogle Scholar
  168. Vater J, Renger G, Stiehl HH and Witt HT (1969) Intermediates and kinetics in the water splitting part of photosynthesis, In: Metzner H (ed) Progress in Photosynthesis Research, Vol II, pp 1006–1008. H. Laupp Jr, Tübingen, GermanyGoogle Scholar
  169. Velthuys BR (1981) Spectrophotometric studies on the S-state transitions of Photosystem II and of the interactions of its charged donor chain with lipid soluble anions. In: Akoyunoglou G (ed) Proceedings of the 5th International Congress on Photosynthesis, Vol 2, pp 75–85. Balaban International Science Services, PhiladelphiaGoogle Scholar
  170. Velthuys BR and Amesz J (1974) Charge accumulation at the reducing side of system 2 of photosynthesis. Biochim Biophys Acta 325: 138–148Google Scholar
  171. Vermaas WFJ, Rutherford AW and Hansson Ö (1988) Site directed mutagenesis in Photosystem II of the cyanobacterium Synechocystis sp. PCC 6803: donor D is a tyrosine resdue in the D2 protein. Proc Natl Acad Sci USA 85: 8477–8481CrossRefGoogle Scholar
  172. Vernon LP (2003) Photosynthesis and the Charles F. Kettering Research Laboratory. Photosynth Res 76: 379–388PubMedCrossRefGoogle Scholar
  173. Völker M, Eckert HJ and Renger G (1987) Effects of trypsin and bivalent cations on P 680+-reduction, fluorescence induction and oxygen evolution in PS II-membrane fragments from spinach. Biochim Biophys Acta 890: 66–77CrossRefGoogle Scholar
  174. Warburg O and Lüttgens W (1944) Weitere Experimente zur Kohlensäureassimilation. Naturwissenschaften 32: 301 [in German]CrossRefGoogle Scholar
  175. Warden JT, Blankenship RE and Sauer K (1976) A flash photolysis ESR study of Photosystem II signal IIvf, the physiological donor to P-680+. Biochim Biophys Acta 423: 462–478PubMedCrossRefGoogle Scholar
  176. Weaver EC and Bishop NI (1963) Photosynthetic mutants separate electron paramagnetic resonance signals of scenedesmus. Science 140: 1095–1097PubMedGoogle Scholar
  177. Weiss W and Renger G (1986) On the functional connection between the reaction center complex and the water oxidizing enzyme system Y. Biochim Biophys Acta 850: 173–183CrossRefGoogle Scholar
  178. Whittingham CP and Brown AH (1958) Oxygen evolution from algae illuminated by short and long flashes of light. J Exp Bot 9: 311–319Google Scholar
  179. Williams JC, Steiner LA, Ogden RC, Simon MI and Feher G (1983) Primary structure of the M subunit of the reaction center from Rhodopseudomonas sphaeroides. Proc Natl Acad Sci USA 80: 6505–6509PubMedCrossRefGoogle Scholar
  180. Williams JC, Steiner LA, Feher G and Simon MI (1984) Primary structure of the L subunit of the reaction center from Rhodopseudomonas sphaeroides. Proc Natl Acad Sci USA 81: 7303–7307PubMedCrossRefGoogle Scholar
  181. Witt HT (1975) Bioenergetics of photosynthesis. In: Govindjee (ed) Primary Acts on Energy Conservation in the Functional Membrane of Photosynthesis, pp 493–554. Academic Press, New YorkGoogle Scholar
  182. Witt HT (1991) Functional mechanism of water splitting photosynthesis. Photosynth Res 29: 55–77CrossRefGoogle Scholar
  183. Yamashita and Butler (1968) Photoreduction and photophosphorylation with tris-washed chloroplasts. Plant Physiol 43: 1978–1986PubMedCrossRefGoogle Scholar
  184. Yocum C, Ferguson, Miller S and Blankenship R (2001) Gerald T. Babcock (1946–2000) obituary. Photosynth Res 68: 89–94PubMedCrossRefGoogle Scholar
  185. Zech SG, Kurreck J, Eckert HJ, Renger G, Lubitz W and Bittl R (1997) Pulsed EPR measurement of the distance between P680 and QA−· in Photosystem II. FEBS Lett 414: 454–456PubMedCrossRefGoogle Scholar
  186. Zech SG, Kurreck J, Renger G, Lubitz W and Bittl R (1999) Determination of the distance between YZOC and QZ−· in Photosystem II by pulsed EPR spectroscopy on light-induced radical pairs. FEBS Lett 442: 79–82PubMedCrossRefGoogle Scholar
  187. 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 Å resolution. Nature 409: 739–743PubMedCrossRefGoogle Scholar
  188. Zurawski G, Bohnert HJ, Whitfeld PR and Botomley W (1982) Nucleotide sequence of the gene for the Mr. 32000 thylakoid membrane protein from Spinacea oleracea and Nicotiana debneyi predicts a totally conserved translation product of Mr. 38950. Proc Natl Acad Sci USA 79: 7699–7703PubMedCrossRefGoogle Scholar

Copyright information

© Springer 2005

Authors and Affiliations

  • Gernot Renger
    • 1
  1. 1.Fakultät II, Institut für Chemie, Max-Volmer-Laboratorium für Biophysikalische ChemieTechnische Universität BerlinBerlinGermany

Personalised recommendations