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Apparatus and mechanism of photosynthetic oxygen evolution: a personal perspective*

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Abstract

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.

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References

  • Adir N, Zer H, Shochat S and Ohad I (2003) Photoinhibition - a historical perspective Photosynth Res 76: 343–370 (this issue)

    CAS  Google Scholar 

  • Allen FA and Franck J (1955) Photosynthetic evolution of oxygen by flashes of light. Arch Biochem Biophys 58: 124–143

    PubMed  CAS  Google Scholar 

  • Ananyev GM, Zaltsman L, Vasko C and Dismukes GC (2001) The inorganic biochemistry of photosynthetic oxygen evolution/ water oxidation. Biochim Biophys Acta 1503: 52–68

    PubMed  CAS  Google Scholar 

  • Anderson JM (2001) Does functional Photosystem II complex have an oxygen channel? FEBS Lett 488: 1–4

    PubMed  CAS  Google Scholar 

  • Anderson JM (2002) Changing concepts about the distribution of Photosystems I and II between grana-appressed and stromaexposed thylakoid membranes. Photosynth Res 73: 157–164

    PubMed  CAS  Google Scholar 

  • 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: 403–412

    CAS  Google Scholar 

  • 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: 506–516

    CAS  Google Scholar 

  • 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 Netherlands

    Google Scholar 

  • Babcock GT and Sauer K (1973) Electron paramagnetic resonance signal II in spinach chloroplasts. I. Kinetic analysis for untreated chloroplasts. Biochim Biophys Acta 325: 483–503

    PubMed  CAS  Google Scholar 

  • 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: 315–328

    PubMed  CAS  Google Scholar 

  • 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: 329–344

    PubMed  CAS  Google Scholar 

  • 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: 286–289

    PubMed  CAS  Google Scholar 

  • 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: 9557–9565

    PubMed  CAS  Google Scholar 

  • Bader KP, Renger G and Schmid GH (1993) A mass spectroscopic analysis of the water-splitting reaction. Photosynth Res 38: 355–361

    CAS  Google Scholar 

  • Barry B and Babcock GT (1987) Tyrosine radicals are involved in the photosynthetic oxygen-evolving system. Proc Natl Acad Sci USA 84: 7099–7103

    PubMed  CAS  Google Scholar 

  • 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: 231–234

    CAS  Google Scholar 

  • 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: 566–573

    CAS  Google Scholar 

  • 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: 287–293

    PubMed  CAS  Google Scholar 

  • Bogorad L (2003) Photosynthesis research: advances through molecular biology - the beginnings, 1975-1980s and on.... Photosynth Res 76: 13–33 (this issue)

    PubMed  Google Scholar 

  • 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: 327–330

    CAS  Google Scholar 

  • Bouges-Bocquet B (1973) Electron transfer between the two photosystems in spinach chloroplasts. Biochim Biophys Acta 314: 250–256

    PubMed  CAS  Google Scholar 

  • Bouges-Bocquet B (1980) Kinetic models for the electron donors of Photosystem II of photosynthesis. Biochim Biophys Acta 594: 85–103

    PubMed  CAS  Google Scholar 

  • 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: 403–415

    CAS  Google Scholar 

  • Britt RD, Sauer K and Yachandra VK (2001) Remembering Melvin P. Klein (1921-2000). Biochim Biophys Acta 1503: 2–6

    PubMed  CAS  Google Scholar 

  • 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 

  • 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: 421–428

    CAS  Google Scholar 

  • Cheniae GM and Martin IF (1969) Photoreactivation of manganese catalyst in photosynthetic oxygen evolution. Plant Physiol 44: 351–360

    PubMed  CAS  Google Scholar 

  • 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: 219–239

    PubMed  CAS  Google Scholar 

  • Christen G and Renger G (1999) The role of hydrogen bonds for the multiphasic P +680 reduction by YZ in Photosystem II with intact oxygen evolution capacity. Analysis of kinetic H/D isotope exchange effects. Biochemistry 38: 2068–2077

    PubMed  CAS  Google Scholar 

  • Christen G, Reifarth F and Renger G (1998) On the origin of the ‘35 µs kinetics' of P +680 reduction in Photosystem II with an intact water oxidising complex. FEBS Lett 429: 49–52

    PubMed  CAS  Google Scholar 

  • Christen G, Seeliger A and Renger G (1999) P +680 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: 6082–6092

    PubMed  CAS  Google Scholar 

  • Clark LC Jr, World R, Granger D and Taylor Z (1953) Continuous recording of blood oxygen tensions by polarography. J Appl Physiol 6: 189–193

    PubMed  CAS  Google Scholar 

  • Clayton RK (2002) Research on photosynthetic reaction centers from 1932-1987. Photosynth Res 73: 63–71

    PubMed  CAS  Google Scholar 

  • Cogdell R (1996) Philip Thornber (1934-1996). Photosynth Res 50: 1–3

    CAS  Google Scholar 

  • Commoner B, Heise JJ and Townsend J (1956) Light-induced paramagnetism in chloroplasts. Proc Natl Acad Sci USA 42: 710–718

    PubMed  CAS  Google Scholar 

  • 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: 353–359

    PubMed  CAS  Google Scholar 

  • 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: 280–291

    PubMed  CAS  Google Scholar 

  • Debus RJ (1992) The manganese and calcium ions in photosynthetic O2 evolution. Biochim Biophys Acta 1102: 269–352

    PubMed  CAS  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

    PubMed  CAS  Google Scholar 

  • 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: 9071–9074

    PubMed  CAS  Google Scholar 

  • Debus RJ, Barry BA, Babcock GT and McIntosh L (1988b) Sitedirected mutagenesis identifies a tyrosine radical involved in the photosynthetic oxygen-evolving system. Proc Natl Acad Sci USA 85: 427–430

    PubMed  CAS  Google Scholar 

  • Deisenhofer J, Epp O, Miki K, Huber R and Michel H (1984) XRay 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: 385–398

    PubMed  CAS  Google Scholar 

  • 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: 1–9

    CAS  Google Scholar 

  • 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/Lancaster

    Google Scholar 

  • 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: 147–163

    PubMed  CAS  Google Scholar 

  • 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: 9265–9281

    PubMed  CAS  Google Scholar 

  • Dismukes GC and Siderer Y (1981) Intermediates of a polynuclear manganese center involved in photosynthetic oxidation of water. Proc Natl Acad Sci USA 78: 274–278

    PubMed  CAS  Google Scholar 

  • Döring G, Renger G, Vater J and Witt HT (1969) Properties of the photoactive chlorophyll-a in photosynthesis. Z Naturforsch 24 b: 1139–1143

    Google Scholar 

  • Dorlet P, DiValentin M, Babcock GT and McCracken JL (1998) Interaction of Y·Z with its environment in acetate-treated Photosystem II membranes and reaction center cores. J Phys Chem B 102: 8239–8247

    CAS  Google Scholar 

  • 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: 425–431

    CAS  Google Scholar 

  • Eckert HJ, Renger G and Witt HT (1984) Reduction kinetics of the photooxidized chlorophyll-aII in the ns-range. FEBS Lett 167: 316–320

    CAS  Google Scholar 

  • Eckert HJ, Wiese N, Bernarding J, Eichler HJ and Renger G (1988) Analysis of the electron transfer from Pheo- to QA in PS II membrane fragments from spinach by time-resolved 325 nm absorption changes in the picosecond domain. FEBS Lett 240: 153–158

    PubMed  CAS  Google Scholar 

  • 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: 15–28

    CAS  Google Scholar 

  • Frasch WD and Sayre RT (2002) Remembering George Cheniae, who never compromised his high standards of science. Photosynth Res 70: 245–247

    Google Scholar 

  • 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: 69–75

    CAS  Google Scholar 

  • 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, Tokyo

    Google Scholar 

  • 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: 191–199

    CAS  Google Scholar 

  • 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: 712–721

    Google Scholar 

  • 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: 12063–12071

    PubMed  CAS  Google Scholar 

  • Gleiter HM, Haag E, Shen JR, Eaton-Rye JJ, Seeliger AG, Inoue Y, Vermaas WFJ and Renger G (1995) Involvement of the CP47protein in stabilization and photoactivation of a functional water oxidizing complex in the cyanobacterium Synechocystis sp. PCC 6803. Biochemistry 34: 15721–15731

    Google Scholar 

  • Govindjee (2000) Milestones in photosynthesis research. In: Yunus M, Pathre U and Mohanty P (eds) Probing Photosynthesis, pp 9–39. Taylor & Francis, New York

    Google Scholar 

  • 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: 2251–2255

    CAS  Google Scholar 

  • 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: 47–53

    PubMed  CAS  Google Scholar 

  • 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: 4444–4454

    PubMed  CAS  Google Scholar 

  • Hales BJ and Gupta AD (1981) Supposition of the origin of signal II from random and orientated chloroplasts. Biochim Biophys Acta 637: 303–311

    CAS  Google Scholar 

  • 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: 346–355

    PubMed  Google Scholar 

  • 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: 11852–11865

    Google Scholar 

  • 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: 197–209

    Google Scholar 

  • Hoganson CW and Babcock GT (1997) A metalloradical mechanism for the generation of oxygen from water in photosynthesis. Science 277: 1953–1956

    PubMed  CAS  Google Scholar 

  • Homann PH (2002) Chloride and calcium in Photosystem II: from effects to enigma. Photosynth Res 73: 169–175

    PubMed  CAS  Google Scholar 

  • 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: 316–322

    CAS  Google Scholar 

  • Irrgang KD, Renger G and Vater J (1986) Identification of Chlbinding proteins in a PS II preparation from spinach. FEBS Lett 204: 67–75

    CAS  Google Scholar 

  • Joliot P (1965) Cinétiques de réactions liées à l'émission d'oxygène photosynthétique (in French). Biochim Biophys Acta 102, 116–134

    PubMed  CAS  Google Scholar 

  • Joliot P (2003) Period-four oscillations of the flash-induced oxygen formation in photosynthesis. Photosynth Res 76: 65–72 (this issue)

    PubMed  CAS  Google Scholar 

  • Joliot P and Kok B (1975) Oxygen evolution in photosynthesis. In: Govindjee (ed) Bioenergetics of Photosynthesis, pp 387–412. Academic Press, New York

    Google Scholar 

  • 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: 1423–1441

    Google Scholar 

  • Joliot P, Barbieri G and Chabaud R (1969) Un nouveau modèle des centres photochimiques du système II. Photochem Photobiol 10: 309–329

    CAS  Google Scholar 

  • Junge W (1975) Physical aspects of the electron transport and photophosphorylation in green plants. Ber Deutsch Bot Ges 88: 283–301

    CAS  Google Scholar 

  • 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: 140–144

    PubMed  CAS  Google Scholar 

  • 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: 8904–8913

    PubMed  CAS  Google Scholar 

  • 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: 209–216

    PubMed  CAS  Google Scholar 

  • Kessler E (1957) Stoffwechselphysiologische Untersuchungen an Hydrogenase enthaltenden Grünalgen. I. Ñber die Rolle des Mangans bei Photoreduktion und Photosynthese (in German). Planta 49: 435–454

    CAS  Google Scholar 

  • Klimov VV (2003) Discovery of pheophytin function in the photosynthetic energy conversion as the primary electron acceptor of Photosystem II. Photosynth Res 76: 247–253 (this issue)

    PubMed  CAS  Google Scholar 

  • Klimov VV, Klevanik AV, Shuvalov VA and Krasnovsky AA (1977) Reduction of pheophytin in the primary light reaction of Photosystem II. FEBS Lett 82: 183–186

    PubMed  CAS  Google Scholar 

  • 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: 536–544

    PubMed  CAS  Google Scholar 

  • 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: 524–533

    CAS  Google Scholar 

  • Kok B, Forbush B and McGloin M(1970) Cooperation of charges in photosynthetic O2 evolution - I. A linear four step mechanism. Photochem Photobiol 11: 457–475

    PubMed  CAS  Google Scholar 

  • Kouchkovsky Y (2002) The laboratory of photosynthesis and its successors at Gif-sur-Yvette, France. Photosynth Res 73: 295–303

    PubMed  Google Scholar 

  • Krasnovsky AA (1992) Excited chlorophyll and related problems. Photosynth Res 33: 177–193

    Google Scholar 

  • 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. publish.csiro.au/ps2001)

    Google Scholar 

  • 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: 12758–12767

    PubMed  CAS  Google Scholar 

  • Lavergne J (1991) Improved UV visible spectra of the S-transitions in the photosynthetic oxygen evolving system. Biochim Biophys Acta 1060: 175–188

    CAS  Google Scholar 

  • Lavergne J and Junge W (1993) Proton release during the redox cycle of the water oxidase. Photosynth Res 38: 269–276

    Google Scholar 

  • 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: 1233–1235

    PubMed  CAS  Google Scholar 

  • 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: 1572–1576

    Google Scholar 

  • Menke W (1940) Untersuchungen über den Feinbau des Protoplasmas mit dem Universal-Elektronenmikroskop. Protoplasma 35: 115-130 [in German] Menke W (1990) Retrospective of a botanist. Photosynth Res 25: 77–82

    Google Scholar 

  • Messinger J and Renger G (1993) Generation, oxidation by Y OXD and possible electronic configuration of the redox states S0, S-1and S-2 of the water oxidase in isolated spinach thylakoids. Biochemistry 32: 9379–9386

    PubMed  CAS  Google Scholar 

  • 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: 3209–3213

    PubMed  CAS  Google Scholar 

  • Messinger J, Seaton GR, Wydrzynski T, Wacker U and Renger G (1997) S-3 state of the water oxidase in Photosystem II. Biochemistry 36: 6862–6873

    PubMed  CAS  Google Scholar 

  • 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: 7804–7820

    PubMed  CAS  Google Scholar 

  • 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 (www.publish.csiro.au/ps2001)

    Google Scholar 

  • 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: 6960–6969

    PubMed  CAS  Google Scholar 

  • Michel H and Deisenhofer J (1988) Relevance of the photosynthetic reaction center from purple bacteria to the structure of Photosystem II. Biochemistry 27: 1–7

    CAS  Google Scholar 

  • 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: 109–112

    PubMed  CAS  Google Scholar 

  • 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: 44–47

    PubMed  CAS  Google Scholar 

  • 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: 167–175

    CAS  Google Scholar 

  • Ogawa T (2003) Physical separation of chlorophyll-protein complexes. Photosynth Res 76: 227–232 (this issue)

    PubMed  CAS  Google Scholar 

  • Ogawa T, Obata F and Shibata K (1966) Two pigment proteins in spinach chloroplasts. Biochim Biophys Acta 112: 223–234

    PubMed  CAS  Google Scholar 

  • Ono T (2001) Metallo-radical hypothesis for photoassembly of (Mn)4-cluster of photosynthetic oxygen evolving complex. Biochim Biophys Acta 1503: 40–51

    PubMed  CAS  Google Scholar 

  • Peloquin JM and Britt RD (2001) EPR/ENDOR characterization of the physical and electronic structure of the OEC Mn cluster. Biochim Biophys Acta 1503: 96–111

    PubMed  CAS  Google Scholar 

  • 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: 981–985

    PubMed  CAS  Google Scholar 

  • Pirson A (1937) Ernährungs-und stoffwechselphysiologische Untersuchungen an Fontinalis chlorella. Z Bot 31: 193–267 [in German]

    CAS  Google Scholar 

  • Pirson A (1994) 60 years in algal physiology and photosynthesis. Photosynth Res 40: 209–221

    Google Scholar 

  • 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: 11563–11578

    CAS  Google Scholar 

  • Rabinowitch E and Govindjee (1965) The role of chlorophyll in photosynthesis. Sci Am 213: 74–83

    PubMed  CAS  Google Scholar 

  • Radmer R and Cheniae GM (1977) Mechanism of O2 evolution. In: Barber J (ed) Primary Processes of Photosynthesis, Vol 2, pp 303–348. Elsevier, Amsterdam

    Google Scholar 

  • Radmer R and Ollinger O (1986) Do the higher oxidation states of the photosynthetic O2-evolving system contain bound H2 O? FEBS Lett 195: 285–289

    PubMed  CAS  Google Scholar 

  • Razeghifard MR and Pace RJ (1997) Electron paramagnetic resonance kinetic studies of the S states in spinach PS II membranes. Biochim Biophys Acta 1322: 141–150

    Google Scholar 

  • Reed DW and Clayton RK (1968) Isolation of a reaction center fraction from Rhodopseudomonas spheroides. Biochem Biophys Res Commun 30: 471–475

    PubMed  CAS  Google Scholar 

  • Renger G (1969a) Untersuchungen über das System der Wasserspaltung in der Photosynthese. PhD Thesis, Technical University, Berlin

    Google Scholar 

  • Renger G (1969b) Reaction of CCCP in photosynthesis on an intermediate between chlorophyll aII and water. Naturwissenschaften 56: 370

    PubMed  CAS  Google Scholar 

  • 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: 428–439

    PubMed  CAS  Google Scholar 

  • 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: 287–300

    PubMed  Google Scholar 

  • 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: 103–116

    PubMed  CAS  Google Scholar 

  • Renger G (1987a) Mechanistic aspects of photosynthetic water cleavage. Photosynthetica 21: 203–224

    CAS  Google Scholar 

  • Renger G (1987b) Biological exploitation of solar energy by photosynthetic water cleavage. Angew Chem (Int Ed English) 26: 643–660

    Google Scholar 

  • Renger G (1993) Water cleavage by solar radiation - an inspiring challenge of photosynthesis research. Photosynth Res 38: 229–247

    CAS  Google Scholar 

  • 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, India

    Google Scholar 

  • Renger G (2001a) Photosynthetic water oxidation to molecular oxygen: apparatus and mechanism. Biochim Biophys Acta 1503: 210–228

    PubMed  CAS  Google Scholar 

  • 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 (www.publish.csiro.au/ps2001)

    Google Scholar 

  • Renger G and Govindjee (1985) The mechanism of photosynthetic water oxidation. Photosynth Res 6: 33–55

    CAS  Google Scholar 

  • Renger G and Govindjee (eds) (1993) How plants and cyanobacteria make oxygen: 25 years of period four oscillations. Photosynth Res 38(3) (special issue): 211–469

  • 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: 28–32

    PubMed  CAS  Google Scholar 

  • 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: 203–207

    CAS  Google Scholar 

  • 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: 217–221

    CAS  Google Scholar 

  • 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: 1–11

    CAS  Google Scholar 

  • Renger G and Weiss W (1986) Functional and structural aspects of photosynthetic water oxidation. Biochem Soc Trans 14: 17–20

    PubMed  CAS  Google Scholar 

  • 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: 610–614

    PubMed  CAS  Google Scholar 

  • 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: 796–807

    PubMed  CAS  Google Scholar 

  • 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, Tokyo

    Google Scholar 

  • 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: 582–591

    CAS  Google Scholar 

  • 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: 247–256

    CAS  Google Scholar 

  • Renger G, Bittner T and Messinger J (1994) Structure-function relationship in photosynthetic water oxidation. Biochem Soc Trans 22: 318–322

    PubMed  CAS  Google Scholar 

  • 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: 167–181

    CAS  Google Scholar 

  • 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: 360–366

    CAS  Google Scholar 

  • Rhee KH, Morris EP, Barber J and Kühlbrandt W (1998) Threedimensional structure of the plant Photosystem II reaction centre atÅ resolution. Nature 396: 283–286

    PubMed  CAS  Google Scholar 

  • 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: 7–23

    PubMed  CAS  Google Scholar 

  • 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: 363–370

    CAS  Google Scholar 

  • Satoh K (2003) The identification of the Photosystem II reaction center: a personal story. Photosynth Res 76: 233–240 (this issue)

    PubMed  CAS  Google Scholar 

  • 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: 3974–3981

    PubMed  CAS  Google Scholar 

  • 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, Amsterdam

    Google Scholar 

  • 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: 328–335

    PubMed  CAS  Google Scholar 

  • 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 Hague

    Google Scholar 

  • Singer SJ and Nicolson GL (1972) The fluid mosaic model of the structure of cell membranes. Science 175: 720–731

    PubMed  CAS  Google Scholar 

  • Spector M and Winget GD (1980) Purification of a manganesecontaining protein involved in photosynthetic oxygen evolution and its use in reconstituting an active membrane. Proc Natl Acad Sci USA 77: 957–959

    PubMed  CAS  Google Scholar 

  • Staehelin LA (2003) Chloroplast structure: from chlorophyll granules to supra-molecular architecture of thylakoid membranes. Photosynth Res 76: 185–196 (this issue)

    PubMed  CAS  Google Scholar 

  • Stemler A (2002) The bicarbonate effect, oxygen evolution and the shadow of Otto Warburg. Photosynth Res 73: 177–183

    PubMed  CAS  Google Scholar 

  • Stiehl HH and Witt HT (1969) Quantitative treatment of the function of plastoquinone in photosynthesis. Z Naturforsch 24b: 1588–1598

    Google Scholar 

  • Strasser RJ and Sironval C (1972) Induction of Photosystem II activity in flashed leaves. FEBS Lett 28: 56–60

    CAS  Google Scholar 

  • Tamura N and Cheniae G (1987) Photoactivation of the wateroxidizing complex in Photosystem II membranes depleted of Mn and extrinsic proteins. Biochim Biophys Acta 890: 179–197

    CAS  Google Scholar 

  • 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: 173–181

    CAS  Google Scholar 

  • Tommos C and Babcock GT (1998) Oxygen production in nature: a light-driven metalloradical enzyme process. Acc Chem Res 31: 18–25

    CAS  Google Scholar 

  • 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, Berlin

    Google Scholar 

  • 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: 178–188

    PubMed  CAS  Google Scholar 

  • 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: 323–330

    CAS  Google Scholar 

  • van Rensen JJS (2002) Role of bicarbonate at the acceptor side of Photosystem II. Photosynth Res 73: 185–192

    PubMed  CAS  Google Scholar 

  • 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, Germany

    Google Scholar 

  • 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, Philadelphia

    Google Scholar 

  • Velthuys BR and Amesz J (1974) Charge accumulation at the reducing side of system 2 of photosynthesis. Biochim Biophys Acta 325: 138–148

    Google Scholar 

  • 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 D2protein. Proc Natl Acad Sci USA 85: 8477–8481

    CAS  Google Scholar 

  • Vernon LP (2003) Photosynthesis and the Charles F. Kettering Research Laboratory. Photosynth Res 76: 379–388 (this issue)

    PubMed  CAS  Google Scholar 

  • 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: 66–77

    Google Scholar 

  • Warburg O and Lüttgens W (1944) Weitere Experimente zur Kohlensäureassimilation. Naturwissenschaften 32: 301 [in German]

    CAS  Google Scholar 

  • 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: 462–478

    PubMed  CAS  Google Scholar 

  • Weaver EC and Bishop NI (1963) Photosynthetic mutants separate electron paramagnetic resonance signals of scenedesmus. Science 140: 1095–1097

    Google Scholar 

  • 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: 173–183

    CAS  Google Scholar 

  • Whittingham CP and Brown AH (1958) Oxygen evolution from algae illuminated by short and long flashes of light. J Exp Bot 9: 311–319

    CAS  Google Scholar 

  • 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: 6505–6509

    PubMed  CAS  Google Scholar 

  • 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: 7303–7307

    PubMed  CAS  Google Scholar 

  • 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 York

    Google Scholar 

  • Witt HT (1991) Functional mechanism of water splitting photosynthesis. Photosynth Res 29: 55–77

    CAS  Google Scholar 

  • Yamashita and Butler (1968) Photoreduction and photophosphorylation with tris-washed chloroplasts. Plant Physiol 43: 1978–1986

    Google Scholar 

  • Yocum C, Ferguson, Miller S and Blankenship R (2001) Gerald T. Babcock (1946-2000) obituary. Photosynth Res 68: 89–94

    PubMed  CAS  Google Scholar 

  • Zech SG, Kurreck J, Eckert HJ, Renger G, Lubitz W and Bittl R (1997) Pulsed EPR measurement of the distance between P 680 and Q ¯·A in Photosystem II. FEBS Lett 414: 454–456

    PubMed  CAS  Google Scholar 

  • Zech SG, Kurreck J, Renger G, Lubitz W and Bittl R (1999) Determination of the distance between Y OCZ and Q ¯·Z in Photosystem II by pulsed EPR spectroscopy on light-induced radical pairs. FEBS Lett 442: 79–82

    PubMed  CAS  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 Å resolution. Nature 409: 739–743

    PubMed  CAS  Google Scholar 

  • 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: 7699–7703

    PubMed  CAS  Google Scholar 

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Renger, G. Apparatus and mechanism of photosynthetic oxygen evolution: a personal perspective* . Photosynthesis Research 76, 269–288 (2003). https://doi.org/10.1023/A:1024907012382

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