Photosystem II: The machinery of photosynthetic water splitting

Photosynthesis Research

Volumn 98, Issue 1-3, 2008, Pages 53-80

  Renger, Gernot ^a   Renger, Thomas ^b  

^a TECHNISCHE UNIVERSITÄT BERLIN   (Germany)

^b FREIE UNIVERSITÄT BERLIN   (Germany)

Author keywords

Charge separation; Mechanisms; Oxidative water splitting; Photosystem II; Reductive plastoquinol formation

Indexed keywords

DRUG DERIVATIVE; OXYGEN; PLASTOQUINOL; PLASTOQUINONE; WATER;

KINETICS; LIGHT; METABOLISM; PHOTOSYNTHESIS; PHOTOSYSTEM II; REVIEW;

KINETICS; LIGHT; OXYGEN; PHOTOSYNTHESIS; PHOTOSYSTEM II PROTEIN COMPLEX; PLASTOQUINONE; WATER;

EID: 57849146011     PISSN: 01668595     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11120-008-9345-7     Document Type: Review

References (219)

1. Aartsma TJ, Matysik J (eds) (2008) Biophysical techniques in photosynthesis, volume II. Advances in photosynthesis and respiration, vol 26. Springer, Dordrecht
2. JM Anderson 2001 Does functional photosystem II complex have an oxygen channel? FEBS Lett 488 1 4
3. EG Andrizhiyevskaya D Frolov R van Grondelle JP Dekker 2004 On the role of the CP47 core antenna in the energy transfer and trapping dynamics of Photosystem II Phys Chem Chem Phys 6 4810 4819
4. AJ Augustine L Quintanar CS Stoj DJ Kosman EI Solomon 2007 Spectroscopic and kinetic studies of perturbed trinuclear copper clusters: The role of protons in reductive cleavage of the O-O bond in the multicopper oxidase Fet3p J Am Chem Soc 129 13118 13126
5. GT Babcock RE Blankenship K Sauer 1976 Reaction kinetics for positive charge accumulation on the water side of chloroplast photosystem II FEBS Lett 61 286 289
6. KP Bader G Renger GH Schmidt 1993 A mass spectroscopic analysis of the water-splitting reaction Photosynth Res 38 355 361
7. LMC Barter M Bianchietti C Jeans MJ Schilstra B Hankamer BA Diner J Barber JR Durrant DR Klug 2001 Relationship between excitation energy transfer, trapping, and antenna size in Photosystem II Biochemistry 40 4026 4034
8. - in different Photosystem II preparations from higher plants Photochem Photobiol 59 566 573
9. TA Betley Q Wu T Van Voorhis DG Nocera 2008 Electronic design criteria for O-O bond formation via metal-oxo complexes Inorg Chem 47 1849 1861
10. MRA Blomberg PEM Siegbahn 2006 Different types of biological proton transfer reactions studied by quantum chemical methods Biochim Biophys Acta 1757 969 980
11. 2+ Biochemistry 27 3476 3483
12. K Broess G Trinkunas CD van der Weide Wit JP Dekker A van Hoek H van Amerongen 2006 Excitation energy transfer and charge separation in Photosystem II membranes visited Biophys J 91 3776 3786
13. K Broess G Trinkunas A van Hoek R Croce H van Amerongen 2008 Determination of the exciton migration time in Photosystem II Consequences for the membrane organization and charge separation parameters Biochim Biophys Acta 1777 404 409
14. R Buick 1992 The antiquity of oxygenic photosynthesis; evidence from stromatolites in sulphate-deficient Archaen lakes Science 255 74 77
15. K Burda KP Bader GH Schmid 2001 An estimation of the size of the water cluster present at the cleavage site of the water splitting enzyme FEBS Lett 491 81 84
16. PA Castelfranco Y-K Lu AJ Stemler 2007 Hypothesis: the peroxydicarbonic acid cycle in photosynthetic oxygen evolution Photosynth Res 94 235 246
17. Chow WS, Aro EM (2005) Photoinactivation and mechanism of recovery. In: Wydrzynski T, Satoh K (eds) Photosystem II: The water/plastoquinone oxido-reductase in photosynthesis, advances in photosynthesis and respiration, vol 22. Springer, Dordrecht, pp 627-648
18. J Clausen W Junge 2004 Detection of an intermediate of photosynthetic water oxidation Nature 430 480 483
19. Clausen J, Debus RJ, Junge W (2004) Time-resolved oxygen production by PS II: chasing chemical intermediates. Biochim Biophys Acta 1655:184-194
20. J Clausen K Beckmann W Junge J Messinger 2005 Evidence that bicarbonate is not the substrate in photosynthetic oxygen evolution Plant Physiol 139 1444 1450
21. B in wild-type and herbicide-resistent mutants of C reinhardtii Z Naturforsch 48c 259 266
22. R Davydov RL Osborne SH Kim JH Dawson BM Hoffman 2008 EPR and ENDOR studies of cryoreduced compounds II of peroxidases and myoglobin. Proton-coupled electron transfer and protonation status of ferryl hemes Biochemistry 47 5147 5155
23. 3 transitions in photosystem II Biochemistry 44 1367 1374
24. JP Dekker EJ Boekema 2005 Supramolecular organization of thylakoid membrane proteins in green plants Biochim Biophys Acta 1706 12 39
25. JP Dekker JJ Plijter L Ouwehand HJ van Gorkom 1984 Kinetics of manganese redox transitions in the oxygen-evolving apparatus of photosynthesis Biochim Biophys Acta 767 176 179
26. DeLano WL (2002) The PyMOL molecular graphics system. DeLano Scientific, Palo Alto, CA, USA. http://www.pymol.org
27. E Derat S Shaik C Rovira P Vidossich MJ Alfonso-Prieto 2007 The effect of a water molecule on the mechanism of formation of compound 0 in horseradish peroxidase Am Chem Soc 129 6346 6347
28. DJ des Marais 2000 Evolution. When did photosynthesis emerge on earth? Science 289 1703 1705
29. R de Wijn HJ van Gorkom 2001 Kinetics of electron transfer from Q(a) to Q(b) in photosystem II Biochemistry 40 11912 11922
30. BA Diner E Schlodder PJ Nixon F Rappaport WJ Coleman J Laverge WFJ Vermaas DA Chisholm 2001 Site-directed mutations at D1-His198 and D2-His197 of photosystem II in Synechosystis PCC 6803: sites of primary charge separation and cation and triplet stabilization Biochemistry 40 9265 9281
31. G Döring HH Stiel HT Witt 1967 A second chlorophyll reaction in the electron chain of photosynthesis-registration by the repetitive excitation technique Z Naturforsch 22 639 644
32. II in photosynthesis Z Naturforsch 24b 1139 1143
33. JR Durrant DR Klug SLS Kwa R van Grondelle G Porter JP Dekker 1995 A multimer model for P680, the primary electron donor of photosystem II Proc Natl Acad Sci USA 92 4798 4802
34. Eaton-Rye JJ, Govindjee (1988a) Electron transfer through the quinone acceptor complex of Photosystem II in bicarbonate-depleted spinach thylakoid membranes as a function of actinic flash number and frequency. Biochim Biophys Acta 935: 237-247
35. JJ Eaton-Rye Govindjee 1988 Electron transfer through the quinone acceptor complex of Photosystem II after one or two actinic flashes in bicarbonate-depleted spinach thylakoid membranes Biochim Biophys Acta 935 248 257
36. K Ferreira TM Iverson K Maghlouni J Barber S Iwata 2004 Architecture of the photosynthetic oxygen-evolving center Science 303 1831 1838
37. A in the T4 mutant of Blastochloris viridis Biochemistry 44 5931 5939
38. C Fufezan CM Gross M Sjödin AW Rutherford A Krieger-Liszkay D Kirilovsky 2007 Influence of the redox potential of the primary quinone electron acceptor on photoinhibition in Photosystem II J Biol Chem 282 12492 12502
39. B in PS II membrane fragments from spinach Biochemistry 37 11399 11404
40. P Glatzel U Bergmann J Yano H Visser JH Robblee WW Gu FMF de Groot G Christou VL Pecoraro SP Cramer VK Yachandra 2004 The electronic structure of Mn in oxides, coordination complexes, and the oxygen-evolving complex of photosystem II studied by resonant inelastic X-ray scattering J Am Chem Soc 126 9946 9959
41. Govindjee, Van Rensen JJS (1993) Photosystem II reaction centers and bicarbonate. In: Deisenhofer J, Norris JR (eds) Photosynthetic reaction centers, vol I. Academic Press, Orlando, pp 357-389
42. Govindjee, Beatty JT, Gest H, Allen JF (eds) (2005) Discoveries in photosynthesis. Advances in photosynthesis and respiration, vol 20. Springer, Dordrecht
43. -• in bacterial reaction centers of Rhodobacter sphaeroides determined by a driving force assay Proc Natl Acad Sci USA 95 11679 11684
44. SR Greenfield M Seibert Govindjee MR Wasielewski 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
45. x band in isolated photosystem II reaction centers at 7 K: energy transfer and charge separation J Phys Chem B 103 8364 8374
46. Grimm B, Porra RJ, Rüdiger W, Scheer H (eds) (2006) Chlorophylls and bacteriochlorophylls: biochemistry, biophysics, functions and applications. Advances in photosynthesis and respiration, vol 25. Springer, Dordrecht
47. ML Groot NP Pawlowicz LJGW Van Wilderen J Breton IHM Van Stokkum R van Grondelle 2005 Initial electron donor and acceptor in isolated photosystem II reaction centers identified with femtosecond mid-IR spectroscopy Proc Natl Acad Sci USA 102 13087 13092
48. 2 state of photosystem II FEBS Lett 195 151 154
49. K Hasegawa T Noguchi 2005 Density functional theory calculations on the dielectric-constant dependence of the oxidation potential of chlorophyll: Implication for the high potential of P680 in Photosystem II Biochemistry 44 8865 8872
50. - site in the oxygen-evolving complex of photosystem II Biophys J 86 1042 1050
51. M Haumann C Müller P Liebisch L Iuzzolino J Dittmer M Grabolle T Neisius W Meyer-Klaucke H Dau 2005 Structural and oxidation state changes of the Photosystem II manganese complex in four transitions of the water oxidation cycle (S0 → S1, S1 → S2, S2 → S3, and S3, S4 → S0) characterized by X-ray absorption spectroscopy at 20 K and room temperature Biochemistry 44 1894 1908
52. 2 formation tracked by time-resolved X-ray experiments Science 310 1019 1021
53. --reconstituted oxygen-evolving Photosystem II: Evidence from X-ray absorption spectroscopy at the Br K-edge Biochemistry 45 13101 13107
54. - reorientation J Am Chem Soc 129 15935 15946
55. Hillier W, Messinger J (2005) Mechanism of photosynthetic oxygen production. In: Wydrzynski T, Satoh K (eds) Photosystem II. The light-driven water: plastoquinone oxidoreductase advances in photosynthesis and respiration, vol 22. Springer, Dordrecht, pp 567-608
56. 2 evolving complex of Photosystem II vary independently during S-state turnover Biochemistry 39 4399 4405
57. 18O-Water exchange in photosystem II: Substrate binding and intermediates of the water splitting cycle Coord Chem Rev 252 306 317
58. W Hillier I McConnell MR Badger A Boussac VV Klimov GC Dismukes T Wydrzynski 2006 Quantitative assessment of intrinsic carbonic anhydrase activity and the capacity for bicarbonate oxidation in Photosystem II Biochemistry 45 2094 2102
59. B Hillmann K Brettel F van Mieghem A Kamlowski WA Rutherford E Schlodder 1995 Charge recombination in photosystem II. 2. Transient absorbance difference spectra and their temperature dependence Biochemistry 34 4814 4827
60. 4 cluster in Photosystem II based on solvent accessibility simulations, with implications for substrate water access Biochim Biophys Acta 1777 140 153
61. AR Holzwarth MG Müller M Reus M Nowaczyk J Sander M Rögner 2006 Kinetics and mechanism of electron transfer in intact photosystem II and in the isolated reaction center: Pheophytin is the primary electron donor Proc Natl Acad Sci USA 103 6895 6900
62. JL Hughes BJ Prince E Krausz PJ Smith RJ Pace H Riesen 2004 Highly efficient spectral hole-burning in oxygen-evolving photosystem II preparations J Phys Chem B 108 10428 10439
63. JL Hughes PJ Smith RJ Pace H Riesen 2005 Probing the lowest chlorophyll a states in photosystem II via selective spectroscopy: new insights on P680 Photosynth Res 84 93 98
64. JL Hughes RJ Pace PJ Smith E Krausz 2006 Charge separation in photosystem II core complexes induced by 690-730 nm excitation at 1.7 K Biochim Biophys Acta 1757 841 851
65. + Biochemistry 37 14450 14456
66. Hunter CN, Daldal F, Thurnauer MC, Beatty JT (eds) (2008) The purple phototrophic bacteria. Advances in photosynthesis and respiration, vol 28. Springer, Dordrecht
67. 2-evolving Photosystem II preparations Biochemistry 47 6292 6300
68. S Isgandarova G Renger J Messinger 2003 Functional differences of photosystem II from Synechococcus elongatus and spinach characterized by flash induced oxygen evolution patterns Biochemistry 42 8929 8938
69. N Ishida M Sugiura F Rappaport T-L Lai AW Rutherford A Boussac 2008 Biosynthetic exchange of bromide for chloride and strontium for calcium in the Photosystem II oxygen-evolving enzymes J Biol Chem 283 13330 13340
70. H Ishikita E-W Knapp 2005 Control of quinone redox potentials in Photosystem II: electron transfer and photoprotection J Am Chem Soc 127 14714 14720
71. H Ishikita W Saenger J Biesiadka B Loll EW Knapp 2006 How photosynthetic reaction centers control oxidation power in chlorophyll pairs P680, P700, and P870 Proc Natl Acad Sci USA 103 9855 9860
72. H Ishikita W Saenger B Loll J Biesiadka EW Knapp 2006 Energetics of a possible proton exit pathway for water oxidation in Photosystem II Biochemistry 45 2063 2071
73. RC Jennings G Elli FM Garlaschi S Santabarbara G Zucchelli 2000 Selective quenching of the fluorescence of core chlorophyll-protein complexes by photochemistry indicates that Photosystem II is partly diffusion limited Photosynth Res 66 225 233
74. P Joliot A Joliot 1973 Different types of quenching involved in Photosystem II centers Biochim Biophys Acta 305 302 316
75. P Joliot G Barbieri R Chabaud 1969 Un nouveau modele des centres photochimiques du système II Photochem Photobiol 10 309 329
76. O Kaminskaya G Renger VA Shuvalov 2003 Effect of dehydration on light induced reactions in Photosystem II: Photoreactions of cytochrome b559 Biochemistry 42 8119 8132
77. O Kaminskaya VA Shuvalov G Renger 2007 Evidence for a novel quinone binding site in the PS II (PS II) complex which regulates the redox potential of Cyt b559 Biochemistry 46 1091 1105
78. N Kamiya J-R Shen 2003 Crystal structure of oxygen-evolving photosystem II from Thermosynechococcus vulcanus at 3.7-Å resolution Proc Natl Acad Sci USA 100 98 103
79. 680 in the D1D2cytb559-complex of Photosystem II Ber Bunsenges Phys Chem 100 2045 2051
80. 2O Biochemistry 36 8904 8913
81. J Kargul K Maghlaoui JW Murray Z Deak A Boussac AW Rutherford I Vaas J Barber 2007 Purification, crystallization and X-ray diffraction analyses of the T. elongatus PS II core dimer with strontium replacing calcium in the oxygen-evolving complex Biochim Biophys Acta 1767 404 413
82. JF Kasting JF Seifert 2002 Life and the evolution of earth's atmosphere Science 296 1066 1067
83. Ke B (2001) Photosynthesis - Photobiochemistry and photobiophysics. Advances in photosynthesis and respiration, vol 10. Kluwer Academic Publishers (now Springer), Dordrecht
84. J Kern G Renger 2007 Photosystem II: Structure and mechanism of the water:plastoquinone oxidoreductase Photosynth Res 94 183 202
85. EH Kim MR Razeghifard JM Anderson WS Chow 2007 Multiple sites of retardation of electron transfer in Photosystem II after hydrolysis of phosphatidylglycerol Photosynth Res 93 149 158
86. 2 evolution Photochem Photobiol 11 457 476
87. E Krausz JL Hughes P Smith R Pace SP Årsköld 2005 Oxygen-evolving photosystem II core complexes: a new paradigm based on the spectral identification of the charge separating state, the primary acceptor and assignment of low-temperature fluorescence Photochem Photobiol Sci 4 744 753
88. A Krieger AW Rutherford GN Johnson 1995 On the determination of redox midpoint potential of the primary quinone electron-acceptor, Q(a), in Photosystem-II Biochim Biophys Acta 1229 193 201
89. + reduction pattern and its temperature dependence in oxygen evolving PS II core complexes from thermophilic cyanobacteria and higher plants Phys Chem Chem Phys 6 4838 4843
90. 55Mn-ENDOR and EPR spectroscopy J Am Chem Soc 129 13421 13435
91. Lane N (2003) Oxygen - The molecule that made the world. Oxford University Press, Oxford
92. Lancaster R (2008) Structures of reaction centers in anoxygenic bacteria. In: Renger G (ed) Primary processes of photosynthesis: principles and apparatus, Part II Reaction centers/photosystems electron transport chains, photophosphorylation and evolution. Royal Society Chemistry, Cambridge, pp 5-56
93. Larkum AWD (2008) The evolution of photosynthesis. In: Renger G (ed) Primary processes of photosynthesis: Principles and apparatus, Part II Reaction centers/photosystems, electron transport chains photophosphorylation and evolution. Royal Society Chemistry, Cambridge, pp 291-349
94. Law CJ, Cogdell RJ (2008) The light-harvesting system of purple anoxygenic photosynthetic bacteria. In: Renger G (ed) Primary processes of photosynthesis: Principles and apparatus, Part I: Reaction centers/photosystems electron transport chains photophosphorylation and evolution. Royal Society Chemistry, Cambridge, pp 205-260
95. JA Leegwater JR Durrant DR Klug 1998 Exciton equilibration induced by phonons: Theory and application to PS II J Phys Chem B 102 5378 5386
96. 3 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 3412
97. F Liu JJ Concepcion JW Jurss T Cardolaccia JL Templeton TJ Meyer 2008 Mechanisms of water oxidation from the blue dimer to photosystem II Inorg Chem 47 1727 1752
98. B Loll J Kern W Saenger A Zouni J Biesiadka 2005 Towards complete cofactor arrangement in the 3.0 Å resolution structure of photosystem II Nature 438 1040 1044
99. 3 from Thermus thermophilus: Structural analysis and role of oxygen transport channels in the heme-Cu oxidases Biochemistry 47 4657 4665
100. JP McEvoy GW Brudvig 2006 Water-splitting chemistry of Photosystem II Chem Rev 106 4455 4483
101. J Messinger G Renger 1990 The reactivity of hydrazine with Photosystem II strongly depends on the redox state of the water oxidizing system FEBS Lett 277 141 146
102. -2 of the water oxidase in isolated spinach thylakoids Biochemistry 32 9379 9386
103. Messinger J, Renger G (2008) Photosynthetic water splitting. In: Renger G (ed) Primary processes of photosynthesis: basic principles and apparatus, vol. II: Reaction centers/photosystems electron transport chains photophosphorylation and evolution. Royal Society Chemistry, Cambridge, pp 291-349
104. 2-induced modifications of flash-induced oxygen evolution in isolated spinach thylakoids Biochemistry 30 7852 7862
105. TJ Meyer M Hang V Huynh HH Thorp 2007 The role of proton coupled electron transfer (PCET) in water oxidation by Photosystem II. Wiring for protons Angew Chem Int Ed 46 5284 5304
106. M Miqyass MA Marosvo lgyi Z Nagel CF Yocum HJ Van Gorkom 2008 S-state dependence of the calcium requirement and binding characteristics in the oxygen-evolving complex of Photosystem II Biochemistry 47 7915 7924
107. Y Miloslavina M Szczepaniak MG Müller J Sander M Nowaczyk M Rögner AR Holzwarth 2006 Charge separation kinetics in intact photosystem II core particles is trap-limited. A picosecond fluorescence study Biochemistry 45 2436 2442
108. Mimuro M, Kobayashi M, Murakami A, Tsuchiya T, Miyashita H (2008) Oxygen evolving cyanobacteria. In: Renger G (ed) Primary processes of photosynthesis: principles and apparatus, Part I: Photophysical principles, pigments and light harvesting/adaptation/stress. Royal Society Chemistry, Cambridge, pp 261-299
109. F Müh ME Madjet J Adolphs A Abdurahman B Rabenstein H Ishikita E-W Knapp T Renger 2007 α-Helices direct excitation energy flow in the Fenna-Matthews-Olson protein Proc Natl Acad Sci USA 104 16862 16867
110. JW Murray J Barber 2007 Structural characteristics of channels and pathways in photosystem II including the identification of an oxygen channel J Struct Biol 159 228 237
111. JW Murray K Maghlaoui J Kargul N Ishida T-L Lai AW Rutherford M Sugoura A Boussac J Barber 2008 X-ray crystallography identifies two chloride binding sites in the oxygen evolving centre of Photosystem II Energy Environ Sci 1 161 166
112. GM Nikolaev PP Knox AA Kononenko NP Grishanova AB Rubin 1980 Photo-induced electron transport and water state in Rhodospirillum rubrum chromatophores Biochim Biophys Acta 590 194 201
113. T Noguchi 2008 FTIR detection of water reactions in the oxygen-evolving centre of photosystem II Phil Trans R Soc B 363 1189 1195
114. T Noguchi M Sugiura 2002 Flash-induced FTIR difference spectra of the water oxidizing complex in moderately hydrated Photosystem II core films: Effect of hydration extent on S-state transitions Biochemistry 41 2322 2330
115. T Noguchi Y Inoue K Satoh 1993 FT-IR studies on the triplet state of P680 in the photosystem II reaction center: triplet equilibrium within a chlorophyll dimer Biochemistry 32 7186 7195
116. VI Novoderezhkin EG Andrizhiyewskaya JP Dekker R Van Grondelle 2005 Pathways and timescales of primary charge separation in the photosystem II reaction center as revealed by a simultaneous fit of time-resolved fluorescence and transient absorption Biophys J 89 1464 1481
117. VI Novoderezhkin JP Dekker R Van Grondelle 2007 Mixing of exciton and charge-transfer states in Photosystem II reaction centers: Modeling of Stark spectra with modified Redfield theory Biophys J 93 1293 1311
118. MY Okamura ML Paddock MS Graige G Feher 2000 Proton and electron transfer in bacterial reaction centers Biochim Biophys Acta 1458 148 163
119. T Okubo T Tomo M Sugiura T Noguchi 2007 Perturbation of the structure of P680 and the charge distribution on its radical cation in isolated reaction center complexes of Photosystem II as revealed by Fourier Transform Infrared Spectroscopy Biochemistry 46 4390 4397
120. K Olesen L-E Andréasson 2003 The function of the chloride ion in photosynthetic oxygen evolution Biochemistry 42 2025 2035
121. CC Page CC Moser X Chen PL Dutton 1999 Natural engineering principles of electron tunneling in biological oxidation-reduction Nature 402 47 52
122. Papageorgiou GC, Govindjee (eds) (2004) Chlorophyll a fluorescence: A signature of photosynthesis. Advances in photosynthesis and respiration, vol 19. Springer, Dordrecht
123. Parson WW (2008) Functional pattern of reaction centers in anoxygenic bacteria. In: Renger G (ed) Primary processes of photosynthesis: Principles and apparatus, Part II Reaction centers/photosystems, electron transport chains photophosphorylation and evolution. Royal Society Chemistry, Cambridge, pp 57-109
124. NP Pawlowicz M-L Groot IHM van Stokkum J Breton R van Grondelle 2007 Charge separation and energy transfer in the photosystem II core complex studied by femtosecond mid-infrared spectroscopy Biophys J 93 2732 2742
125. VL Pecoraro MJ Baldwin MT Caudle W-Y Hsieh NA Law 1998 A proposal for water oxidation in photosystem II Pure and Applied Chemistry 70 925 929
126. J Pieper T Hauß A Buchsteiner K Baczyński K Adamiak RE Lechner G Renger 2007 Temperature- and hydration-dependent protein dynamics in photosystem II of green plants studied by quasielastic neutron scattering Biochemistry 46 11398 11409
127. J Pieper T Hauß A Buchsteiner G Renger 2008 The effect of hydration on protein flexibility in photosystem II of green plants studied by quasielastic neutron scattering Eur Biophys J 37 657 663
128. V Prokhorenko AR Holzwarth 2000 Primary processes and structure of the photosystem II reaction center: a photon echo study J Phys Chem B 104 11563 11578
129. 4Ca cluster and the mechanism of photosynthetic water splitting Proc Natl Acad Sci USA 105 1879 1884
130. F Rappaport M Blanchard-Desce J Lavergne 1994 Kinetics of the electron transfer and electrochromic change during the redox transitions of the photosynthetic oxygen-evolving complex Biochim Biophys Acta 1184 178 192
131. F Rappaport A Cuni L Xiong R Sayre J Lavergne 2005 Charge Recombination and thermoluminescence in Photosystem II Biophys J 88 1948 1958
132. G Raszewski T Renger 2008 Light-harvesting in photosystem II core complexes is limited by the transfer to the trap: Can the core complex turn into a photoprotective mode? J Am Chem Soc 130 4431 4446
133. G Raszewski W Saenger T Renger 2005 Theory of optical spectra of photosystem II reaction centers: Location of the triplet state and the identity of the primary electron donor Biophys J 88 986 998
134. G Raszewski BA Diner E Schlodder T Renger 2008 The evolutionary development of the protein complement of Photosystem 2 Biophys J 95 105 119
135. J Raymond RE Blankenship 2004 The evolutionary development of the protein complement of Photosystem 2 Biochim Biophys Acta 1655 133 139
136. MR Razeghifard RJ Pace 1997 Electron paramagnetic resonance kinetic studies of the S states in spinach PSII membranes Biochim Biophys Acta 1322 141 150
137. 0 transition Biochemistry 38 1252 1257
138. -• formation in Photosystem II FEBS Lett 428 123 126
139. F Reifarth G Christen AG Seeliger P Dörmann C Benning G Renger 1997 Modification of the water oxidising complex in leaves of the dgd1 mutant of Arabidopsis thaliana deficient in the galactolipid digalactosyldiacylglycerol Biochemistry 36 11769 11776
140. Renger G (1978) Theoretical studies about the functional and structural organization of the photosynthetic oxygen evolution. In: Metzner H (ed) Photosynthetic oxygen evolution. Academic Press, London, pp 229-248
141. Renger G (1983) Biological energy conservation. In: Hoppe W, Lohmann W, Markl H, Ziegler H (eds) Biophysics. Springer, Berlin, pp 347-371
142. G Renger 1987 Mechanistic aspects of photosynthetic water cleavage Photosynthetica 21 203 224
143. 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. Kluwer Academic Publishers (now Springer) and Narosa Publishing Co, Dordrecht, Delhi, pp 292-329
144. G Renger 2001 Photosynthetic water oxidation to molecular oxygen: apparatus and mechanism Biochim Biophys Acta 1503 210 228
145. G Renger 2004 Coupling of electron and proton transfer in oxidative water cleavage in photosynthesis Biochim Biophys Acta 1655 195 204
146. G Renger 2007 Oxidative photosynthetic water splitting: energetics, kinetics and mechanism Photosynth Res 92 407 425
147. Renger G (2008a) Overview on primary processes of photosynthesis. In: Renger G (ed) Primary processes of photosynthesis: principles and apparatus, Part I Photophysical principles pigments and light harvesting/adaptation/stress. Royal Society Chemistry, Cambridge, pp 5-35
148. Renger G (2008b) Functional pattern of Photosystem II in oxygen evolving organisms. In: Renger G (ed) Primary processes of photosynthesis: principles and apparatus, Part II Reaction centers/photosystems electron transport chains, photophosphorylation and evolution. Royal Society Chemistry, Cambridge, pp 237-290
149. G Renger B Hanssum 1992 Studies on the reaction coordinates of the water oxidase in PS II membrane fragments from spinach FEBS Lett 299 28 32
150. Renger G, Holzwarth AR (2005) Primary electron transfer. In: Wydrzynski T, Satoh K (eds) Photosystem II: The water: plastoquinone oxido-reductase in photosynthesis. Springer, Dordrecht, pp 139-175
151. G Renger P Kühn 2007 Reaction pattern and mechanism of light induced oxidative water splitting in photosynthesis Biochim Biophys Acta 1767 458 471
152. G Renger W Weiss 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 chloroplasts FEBS Lett 137 217 221
153. G Renger W Weiss 1986 Functional and structural aspects of photosynthetic water oxidation Biochem Soc Trans 14 17 20
154. + in PS II membrane fragments from spinach Photosynth Res 22 247 256
155. -•) and deleterious effects of copper (II) Z Naturforsch 48c 234 240
156. G Renger H-J Eckert A Bergmann J Bernarding B Liu A Napiwotzki F Reifarth JH Eichler 1995 Fluorescence and spectroscopic studies on exciton trapping and electron transfer in photosystem II of higher plants Austr J Plant Physiol 22 167 181
157. G Renger G Christen M Karge H-J Eckert K-D Irrgang 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
158. T Renger 2004 Theory of optical spectra involving charge transfer States: dynamic localization predicts a temperature dependent optical band shift Phys Rev Lett 93 1-4 101 188
159. T Renger RA Marcus 2002 On the relation of protein dynamics and exciton relaxation in pigment-protein complexes: an estimation of the spectral density and a theory for the calculation of optical spectra J Chem Phys 116 9997 10019
160. T Renger V May O Kühn 2001 Ultrafast excitation energy transfer dynamics in photosynthetic pigment-protein complexes Phys Rev 343 137 254
161. PR Rich DS Bendall 1980 The kinetics and thermodynamics of the reduction of cytochrome c by substituted p-benzoquinols in solution Biochim Biophys Acta 592 506 518
162. S Riistama A Puustinen A García-Horsman S Iwata H Michel M Wikström 1996 Channelling of dioxygen into the respiratory enzyme Biochim Biophys Acta 12275 1 4
163. HH Robinson AR Crofts 1984 Kinetics of the oxidation-reduction reactions of the photosystem II acceptor complex and the pathway for deactivation FEBS Lett 151 221 226
164. 2 moieties in the tetranuclear Mn complex? J Am Chem Soc 124 7459 7471
165. AW Rutherford P Faller 2002 Photosystem II: evolutionary perspectives Phil Trans R Soc Lond B 358 245 253
166. 2 evolving enzyme Biochim Biophys Acta 767 548 556
167. S Sacquin-Mora P Sebban V Derrien B Frick R Lavery C Alba-Simionesco 2007 Probing the flexibility of the bacterial reaction center: The wild-type protein is more rigid than two site-specific mutants Biochemistry 46 14960 14968
168. K Sauer J Yano VK Yachandra 2008 X-ray spectroscopy of the photosynthetic oxygen-evolving complex Coord Chem Rev 252 318 335
169. GH Schatz H Brock AR Holzwarth 1987 Picosecond kinetics of fluorescence and absorbance changes in photosystem II particles excited at low photon density Proc Natl Acad Sci USA 84 8414 8418
170. GH Schatz H Brock AR Holzwarth 1988 Kinetic and energetic model for the primary processes in photosystem II Biophys J 54 397 405
171. E Schlodder T Renger G Raszewski WJ Coleman PJ Nixon RO Cohen B Diner 2008 Site-directed mutations at D1-Thr179 of Photosystem II in Synechocystis sp. PCC modify the spectroscopic properties of the accessory chlorophyll in the D1-branch of the reaction center Biochemistry 47 3143 3154
172. 2 activation J Am Chem Soc 130 7098 7109
173. D Shevela B Nöring H-J Eckert J Messinger G Renger 2006 Characterization of the water oxidizing complex of photosystem II of the Chl d - containing cyanobacterium Acaryochloris marina via its reactivity towards endogenous electron donors and acceptors Phys Chem Chem Phys 8 3460 3466
174. D Shevela J-H Su V Klimov J Messinger 2008 Hydrogen carbonate is not a tightly bound constituent of the water oxidizing complex in photosystem II Biochim Biophys Acta 1777 532 539
175. L-X Shi WP Schröder 2004 The low molecular mass subunits of the photosynthetic supracomplex, photosystem II Biochim Biophys Acta 1608 75 96
176. O Shlyk-Kerner I Samish D Kaftan N Holland PS Maruthi Sai H Kless A Scherz 2006 Protein flexibility acclimatizes photosynthetic energy conversion to the ambient temperature Nature 442 827 830
177. T Shutova K-D Irrgang V Shubin VV Klimov G Renger 1997 Analysis of pH-induced structural changes of the isolated extrinsic 33 kDa protein of Photosystem II Biochemistry 36 6350 6358
178. T Shutova VV Klimov B Andersson G Samuelsson 2007 A cluster of carboxylic groups in PsbO protein is involved in proton transfer from the water oxidizing complex of Photosystem II Biochim Biophys Acta 1767 434 440
179. W Sicking H-G Korth H de Groot RJ Sustmann 2008 On the functional role of a water molecule in clade 3 catalases: A proposal for the mechanism by which NADPH prevents the formation of compound II J Am Chem Soc 130 7345 7356
180. 4 state of the oxygen-evolving complex in Photosystem Chem Eur J 12 9217 9227
181. PEM Siegbahn 2008 Theoretical studies of O-O bond formation in Photosystem II Inorg Chem 47 1779 1786
182. JD Soper SV Kryatov EV Rybak-Akimova DG Nocera 2007 Proton-directed redox control of O-O bond activation by heme hydroperoxidase models J Am Chem Soc 129 5069 5075
183. 2-evolving complex of Photosystem II J Chem Theor Comput 2 1119 1134
184. EM Sproviero JA Gascon JP McEvoy GW Brudvig VS Batista 2008 Quantum Mechanics/Molecular Mechanics study of the catalytic cycle of water splitting in Photosystem II J Am Chem Soc 130 3428 3442
185. K Strzalka T Walczak T Sarna HM Swartz 1990 Measurement of time-resolved oxygen concentration changes in photosynthetic systems by nitroxide-based EPR oximetry Arch Biochem Biophys 281 312 318
186. H Suzuki M Nagasaka M Sugiura T Noguchi 2005 Fourier transform infrared spectrum of the secondary quinone electron acceptor Q(B) in photosystem II Biochemistry 44 11323 11328
187. R Takahashi K Hasegawa T Noguchi 2008 Effect of charge distribution over a chlorophyll dimer on the redox potential of P680 in photosystem II as studied by density functional theory calculations Biochemistry 47 6289 6291
188. A in photosystem II as studied by Fourier transform infrared spectroscopy. Photosynth Res 10.1007/s11120-008-9302-5
189. E Tyystjärvi 2008 Photoinhibition of Photosystem II and photodamage of the oxygen evolving manganese cluster Coord Chem Rev 252 361 376
190. 2-evolving complex of Photosystem II Biochemistry 47 3073 3075
191. van Amerongen H, Croce R (2008) Structure and function of Photosystem II light-harvesting proteins (Lhcb) of higher plants. In: Renger G (ed) Primary processes of photosynthesis: principles and apparatus, Part I: Photophysical principles, pigments and light harvesting/adaptation/stress. Royal Society Chemistry, Cambridge, pp 329-367
192. ME van Brederode R van Grondelle 1999 New and unexpected routes for ultrafast electron transfer in photosynthetic reaction centers FEBS Lett 455 1 7
193. ME van Brederode MR Jones F van Mourik IHM van Stokkum R Van Grondelle 1997 A new pathway for transmembrane electron transfer in photosynthetic reaction centers of Rhodobacter sphaeroides not involving the excited special pair Biochemistry 36 6855 6861
194. ME van Brederode F van Mourik IHM van Stokkum MR Jones R van Grondelle 1999 Multiple pathways for ultrafast transduction of light energy in the photosynthetic reaction center of Rhodobacter sphaeroides Proc Natl Acad Sci USA 96 2054 2059
195. van Gorkom HJ, Yocum CF (2005) The calcium and chloride cofactors. In: Wydrzynski T, Satoh K (eds) Photosystem II: The water/plastoquinone oxido-reductase in photosynthesis. Advances in photosynthesis and respiration, vol 22. Springer, Dordrecht, pp 307-327
196. FJE van Mieghem K Satoh AW Rutherford 1991 A chlorophyll tilted 30 ° relative to the membrane in the photosystem II reaction center Biochim Biophys Acta 1058 379 385
197. S Vasilev P Orth A Zouni TG Owens D Bruce 2001 Excited-state dynamics in photosystem II: Insights from the x-ray crystal structure Proc Natl Acad Sci USA 98 8602 8607
198. S Vasilev C-I Lee GW Brudvig D Bruce 2002 Structure-based kinetic modeling of excited-state transfer and trapping in histidine-tagged photosystem II core complexes from Synechocystis Biochemistry 41 12236 12243
199. Vass I, Aro E (2008) Photoinhibition of photosynthetic electron transport. In: Renger G (ed) Primary processes of photosynthesis: principles and apparatus, Part I Photophysical principles pigments and light harvesting/adaptation/stress. Royal Society Chemistry, Cambridge, pp 393-425
200. I Vass Govindjee 1996 Thermoluminescence from the photosynthetic apparatus Photosynth Res 48 117 126
201. Vass I, Inoue Y (1992) Thermoluminescence in the study of Photsystem II. In: Barber J (ed) Topics in photosynthesis, the photosystems: structure, function and molecular biology. Elsevier, Amsterdam, pp 259-294
202. Velthuys B (1981) Spectrophotometric studies of the S-state transitions of Photosystem II and of the interaction of its charged donor chains with lipid-soluble anions. In: Akoyunoglou G (ed) Photosynthesis II. Electron transport and photophosphorylation. Balaban, Philadelphia, pp 75-85
203. WCJ Vermaas G Renger G Dohnt 1984 The reduction of the oxygen-evolving system in chloroplasts by thylakoid components Biochim Biophys Acta 764 194 202
204. JS Vrettos J Limburg GW Brudvig 2001 Mechanism of photosynthetic water oxidation: combining biophysical studies of photosystem II with inorganic model chemistry Biochim Biophys Acta 1503 229 245
205. D Wang J Zheng S Shaik W Thiel 2008 Quantum and molecular mechanical study of the first proton transfer in the catalytic cycle of cytochrome P450cam and its mutant D251 N J Phys Chem B 112 5126 5138
206. A Warshel WW Parson 1987 Spectroscopic properties of photosynthetic reaction centers. 1. Theory J Am Chem Soc 109 6143 6152
207. W Weiss G Renger 1984 UV-Spectral characterization in Tris-washed chloroplasts of the redox component-D1 which functionally connects the reaction center with the water-oxidizing enzyme system-Y in photosynthesis FEBS Lett 169 219 223
208. 3 state of the oxygen-evolving complex J Am Chem Soc 126 8070 8071
209. 2+ substitution on the reduction rates of YZ in PS II membranes: evidence for concerted hydrogen atom transfer in oxygen evolution Biochemistry 39 16220 16229
210. CA Wraight 2004 Proton and electron transfer in the acceptor quinone complex of photosynthetic reaction centers from Rhodobacter sphaeroides Front Biosci 9 309 337
211. Wydrzynski T, Satoh K (eds) (2005) Photosystem II: light-induced water: Plastoquinone oxidoreductase, advances in photosynthesis and respiration, vol 22. Springer, Dordrecht
212. J Xiong CE Bauer 2002 Complex evolution of photosynthesis Annu Rev Plant Biol 53 503 521
213. VK Yachandra K Sauer MP Klein 1996 Manganese cluster in photosynthesis: where plants oxidize water to dioxygen Chem Rev 96 2927 2950
214. J Yano Y Pushkar P Glatzel A Lewis K Sauer J Messinger U Bergmann VK Yachandra 2005 High-resolution Mn EXAFS of the oxygen-evolving complex in photosystem II: structural implications for the Mn4Ca cluster J Am Chem Soc 127 14974 14975
215. 4Ca cluster Science 314 821 825
216. - in photosystem II Biophys Chem 12 83 91
217. S Zein LV Kulik J Yano J Kern Y Pushkar A Zouni VK Yachandra W Lubitz F Neese J Messinger 2008 Focusing the view on nature's water-splitting catalyst Phil Trans R Soc B 363 1167 1177
218. W Zinth J Wachtveitl 2005 The first picoseconds in bacterial photosynthesis-ultrafast electron transfer for the efficient conversion of light energy Chem Phys Chem 6 871 880
219. A Zouni HT Witt J Kern P Fromme N Krauß W Saenger P Orth 2001 Crystal structure of photosystem II from Synechococcus elongatus at 3.8 Å resolution Nature 409 739 743