Misses during water oxidation in photosystem II are S state-dependent

Journal of Biological Chemistry

Volumn 287, Issue 16, 2012, Pages 13422-13429

  Han, Guangye ^a,b   Mamedov, Fikret ^a   Styring, Stenbjörn ^a  

^a UPPSALA UNIVERSITY   (Sweden)

^b UMEÅ UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

ELECTRON ACCEPTOR; EPR SIGNALS; MEMBRANE PREPARATION; PHOTOSYSTEM II; RECOMBINATION REACTIONS; S STATE; S-STATE TRANSITIONS; STATE-DEPENDENT; TEMPERATURE DEPENDENCE; WATER OXIDATION;

BIOCHEMISTRY; BIOLOGY;

FACTOR ANALYSIS;

CHEMICAL COMPOUND; ELECTRON ACCEPTOR; UNCLASSIFIED DRUG; WATER;

ANALYTICAL PARAMETERS; ARTICLE; CHEMICAL REACTION; CONTROLLED STUDY; MAGNETIC FIELD; MEMBRANE; NONHUMAN; OXIDATION; PHOTOSYSTEM II; PRIORITY JOURNAL; SPINACH; TEMPERATURE; WATER OXIDATION;

CYANOBACTERIA; ELECTRON SPIN RESONANCE SPECTROSCOPY; MODELS, CHEMICAL; OXIDATION-REDUCTION; OXYGEN; PHOTOSYSTEM II PROTEIN COMPLEX; PLANTS; TEMPERATURE; WATER;

SPINACIA OLERACEA;

EID: 84859753093     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.342543     Document Type: Article

References (55)

1. Wydrzynski, T. J., and Satoh, K. (eds) (2005) Photosystem II: The Lightdriven Water:Plastoquinone Oxidoreductase. Springer, The Netherlands
2. Renger, G. (2008) in Primary Processes of Photosynthesis (Renger, G., ed) Vol. 2, pp. 237-290, RSC Publishing, Cambridge, UK
3. Rappaport, F., and Diner, B. A. (2008) Primary photochemistry and energetics leading to the oxidation of the Mn4Ca cluster and to the evolution of molecular oxygen in photosystem II. Coord. Chem. Rev. 252, 259-272
4. McEvoy, J. P., and Brudvig, G. W. (2006) Water-splitting chemistry of photosystem II. Chem. Rev. 106, 4455-4483 (Pubitemid 44816649)
5. Dau, H., and Haumann, M. (2008) The manganese complex of photosystem II in its reaction cycle: basic framework and possible realization at the atomic level. Coord. Chem. Rev. 252, 273-295
6. Messinger, J., and Renger, G. (2008) in Primary Processes of Photosynthesis (Renger, G., ed) Vol. 2, pp. 291-349, RSC Publishing, Cambridge, UK
7. Kamiya, N., and Shen, J. R. (2003) Crystal structure of oxygen-evolving photosystem II from Thermosynechococcus vulcanus at 3.7-A resolution. Proc. Natl. Acad. Sci. U.S.A. 100, 98-103 (Pubitemid 36078036)
8. Ferreira, K. N., Iverson, T. M., Maghlaoui, K., Barber, J., and Iwata, S. (2004) Architecture of the photosynthetic oxygen-evolving center. Science 303, 1831-1838 (Pubitemid 38374869)
9. Loll, B., Kern, J., Saenger, W., Zouni, A., and Biesiadka, J. (2005) Towards complete cofactor arrangement in the 3.0 A resolution structure of photosystem II. Nature 438, 1040-1044 (Pubitemid 43093979)
10. Umena, Y., Kawakami, K., Shen, J. R., and Kamiya, N. (2011) Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 Å. Nature 473, 55-60
11. 2 evolution. I. A linear four step mechanism. Photochem. Photobiol. 11, 457-475
12. Forbush, B., Kok, V., and McGloin, M. (1971) Cooperation of charges in photosynthetic O2 evolution. 2. Damping of flash yield oscillation, deactivation. Photochem. Photobiol. 14, 307-321
13. Styring, S., and Rutherford, A. W. (1988) Deactivation kinetics and temperature dependence of the S state transitions in the oxygen-evolving system of photosystem II measured by electron paramagnetic resonance spectroscopy. Biochim. Biophys. Acta 933, 378-387
14. Chen, G., Han, G., Göransson, E., Mamedov, F., and Styring, S. (2012) Stability of the S3 and S2 state intermediates in photosystem II directly probed by EPR spectroscopy. Biochemistry 51, 138-148
15. slow). Biochemistry 26, 2401-2405
16. Joliot, P., Barbieri, G., and Chabaud, R. (1969) Un nouveau modele des centres photochimiques du systeme II. Photochem. Photobiol. 10, 309-329
17. Shinkarev, V. P., and Wraight, C. A. (1993) Oxygen evolution in photosynthesis: from unicycle to bicycle. Proc. Natl. Acad. Sci. U.S.A. 90, 1834-1838 (Pubitemid 23069951)
18. Lavergne, J., and Rappaport, F. (1998) Stabilization of charge separation and photochemical misses in photosystem II. Biochemistry 37, 7899-7906 (Pubitemid 28248651)
19. Meunier, P. C. (1993) Oxygen evolution by photosystem II: the contribution of backward transitions to the anomalous behaviour of double-hits revealed by a new analysis method. Photosynth. Res. 36, 111-118
20. Shinkarev, V. P. (2005) Flash-induced oxygen evolution in photosynthesis: simple solution for the extended S-state model that includes misses, double- hits, inactivation, and backward-transitions. Biophys. J. 88, 412-421
21. de Wijn, R., and van Gorkom, H. J. (2002) S-state dependence of the miss probability in photosystem II. Photosynth. Res. 72, 217-222
22. Packham, N. K., Hodges, M., Etienne, A. L., and Briantais, J. M. (1988) Changes in the flash-induced oxygen yield pattern by thylakoid membrane phosphorylation. Photosynth. Res. 15, 221-232
23. Messinger, J., Schröder, W. P., and Renger, G. (1993) Structure-function relations in photosystem II: effects of temperature and chaotropic agents on the period four oscillation of flash-induced oxygen evolution. Biochemistry 32, 7658-7668 (Pubitemid 23240809)
24. Messinger, J., and Renger, G. (1994) Analyses of pH-induced modifications of the period four oscillation of flash-induced oxygen evolution reveal distinct structural changes of the photosystem II donor side at characteristic pH values. Biochemistry 33, 10896-10905 (Pubitemid 24296343)
25. Meunier, P. C., Burnap, R. L., and Sherman, L. A. (1996) Improved 5-step modeling of the photosystem II S-state mechanism in cyanobacteria. Photosynth. Res. 47, 61-76 (Pubitemid 3044244)
26. Isgandarova, S., Renger, G., and Messinger, J. (2003) Functional differences of photosystem II from Synechococcus elongatus and spinach characterized by flash-induced oxygen evolution patterns. Biochemistry 42, 8929-8938 (Pubitemid 36935400)
27. Lavorel, J. (1976) Matrix analysis of the oxygen evolving system of photosynthesis. J. Theor. Biol. 57, 171-185
28. Ahrling, K. A., Peterson, S., and Styring, S. (1997) An oscillating manganese electron paramagnetic resonance signal from the S0 state of the oxygen evolving complex in photosystem II. Biochemistry 36, 13148-13152 (Pubitemid 27473358)
29. Roelofs, T. A., Liang, W., Latimer, M. J., Cinco, R. M., Rompel, A., Andrews, J. C., Sauer, K., Yachandra, V. K., and Klein, M. P. (1996) Oxidation states of the manganese cluster during the flash-induced S-state cycle of the photosynthetic oxygen-evolving complex. Proc. Natl. Acad. Sci. U.S.A. 93, 3335-3340
30. 3 transition: implications for the mechanism of photosynthetic water oxidation. J. Am. Chem. Soc. 123, 7804-7820
31. 0) characterized by X-ray absorption spectroscopy at 20 K and room temperature. Biochemistry 44, 1894-1908
32. +* reduction by YZ in photosystem II with intact oxygen evolution capacity: analysis of kinetic H/D isotope exchange effects. Biochemistry 38, 2068-2077
33. 3 transitions of the water oxidation cycle. Biochemistry 37, 17112-17119
34. 4Ca cluster and the mechanism of photosynthetic water splitting. Proc. Natl. Acad. Sci. U.S.A. 105, 1879-1884
35. Bernát, G., Morvaridi, F., Feyziyev, Y., and Styring, S. (2002) pH dependence of the four individual transitions in the catalytic S-cycle during photosynthetic oxygen evolution. Biochemistry 41, 5830-5843 (Pubitemid 34462704)
36. Han, G., Ho, F. M., Havelius, K. G. V., Morvaridi, S. F., Mamedov, F., and Styring, S. (2008) Direct quantification of the four individual S states in photosystem II using EPR spectroscopy. Biochim. Biophys. Acta 1777, 495-503
37. Z·S state intermediates in photosystem II. Appl. Magnetic Resonance 37, 151-176
38. Petrouleas, V., Koulougliotis, D., and Ioannidis, N. (2005) Trapping of metalloradical intermediates of the S-states at liquid helium temperatures: overview of the phenomenology and mechanistic implications. Biochemistry 44, 6723-6728 (Pubitemid 40632391)
39. Berthold, D. A., Babcock, G. T., and Yocum, C. F. (1981)Ahighly resolved, oxygen-evolving photosystem II preparation from spinach thylakoid membranes: EPR and electron-transport properties. FEBS Lett. 134, 231-234
40. Völker, M., Ono, T., Inoue, Y., and Renger, G. (1985) Effect of trypsin on PS-II particles: correlation between Hill activity, Mn abundance, and peptide pattern. Biochim. Biophys. Acta 806, 25-34
41. + in oxygen-evolving photosystem II particles from Chlamydomonas. Biochemistry 41, 15754-15761
42. Saygin, Ö., and Witt, H. T. (1987) Optical characterization of intermediates in the water splitting enzyme system of photosynthesis: possible states and configurations of manganese and water. Biochim. Biophys. Acta 893, 452-469
43. Hwang, H. J., Dilbeck, P., Debus, R. J., and Burnap, R. L. (2007) Mutation of arginine 357 of the CP43 protein of photosystem II severely impairs the catalytic S-state cycle of the H2O oxidation complex. Biochemistry 46, 11987-11997 (Pubitemid 350022356)
44. Joliot, P., and Kok, B. (1975) in Bioenergetics of Photosynthesis (Govindjee, ed) pp. 388-413, Academic Press, New York
45. Reinman, S., and Mathis, P. (1981) Influence of temperature on photosystem II electron transfer reactions. Biochim. Biophys. Acta 635, 249-258
46. Mamedov, F., Sayre, R. T., and Styring, S. (1998) Involvement of histidine 190 on the D1 protein in electron/proton transfer reactions on the donor side of photosystem II. Biochemistry 37, 14245-14256 (Pubitemid 28471261)
47. Delrieu, M. J. (1983) Evidence for unequal misses in oxygen flash yield sequence in photosynthesis. Zeitschrift Naturforschung C 38, 247-258
48. Haumann, M., Grundmeier, A., Zaharieva, I., and Dau, H. (2008) Photosynthetic water oxidation at elevated dioxygen partial pressure monitored by time-resolved x-ray absorption measurements. Proc. Natl. Acad. Sci. U.S.A. 105, 17384-17389
49. Shevela, D., Beckmann, K., Clausen, J., Junge, W., and Messinger, J. (2011) Membrane-inlet mass spectrometry reveals a high driving force for oxygen production by photosystem II. Proc. Natl. Acad. Sci. U.S.A. 108, 3602-3607
50. Suzuki, H., Sugiura, M., and Noguchi, T. (2005) pH dependence of the flash-induced S-state transitions in the oxygen-evolving center of photosystem II from Thermosynechoccocus elongatus as revealed by Fourier transform infrared spectroscopy. Biochemistry 44, 1708-1718 (Pubitemid 40204412)
51. Schlodder, E., and Witt, H. T. (1999) Stoichiometry of proton release from the catalytic center in photosynthetic water oxidation: reexamination by a glass electrode study at pH 5.5-7.2. J. Biol. Chem. 274, 30387-30392
52. Robblee, J. H., Cinco, R. M., and Yachandra, V. K. (2001) X-ray spectroscopy- based structure of the Mn cluster and mechanism of photosynthetic oxygen evolution. Biochim. Biophys. Acta 1503, 7-23
53. Haumann, M., Grabolle, M., Neisius, T., and Dau, H. (2002) The first room-temperature x-ray absorption spectra of higher oxidation states of the tetramanganese complex of photosystem II. FEBS Lett. 512, 116-120 (Pubitemid 34164462)
54. Yano, J., Pushkar, Y., Glatzel, P., Lewis, A., Sauer, K., Messinger, J., Bergmann, U., and Yachandra, V. (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 (Pubitemid 41547334)
55. +* reduction kinetics and redox transition probability of the water oxidizing complex as a function of pH and H/D isotope exchange in spinach thylakoids. Biochemistry 38, 6082-6092