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Philosophical Transactions of the Royal Society B: Biological Sciences logoLink to Philosophical Transactions of the Royal Society B: Biological Sciences
. 2002 Oct 29;357(1426):1421–1470. doi: 10.1098/rstb.2002.1138

Structural and functional dynamics of plant photosystem II.

Jan M Anderson 1, W S Chow 1
PMCID: PMC1693045  PMID: 12437881

Abstract

Given the unique problem of the extremely high potential of the oxidant P(+)(680) that is required to oxidize water to oxygen, the photoinactivation of photosystem II in vivo is inevitable, despite many photoprotective strategies. There is, however, a robustness of photosystem II, which depends partly on the highly dynamic compositional and structural heterogeneity of the cycle between functional and non-functional photosystem II complexes in response to light level. This coordinated regulation involves photon usage (energy utilization in photochemistry) and excess energy dissipation as heat, photoprotection by many molecular strategies, photoinactivation followed by photon damage and ultimately the D1 protein dynamics involved in the photosystem II repair cycle. Compelling, though indirect evidence suggests that the radical pair P(+)(680)Pheo(-) in functional PSII should be protected from oxygen. By analogy to the tentative oxygen channel of cytochrome c oxidase, oxygen may be liberated from the two water molecules bound to the catalytic site of the Mn cluster, via a specific pathway to the membrane surface. The function of the proposed oxygen pathway is to prevent O(2) from having direct access to P(+)(680)Pheo(-) and prevent the generation of singlet oxygen via the triplet-P(680) state in functional photosytem IIs. Only when the, as yet unidentified, potential trigger with a fateful first oxidative step destroys oxygen evolution, will the ensuing cascade of structural perturbations of photosystem II destroy the proposed oxygen, water and proton pathways. Then oxygen has direct access to P(+)(680)Pheo(-), singlet oxygen will be produced and may successively oxidize specific amino acids of the phosphorylated D1 protein of photosystem II dimers that are confined to appressed granal domains, thereby targeting D1 protein for eventual degradation and replacement in non-appressed thylakoid domains.

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Selected References

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  1. Ananyev G. M., Zaltsman L., Vasko C., Dismukes G. C. The inorganic biochemistry of photosynthetic oxygen evolution/water oxidation. Biochim Biophys Acta. 2001 Jan 5;1503(1-2):52–68. doi: 10.1016/s0005-2728(00)00215-2. [DOI] [PubMed] [Google Scholar]
  2. Anderson J. M. Does functional photosystem II complex have an oxygen channel? FEBS Lett. 2001 Jan 12;488(1-2):1–4. doi: 10.1016/s0014-5793(00)02358-9. [DOI] [PubMed] [Google Scholar]
  3. Aro E. M., Virgin I., Andersson B. Photoinhibition of Photosystem II. Inactivation, protein damage and turnover. Biochim Biophys Acta. 1993 Jul 5;1143(2):113–134. doi: 10.1016/0005-2728(93)90134-2. [DOI] [PubMed] [Google Scholar]
  4. Baena-González Elena, Aro Eva-Mari. Biogenesis, assembly and turnover of photosystem II units. Philos Trans R Soc Lond B Biol Sci. 2002 Oct 29;357(1426):1451–1460. doi: 10.1098/rstb.2002.1141. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Barber J., Nield J. Organization of transmembrane helices in photosystem II: comparison of plants and cyanobacteria. Philos Trans R Soc Lond B Biol Sci. 2002 Oct 29;357(1426):1329-35; discussion 1335, 1367. doi: 10.1098/rstb.2002.1132. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Barber J. Photosystem two. Biochim Biophys Acta. 1998 Jun 10;1365(1-2):269–277. doi: 10.1016/s0005-2728(98)00079-6. [DOI] [PubMed] [Google Scholar]
  7. Dekker J. P., Van Grondelle R. Primary charge separation in Photosystem II. Photosynth Res. 2000;63(3):195–208. doi: 10.1023/A:1006468024245. [DOI] [PubMed] [Google Scholar]
  8. Ferguson-Miller Shelagh, Babcock Gerald T. Heme/Copper Terminal Oxidases. Chem Rev. 1996 Nov 7;96(7):2889–2908. doi: 10.1021/cr950051s. [DOI] [PubMed] [Google Scholar]
  9. Haumann M, Junge W. Photosynthetic water oxidation: a simplex-scheme of its partial reactions . Biochim Biophys Acta. 1999 Apr 21;1411(1):86–91. doi: 10.1016/s0005-2728(99)00042-0. [DOI] [PubMed] [Google Scholar]
  10. Hofacker I., Schulten K. Oxygen and proton pathways in cytochrome c oxidase. Proteins. 1998 Jan;30(1):100–107. [PubMed] [Google Scholar]
  11. Horton P., Ruban A. V., Walters R. G. REGULATION OF LIGHT HARVESTING IN GREEN PLANTS. Annu Rev Plant Physiol Plant Mol Biol. 1996 Jun;47(NaN):655–684. doi: 10.1146/annurev.arplant.47.1.655. [DOI] [PubMed] [Google Scholar]
  12. Hummer G., Rasaiah J. C., Noworyta J. P. Water conduction through the hydrophobic channel of a carbon nanotube. Nature. 2001 Nov 8;414(6860):188–190. doi: 10.1038/35102535. [DOI] [PubMed] [Google Scholar]
  13. Iwata S., Ostermeier C., Ludwig B., Michel H. Structure at 2.8 A resolution of cytochrome c oxidase from Paracoccus denitrificans. Nature. 1995 Aug 24;376(6542):660–669. doi: 10.1038/376660a0. [DOI] [PubMed] [Google Scholar]
  14. Jones L. W., Kok B. Photoinhibition of chloroplast reactions. I. Kinetics and action spectra. Plant Physiol. 1966 Jun;41(6):1037–1043. doi: 10.1104/pp.41.6.1037. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Jordan P., Fromme P., Witt H. T., Klukas O., Saenger W., Krauss N. Three-dimensional structure of cyanobacterial photosystem I at 2.5 A resolution. Nature. 2001 Jun 21;411(6840):909–917. doi: 10.1038/35082000. [DOI] [PubMed] [Google Scholar]
  16. Kruse O., Hankamer B., Konczak C., Gerle C., Morris E., Radunz A., Schmid G. H., Barber J. Phosphatidylglycerol is involved in the dimerization of photosystem II. J Biol Chem. 2000 Mar 3;275(9):6509–6514. doi: 10.1074/jbc.275.9.6509. [DOI] [PubMed] [Google Scholar]
  17. Kühlbrandt W., Wang D. N., Fujiyoshi Y. Atomic model of plant light-harvesting complex by electron crystallography. Nature. 1994 Feb 17;367(6464):614–621. doi: 10.1038/367614a0. [DOI] [PubMed] [Google Scholar]
  18. Mulkidjanian AY. Photosystem II of green plants: on the possible role of retarded protonic relaxation in water oxidation1 . Biochim Biophys Acta. 1999 Jan 27;1410(1):1–6. doi: 10.1016/s0005-2728(98)00174-1. [DOI] [PubMed] [Google Scholar]
  19. Nugent J. H., Rich A. M., Evans M. C. Photosynthetic water oxidation: towards a mechanism. Biochim Biophys Acta. 2001 Jan 5;1503(1-2):138–146. doi: 10.1016/s0005-2728(00)00223-1. [DOI] [PubMed] [Google Scholar]
  20. Oxborough K., Baker N. R. An evaluation of the potential triggers of photoinactivation of photosystem II in the context of a Stern-Volmer model for downregulation and the reversible radical pair equilibrium model. Philos Trans R Soc Lond B Biol Sci. 2000 Oct 29;355(1402):1489–1498. doi: 10.1098/rstb.2000.0709. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Rappaport F., Lavergne J. Coupling of electron and proton transfer in the photosynthetic water oxidase. Biochim Biophys Acta. 2001 Jan 5;1503(1-2):246–259. doi: 10.1016/s0005-2728(00)00228-0. [DOI] [PubMed] [Google Scholar]
  22. Renger G. Photosynthetic water oxidation to molecular oxygen: apparatus and mechanism. Biochim Biophys Acta. 2001 Jan 5;1503(1-2):210–228. doi: 10.1016/s0005-2728(00)00227-9. [DOI] [PubMed] [Google Scholar]
  23. Riistama S., Puustinen A., García-Horsman A., Iwata S., Michel H., Wikström M. Channelling of dioxygen into the respiratory enzyme. Biochim Biophys Acta. 1996 Jul 18;1275(1-2):1–4. doi: 10.1016/0005-2728(96)00040-0. [DOI] [PubMed] [Google Scholar]
  24. Schatz G. H., Brock H., Holzwarth A. R. Kinetic and Energetic Model for the Primary Processes in Photosystem II. Biophys J. 1988 Sep;54(3):397–405. doi: 10.1016/S0006-3495(88)82973-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Sui H., Han B. G., Lee J. K., Walian P., Jap B. K. Structural basis of water-specific transport through the AQP1 water channel. Nature. 2001 Dec 20;414(6866):872–878. doi: 10.1038/414872a. [DOI] [PubMed] [Google Scholar]
  26. Telfer Alison. What is beta-carotene doing in the photosystem II reaction centre? Philos Trans R Soc Lond B Biol Sci. 2002 Oct 29;357(1426):1431-39; discussion 1439-40, 1469-70. doi: 10.1098/rstb.2002.1139. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Tsukihara T., Aoyama H., Yamashita E., Tomizaki T., Yamaguchi H., Shinzawa-Itoh K., Nakashima R., Yaono R., Yoshikawa S. Structures of metal sites of oxidized bovine heart cytochrome c oxidase at 2.8 A. Science. 1995 Aug 25;269(5227):1069–1074. doi: 10.1126/science.7652554. [DOI] [PubMed] [Google Scholar]
  28. Tsukihara T., Aoyama H., Yamashita E., Tomizaki T., Yamaguchi H., Shinzawa-Itoh K., Nakashima R., Yaono R., Yoshikawa S. The whole structure of the 13-subunit oxidized cytochrome c oxidase at 2.8 A. Science. 1996 May 24;272(5265):1136–1144. doi: 10.1126/science.272.5265.1136. [DOI] [PubMed] [Google Scholar]
  29. Zouni A., Witt H. T., Kern J., Fromme P., Krauss N., Saenger W., Orth P. Crystal structure of photosystem II from Synechococcus elongatus at 3.8 A resolution. Nature. 2001 Feb 8;409(6821):739–743. doi: 10.1038/35055589. [DOI] [PubMed] [Google Scholar]

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