Role of charge recombination processes in photodamage and photoprotection of the photosystem II complex

Physiologia Plantarum

Volumn 142, Issue 1, 2011, Pages 6-16

  Vass, Imre ^a  

^a INSTITUTE OF BIOCHEMISTRY   (Hungary)

Author keywords

[No Author keywords available]

Indexed keywords

SINGLET OXYGEN;

ARTICLE; ELECTRON; LIGHT; METABOLISM; OXIDATION REDUCTION REACTION; PHOTOSYNTHESIS; PHOTOSYSTEM II; RADIATION EXPOSURE;

ELECTRONS; LIGHT; OXIDATION-REDUCTION; PHOTOSYNTHESIS; PHOTOSYSTEM II PROTEIN COMPLEX; SINGLET OXYGEN;

EID: 79954575978     PISSN: 00319317     EISSN: 13993054     Source Type: Journal    
DOI: 10.1111/j.1399-3054.2011.01454.x     Document Type: Article

References (82)

1. Adir N, Zer H, Shochat S, Ohad I (2003) Photoinhibition - a historical perspective. Photosynth Res 76: 343-370
2. Andersson B, Styring S (1991) Photosystem II: molecular organization, function, and acclimation. Curr Top Bioenerg 16: 1-81
3. Aro E-M, Virgin I Andersson B (1993) Photoinhibition of photosystem II. Inactivation, protein damage and turnover. Biochim Biophys Acta 1143: 113-134
4. Asada K (1999) The water-water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons. Annu Rev Plant Physiol 50: 601-639
5. Bumann D, Oesterhelt D (1995) Destruction of a single chlorophyll is correlated with the photoinhibition of photosystem II with a transiently inactive donor side. Proc Natl Acad Sci USA 92: 12195-12199
6. Cser K, Vass I (2007) Radiative and non-radiative charge recombination pathways in photosystem II studied by thermoluminescence and chlorophyll fluorescence in the cyanobacterium Synechocystis 6803. Biochim Biophys Acta 1767: 233-243
7. Cser K, Vass I (2008) Regulation of photoprotection by non-radiative charge recombination in photosystem II. In: Allen JF, Gantt E, Golbeck JH, Osmond B (eds) Photosynthesis Energy from the Sun. Springer, Dordrecht, pp 47-50
8. Debus RJ (1992) The manganese and calcium ions of photosynthetic oxygen evolution. Biochim Biophys Acta 1102: 269-352
9. Ferreira KN, Iverson TM, Maghlaoui K, Barber J, Iwata S (2004) Architecture of the photosynthetic oxygen-evolving center. Science 303: 1831-1838
10. Frank HA, Cogdell RJ (1996) Carotenoids in photosynthesis. Photochem Photobiol 63: 257-264
11. Fufezan C, Rutherford AW, Krieger-Liszkay A (2002) Singlet oxygen production in herbicide-treated photosystem II. FEBS Lett 532: 407-410
12. Fufezan C, Gross CM, Sjödin M, Rutherford AW, Krieger-Liszkay A, Kirilovsky D (2007) Influence of the redox potential of the primary quinone electron acceptor on photoinhibition in photosystem II. J Biol Chem 282: 12492-12502
13. Golden SS (1995) Light-responsive gene expression in cyanobacteria. J Bacteriol 177: 1651-1654
14. Guskov A, Kern J, Gabdulkhakov A, Broser M, Zouni A, Saenger W (2009) Cyanobacterial photosystem II at 2.9-Å resolution and the role of quinones, lipids, channels and chloride. Nat Struct Mol Biol 16: 334-342
15. Hakala M, Tuominen I, Keranen M, Tyystjarvi T, Tyystjarvi E (2005) Evidence for the role of the oxygen-evolving manganese complex in photoinhibition of photosystem II. Biochim Biophys Acta 1706: 68-80
16. Hideg É, Spetea C, Vass I (1994) Singlet oxygen and free radical production during acceptor- and donor-side-induced photoinhibition. Studies with spin trapping EPR spectroscopy. Biochim Biophys Acta 1186: 143-152
17. Hideg É, Kálai T, Hideg K, Vass I (1998) Photoinhibition of photosynthesis in vivo results in singlet oxygen production. Detection via nitroxide-induced fluorescence quenching in broad bean leaves. Biochemistry 37: 11405-11411
18. Hideg É, Vass I, Kálai T, Hideg K (2000) Singlet oxygen detection with sterically hindered amine derivatives in plants under light stress. Methods Enzymol 319: 77-85
19. Hideg É, Kós PB, Vass I (2007) Photosystem II damage induced by chemically generated singlet oxygen in tobacco leaves. Physiol Plant 131: 33-40
20. Hoganson CW, Babcock GT (1997) A metalloradical mechanism for the generation of oxygen from water in photosynthesis. Science 277: 1953-1956
21. Ivanov AG, Sane PV, Hurry V, Öquist G, Huner NPA (2008) Photosystem II reaction centre quenching: mechanisms and physiological role. Photosynth Res 98: 565-574
22. A in photosystem II associated with photoactivation of oxygen evolution. Biochim Biophys Acta 1229: 202-207
23. Kamiya N, Shen J-R (2003) Crystal structure of oxygen-evolving photosystem II from Thermosynechococcus vulcanus at 3.7-Å resolution. Proc Natl Acad Sci USA 100: 98-103
24. Keren N, Gong H, Ohad I (1995a) Oscillations of reaction center II-D1 protein degradation in vivo induced by repetitive light flashes. Correlation between the level of RCII-Q and protein degradation in low light. J Biol Chem 270: 806-814
25. Keren N, van Kan PJM, Berg A, Gong H, Schochat S, Levanon H, Styring S, Andersson B, Ohad I (1995b) On the mechanism of the low-light induced degradation of the D1 protein: involvement of back electron transfer in photosystem II. Photosynth Res 4: 299-302
26. Keren N, Berg A, van Kan PJM, Levanon H, Ohad I (1997) Mechanism of photosystem II photoinactivation and D1 protein degradation at low light: the role of back electron flow. Proc Natl Acad Sci USA 94: 1579-1584
27. Keren N, Ohad I, Rutherford AW, Drepper F, 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
28. Kornyeyev D, Logan BA, Holaday AS (2010) Excitation pressure as a measure of the sensitivity of photosystem II to photoinactivation. Funct Plant Biol 37: 943-951
29. Kós PB, Deák Z, Cheregi O, Vass I (2008) Differential regulation of psbA and psbD gene expression, and the role of the different D1 protein copies in the cyanobacterium Thermosynechococcus elongatus BP-1. Biochim Biophys Acta 1777: 74-83
30. A and susceptibility to photodamage. Biochim Biophys Acta 1319: 91-98
31. Krieger A, Weis E (1992) Energy-dependent quenching of chlorophyll-a-fluorescence: the involvement of proton-calcium exchange at photosystem II. Photosynthetica 27: 89-98
32. Krieger-Liszkay A (2005) Singlet oxygen production in photosynthesis. J Exp Bot 56: 337-346
33. Krieger-Liszkay A, Rutherford AW (1998) Influence of herbicide binding on the redox potential of the quinone acceptor in photosystem II: relevance to photodamage and phytotoxicity. Biochemistry 37: 17339-17344
34. Krieger-Liszkay A, Fufezan C, Trebst A (2008) Singlet oxygen production in photosystem II and related protection mechanism. Photosynth Res 98: 551-564
35. Kyle DJ, Ohad I, Arntzen CJ (1984) Membrane protein damage and repair: Selective loss of a quinone-protein function in chloroplast membranes. Proc Natl Acad Sci USA 81: 4070-4074
36. Larkum AWD, Karge M, Reifarth F, Eckert H-J, Post A, Renger G (2001) Effect of monochromatic UV-B radiation on electron transfer reactions of photosystem II. Photosynth Res 68: 49-60
37. Li X-P, Bjorkman O, Shih C, Grossman AR, Rosenquist M, Jansson S, Niyogi KK (2000) A pigment-binding protein essential for regulation of photosynthetic light harvesting. Nature 403: 391-395
38. Loll B, Kern J, Saenger W, Zouni A, Biesiadka J (2005) Towards complete cofactor arrangement in the 3.0 Å resolution structure of photosystem II. Nature 438: 1040-1044
39. Loll B, Broser M, Kós PB, Kern J, Biesiadka J, Vass I, Saenger W, Zouni A (2008) Modeling of variant copies of subunit D1 in the structure of photosystem II from Thermosynechococcus elongatus. Biol Chem 389: 609-617
40. Macpherson AN, Telfer A, Barber J, Truscott TG (1993) Direct detection of singlet oxygen from isolated photosystem II reaction centres. Biochim Biophys Acta 1143: 301-309
41. 2 branch in photosystem II cores with closed reaction centers. Photochem Photobiol Sci 7: 1337-1343
42. Merry SAP, Nixon PJ, Barter LMC, Schilstra M, Porter G, Barber J (1998) Modulation of quantum yield of primary radical pair formation in photosystem II by site-directed mutagenesis affecting radical cations and anions. Biochemistry 37: 17439-17447
43. xCa structures for the catalytic site and spectroscopic data. Phys Chem Chem Phys 6: 4764-4771
44. Müller P, Li X-P, Niyogi KK (2001) Non-photochemical quenching. A response to excess light energy. Plant Physiol 125: 1558-1566
45. Nishiyama Y, Allakhverdiev SI, Murata N (2005) Inhibition of the repair of photosystem II by oxidative stress in cyanobacteria. Photosynth Res 84: 1-7
46. Nixon PJ, Michoux F, Yu J, Boehm M, Komenda J (2010) Recent advances in understanding the assembly and repair of photosystem II. Ann Bot 106: 1-16
47. Ohad I, Raanan H, Keren N, Tchernov D, Kaplan A (2010) Light-induced changes within photosystem II protects Microcoleus sp. in biological desert sand crusts against excess light. PLoS One 5: e11000
48. Ohnishi N, Allakhverdiev SI, Takahashi S, Higashi S, Watanabe M, Nishiyama Y, Murata N (2005) Two-step mechanism of photodamage to photosystem II: step 1 occurs at the oxygen-evolving complex and step 2 occurs at the photochemical reaction center. Biochemistry 44: 8494-8499
49. Peers G, Truong TB, Ostendorf E, Busch A, Elrad D, Grossman AR, Hippler M, Niyogi KK (2009) An ancient light-harvesting protein is critical for the regulation of algal photosynthesis. Nature 462: 518-522
50. Pospísil P (2009) Production of reactive oxygen species by photosystem II. Biochim Biophys Acta 1787: 1151-1160
51. Rappaport F, Guergova-Kuras M, Nixon PJ, Diner BA, Lavergne J (2002) Kinetics and pathways of charge recombination in Photosystem II. Biochemistry 41: 8518-8527
52. Renger G (1997) Mechanistic and structural aspects of photosynthetic water oxidation. Physiol Plant 100: 828-841
53. Renger G (2007) Oxidative photosynthetic water splitting: energetics, kinetics and mechanism. Photosynth Res 92: 407-425
54. Renger G, Völker M, Eckert HJ, Fromme R, Hohm-Veit S, Graber P (1989) On the mechanism of photosystem II deterioration by UV-B irradiation. Photochem Photobiol 49: 97-105
55. Rinalducci S, Pedersen JZ, Zolla L (2004) Formation of radicals from singlet oxygen produced during photoinhibition of isolated light-harvesting proteins of photosystem II. Biochim Biophys Acta 1608: 63-73
56. Rutherford AW, Krieger-Liszkay A (2001) Herbicide-induced oxidative stress in photosystem II. Trends Biochem Sci 26: 648-653
57. Sander J, Nowaczyk M, Buchta J, Dau H, Vass I, Deak Z, Dorogi M, Iwai M, Rögner M (2010) Functional characterization and quantification of the alternative PsbA copies in Thermosynechococcus elongatus and their role in photoprotection. J Biol Chem 285: 29851-29856
58. B. J Biol Chem 277: 32739-32745
59. Sane PV, Ivanov AG, Hurry V, Huner NPA, Oquist G (2003) Changes in the redox potential of primary and secondary electron-accepting quinones in photosystem II confer increased resistance to photoinhibition in low-temperature-acclimated Arabidopsis. Plant Physiol 132: 2144-2151
60. Santabarbara S, Neverov KV, Garlaschi FM, Zucchelli G, Jennings RC (2001) Involvement of uncoupled antenna chlorophylls in photoinhibition in thylakoids. FEBS Lett 491: 109-113
61. Sarvikas P, Hakala-Yatkin M, Dönmez S, Tyystjärvi E (2010) Short flashes and continuous light have similar photoinhibitory efficiency in intact leaves. J Exp Bot 61: 4239-4247
62. Schatz GH, Brock H, Holzwarth AR (1988) Kinetic and energetic model for the primary processes in photosystem II. Biophys J 54: 397-405
63. Scheller HV, Haldrup A (2005) Photoinhibition of photosystem I. Planta 221: 5-8
64. 3 gene. Biochim Biophys Acta 1797: 1491-1499
65. Szilárd A, Sass L, Hideg É, Vass I (2005) Photoinactivation of photosystem II by flashing light. Photosynth Res 84: 15-20
66. Takahashi S, Milward SE, Fan D-Y, Chow WS, Badger MR (2009) How does cyclic electron flow alleviate photoinhibition in Arabidopsis? Plant Physiol 149: 1560-1567
67. Tichy M, Lupínková L, Sicora C, Vass I, Kuvikova S, Prasil O, Komenda J (2003) Synechocystis 6803 mutants expressing distinct forms of the photosystem II D1 protein from Synechococcus 7942: relationship between the psbA coding region and sensitivity to visible and UV-B radiation. Biochim Biophys Acta 1605: 55-66
68. Triantaphylides C, Havaux M (2009) Singlet oxygen in plants: production, detoxification and signaling. Trends Plant Sci 14: 219-228
69. Triantaphylides C, Krischke M, Hoeberichts FA, Ksas B, Gresser G, Havaux M, Van Breusegem F, Mueller MJ (2008) Singlet oxygen is the major reactive oxygen species involved in photooxidative damage to plants. Plant Physiol 148: 960-968
70. Tyystjarvi E (2008) Photoinhibition of photosystem II and photodamage of the oxygen evolving manganese cluster. Coord Chem Rev 252: 361-376
71. Tyystjarvi E, Aro EM (1996) The rate constant of photoinhibition, measured in lincomycin-treated leaves, is directly proportional to light intensity. Proc Natl Acad Sci USA 93: 2213-2218
72. van Gorkom HJ (1985) Electron transfer in photosystem II. Photosynth Res 6: 97-112
73. van Mieghem FJE, Nitschke W, Mathis P, Rutherford AW (1989) The influence of the quinone-iron electron acceptor complex on the reaction centre photochemistry of photosystem II. Biochim Biophys Acta 977: 207-214
74. van Mieghem F, Brettel K, Hillmann B, Kamlowski A, Rutherford AW, Schlodder E (1995) Charge recombination reactions in photosystem II. 1. Yields, recombination pathways, and kinetics of the primary pair. Biochemistry 34: 4798-4813
75. Vass I, Cser K (2009) Janus-faced charge recombinations in photosystem II photoinhibition. Trends Plant Sci 14: 200-205
76. Vass I, Styring S (1993) Characterization of chlorophyll triplet promoting states in photosystem II sequentially induced during photoinhibition. Biochemistry 32: 3334-3341
77. A species promote chlorophyll triplet formation. Proc Natl Acad Sci USA 89: 1408-1412
78. Vass I, Sass L, Spetea C, Bakou A, Ghanotakis D, Petrouleas V (1996) UV-B induced inhibition of photosystem II electron transport studied by EPR and chlorophyll fluorescence. Impairment of donor and acceptor side components. Biochemistry 35: 8964-8973
79. Vass I, Turcsányi E, Touloupakis E, Ghanotakis D, Petroluleas V (2002) The mechanism of UV-A radiation-induced inhibition of photosystem II electron transport studied by EPR and chlorophyll fluorescence. Biochemistry 41: 10200-10208
80. Virgin I, Styring S, Andersson B (1988) Photosystem II disorganization and manganese release after photoinhibition of isolated spinach thylakoid membranes. FEBS Lett 233: 408-412
81. Wilson A, Ajlani G, Verbavatz J-M, Vass I, Kerfeld CA, Kirilovsky D (2006) A soluble carotenoid protein involved in phycobilisome-related energy dissipation in cyanobacteria. Plant Cell 18: 992-107
82. Zouni A, Witt HT, Kern J, Fromme P, Kraus N, Saenger W, Orth P (2001) Crystal structure of photosystem II from Synechococcus elongatus at 3.8 Å resolution. Nature 409: 739-743