Recent advances in understanding the assembly and repair of photosystem II

Annals of Botany

Volumn 106, Issue 1, 2010, Pages 1-16

  Nixon, Peter J ^a   Michoux, Franck ^a   Yu, Jianfeng ^a   Boehm, Marko ^a   Komenda, Josef ^b  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b INSTITUTE OF MICROBIOLOGY   (Czech Republic)

Author keywords

Assembly factor; D1 turnover; Deg protease; FtsH protease; Membrane protein; Photoinhibition; Photosynthesis; Photosystem II

Indexed keywords

BACTERIAL PROTEIN; PHOTOSYSTEM II;

BIODEGRADATION; CHLOROPLAST; CYANOBACTERIUM; DIVERGENCE; ENVIRONMENTAL STRESS; ENZYME ACTIVITY; LIGHT EFFECT; MEMBRANE; NUMERICAL MODEL; PHOTOINHIBITION; PHOTOSYNTHESIS; PROTEIN;

BIOLOGICAL MODEL; CYANOBACTERIUM; METABOLISM; PHOTOSYNTHESIS; PHOTOSYSTEM II; PHYSIOLOGY; REVIEW;

BACTERIAL PROTEINS; CYANOBACTERIA; MODELS, BIOLOGICAL; PHOTOSYNTHESIS; PHOTOSYSTEM II PROTEIN COMPLEX;

CYANOBACTERIA; EMBRYOPHYTA; SYNECHOCYSTIS SP. PCC 6803;

EID: 77956375190     PISSN: 03057364     EISSN: 10958290     Source Type: Journal    
DOI: 10.1093/aob/mcq059     Document Type: Review

References (157)

1. Adam Z, Clarke AK. 2002. Cutting edge of chloroplast proteolysis. Trends in Plant Science 7:451-456.
2. Adam Z, Zaltsman A, Sinvany-Villalobo G, Sakamoto W. 2005. FtsH proteases in chloroplasts and cyanobacteria. Physiologia Plantarum 123:386-390.
3. Adir N, Zer H, Shochat S, Ohad I. 2003. Photoinhibition - a historical perspective. Photosynthesis Research 76:343-370.
4. Akiyama Y, Ito K. 2003. Reconstitution of membrane proteolysis by FtsH. Journal of Biological Chemistry 278:18146-18153.
5. Anbudurai PR, Mor TS, Ohad I, Shestakov SV, Pakrasi HB. 1994. The ctpA gene encodes the C-terminal processing protease for the D1 protein of the photosystem-II reaction-center complex. Proceedings of the National Academy of Sciences, USA 91:8082-8086.
6. Aro EM, Virgin I, Andersson B. 1993. Photoinhibition of photosystem 2 - inactivation, protein damage and turnover. Biochimica et Biophysica Acta 1143:113-134.
7. Aro EM, Suorsa M, Rokka A, et al. 2005. Dynamics of photosystem II: a proteomic approach to thylakoid protein complexes. Journal of Experimental Botany 56:347-356.
8. Bailey S, Thompson E, Nixon PJ, et al. 2002. A critical role for the Var2 FtsH homologue of Arabidopsis thaliana in the photosystem II repair cycle in vivo. Journal of Biological Chemistry 277:2006-2011.
9. Barber J, Andersson B. 1992. Too much of a good thing - light can be bad for photosynthesis. Trends in Biochemical Sciences 17:61-66.
10. Barber J, Iwata S. 2005. Refined X-ray structure of photosystem II and its implications. In: Wydrzynski T, Satoh K. eds. Photosystem II: the lightdriven water: plastoquinone oxidoreductase. Springer: The Netherlands, 469-489.
11. Barker M, de Vries R, Nield J, Komenda J, Nixon PJ. 2006. The Deg proteases protect Synechocystis sp PCC 6803 during heat and light stresses but are not essential for removal of damaged D1 protein during the photosystem two repair cycle. Journal of Biological Chemistry 281:30347-30355.
12. Barker M, Boehm M, Nixon PJ, Nield J. 2008. Structural analysis of an FtsH2/FtsH3 complex isolated from Synechocystis sp. PCC 6803. In: Allen JF, Gantt E, Golbeck JH, Osmond B. eds. Photosynthesis. Energy from the sun. 14th International Congress on Photosynthesis. Springer: The Netherlands, 738-740.
13. Bautista JA, Tracewell CA, Schlodder E, Cunningham FX, Brudvig GW, Diner BA. 2005. Construction and characterization of genetically modified Synechocystis sp. PCC 6803 photosystem II core complexes containing carotenoids with shorter pi-conjugation than beta-carotene. Journal of Biological Chemistry 280:38839-38850.
14. Bentley FK, Luo H, Dilbeck P, Burnap RL, Eaton-Rye JJ. 2008. Effects of inactivating psbM and psbT on photodamage and assembly of photosystem II in Synechocystis sp PCC 6803. Biochemistry 47:11637-11646.
15. Boehm M, Nield J, Zhang PP, Aro EM, Komenda J, Nixon PJ. 2009. Structural and mutational analysis of Band 7 proteins in the cyanobacterium Synechocystis sp strain PCC 6803. Journal of Bacteriology 191:6425-6435.
16. 2O oxidation complex in Synechocystis sp. PCC6803. Biochemistry 35:874-882.
17. Canovas PM, Barber J. 1993. Detection of a 10 kDa breakdown product containing the c-terminus of the D1-protein in photoinhibited wheat leaves suggests an acceptor side mechanism. FEBS Letters 324:341-344.
18. Chen H, Zhang DY, Guo JK, et al. 2006. A Psb27 homologue in Arabidopsis thaliana is required for efficient repair of photodamaged photosystem II. Plant Molecular Biology 61:567-575.
19. Cheregi O, Sicora C, Kos PB, Barker M, Nixon PJ, Vass I. 2007. The role of the FtsH and Deg proteases in the repair of UV-B radiation-damaged photosystem II in the cyanobacterium Synechocystis PCC 6803. Biochimica et Biophysica Acta 1767:820-828.
20. Cormann KU, Bangert JA, Ikeuchi M, Rogner M, Stoll R, Nowaczyk MM. 2009. Structure of Psb27 in solution: implications for transient binding to photosystem II during biogenesis and repair. Biochemistry 48:8768-8770.
21. Daley DO. 2008. The assembly of membrane proteins into complexes. Current Opinion in Structural Biology 18:420-424.
22. De Las Rivas J, Roman A. 2005. Structure and evolution of the extrinsic proteins that stabilize the oxygen-evolving engine. Photochemical and Photobiological Sciences 4:1003-1010.
23. Dewez D, Park S, Garcia-Cerdan JG, Lindberg P, Melis A. 2009. Mechanism of REP27 protein action in the D1 protein turnover and photosystem II repair from photodamage. Plant Physiology 151:88-99.
24. Dobakova M, Tichy M, Komenda J. 2007. Role of the PsbI protein in photosystem II assembly and repair in the cyanobacterium Synechocystis sp PCC 6803. Plant Physiology 145:1681-1691.
25. Dobakova M, Sobotka R, Tichy M, Komenda J. 2009. Psb28 protein is involved in the biogenesis of the photosystem II inner antenna CP47 (PsbB) in the cyanobacterium Synechocystis sp PCC 6803. Plant Physiology 149:1076-1086.
26. Dolganov NAM, Bhaya D, Grossman AR. 1995. Cyanobacterial protein with similarity to the chlorophyll a/b binding-proteins of higher-plants - evolution and regulation. Proceedings of the National Academy of Sciences, USA 92:636-640.
27. Drath M, Kloft N, Batschauer A, Marin K, Novak J, Forchhammer K. 2008. Ammonia triggers photodamage of photosystem II in the cyanobacterium Synechocystis sp. strain PCC 6803. Plant Physiology 147:206-215.
28. Edelman M, Mattoo AK. 2008. D1-protein dynamics in photosystem II: the lingering enigma. Photosynthesis Research 98:609-620.
29. Enami I, Okumura A, Nagao R, Suzuki T, Iwai M, Shen JR. 2008. Structures and functions of the extrinsic proteins of photosystem II from different species. Photosynthesis Research 98:349-363.
30. Ermakova-Gerdes S, Vermaas W. 1999. Inactivation of the open reading frame slr0399 in Synechocystis sp PCC 6803 functionally complements mutations near the Q (A) niche of photosystem II - a possible role of slr0399 as a chaperone for quinone binding. Journal of Biological Chemistry 274:30540-30549.
31. 559, chlorophyll Z and β-carotene. In: Wydrzynski T, Satoh K. eds. Photosystem II: the light-driven water: plastoquinone oxidoreductase. Springer: The Netherlands, 347-365.
32. Ferreira KN, Iverson TM, Maghlaoui K, Barber J, Iwata S. 2004. Architecture of the photosynthetic oxygen-evolving center. Science 303:1831-1838.
33. Funk C, Vermaas W. 1999. A cyanobacterial gene family coding for singlehelix proteins resembling part of the light-harvesting proteins from higher plants. Biochemistry 38:9397-9404.
34. Gombos Z, Varkonyi Z, Hagio M, et al. 2002. Phosphatidylglycerol requirement for the function of electron acceptor plastoquinone QB in the photosystem II reaction center. Biochemistry 41:3796-3802.
35. Green BR, Gantt E. 2005. Distal and extrinsic photosystem II antennas In: Wydrzynski T, Satoh K. eds. Photosystem II: the light-driven water: plastoquinone oxidoreductase. Springer: The Netherlands, 23-44.
36. Greenberg BM, Gaba V, Mattoo AK, Edelman M. 1987. Identification of a primary in vivo degradation product of the rapidly-turning-over 32 kd protein of photosystem II. EMBO Journal 6:2865-2869.
37. Guskov A, Kern J, Gabdulkhakov A, Broser M, Zouni A, Saenger W. 2009. Cyanobacterial photosystem II at 2.9-angstrom resolution and the role of quinones, lipids, channels and chloride. Nature Structural and Molecular Biology 16:334-342.
38. Hakala M, Tuominen I, Keränen M, Tyystjärvi T, Tyystjärvi E. 2005. Evidence for the role of the oxygen-evolving manganese complex in photoinhibition of photosystem II. Biochimica et Biophysica Acta 1706:68-80.
39. Haussuhl K, Andersson B, Adamska I. 2001. A chloroplast DegP2 protease performs the primary cleavage of the photodamaged D1 protein in plant photosystem II. EMBO Journal 20:713-722.
40. He QF, Vermaas W. 1998. Chlorophyll a availability affects psbA translation and D1 precursor processing in vivo in Synechocystis sp. PCC 6803. Proceedings of the National Academy of Sciences, USA 95:5830-5835.
41. Henmi T, Iwai M, Ikeuchi M, Kawakami K, Shen JR, Kamiya N. 2008. X-ray crystallographic and biochemical characterizations of a mutant photosystem II complex from Thermosynechococcus vulcanus with the psbTc gene inactivated by an insertion mutation. Journal of Synchrotron Radiation 15:304-307.
42. Huesgen PF, Schuhmann H, Adamska I. 2006. Photodamaged D1 protein is degraded in Arabidopsis mutants lacking the Deg2 protease. FEBS Letters 580:6929-6932.
43. Huesgen PF, Schuhmann H, Adamska I. 2009. Deg/HtrA proteases as components of a network for photosystem II quality control in chloroplasts and cyanobacteria. Research in Microbiology 160:726-732.
44. Inagaki N, Yamamoto Y, Satoh K. 2001. A sequential two-step proteolytic process in the carboxyl-terminal truncation of precursor D1 protein in Synechocystis sp PCC6803. FEBS Letters 509:197-201.
45. Inoue-Kashino N, Takahashi T, Ban A, et al. 2008. Evidence for a stable association of Psb30 (Ycf12) with photosystem II core complex in the cyanobacterium Synechocystis sp PCC 6803. Photosynthesis Research 98:323-335.
46. Ishihara S, Takabayashi A, Ido K, Endo T, Ifuku K, Sato F. 2007. Distinct functions for the two PsbP-like proteins PPL1 and PPL2 in the chloroplast thylakoid lumen of Arabidopsis. Plant Physiology 145:668-679.
47. Ishikawa Y, Schroder WP, Funk C. 2005. Functional analysis of the PsbP-like protein (sll1418) in Synechocystis sp PCC 6803. Photosynthesis Research 84:257-262.
48. Ito K, Akiyama Y. 2005. Cellular functions, mechanism of action, and regulation of FtsH protease. Annual Review of Microbiology 59:211-231.
49. Ivleva NB, Shestakov SV, Pakrasi HB. 2000. The carboxyl-terminal extension of the precursor D1 protein of photosystem II is required for optimal photosynthetic performance of the cyanobacterium Synechocystis sp PCC 6803. Plant Physiology 124:1403-1411.
50. Iwai M, Katayama M, Ikeuchi M. 2006. Absence of the psbH gene product destabilizes the photosystem II complex and prevents association of the photosystem II-X protein in the thermophilic cyanobacterium Thermosynechococcus elongatus BP-1. Photosynthesis Research 87:313-322.
51. Iwai M, Suzuki T, Dohmae N, Inoue Y, Ikeuchi M. 2007. Absence of the PsbZ subunit prevents association of PsbK and Ycf12 with the PSII complex in the thermophilic cyanobacterium Thermosynechococcus elongatus BP-1. Plant and Cell Physiology 48:1758-1763.
52. Kamata T, Hiramoto H, Morita N, Shen JR, Mann NH, Yamamoto Y. 2005. Quality control of photosystem II: an FtsH protease plays an essential role in the turnover of the reaction center D1 protein in Synechocystis PCC 6803 under heat stress as well as light stress conditions. Photochemical and Photobiological Sciences 4:983-990.
53. Kapri-Pardes E, Naveh L, Adam Z. 2007. The thylakoid lumen protease Deg1 is involved in the repair of photosystem II from photoinhibition in Arabidopsis. The Plant Cell 19:1039-1047.
54. Kashino Y, Lauber WM, Carroll JA, et al. 2002. Proteomic analysis of a highly active photosystem II preparation from the cyanobacterium Synechocystis sp PCC 6803 reveals the presence of novel polypeptides. Biochemistry 41:8004-8012.
55. Kato Y, Miura E, Ido K, Ifuku K, Sakamoto W. 2009. The variegated mutants lacking chloroplastic FtsHs are defective in D1 degradation and accumulate reactive oxygen species. Plant Physiology 151:1790-1801.
56. Katoh H, Ikeuchi M. 2001. Targeted disruption of psbX and biochemical characterization of photosystem II complex in the thermophilic cyanobacterium Synechococcus elongatus. Plant and Cell Physiology 42:179-188.
57. Kawabata Y, Henmi T, Iwai M, et al. 2007. Crystal structure analysis of a mutant photosystem II complex lacking PsbM from Thermosynechococcus vulcanus. Plant and Cell Physiology 48:S97.
58. Kawakami K, Iwai M, Ikeuchi M, Kamiya N, Shen JR. 2007. Location of PsbY in oxygen-evolving photosystem II revealed by mutagenesis and X-ray crystallography. FEBS Letters 581:4983-4987.
59. Keren N, Berg A, Vankan PJM, Levanon H, Ohad I. 1997. Mechanism of photosystem II photoinactivation and D1 protein degradation at low light: the role of back electron flow. Proceedings of the National Academy of Sciences, USA 94:1579-1584.
60. Keren N, Liberton M, Pakrasi HB. 2005a. Photochemical competence of assembled photosystem II core complex in cyanobacterial plasma membrane. Journal of Biological Chemistry 280:6548-6553.
61. Keren N, Ohkawa H, Welsh EA, Liberton M, Pakrasi HB. 2005b. Psb29, a conserved 22-kD protein, functions in the biogenesis of photosystem II complexes in Synechocystis and Arabidopsis. The Plant Cell 17:2768-2781.
62. Kim J, Eichacker LA, Rudiger W, Mullet JE. 1994. Chlorophyll regulates accumulation of the plastid-encoded chlorophyll proteins P700 and D1 by increasing apoprotein stability. Plant Physiology 104:907-916.
63. Klinkert B, Ossenbuhl F, Sikorski M, Berry S, Eichacker L, Nickelsen J. 2004. PratA, a periplasmic tetratricopeptide repeat protein involved in biogenesis of photosystem II in Synechocystis sp PCC 6803. Journal of Biological Chemistry 279:44639-44644.
64. Komenda J, Barber J. 1995. Comparison of PsbO and PsbH deletion mutants of Synechocystis PCC-6803 indicates that degradation of D1 protein is regulated by the Q (B) site and dependent on protein-synthesis. Biochemistry 34:9625-9631.
65. Komenda J, Hassan HAG, Diner BA, Debus RJ, Barber J, Nixon PJ. 2000. Degradation of the photosystem II D1 and D2 proteins in different strains of the cyanobacterium Synechocystis PCC 6803 varying with respect to the type and level of psbA transcript. Plant Molecular Biology 42:635-645.
66. Komenda J, Reisinger V, Muller BC, Dobakova M, Granvogl B, Eichacker LA. 2004. Accumulation of the D2 protein is a key regulatory step for assembly of the photosystem II reaction center complex in Synechocystis PCC 6803. Journal of Biological Chemistry 279:48620-48629.
67. Komenda J, Tichy M, Eichacker LA. 2005. The PsbH protein is associated with the inner antenna CP47 and facilitates D1 processing and incorporation into PSII in the cyanobacterium Synechocystis PCC 6803. Plant and Cell Physiology 46:1477-1483.
68. Komenda J, Barker M, Kuvikova S, et al. 2006. The FtsH protease slr0228 is important for quality control of photosystem II in the thylakoid membrane of Synechocystis sp PCC 6803. Journal of Biological Chemistry 281:1145-1151.
69. Komenda J, Kuvikova S, Granvogl B, Eichacker LA, Diner BA, Nixon PJ. 2007a. Cleavage after residue Ala352 in the C-terminal extension is an early step in the maturation of the D1 subunit of photosystem II in Synechocystis PCC 6803. Biochimica et Biophysica Acta 1767:829-837.
70. Komenda J, Tichy M, Prasil O, et al. 2007b. The exposed N-terminal tail of the D1 subunit is required for rapid D1 degradation during photosystem II repair in Synechocystis sp PCC 6803. The Plant Cell 19:2839-2854.
71. Komenda J, Nickelsen J, Tichy M, Prasil O, Eichacker LA, Nixon PJ. 2008. The cyanobacterial homologue of HCF136/YCF48 is a component of an early photosystem II assembly complex and is important for both the efficient assembly and repair of photosystem II in Synechocystis sp PCC 6803. Journal of Biological Chemistry 283:22390-22399.
72. 4 cluster. Biochimica et Biophysica Acta, in press. doi:10.1016/j.bbabio.2010.02.006.
73. Krieger-Liszkay A, Fufezan C, Trebst A. 2008. Singlet oxygen production in photosystem II and related protection mechanism. Photosynthesis Research 98:551-564.
74. Kruse O, Hankamer B, Konczak C, et al. 2000. Phosphatidylglycerol is involved in the dimerization of photosystem II. Journal of Biological Chemistry 275:6509-6514.
75. Kufryk GI, Vermaas WFJ. 2001. A novel protein involved in the functional assembly of the oxygen-evolving complex of photosystem II in Synechocystis sp PCC 6803. Biochemistry 40:9247-9255.
76. Kufryk GI, Vermaas WFJ. 2003. Slr2013 is a novel protein regulating functional assembly of photosystem II in Synechocystis sp strain PCC 6803. Journal of Bacteriology 185:6615-6623.
77. Kufryk G, Hernandez-Prieto MA, Kieselbach T, Miranda H, Vermaas W, Funk C. 2008. Association of small CAB-like proteins (SCPs) of Synechocystis sp PCC 6803 with photosystem II. Photosynthesis Research 95:135-145.
78. Kunkel DD. 1982. Thylakoid centers: structures associated with the cyanobacterial photosynthetic membrane system. Archives of Microbiology 133:97-99.
79. Kuvikova S, Tichy M, Komenda J. 2005. A role of the C-terminal extension of the photosystem II D1 protein in sensitivity of the cyanobacterium Synechocystis PCC 6803 to photoinhibition. Photochemical and Photobiological Sciences 4:1044-1048.
80. Laczko-Dobos H, Ughy B, Toth SZ, et al. 2008. Role of phosphatidylglycerol in the function and assembly of photosystem II reaction center, studied in a cdsA-inactivated PAL mutant strain of Synechocystis sp. PCC6803 that lacks phycobilisomes. Biochimica et Biophysica Acta 1777:1184-1194.
81. Liberton M, Berg RH, Heuser J, Roth R, Pakrasi HB. 2006. Ultrastructure of the membrane systems in the unicellular cyanobacterium Synechocystis sp strain PCC 6803. Protoplasma 227:129-138.
82. Lindahl M, Spetea C, Hundal T, Oppenheim AB, Adam Z, Andersson B. 2000. The thylakoid FtsH protease plays a role in the light-induced turnover of the photosystem II D1 protein. The Plant Cell 12:419-431.
83. Loll B, Kern J, Saenger W, Zouni A, Biesiadka J. 2005. Towards complete cofactor arrangement in the 3.0 angstrom resolution structure of photosystem II. Nature 438:1040-1044.
84. Loll B, Kern J, Saenger W, Zouni A, Biesiadka J. 2007. Lipids in photosystem II: interactions with protein and cofactors. Biochimica et Biophysica Acta 1767:509-519.
85. Lundin B, Hansson M, Schoefs B, Vener AV, Spetea C. 2007. The Arabidopsis PsbO2 protein regulates dephosphorylation and turnover of the photosystem II reaction centre D1 protein. The Plant Journal 49:528-539.
86. Lundin B, Nurmi M, Rojas-Stuetz M, Aro EM, Adamska I, Spetea C. 2008. Towards understanding the functional difference between the two PsbO isoforms in Arabidopsis thaliana - insights from phenotypic analyses of psbO knockout mutants. Photosynthesis Research 98:405-414.
87. Lupinkova L, Komenda J. 2004. Oxidative modifications of the photosystem II D1 protein by reactive oxygen species: from isolated protein to cyanobacterial cells. Photochemistry and Photobiology 79:152-162.
88. Ma JF, Peng LW, Guo JK, Lu QT, Lu CM, Zhang LX. 2007. LPA2 is required for efficient assembly of photosystem II in Arabidopsis thaliana. The Plant Cell 19:1980-1993.
89. Mabbitt PD, Rautureau GJP, Day CL, Wilbanks SM, Eaton-Rye JJ, Hinds MG. 2009. Solution structure of Psb27 from cyanobacterial photosystem II. Biochemistry 48:8771-8773.
90. Masamoto K, Hisatomi S, Sakurai I, Gombos Z, Wada H. 2004. Requirement of carotene isomerization for the assembly of photosystem II in Synechocystis sp PCC 6803. Plant and Cell Physiology 45:1325-1329.
91. van de Meene AML, Hohmann-Marriott MF, Vermaas WFJ, Roberson RW. 2006. The three-dimensional structure of the cyanobacterium Synechocystis sp PCC 6803. Archives of Microbiology 184:259-270.
92. Metz JG, Nixon PJ, Rogner M, Brudvig GW, 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-donor, P680. Biochemistry 28:6960-6969.
93. Meurer J, Plucken H, Kowallik KV, Westhoff P. 1998. A nuclear-encoded protein of prokaryotic origin is essential for the stability of photosystem II in Arabidopsis thaliana. EMBO Journal 17:5286-5297.
94. Miyao M. 1994. Involvement of active oxygen species in degradation of the D1 protein under strong illumination in isolated subcomplexes of photosystem II. Biochemistry 33:9722-9730.
95. Mizusawa N, Sakurai I, Sato N, Wada H. 2009. Lack of digalactosyldiacylglycerol increases the sensitivity of Synechocystis sp PCC 6803 to high light stress. FEBS Letters 583:718-722.
96. Muh F, Renger T, Zouni A. 2008. Crystal structure of cyanobacterial photosystem II at 3.0 angstrom resolution: a closer look at the antenna system and the small membrane-intrinsic subunits. Plant Physiology and Biochemistry 46:238-264.
97. Mullineaux CW, Sarcina M. 2002. Probing the dynamics of photosynthetic membranes with fluorescence recovery after photobleaching. Trends in Plant Science 7:237-240.
98. Mulo P, Sirpio S, Suorsa M, Aro EM. 2008. Auxiliary proteins involved in the assembly and sustenance of photosystem II. Photosynthesis Research 98:489-501.
99. Nevo R, Charuvi D, Shimoni E, et al. 2007. Thylakoid membrane perforations and connectivity enable intracellular traffic in cyanobacteria. EMBO Journal 26:1467-1473.
100. Nixon PJ, Trost JT, Diner BA. 1992. Role of the carboxy terminus of polypeptide D1 in the assembly of a functional water-oxidizing manganese cluster in photosystem II of the cyanobacterium Synechocystis sp PCC 6803 - assembly requires a free carboxyl group at C-terminal position 344. Biochemistry 31:10859-10871.
101. Nixon PJ, Barker M, Boehm M, de Vries R, Komenda J. 2005. FtsH-mediated repair of the photosystem II complex in response to light stress. Journal of Experimental Botany 56:357-363.
102. Nowaczyk MM, Hebeler R, Schlodder E, Meyer HE, Warscheid B, Rogner M. 2006. Psb27, a cyanobacterial lipoprotein, is involved in the repair cycle of photosystem II. The Plant Cell 18:3121-3131.
103. Ohad I, Kyle DJ, Arntzen CJ. 1984. Membrane-protein damage and repair - removal and replacement of inactivated 32-kilodalton polypeptide in chloroplast membranes. Journal of Cell Biology 99:481-485.
104. Ohnishi N, Allakhverdiev SI, Takahashi S, et al. 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.
105. Ortega J, Iwanczyk J, Jomaa A. 2009. Escherichia coli DegP: a structuredriven functional model. Journal of Bacteriology 191:4705-4713.
106. Peng LW, Ma JF, Chi W, et al. 2006. LOW PSII ACCUMULATION1 is involved in efficient assembly of photosystem II in Arabidopsis thaliana. The Plant Cell 18:955-969.
107. Ploscher M, Granvogl B, Zoryan M, Reisinger V, Eichacker LA. 2009. Mass spectrometric characterization of membrane integral low molecular weight proteins from photosystem II in barley etioplasts. Proteomics 9:625-635.
108. Plucken H, Muller B, Grohmann D, Westhoff P, Eichacker LA. 2002. The HCF136 protein is essential for assembly of the photosystem II reaction center in Arabidopsis thaliana. FEBS Letters 532:85-90.
109. Promnares K, Komenda J, Bumba L, Nebesarova J, Vacha F, Tichy M. 2006. Cyanobacterial small chlorophyll-binding protein ScpD (HliB) is located on the periphery of photosystem II in the vicinity of PsbH and CP47 subunits. Journal of Biological Chemistry 281:32705-32713.
110. 4Ca cluster and to the evolution of molecular oxygen in photosystem II. Coordination Chemistry Reviews 252:259-272.
111. Rogner M, Chisholm DA, Diner BA. 1991. Site-directed mutagenesis of the psbC gene of photosystem II - isolation and functional characterization of CP43-less photosystem II core complexes. Biochemistry 30:5387-5395.
112. Roose JL, Pakrasi HB. 2008. The Psb27 protein facilitates manganese cluster assembly in photosystem II. Journal of Biological Chemistry 283:4044-4050.
113. Roose JL, Wegener KM, Pakrasi HB. 2007a. The extrinsic proteins of photosystem II. Photosynthesis Research 92:369-387.
114. Roose JL, Kashino Y, Pakrasi HB. 2007b. The PsbQ protein defines cyanobacterial photosystem II complexes with highest activity and stability. Proceedings of the National Academy of Sciences, USA 104:2548-2553.
115. Sakamoto W. 2006. Protein degradation machineries in plastids. Annual Review of Plant Biology 57:599-621.
116. Sakamoto W, Zaltsman A, Adam Z, Takahashi Y. 2003. Coordinated regulation and complex formation of YELLOW VARIEGATED1 and YELLOW VARIEGATED2, chloroplastic FtsH metalloproteases involved in the repair cycle of photosystem II in Arabidopsis thylakoid membranes. The Plant Cell 15:2843-2855.
117. Sakurai I, Hagio M, Gombos Z, Tyystjarvi T, Paakkarinen V, Aro EM, Wada H. 2003. Requirement of phosphatidylglycerol for maintenance of photosynthetic machinery. Plant Physiology 133:1376-1384.
118. Sakurai I, Mizusawa N, Ohashi S, Kobayashi M, Wada H. 2007. Effects of the lack of phosphatidylglycerol on the donor side of photosystem II. Plant Physiology 144:1336-1346.
119. Sarcina M, Bouzovitis N, Mullineaux CW. 2006. Mobilization of photosystem II induced by intense red light in the cyanobacterium Synechococcus sp PCC7942. The Plant Cell 18:457-464.
120. Satoh K, Yamamoto Y. 2007. The carboxyl-terminal processing of precursor D1 protein of the photosystem II reaction center. Photosynthesis Research 94:203-215.
121. Satoh S, Ikeuchi M, Mimuro M, Tanaka A. 2001. Chlorophyll b expressed in cyanobacteria functions as a light harvesting antenna in photosystem I through flexibility of the proteins. Journal of Biological Chemistry 276:4293-4297.
122. Schneider D, Fuhrmann E, Scholz I, Hess WR, Graumann PL. 2007. Fluorescence staining of live cyanobacterial cells suggest non-stringent chromosome segregation and absence of a connection between cytoplasmic and thylakoid membranes. BMC Cell Biology 8:39. doi:10.1186/1471-2121-8-39.
123. Schottkowski M, Gkalympoudis S, Tzekova N, et al. 2009. Interaction of the periplasmic PratA factor and the PsbA (D1) protein during biogenesis of photosystem II in Synechocystis sp PCC 6803. Journal of Biological Chemistry 284:1813-1819.
124. Shen J-R, Qian M, Inoue Y, Burnap RL. 1998. Functional characterization of Synechocystis sp. PCC 6803 ΔpsbU and ΔpsbV mutants reveals important roles of cytochrome c-550 in cyanobacterial oxygen evolution. Biochemistry 37:1551-1558.
125. Shimada Y, Tsuchiya T, Akimoto S, et al. 2008. Spectral properties of the CP43-deletion mutant of Synechocystis sp PCC 6803. Photosynthesis Research 98:303-314.
126. Shipton CA, Barber J. 1992. Characterization of photoinduced breakdown of the D1-polypeptide in isolated reaction centers of photosystem-II. Biochimica et Biophysica Acta 1099:85-90.
127. Silva P, Thompson E, Bailey S, et al. 2003. FtsH is involved in the early stages of repair of photosystem II in Synechocystis sp PCC 6803. The Plant Cell 15:2152-2164.
128. Smith D, Howe CJ. 1993. The distribution of photosystem-I and photosystem-II polypeptides between the cytoplasmic and thylakoid membranes of cyanobacteria. FEMS Microbiology Letters 110:341-347.
129. Sobotka R, Komenda J, Bumba L, Tichy M. 2005. Photosystem II assembly in CP47 mutant of Synechocystis sp PCC 6803 is dependent on the level of chlorophyll precursors regulated by ferrochelatase. Journal of Biological Chemistry 280:31595-31602.
130. Sobotka R, McLean S, Zuberova M, Hunter CN, Tichy M. 2008. The C-terminal extension of ferrochelatase is critical for enzyme activity and for functioning of the tetrapyrrole pathway in Synechocystis strain PCC 6803. Journal of Bacteriology 190:2086-2095.
131. Spetea C, Hundal T, Lohmann F, Andersson B. 1999. GTP bound to chloroplast thylakoid membranes is required for light-induced, multienzyme degradation of the photosystem II D1 protein. Proceedings of the National Academy of Sciences, USA 96:6547-6552.
132. Srivastava R, Battchikova N, Norling B, Aro EM. 2006. Plasma membrane of Synechocystis PCC 6803: a heterogeneous distribution of membrane proteins. Archives of Microbiology 185:238-243.
133. Summerfield TC, Shand JA, Bentley FK, Eaton-Rye JJ. 2005a. PsbQ (Sll1638) in Synechocystis sp PCC 6803 is required for photosystem II activity in specific mutants and in nutrient-limiting conditions. Biochemistry 44:805-815.
134. Summerfield TC, Winter RT, Eaton-Rye JJ. 2005b. Investigation of a requirement for the PsbP-like protein in Synechocystis sp PCC 6803. Photosynthesis Research 84:263-268.
135. Sun XW, Wang LY, Zhang LX. 2007. Involvement of DEG5 and DEG8 proteases in the turnover of the photosystem II reaction center D1 protein under heat stress in Arabidopsis thaliana. Chinese Science Bulletin 52:1742-1745.
136. Takahashi S, Murata N. 2008. How do environmental stresses accelerate photoinhibition? Trends in Plant Science 13:178-182.
137. Takahashi T, Inoue-Kashino N, Ozawa S, Takahashi Y, Kashino Y, Satoh K. 2009. Photosystem II complex in vivo is a monomer. Journal of Biological Chemistry 284:15598-15606.
138. Takasaka K, Iwai M, Umena Y, et al. 2010. Structural and functional studies on Ycf12 (Psb30) and PsbZ-deletion mutants from a thermophilic cyanobacterium. Biochimica et Biophysica Acta 1797:278-284.
139. Thornton LE, Ohkawa H, Roose JL, Kashino Y, Keren N, Pakrasi HB. 2004. Homologs of plant PsbP and PsbQ proteins are necessary for regulation of photosystem II activity in the cyanobacterium Synechocystis 6803. The Plant Cell 16:2164-2175.
140. Tomo T, Akimoto S, Ito H, et al. 2009. Replacement of chlorophyll with di-vinyl chlorophyll in the antenna and reaction center complexes of the cyanobacterium Synechocystis sp PCC 6803: characterization of spectral and photochemical properties. Biochimica et Biophysica Acta 1787:191-200.
141. Trebst A, Depka B. 1997. Role of carotene in the rapid turnover and assembly of photosystem II in Chlamydomonas reinhardtii. FEBS Letters 400:359-362.
142. Vass I, Cser K. 2009. Janus-faced charge recombinations in photosystem II photoinhibition. Trends in Plant Science 14:200-205.
143. Vavilin D, Vermaas W. 2007. Continuous chlorophyll degradation accompanied by chlorophyllide and phytol reutilization for chlorophyll synthesis in Synechocystis sp PCC 6803. Biochimica et Biophysica Acta 1767:920-929.
144. Vavilin D, Brune DC, Vermaas W. 2005. N-15-labeling to determine chlorophyll synthesis and degradation in Synechocystis sp PCC 6803 strains lacking one or both photosystems. Biochimica et Biophysica Acta 1708:91-101.
145. Vavilin D, Yao D, Vermaas W. 2007. Small Cab-like proteins retard degradation of photosystem II-associated chlorophyll in Synechocystis sp PCC 6803 - kinetic analysis of pigment labeling with N-15 and C-13. Journal of Biological Chemistry 282:37660-37668.
146. Vermaas WF, Timlim JA, Jones HD, et al. 2008. In vivo hyperspectral confocal fluorescence imaging to determine pigment localization and distribution in cyanobacterial cells. Proceedings of the National Academy of Sciences, USA 105:4050-4055.
147. Wang Q, Sullivan RW, Kight A, et al. 2004. Deletion of the chloroplast-localized Thylakoid formation1 gene product in Arabidopsis leads to deficient thylakoid formation and variegated leaves. Plant Physiology 136:3594-3604.
148. Watanabe M, Iwai M, Narikawa R, Ikeuchi M. 2009. Is the photosystem II complex a monomer or a dimer? Plant and Cell Physiology 50:1674-1680.
149. Wegener KM, Welsh EA, Thornton LE, et al. 2008. High sensitivity proteomics assisted discovery of a novel operon involved in the assembly of photosystem II, a membrane protein complex. Journal of Biological Chemistry 283:27829-27837.
150. Williams JGK. 1988. Construction of specific mutations in photosystem II photosynthetic reaction center by genetic-engineering methods in Synechocystis 6803. Methods in Enzymology 167:766-778.
151. Wu QG, Vermaas WFJ. 1995. Light-dependent chlorophyll a biosynthesis upon chlL deletion in wild-type and photosystem I-less strains of the cyanobacterium Synechocystis sp PCC 6803. Plant Molecular Biology 29:933-945.
152. Xu H, Vavilin D, Vermaas W. 2001. Chlorophyll b can serve as the major pigment in functional photosystem II complexes of cyanobacteria. Proceedings of the National Academy of Sciences, USA 98:14168-14173.
153. Yao D, Kieselbach T, Komenda J, et al. 2007. Localization of the small CAB-like proteins in photosystem II. Journal of Biological Chemistry 282:267-276.
154. Yi L, Dalbey RE. 2005. Oxa1/Alb3/YidC system for insertion of membrane proteins in mitochondria, chloroplasts and bacteria (Review). Molecular Membrane Biology 22:101-111.
155. Zak E, Norling B, Maitra R, Huang F, Andersson B, Pakrasi HB. 2001. The initial steps of biogenesis of cyanobacterial photosystems occur in plasma membranes. Proceedings of the National Academy of Sciences, USA 98:13443-13448.
156. Zhang LG, Wei Q, Wu WJ, et al. 2009. Activation of the heterotrimeric G protein alpha-subunit GPA1 suppresses the FtsH-mediated inhibition of chloroplast development in Arabidopsis. The Plant Journal 58:1041-1053.
157. Zhang LX, Paakkarinen V, van Wijk KJ, Aro EM. 1999. Co-translational assembly of the D1 protein into photosystem II. Journal of Biological Chemistry 274:16062-16067.