Dynamics of photosystem II: A proteomic approach to thylakoid protein complexes

Journal of Experimental Botany

Volumn 56, Issue 411, 2005, Pages 347-356

  Aro, E M ^a   Suorsa, M ^a   Rokka, A ^a   Allahverdiyeva, Y ^a   Paakkarinen, V ^a   Saleem, A ^a   Battchikova, N ^a   Rintamaki E ^a  

^a UNIVERSITY OF TURKU   (Finland)

Author keywords

Arabidopsis thylakoid membrane proteome; Assembly of photosystem II; D1 protein; Light stress; Photosystem II photoinhibition; Repair of photosystem II

Indexed keywords

BIOLOGICAL MEMBRANES; CHLOROPHYLL; COMPLEXATION; DIMERS; GELS; LIGHT ABSORPTION; MONOMERS; PROTEINS; REACTION KINETICS;

LIGHT INTENSITIES; OXYGENIC PHOTOSYNTHESIS; PHOTODAMAGE; PHOTOSYSTEM II (PSII);

PHOTOSYNTHESIS;

OXYGEN;

CONFERENCE PAPER; LIGHT; LIGHT HARVESTING SYSTEM; METABOLISM; OXIDATION REDUCTION REACTION; PHOSPHORYLATION; PHOTOSYSTEM II; PHYSIOLOGY; RADIATION EXPOSURE; THYLAKOID;

LIGHT; LIGHT-HARVESTING PROTEIN COMPLEXES; OXIDATION-REDUCTION; OXYGEN; PHOSPHORYLATION; PHOTOSYSTEM II PROTEIN COMPLEX; THYLAKOIDS;

ARABIDOPSIS;

EID: 13944253668     PISSN: 00220957     EISSN: None     Source Type: Journal    
DOI: 10.1093/jxb/eri041     Document Type: Conference Paper

References (73)

1. Adam Z, Clarke AK. 2002. Cutting edge of chloroplast proteolysis. Trends in Plant Science 7, 451-456.
2. Ananyev GM, Zaltsman L, Vasko C, Dismukes GC. 2001. The inorganic biochemistry of photosynthetic oxygen evolution/water oxidation. Biochimica et Biophysica Acta 1503, 52-68.
3. 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.
4. Anderson JM, Park YI, Chow WS. 1997. Photoinactivation and photoprotection of photosystem II in nature. Physiologia Plantarum 100, 314-323.
5. Andersson B, Aro E-M. 1997. Proteolytic activities and proteases of plant chloroplasts. Physiologia Plantarum 100, 780-793.
6. Aro EM, Virgin I, Andersson B. 1993. Photoinhibition of photosystem II: inactivation, protein damage and turnover. Biochimica et Biophysica Acta 1143, 113-134.
7. Baena-Gonzalez E, Barbato R, Aro E-M. 1999. Role of PSII phosphorylation in the PSII repair cycle and oligomeric structure. Planta 208, 196-204.
8. Bailey S, Thompson E, Nixon PJ, Horton P, Mullineaux CW, Robinson C, Mann NH. 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. Bassi R, Sandona D, Croce R. 1997. Novel aspects of chlorophyll a/b-binding proteins. Physiologia Plantarum 100, 769-779.
10. Bennett J. 1977. Phosphorylation of chloroplast membrane polypeptides. Nature 269, 344-346.
11. Bennett J. 1991. Protein phosphorylation in green plant chloroplasts. Annual Review of Plant Physiology and Plant Molecular Biology 42, 281-311.
12. Bergantino E, Brunetta A, Touloupakis E, Segalla A, Szabò I, Giacometti GM. 2003. Role of the PSII-H subunit in photoprotection. Novel aspects of D1 turnover in Synechocystis 6803. Journal of Biological Chemistry 278, 41820-41829.
13. Bergantino E, Dainese P, Cerovic Z, Sechi S, Bassi R. 1995. A post-translational modification of the photosystem II subunit CP29 protects maize from cold stress. Journal of Biological Chemistry 270, 8474-8481.
14. 4 plants as suggested by sequence analysis. Plant Molecular Biology 36, 11-22.
15. Bowyer JR, Packer JCL, McCormack BA, Whitelegge JP, Robinson C, Taylor M. 1992. Carboxyl-terminal processing of the D1 protein and photoactivation of water splitting in photosystem II. Journal of Biological Chemistry 267, 5424-5433.
16. Dèpege N, Bellafiore S, Rochaix JD. 2003. Role of chloroplast protein kinase Stt7 in LHCII phosphorylation and state transition in Chlamydomonas. Science 299, 1572-1575.
17. Diner BA, Ries DF, Cohen BN, Metz JG. 1988. COOH-terminal processing of polypeptide D1 of the photosystem II reaction center of Scenedesmus obliquus is necessary for the assembly of the oxygen-evolving complex. Journal of Biological Chemistry 263, 8972-8980.
18. Ferreira K, Iverson TM, Maghlaoui K, Barber J, Iwata S. 2004. Architecture of the photosynthetic oxygen-evolving center. Science 303, 1831-1838.
19. Guenther J, Melis A. 1990. The physiological significance of photosystem II heterogeneity in chloroplasts. Photosynthesis Research 23, 105-109.
20. Hager M, Hermann M, Biehler K, Krieger-Liszkay A, Bock R. 2002. Lack of the small plastid-encoded PsbJ polypeptide results in a defective water-splitting apparatus of photosystem II, reduced photosystem I levels and hypersensitivitv to light. Journal of Biological Chemistry 277, 14031-14039.
21. Hammer MF, Markwell J, Sarath G. 1997. Purification of a protein phosphatase from chloroplast stroma capable of dephosphorylating the light-harvesting complex- II. Plant Physiology 113, 227-233.
22. Hansson M, Vener AV. 2003. Identification of three previously unknown in vivo phosphorylation sites in thylakoid membranes of Arabidopsis thaliana. Molecular and Cellular Proteomics 2, 550-559.
23. Hashimoto A, Ettinger WF, Yamamoto Y, Theg SM. 1997. Assembly of newly incorporated oxygen-evolving complex sub-units in isolated chloroplasts: sites of assembly and mechanism of binding. The Plant Cell 9, 441-452.
24. Haußühl 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, 1-10.
25. Heinemeyer J, Eubel H, Wehmhöner D, Jänsch L, Braun H-P. 2004. Proteomic approach to characterize the supramolecular organization of photosystems in higher plants. Phytochemistry 65, 1683-1692.
26. Herranen M, Battchikova N, Zhang P, Graf A, Sirpiö S, Paakkarinen V, Aro E-M. 2004. Towards functional proteomics of membrane protein complexes in Synechocystis sp. PCC 6803. Plant Physiology 134, 470-481.
27. Hou C-X, Pursiheimo S, Rintamäki E, Aro E-M. 2002. Environmental and metabolic control of LHCII protein phosphorylation: revealing the mechanisms for dual regulation of the LHCII kinase. Plant, Cell and Environment 25, 1515-1525.
28. Ivanov B, Khorobrykh S. 2003. Participation of photosynthetic electron transport in production and scavenging of reactive oxygen species. Antioxidant Redox Signaling 5, 43-53.
29. Jansen MAK, Greenberg BM, Edelman M, Mattoo AK, Gaba V. 1996. Accelerated degradation of the D2 protein of photosystem II under ultraviolet radiation. Photochemistry and Photobiology 63, 814-817.
30. Kanervo E, Spetea C, Nishiyama Y, Murata N, Andersson B, Aro E-M. 2003. Dissecting a cyanobacterial proteolytic system: efficiency in inducing degradation of the D1 protein of photosystem II in cyanobacteria and plants. Biochimica et Biophysica Acta 1607, 131-140.
31. Koivuniemi A, Aro E-M, Andersson B. 1995. Degradation of the D1 and D2 proteins of photosystem II in higher plants is regulated by reversible phosphorylation. Biochemistry 34, 16022-16029.
32. Kettunen R, Pursiheimo S, Rintamäki E, van Wijk KJ, Aro E-M. 1997. Transcriptional and translational adjustments of psbA gene expression in mature chloroplasts during photoinhibition and subsequent repair of photosystem II. European Journal of Biochemistry 247, 441-448.
33. Kim J, Klein PG, Mullet JE. 1991. Ribosomes pause at specific sites during synthesis of membrane-bound chloroplast reaction centre protein D1. Journal of Biological Chemistry 266, 14931-14938.
34. Kyle DJ, Kuang TY, Watson JL, Arntzen CJ. 1984. Movement of a sub-population of the light-harvesting complez (LHCII) from grana to stroma lamellae as a consequence of its phosphorylation. Biochimica et Biophysica Acta 765, 89-96.
35. Laemmli UK. 1970. Cleavage of structural proteins during the assembly of head of bacteriophage T4. Nature 227, 680-685.
36. Lindahl M, Tabak S, Cseke L, Pichersky E, Andersson B, Adam Z. 1996. Identification, characterization, and molecular cloning of a homologue of the bacterial FtsH protease in chloroplasts of higher plants. Journal of Biological Chemistry 271, 29329-29334.
37. 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.
38. Martinsuo P, Pursiheimo S, Aro E-M, Rintamäki E. 2003. Dithiol oxidant and disulfide reductant dynamically regulate the phosphorylation of light harvesting complex II proteins in thylakoid membranes. Plant Physiology 133, 37-46.
39. Mattoo AK, Hoffman-Falk H, Marder JB, Edelman M. 1984. Regulation of protein metabolism: coupling of photosynthetic electron transport to in vivo degradation of the rapidly metabolized 32-kilodalton protein of the chloroplast membranes. Proceedings of the National Academy of Sciences, USA 81, 1380-1384.
40. Mauro S, Dainese P, Lannoye R, Bassi R. 1997. Cold-resistant and cold-sensitive maize lines differ in the phosphorylation of the photosystem II subunit, CP29. Plant Physiology 115, 171-180.
41. Melis A. 1999. Photosystem-II damage and repair cycle in chloroplasts: what modulates the rate of photodamage in vivo? Trends in Plant Science 4, 130-135.
42. Michel H, Griffin PR, Shabanowitz J, Hunt DF, Bennett J. 1991. Tandem mass spectrometry identifies sites of three post-translational modifications of spinach light-harvesting chlorophyll protein II. Proteolytic cleavage, acetylation, and phosphorylation. Journal of Biological Chemistry 266, 17584-17591.
43. Muller P, Li XP, Niyogi KK. 2001. Non-photochemical quenching. A response to excess light energy. Plant Physiology 125, 1558-1566.
44. Nield J, Kruse O, Ruprecht J, da Fonseca P, Büchel C, Barber J. 2000. Three-dimensional structure of Chlamydomonas reinhardtii and Synechococcus elongatus photosystem II complexes allows for comparison of their oxygen-evolving complex organization. Journal of Biological Chemistry 275, 27940-27946.
45. Nilsson R, Brunner J, Hoffman NE, van Wijk KJ. 1999. Interactions of ribosome nascent chain complexes of the chloroplast-encoded D1 thylakoid membrane protein with cpSRP54. EMBO Journal 18, 733-742.
46. Prasil O, Adir N, Ohad I. 1992. Dynamics of photosystem II. Mechanism of photoinhibition and recovery processes. In: Barber K, ed. Topics in photosynthesis, Vol. II. The Netherlands: Elsevier, 293-348.
47. Pursiheimo S, Martinsuo P, Rintamäki E, Aro E-M. 2003. Photosystem II protein phosphorylation follows four distinctly different regulatory patterns induced by environmental cues. Plant, Cell and Environment 26, 1995-2003.
48. Pursiheimo S, Mulo P, Rintamäki E, Aro E-M. 2001. Coregulation of light-harvesting complex II phosphorylation and lhcb mRNA accumulation in winter rye. The Plant Journal 26, 317-327.
49. Regel RE, Ivleva NB, Zer H, Meurer J, Shestakov SV, Herrmann RG, Pakrasi HB, Ohad I. 2001. Deregulation of electron flow within photosystem II in the absence of the PsbJ protein. Journal of Biological Chemistry 276, 41473-41478.
50. Rintamäki E, Kettunen R, Aro E-M. 1996. Differential D1 dephosphorylation in functional and photodamaged photosystem II centres. Dephosphorylation is a prerequisite for degradation of damaged D1*. Journal of Biological Chemistry 271, 14870-14875.
51. Rintamaki E, Salonen M, Suoranta U-M, Carlberg I, Andersson B, Aro E-M. 1997. Phosphorylation of light-harvesting complex II and photosystem II core proteins shows different irradiance-dependent regulation in vivo. Application of phosphothreonine antibodies to analysis of thylakoid phosphoproteins. Journal of Biological Chemistry 272, 30476-30482.
52. Rintamäki E, Martinsuo P, Pursiheimo S, Aro E-M. 2000. Cooperative regulation of light-harvesting complex II phosphorylation via the plastoquinol and the ferredoxin-thioredoxin system in chloroplasts. Proceedings of the National Academy of Sciences, USA 97, 11644-11649.
53. Sakurai I, Hagio M, Gombos Z, Tyystjärvi T, Paakkarinen V, Aro E-M, Wada H. 2003. Requirement of phosphatidylglycerol for maintenance of photosynthetic machinery. Plant Physiology 133, 1376-1384.
54. Silva P, Thompson E, Bailey S, Kruse O, Mullineaux CW, Robinson C, Mann NH, Nixon PJ. 2003. FtsH is involved in the early stages of repair of photosystem II in Synechocystis sp PCC 6803. The Plant Cell 15, 2152-2164.
55. Schuster G, Timberg R, Ohad I. 1988. Turnover of thylakoid photosystem II proteins during photoinhibition of Chlamydomonas reinhardtii. European Journal of Biochemistry 177, 403-410.
56. Snyders S, Kohorn BD. 2001. Disruption of thylakoid-associated kinase 1 leads to alteration of light harvesting in Arabidopsis. Journal of Biological Chemistry 276, 32169-32176.
57. Sun G, Bailey D, Jones MW, Markwell J. 1989. Chloroplast thylakoid protein phosphatase is a membrane surface-associated activity. Plant Physiology 89, 238-243.
58. Suorsa M, Regel R, Paakkarinen V, Battchikova N, Herrmann RG, Aro E-M. 2004. Protein assembly of photosystem II and accumulation of subcomplexes in the absence of low molecular mass subunits PsbL and PsbJ. European Journal of Biochemistry 271, 96-107.
59. Swiatek M, Kuras R, Sokolenko A, et al. 2001. The chloroplast gene ycf9 encodes a photosystem II (PSII) core subunit, PsbZ, that participates in PSII supramolecular architecture. The Plant Cell 13, 347-367.
60. Swiatek M, Regel R, Meurer J, Wanner G, Pakrasi HB, Ohad I, Herrmann RG. 2003. Effects of selective inactivation of individual genes for low-molecular-mass subunits on the assembly of photosystem II, as revealed by chloroplast transformation: the psbEFLJ operon in Nicotiana tabacum. Molecular and General Genomics 268, 699-710.
61. Testi MG, Croce R, Polverino-De Laureto P, Bassi R. 1996. A CK2 site is reversibly phosphorylated in the photosystem II subunit CP29. FEBS Letters 399, 245-250.
62. Tyystjärvi E, Aro E-M. 1996. The rate constant of photoinhibition, measured in lincomycin-treated leaves, is directly proportional to light intensity. Proceedings of the National Academy of Sciences, USA 93, 2213-2218.
63. van Wijk KJ, Roobol-Boza M, Kettunen R, Andersson B, Aro E-M. 1997. Synthesis and assembly of the D1 protein into photosystem II: processing of C-terminus and identification of the initial assembly partners and complexes during photosystem II repair. Biochemistry 36, 6178-6186.
64. Vener AV, Rokka A, Fulgosi H, Andersson B, Herrmann RG. 1999. A cyclophilin-regulated PP2A-like protein phosphatase in thylakoid membranes of plant chloroplasts. Biochemistry 38, 14955-14965.
65. Vener AV, Harms A, Sussman R, Vierstra RD. 2001. Mass spectrometric resolution of reversible protein phosphorylation in photosynthetic membranes of Arabidopsis thaliana. Journal of Biological Chemistry 276, 6959-6966.
66. Wollman F-A, Minai L, Nechushtai R. 1999. The biogenesis and assembly of photosynthetic proteins in thylakoid membranes. Biochimica et Biophysica Acta 1411, 21-85.
67. Zerges W. 2000. Translation in chloroplasts. Biochimie 82, 583-601.
68. Zhang L, Aro E-M. 2002. Synthesis, membrane insertion and assembly of the chloroplast-encoded D1 protein into photosystem II. FEBS Letters 512, 13-18.
69. Zhang L, Paakkarinen V, Suorsa M, Aro E-M. 2001. A SecY homologue is involved in chloroplast-encodcd D1 protein biogenesis. Journal of Biological Chemistry 276, 37809-37814.
70. Zhang L, Paakkarinen V, van Wijk KJ, Aro E-M. 1999. Cotranslational assembly of the D1 protein into photosystem II. Journal of Biological Chemistry 274, 16062-16067.
71. Zhang L, Paakkarinen V, van Wijk KJ, Aro E-M. 2000. Biogenesis of the chloroplast-encoded D1 protein: regulation of translation elongation, insertion, and assembly into photosystem II. The Plant Cell 12, 1769-1781.
72. Zheleva D, Sharma J, Panico M, Morris HR, Barber J. 1998. Isolation and characterization of monomeric and dimeric CP47-reaction center photosystem II complexes. Journal of Biological Chemistry 273, 16122-16127.
73. Zouni A, Witt HT, Kern J, Fromme P, Krauss N, Saenger W, Orth P. 2001. Crystal structure of photosystem II from Synechococcus elongatus at 3.8 Å resolution. Nature 409, 739-743.