Redox regulation of thylakoid protein phosphorylation

Antioxidants and Redox Signaling

Volumn 5, Issue 1, 2003, Pages 55-67

  Aro, Eva Mari ^a   Ohad, Itzhak ^b  

^a UNIVERSITY OF TURKU   (Finland)

^b HEBREW UNIVERSITY OF JERUSALEM   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOCHROME B; PHOSPHOPROTEIN; PROTEIN KINASE;

AMINO ACID SEQUENCE; CHLOROPLAST; ELECTRON TRANSPORT; ENZYME ACTIVATION; ENZYME SUBSTRATE; LIGHT HARVESTING SYSTEM; NONHUMAN; OXIDATION REDUCTION REACTION; PHOTOSYSTEM II; PLANT; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; REVIEW; SIGNAL TRANSDUCTION; THYLAKOID;

EID: 0037298310     PISSN: 15230864     EISSN: None     Source Type: Journal    
DOI: 10.1089/152308603321223540     Document Type: Review

References (96)

1. Adir N, Shochat S, and Ohad I. Light-dependent D1 protein synthesis and translocation is regulated by reaction center II. J Biol Chem 265: 12563-12568, 1990.
2. Allen JF. Protein phosphorylation in regulation of photosynthesis. Biochim Biophys Acta 1098: 275-335, 1992.
3. Allen JF. Thylakoid protein phosphorylation, state-l-state- 2 transitions, and photosystem stoichiometry adjustment: redox control at multiple levels of gene expression. Physiol Plant 93: 196-205, 1995.
4. Allen JF and Forsberg J. Molecular recognition in thylakoid structure and function. Trends Plant Sci 6: 317-326, 2001.
5. Andersson B and Aro EM. Photodamage and D1 protein turnover in photosystem II. In: Regulation of Photosynthesis, edited by Aro EM and Andersson B. Dordrecht: Kluwer Academic Publishers, 2001, pp. 377-393.
6. Barzda V, Istokovics A, Simidjiev I, and Garab G. Structural flexibility of chiral macroaggregates of light-harvesting chlorophyll a/b pigment-protein complexes. Light-induced reversible structural changes associated with energy dissipation. Biochemistry 35: 8981-8985, 1996.
7. Bennett J. Phosphorylation of chloroplast membrane polypeptides. Nature 269: 344-346, 1977.
8. Bennett J. Protein phosphorylation in green plant chloroplasts. Annu Rev Plant Physiol Plant Mol Biol 42: 281-311, 1991.
9. Bergantino E, Dainese P, Cerovic Z, Sechi S, and Bassi R. A post-translational modification of the photosystem II subunit CP29 protects maize from cold stress. J Biol Chem 270: 8474-8481, 1995.
10. Bergantino E, Sandona D, Cugini D, and Bassi R. The photosystem II subunit CP29 can be phosphorylated in both C3 and C4 plants as suggested by sequence analysis. Plant Mol Biol 36: 11-22, 1998.
11. Bergo E, Pursiheimo SL, Paakkarinen V, Giagometti GM, Donella-Deana A, Andreucci F, Barbato R, and Aro EM. Rapid and highly specific monitoring of reversible thylakoid protein phosphorylation by polyclonal antibody to phosphothreonine-containing proteins. J Plant Physiol 159: 371-377, 2002.
12. 6f complex induced by inhibitor binding. J Biol Chem 275: 13195-13201, 2000.
13. 6f complex: structural studies and comparison with the bcl complex. Biochim Biophys Acta 1459: 467-474, 2000.
14. Cabrillac D, Cock MJ, Dumas C, and Gaude T. The S-locus receptor kinase is inhibited by thioredoxins and activated by pollen coat proteins. Nature 410: 220-223, 2001.
15. Carlberg I and Andersson B. Phosphatase activities in spinach thylakoid membranes - effectors, regulation and location. Photosynth Res 47: 145-156, 1996.
16. Cseh Z, Rajagopal S, Tsonev T, Busheva M, Papp E, and Garab G. Thermooptic effect in chloroplast thylakoid membranes. Thermal and light stability of pigment arrays with different levels of structural complexity. Biochemistry 39: 15250-15257, 2000.
17. deVitry C, Diner BA, and Popot JL. Photosystem II particles from Chlamydomonas reinhardtii. Purification, molecular weight, small subunit composition, and protein phosphorylation. J Biol Chem 266: 16614-16621, 1991.
18. Dilly-Hartwig H, Allen JF, Paulsen H, and Race HL. Truncated recombinant light harvesting complex II proteins are substrates for a protein kinase associated with photosystem II core complexes. FEBS Lett 435: 101-104, 1998.
19. Ebbert V and Godde D. Regulation of thylakoid protein phosphorylation in intact chloroplasts by the activity of kinases and phosphatases. Biochim Biophys Acta 1187: 335-346, 1994.
20. Ebbert V and Godde D. Phosphorylation of PSII polypeptides inhibits protein-degradation and increases PSII stability. Photosynth Res 50: 257-269, 1996.
21. Elich TD, Edelman M, and Mattoo AK. Identification, characterization, and resolution of the in vivo phosphorylated form of the D1 photosystem II reaction center protein. J Biol Chem 267: 3523-3529, 1992.
22. Elich TD, Edelman M, and Mattoo AK. Dephosphorylation of photosystem II core proteins is light-regulated in vivo. EMBO J 12: 4857-4862, 1993.
23. Escoubas JM, Lomas M, LaRoche J, and Falkowski PG. Light intensity regulation of cab gene transcription is signalled by the redox state of the plastoquinol pool. Proc Natl Acad Sci U S A 92: 10237-10241, 1995.
24. Eskling M, Arvidsson PO, and Akerlund HE. The xanthophyll cycle, its regulation and components. Physiol Plant 100: 806-816, 1997.
25. Finazzi G, Furia A, Barbagallo RP, and Forti G. State transition, cyclic and linear electron transport and photophosphorylation in Chlamydomonas reinhardtii. Biochim Biophys Acta 1413: 117-129, 1999.
26. 0 site occupancy in LHCII-kinase activation. J Biol Chem 276: 9770-9774, 2001.
27. Fulgosi H, Vener AV, Altschmied L, Herrmann RG, and Andersson B. A novel multifunctional chloroplast protein: identification of a 40 kDa immunophilin-like protein located in the thylakoid lumen. EMBO J 17: 1577-1587, 1998.
28. 6f complex. FEBS Lett 221: 205-210, 1987.
29. 6f complex. In vitro control of kinase activity. J Biol Chem 265: 19742-19749, 1990.
30. Gal A, Zer H, Roobol-Boza M, Fulgosi H, Herrmann RG, Ohad I, and Andersson B. Use of perfusion chromatography for the rapid isolation of thylakoid kinase enriched preparations. In: Photosynthesis: From Light to Biosphere, edited by Mathis P. Dordrecht: Kluwer Academic Publishers, 1995, Vol. 11, pp. 787-789.
31. Gal A, Zer H, and Ohad I. Redox-controlled thylakoid protein phosphorylation. News and Views. Physiol Plant 100: 863-868, 1997.
32. Gilmore AM, Hazlett TL, Debrunner PG, and Govindjee. Photosystem II chlorophyll a fluorescence lifetimes and intensity are independent of the antenna size differences between barley wild-type and chlorina mutants: photochemical quenching and xanthophyll cycle-dependent nonphotochemical quenching of fluorescence. Photosynth Res 48: 171-187, 1996.
33. Goldschmidt-Clermont M. Coordination of nuclear and chloroplast gene expression in plant cells. Int Rev Cytol 117: 115-180, 1998.
34. Haldrup A, Jensen PE, Lunde C, and Scheller HV. Balance of power: a view of the mechanism of photosynthetic state transitions. Trends Plant Sci 6: 301-305, 2001.
35. 6f complex undergoes reversible phosphorylation upon state transition. J Biol Chem 275: 17072-17079, 2000.
36. Hammer MF, Sarath G, and Markwell J. Dephosphorylation of the thylakoid membrane light-harvesting complex-II by stromal protein phosphatase. Photosynth Res 45: 195-201, 1995.
37. Hammer MF, Sarath G, Osterman JC, and Markwell J. Assessing modulation of stromal and thylakoid light-harvesting complex-II phosphatase activities with phosphopeptide substrates. Photosynth Res 44: 107-115, 1995.
38. Hammer MF, Markwell J, and Sarath G. Purification of a protein phosphatase from chloroplast stroma capable of dephosphorylating the light-harvesting complex-II. Plant Physiol 113: 227-233, 1997.
39. Hast T and Follmann H. Identification of two thylakoid- associated phosphatases with protein phosphatase activity in chloroplasts of the soybean (Glycine max). J Photochem Photobiol B 36: 313-319, 1996.
40. Hind G, Marshak DR, and Coughlan SJ. Polyphenol oxidase, cloning, characterization and relation to a putative protein kinase. Biochemistry 34: 8157-8164, 1995.
41. Huner NPA, Maxwell DP, Gray GR, Savitch LV, Krol M, Ivanov AG, and Falk S. Sensing environmental temperature change through imbalances between energy supply and energy consumption: redox state of photosystem II. Physiol Plant 98: 358-364, 1996.
42. Iwata S, Lee JW, Okada K, Iwata M, Rasmussen B, Link TA, Ramaswamy S, and Jap BK. Complex structure of the 11-subunit bovine mitochondrial cytochrome bcl complex. Science 281: 64-71, 1998.
43. Jansson S. A guide to the lhc genes and their relatives in Arabidopsis. Trends Plant Sci 4: 236-240, 1994.
44. Keren N and Ohad I. State transition and photoinhibition. In: Molecular Biology of Chlamydomonas reinhardtii, edited by Rochaix DJ, Goldschmidt-Clermont M, and Merchant S. Dordrecht: Kluwer Academic Publishers, pp. 569-596, 1998.
45. Kieselbach T, Hagman A, Andersson B, and Schröder W. The thylakoid lumen of chloroplasts. Isolation and characterization. J Biol Chem 273: 6710-6716, 1998.
46. Koivuniemi A, Aro EM, and Andersson B. Degradation of D1- and D2-proteins of photosystem II in higher plants is regulated by reversible phosphorylation. Biochemistry 34: 16022-16029, 1995.
47. Kruse O, Zheleva D, and Barber J. Stabilization of photosystem II dimers by phosphorylation: implication for the regulation of the turnover of D1 protein. FEBS Lett 408: 276-280, 1997.
48. Lin ZF, Lucero HA, and Racker E. Protein kinases from spinach chloroplasts. I. Purification and identification of two distinct protein kinases. J Biol Chem 257: 12153-12156, 1982.
49. Mann NH. Protein phosphorylation in cyanobacteria. Microbiology 140: 3207-3215, 1994.
50. Massague J and Chen Y-G. Controlling TGF-β signalling. Genes Dev 14: 627-644, 2000.
51. 2 termini. J Biol Chem 263: 1123-1130, 1988.
52. Michel H, Griffin PR, Shabanowitch J, Hunt DF, and Bennett J. Tandem mass spectrometry identifies sites of three post-translational modifications of spinach light-harvesting chlorophyll protein II. J Biol Chem 266: 17584-17591, 1991.
53. Niyogi KK. Photoprotection revisited: genetic and molecular approaches. Annu Rev Plant Physiol Plant Mol Biol 50: 333-359, 1999.
54. Ohad I, Vink M, Zer H, Herrmann RG, and Andersson B. Novel aspects on the regulation of thylakoid protein phosphorylation. In: Regulation of Photosynthesis, edited by Aro EM and Andersson B. Dordrecht: Kluwer Academic Publishers, 2001, pp. 419-432.
55. Owens CG and Ohad I. Phosphorylation of Chlamydomonas reinhardtii chloroplast membranes in vivo and in vitro. J Cell Biol 93: 712-718, 1982.
56. Pfannschmidt T, Schutze K, Brost M, and Oelmuller R. A novel mechanism of nuclear photosynthesis gene regulation by redox signals from the chloroplast during photosystem stoichiometry adjustment. J Biol Chem 276: 36125-36130, 2001.
57. Pursiheimo S, Rintamiki E, Baena-Gonzalez E, and Aro EM. Thylakoid protein phosphorylation in evolutionally divergent species with oxygenic photosynthesis. FEBS Lett 423: 178-182, 1998.
58. Pursiheimo S, Mulo P, Rintamiki E, and Aro EM. Coregulation of light-harvesting complex II phosphorylation and lhcb mRNA accumulation in winter rye. Plant J 26: 317-327, 2001.
59. Race HL and Hind G. A protein kinase in the core of photosystem II. Biochemistry 35: 13006-13010, 1996.
60. Rhee KH, Photosytem II: the solid structural era. Annu Rev Biophys Biomol Struct 30: 307-328, 2001.
61. Rhee KH, Morris, EP, Barber J, and Kühlbrandt W. Three-dimensional structure of the plant photosystem II reaction centre at 8 Å resolution. Nature 389: 283-286, 1998.
62. Rintamäki E and Aro EM. Phosphorylation of photosystem II proteins. In: Regulation of Photosynthesis, edited by Aro EM and Andersson B. Dordrecht: Kluwer Academic Publishers, 2001, pp. 395-418.
63. Rintamäki E, Kettunen R, and Aro EM. Differential D1 dephosphorylation in functional and photodamaged photosystem II centres. Dephosphorylation is a prerequisite for degradation of damaged D1*. J Biol Chem 271: 14870-14875, 1996.
64. Rintamäki E, Salonen M, Suoranta UM, Carlberg I, Andersson B, and Aro EM. 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. J Biol Chem 272: 30476-30482, 1997.
65. Rintamäki E, Martinsuo P, Pursiheimo S, and Aro EM. Cooperative regulation of light-harvesting complex II phosphorylation via plastoquinol and ferredoxin-thioredoxin system in chloroplast. Proc Natl Acad Sci U S A 97: 11644-11649, 2000.
66. Rokka A, Aro EM, Herrmann RG, Andersson B, and Vener A. Dephosphorylation of photosystem II reaction center proteins in plant photosynthetic membranes as an immediate response to abrupt elevation of temperature. Plant Physiol 123: 1525-1535, 2000.
67. Saitoh M, Nishitoh H, Fuji M, Takeda K, Tobiume K, Sawada Y, Kaw M, Miyazono K, and Ichijo H. Mammalian thioredoxin is a direct inhibitor of apoptosis signal-regulating kinase (ASK) 1. EMBO J 17: 2596-2606, 1998.
68. Salonen M, Aro EM, and Rintamäki E. Reversible phosphorylation and turnover of the D1 protein under various redox states of photosystem II induced by low temperature photoinhibition. Photosynth Res 58: 143-151, 1998.
69. Schuster G, Dewit M, Staehelin LA, and Ohad I. Transient inactivation of the thylakoid photosystem II light-harvesting protein kinase system and concomitant changes in intramembrane particle size during photoinhibition of Chlamydomonas reinhardtii. J Biol Chem 103: 71-80, 1986.
70. Silversteen T, Cheng L, and Allen JF. Redox titration of multiple protein phosphorylations in pea chloroplast thylakoids. Biochim Biophys Acta 1183: 215-220, 1993.
71. Silversteen T, Cheng L, and Allen JF. Chloroplast thylakoid protein phosphatase reactions are redox-independent and kinetically heterogeneous. FEBS Lett 332: 101-105, 1993.
72. Simpson DJ and Knoetzel J. Light-harvesting of plants and algae: introduction, survey and nomenclature. In: Oxygenic Photosynthesis: The Light Reactions, edited by Ort DR and Yocum CF. Dordrecht: Kluwer Academic Publishers, 1996, pp. 493-506.
73. Snyders S and Kohorn BD. TAKs, thylakoid membrane protein kinases associated with energy transduction. J Biol Chem 274: 9137-9140, 1999.
74. Snyders S and Kohorn BD. Disruption of thylakoid-associated kinase I leads to alteration of light harvesting in Arabidopsis. J Biol Chem 276: 32169-32176, 2001.
75. Sokolenko A, Fulgosi H, Gal A, Altschmied L, Ohad I, and Herrmann RG. The 67 kDa polypeptide of spinach may not be the LHCII kinase but a lumenal located polyphenol oxidase. FEBS Lett 371: 176-180, 1995.
76. Sun G and Markwell J. Lack of types 1 and 2A protein serine(P)/threonine(P) phosphatase activities in chloroplasts. Plant Physiol 100: 620-624, 1992.
77. Sun G, Bailey D, Jones MW, and Markwell J. Chloroplast thylakoid protein phosphatase is a membrane surface-associated activity. Plant Physiol 89: 238-243, 1989.
78. Testi MG, Croce R, Polverino-De Laureto P, and Bassi R. A CK2 site is reversibly phosphorylated in the photosystem II subunit CP29. FEBS Lett 399: 245-250, 1996.
79. Tullberg A, Håkansson G, and Race HL. A protein tyrosine kinase of chloroplast thylakoid membranes phosphorylates light-harvesting complex II proteins. Biochem Biophys Res Commun 250: 617-622, 1998.
80. 6f complex along the thylakoid membrane upon state transition. Proc Natl Acad Sci U S A 88: 8262-8266, 1991.
81. Vener AV, van Kan PJM, Gal A, Andersson B, and Ohad I. Activation/deactivation cycle of redox-controlled thylakoid protein phosphorylation. Role of quinone bound to the reduced cytochrome bf complex. J Biol Chem 270: 25225-25232, 1995.
82. Vener AV, van Kan PJM, Rich PR, Ohad I, and Andersson B. Plastoquinol at the quinol oxidation site of the reduced cytochrome bf mediates signal transduction between light and protein phosphorylation: thylakoid protein kinase deactivation by a single turnover flash. Proc Natl Acad Sci U S A 94: 1585-1590, 1997.
83. Vener AV, Ohad I, and Andersson B. Protein phosphorylation and redox sensing in chloroplast thylakoids. Curr Opin Plant Biol 1: 217-223, 1998.
84. Vener AV, Rokka A, Fulgosi H, Andersson B, and Herrmann RG. A cyclophilin-regulated PP2A-like protein phosphatase in thylakoid membranes of plant chloroplasts. Biochemistry 38: 14955-14965, 1999.
85. Vener AV, Harms A, Sussman MR, and Vierstra RD. Mass spectrometric resolution of reversible protein phosphorylation in photosynthetic membranes of Arabidopsis thaliana. J Biol Chem 276: 6959-6966, 2001.
86. Vink M, Zer H, Herrmann RG, Andersson B, and Ohad I. Regulation of photosystem II core protein phosphorylation at the substrate level: light induces exposure of the CP43 chlorophyll aprotein complex to thylakoid protein kinase(s). Photosynth Res 64: 209-219, 2000.
87. Weber P, Fulgosi H, Sokolenko A, Karnauchov I, Andersson B, Ohad I, and Herrmann RG. Evidence for four thylakoid-located kinases. In: Photosynthesis: Mechanisms and Effects, edited by Garab G. Dordrecht: Kluwer Academic Publishers, 1998, Vol III, pp. 1883-1886.
88. Wettern M, Owens JC, and Ohad I. Role of thylakoid polypeptide phosphorylation and turnover in the assembly and function of photosystem II. In: Methods in Enzymology, Vol. 97: Biomembranes, Part K: Membrane Biogenesis, edited by Fleischer S and Fleischer B. Academic Press, 1983, pp. 554-567.
89. Wollman FA and Lemaire C. Phosphorylation processes interacting in vivo in the thylakoid membranes from C. reinhardtii. In: Photocatalytic Production of Energy Rich Compounds, edited by Hall DO and Grassi G. Amsterdam, Elsevier, 1988, pp. 210-214.
90. 6f mutants from Chlamydomonas reinhardtii which lack quinone binding proteins. Biochim Biophys Acta 933: 85-94, 1988.
91. Yang DH, Andersson B, Aro EM, and Ohad I. The redox state of the plastoquinone pool controls the level of the light-harvesting chlorophyll a/b binding protein complex II (LHC II) during photoacclimation. Photosynth Res 68: 163-174, 2001.
92. Zer H, Vink M, Keren N, Dilly-Hartwig HG, Paulsen H, Herrmann RG, Andersson B, and Ohad I. Regulation of thylakoid protein phosphorylation at substrate level: reversible light-induced conformational changes expose the phosphorylation site of the light-harvesting complex II. Proc Natl Acad Sci U S A 96: 8277-8282, 1999.
93. Zhang L, Paakkarinen V, vanWijk KJ, and Aro EM. Cotranslational assembly of the D1 protein into photosystem II. J Biol Chem 274: 16062-16067, 1999.
94. Zhang Z, Huang L, Shulmeister VM, Chi YI, Kim KK, Hung LW, Crofts AR, Berry EA, and Kim SH. Electron transfer by domain movement in cytochrome bcl. Nature 392: 677-684, 1998.
95. o site of cytochrome b6f complexes controls the activation of the LHCII kinase. EMBO J 18: 2961-2969, 1999.
96. Zouni A, Witt HT, Kern J, Fromme P, Krauss N, Saenger W, and Orth P. Crystal structure of photosystem II from Synechocystis elongatus at 3.8 Å Ångtrom resolution. Nature 409: 739-743, 2001.