Functional flexibility and acclimation of the thylakoid membrane

Photochemical and Photobiological Sciences

Volumn 4, Issue 12, 2005, Pages 1072-1080

  Kanervo, Eira ^a   Suorsa, Marjaana ^a   Aro, Eva Mari ^a  

^a UNIVERSITY OF TURKU   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

REACTIVE OXYGEN METABOLITE; WATER;

ARTICLE; ELECTRON TRANSPORT; ENERGY TRANSFER; LIGHT ABSORPTION; LIGHT HARVESTING SYSTEM; LIGHT IRRADIANCE; MOLECULAR DYNAMICS; PHASE TRANSITION; PHOTOCHEMICAL EFFICIENCY; PHOTOCHEMICAL QUENCHING; PHOTOSYSTEM II; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN STABILITY; THYLAKOID MEMBRANE;

EID: 29144491759     PISSN: 1474905X     EISSN: 14749092     Source Type: Journal    
DOI: 10.1039/b507866k     Document Type: Article

References (141)

1. P. J. Nixon and C. W. Mullineaux, in Regulation of Photosynthesis, ed. E.-M. Aro and B. Andersson, Kluwer Academic Publishers, Dordrecht, 2001, pp. 533–555.
2. D. A. Walker The Z-scheme-down hill all the way Trends Plant Sci. 2002 7 183-185.
3. J. F. Allen Cyclic, pseudocyclic and noncyclic photophosphorylation: new links in the chain Trends Plant Sci. 2003 8 15-19.
4. K. Asada and M. Takahashi, in Photoinhibition, ed. D. J. Kyle, C. B. Osmond and C. J. Arntzen, Elsevier, Amsterdam, 1987, pp. 227–287.
5. J. Barber B. Andersson Too much of a good thing: Light can be bad for photosynthesis Trends Biochem. Sci. 1992 17 61-66.
6. K. Niyogi Photoprotection revisited: Genetic and Molecular Approaches Annu. Rev. Plant Physiol. Plant Mol. Biol. 1999 50 333-359.
7. B. Andersson and E.-M. Aro, in Regulation of Photosynthesis, ed. E.-M. Aro and B. Andersson, Kluwer Academic Publishers, Dordrecht, 2001, pp. 377–393.
8. D. S. Bendall R. S. Manasse Cyclic photophosphorylation and electron transport Biochim. Biophys. Acta 1995 1229 23-38.
9. K. Asada The water-water cycle in chloroplasts: Scavenging of active oxygens and dissipation of excess photons Annu. Rev. Plant Physiol. Plant Mol. Biol. 1999 50 601-639.
10. G. N. Johnson Cyclic electron transport in C3 plants: fact or artefact? J. Exp. Bot. 2005 56 407-416.
11. P. Horton A. V. Ruban R. G. Walters Regulation of light harvesting in green plants Annu. Rev. Plant Physiol. Plant Mol. Biol. 1996 47 655-684.
12. J. A. Cruz T. J. Avenson A. Kanazawa K. Takizawa G. E. Edwards D. M. Kramer Plasticity in light reactions of photosynthesis for energy production and photoprotection J. Exp. Bot. 2005 56 395-406.
13. P. Horton A. Ruban Molecular design of the photosystem II light-harvesting antenna: photosynthesis and photoprotection J. Exp. Bot. 2005 56 365-373.
14. K. Niyogi X.-P. Li V. Rosenberg H.-S. Jung Is PsbS the site of non-photochemical quenching in photosynthesis? J. Exp. Bot. 2005 56 375-382.
15. Baena-Gonzalez E.-M. Aro Biogenesis, assembly and turnover of photosystem II units Philos. Trans. R. Soc. London, Ser. B 2002 357 1451-1460.
16. N. Murata Control of excitation transfer in photosynthesis. I. Light-induced change of chlorophyll a fluorescence in Porphyridium cruentum Biochim. Biophys. Acta 1969 172 242-251.
17. J. F. Allen Protein phosphorylation in regulation of photosynthesis Biochim. Biophys. Acta 1992 1098 275-335.
18. F. A. Wollman State transitions reveal the dynamics and flexibility of the photosynthetic apparatus EMBO J. 2001 20 3623-3630.
19. M. D. McConnell R. Koop S. Vasilev D. Bruce Regulation of the distribution of chlorophyll and phycobilin-absorbed excitation energy in cyanobacteria. A structure-based model for the light state transitions Plant Physiol. 2002 130 1201-1212.
20. C. W. Mullineaux D. Emlyn-Jones State transitions: an example of acclimation to low-light stress J. Exp. Bot. 2005 56 389-393.
21. S. Bellafiore F. Barneche G. Peltier J.-D. Rochaix State transitions and light adaptation require chloroplast thylakoid protein kinase STN7 Nature 2005 433 892-895.
22. A. Gal H. Zer I. Ohad Redox-controlled thylakoid protein phosphorylation. News and views Physiol. Plant. 1997 100 869-885.
23. A. Nilsson D. Stys T. Drakenberg M. D. Spangfort S. Forsen J. F. Allen Phosphorylation controls the three-dimensional structure of plant light-harvesting complex II J. Biol. Chem. 1997 272 18350-18357.
24. C. Lunde P. E. Jensen A. Haldrup J. Knoetzel H. V. Scheller The PSI-H subunit of photosystem I is essential for state transitions in plant photosynthesis Nature 2000 408 613-615.
25. J. F. Allen J. Bennett K. E. Steinback C. J. Arntzen Chloroplast protein phosphorylation couples plastoquinone redox state to distribution of excitation energy between photosystems Nature 1981 291 25-29.
26. A. V. Vener P. J. van Kan P. R. Rich I. Ohad B. Andersson Plastoquinol at the quinol oxidation site of the reduced cytochrome bf mediates signal transduction between light and protein phosphorylation: thylakoid protein kinase deactivation by single-turnover flash Proc. Natl. Acad. Sci. U. S. A. 1997 94 1585-1590.
27. E. Rintamäki M. Salonen U.-M. Suoranta I. Carlberg B. Andersson E.-M. Aro 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. 1997 272 30476-30482.
28. H. Mctavish A demonstration of photosynthetic state transitions in nature-shading by photosynthetic tissue causes conversion to state-1 Photosynth. Res. 1988 17 247-254.
29. o site of cytochrome b6f complexes controls the activation of the LHCII kinase EMBO J. 1999 18 2961-2969.
30. A. V. Vener I. Ohad B. Andersson Protein phosphorylation and redox sensing in chloroplast thylakoids Curr. Opin. Plant Biol. 1998 1 217-223.
31. G. Finazzi F. Zito R. P. Barbagallo F. A. Wollman Contrasted effects of inhibitors of cytochrome b6f complex on state transitions in C. reinhardtii: the role of Qo site occupancy in LHCII-kinase activation J. Biol. Chem. 2001 276 9770-9774.
32. N. Depège S. Bellafiore J.-D. Rochaix Role of chloroplast protein kinase Stt7 in LHCII phosphorylation and state transition in Chlamydomonas Science 2003 299 1572-1575.
33. G. Finazzi The central role of the green alga Chlamydomonas reinhardtii in revealing the mechanism of state transitions J. Exp. Bot. 2005 56 383-388.
34. A. Gal, H. Zer, M. Roobol-Boza, H. Fulgosi, R. G. Herrmann, I. Ohad and B. Andersson, in Photosynthesis: From Light to Biosphere, ed. P. Mathis, Kluwer Academic Publishers, Dordrecht, 1995, vol. 3, pp. 341–344.
35. H. L. Race G. Hind A protein kinase in the core of photosystem II Biochemistry 1996 35 13006-13010.
36. H. Zer M. Vink N. Keren H. G. Dilly-Hartwig H. Paulsen R. G. Herrmann B. Andersson I. Ohad Regulation of thylakoid protein phosphorylation at the substrate level: reversible light-induced conformational changes expose the phosphorylation site of the light-harvesting complex II Proc. Natl. Acad. Sci. U. S. A. 1999 96 8277-8282.
37. S. Snyders B. D. Kohorn TAKs, thylakoid membrane protein kinases associated with energy transduction J. Biol. Chem. 1999 274 9137-9140.
38. S. Snyders B. D. Kohorn Disruption of thylakoid-associated kinase 1 leads to alteration of light harvesting in Arabidopsis J. Biol. Chem. 2001 276 32169-32176.
39. C. Bonaventura J. Myers Fluorescence and oxygen evolution from Chlorella pyrenoidosa Biochim. Biophys. Acta 1969 189 366-383.
40. A. Telfer M. Hodges J. Barber Analysis of chlorophyll fluorescence induction curves in the presence of 3-(3,4-dichlorophenyl)-1,1-dimethylurea as a function of magnesium concentration and NADPH-activated light-harvesting chlorophyll a/b-protein phosphorylation Biochim. Biophys. Acta 1983 724 167-175.
41. C. Lunde P. E. Jensen L. Rosgaard A. Haldrup M. J. Gilpin H. V. Scheller Plants impaired in state transitions can to a large degree compensate for their defect Plant Cell Physiol. 2003 44 44-54.
42. O. Vallon L. Bulté P. Dainese J. Olive R. Bassi F. A. Wollman Lateral redistribution of cytochrome b6f complexes along thylakoid membranes upon state transitions Proc. Natl. Acad. Sci. U. S. A. 1991 88 8262-8266.
43. C. W. Mullineaux J. F. Allen State 1–state 2 transitions in the cyanobacterium Synechococcus 6301 are controlled by the redox state of electron carriers between photosystems I and II Photosynth. Res. 1990 22 157-166.
44. A. N. Glazer Phycobilisome: a macromolecular complex optimized for light energy transfer Biochim. Biophys. Acta 1984 768 29-51.
45. D. Emlyn-Jones M. K. Ashby C. W. Mullineaux A gene required for the regulation of photosynthetic light harvesting in the cyanobacterium Synechocystis 6803 Mol. Microbiol. 1999 33 1050-1058.
46. Y. Hihara A. Kamei M. Kanehisa A. Kaplan M. Ikeuchi DNA microarray analysis of cyanobacterial gene expression during acclimation to high light Plant Cell 2001 13 793-806.
47. C.-X. Hou S. Pursiheimo E. Rintamäki E.-M. Aro Environmental and metabolic control of LHCII protein phosphorylation: revealing the mechanisms for dual regulation of the LHCII kinase Plant, Cell Environ. 2002 25 1515-1525.
48. E. Rintamäki P. Martinsuo S. Pursiheimo E.-M. Aro Cooperative regulation of light-harvesting complex II phosphorylation via the plastoquinol and ferredoxin-thioredoxin system in chloroplasts Proc. Natl. Acad. Sci. U. S. A. 2000 97 11644-11649.
49. J. Standfuss A. C. Terwisscha van Scheltinga M. Lamborghini W. Kuhlbrandt Mechanisms of photoprotection and nonphotochemical quenching in pea light-harvesting complex at 2.5 Å resolution EMBO J. 2005 24 919-928.
50. P. Martinsuo S. Pursiheimo E.-M. Aro E. Rintamäki Dithiol oxidant and disulfide reductant dynamically regulate the phosphorylation of light-harvesting complex II proteins in thylakoid membrane Plant Physiol. 2003 133 37-46.
51. K. Maxwell G. N. Johnson Chlorophyll fluorescence: a practical guide J. Exp. Bot. 2000 51 659-668.
52. B. Demmig-Adams W. W. Adams D. H. Baker B. A. Logan D. R. Bowling A. S. Verhoeven Using chlorophyll fluorescence to assess the fraction of absorbed light allocated to thermal dissipation of excess excitation Physiol. Plant. 1996 98 253-264.
53. P. Muller X.-P. Li K. K. Niyogi Non-photochemical quenching. A response to excess light energy Plant Physiol. 2001 125 1558-1566.
54. B. Demmig-Adams Carotenoids and photoprotection in plants: a role for the xanthophyll zeaxanthin Biochim. Biophys. Acta 1990 1020 1-24.
55. G. N. Johnson A. J. Young J. D. Scholes P. Horton The dissipation of excess excitation energy in British plant species Plant, Cell Environ. 1993 16 673-679.
56. B. Demmig-Adams W. W. Adams, III The role of xanthophyll cycle carotenoids in the protection of photosynthesis Trends Plant Sci. 1996 1 21-26.
57. M. Eskling, A. Emanuelsson and H.-E. Åkerlund, in Regulation of Photosynthesis, ed. E.-M. Aro and B. Andersson, Kluwer Academic Publishers, Dordrecht, 2001, pp. 806–816.
58. B. Demmig-Adams W. W. Adams Photosynthesis-Harvesting sunlight safety Nature 2000 403 371.
59. X.-P. Li O. Björkman C. Shin A. R. Grossman M. Rosenquist S. Jansson K. K. Niyogi A pigment-binding protein essential for regulation of photosynthetic light harvesting Nature 2000 403 391-395.
60. P. Horton A. V. Ruban M. Wentworth Allosteric regulation of the light-harvesting system of photosystem II Philos. Trans. R. Soc. London, Ser. B 2000 355 1361-1370.
61. B. Robert A. A. Pascal P. Horton A. V. Ruban Insights into the molecular dynamics of the plant light-harvesting proteins in vivo Trends Plant Sci. 2004 9 385-390.
62. A. V. Ruban A. J. Young P. Horton Induction of nonphotochemical energy dissipation and absorbance changes in leaves. Evidence for changes in the state of the light-harvesting system of photosystem II in vivo Plant Physiol. 1993 102 741-750.
63. Z. Liu H. Yan K. Wang T. Kuang J. Zhang L. Gui X. An W. Chang Crystal structure of spinach major light-harvesting complex at 2.72 Å resolution Nature 2004 428 287-292.
64. A. V. Ruban P. J. Lee M. Wentworth A. J. Young P. Horton Determination of the stoichiometry and strength of binding of xanthophylls to the photosystem II light harvesting complexes J. Biol. Chem. 1999 274 10458-10465.
65. M. Rogner E. J. Boekema J. Barber How does photosystem 2 split water? The structural basis of efficient energy concersion Trends Biochem. Sci. 1996 21 44-49.
66. J. Komenda J. Masojídek Functional and structural changes of the PSII complex induced by high irradiance in cyanobacterial cells Eur. J. Biochem. 1995 233 677-682.
67. A. Rokka M. Suorsa A. Saleem N. Battchikova E.-M. Aro Synthesis and assembly of thylakoid protein complexes: multiple assembly steps of photosystem II Biochem. J. 2005 388 159-168.
68. H.-Y. Lee Y.-N. Hong W. S. Chow Photoinactivation of Photosystem II complexes and photoprotection by nonfunctional neighbours in Capsicum annuum L. leaves Planta 2001 212 332-342.
69. S. Matsubara W. S. Chow Populations of photoinactivated photosystem II reaction centers characterized by chlorophyll a fluorescence lifetime in vivo Proc. Natl. Acad. Sci. U. S. A. 2004 101 18234-18239.
70. O. Prasil, N. Adir and I. Ohad, in The Photosystems: Structure, Function and Molecular Biology. Topics in Photosynthesis, ed. J. Barber, Elsevier, The Netherlands, vol. II, pp. 293–348.
71. E.-M. Aro I. Virgin B. Andersson Photoinhibition of photosystem II-inactivation, protein damage and turnover Biochim. Biophys. Acta 1993 1143 113-134.
72. A. Melis Photosystem-II damage and repair cycle in chloroplasts: what modulates the rate of photodamage in vivo? Trends Plant Sci. 1999 4 130-135.
73. E. J. Boekema B. Hankamer D. Bald J. Kruip J. Nield A. F. Boonstra J. Barber M. Rogner Supramolecular structure of the photosystem II complex from green plants and cyanobacteria Proc. Natl. Acad. Sci. U. S. A. 1995 92 175-179.
74. B. Hankamer J. Nield D. Zheleva E. Boekema S. Jansson J. Barber Isolation and biochemical characterisation of monomeric and dimeric photosystem II complexes from spinach and their relevance to the organisation of photosystem II in vivo Eur. J. Biochem. 1997 243 422-429.
75. R. Barbato G. Friso F. Rigoni F. D. Vecchia G. M. Giacometti Structural changes and lateral redistribution of photosystem II during donor side photoinhibition of thylakoids J. Cell Biol. 1992 119 325-335.
76. E.-M. Aro M. Suorsa A. Rokka Y. Allahverdiyeva V. Paakkarinen A. Saleem N. Battchikova E. Rintamäki Dynamics of photosystem II; a proteomic approach to thylakoid protein complexes J. Exp. Bot. 2005 56 347-356.
77. V. Ebbert D. Godde Regulation of thylakoid protein phosphorylation in intact chloroplasts by the activity of kinases and phosphatases Biochim. Biophys. Acta 1994 1187 335-346.
78. A. Koivuniemi E.-M. Aro B. Andersson Degradation of the D1 and D2 proteins of photosystem II in higher plants is regulated by reversible phosphorylation Biochemistry 1995 34 16022-16029.
79. E. Rintamäki R. Kettunen E.-M. Aro Differential D1 dephosphorylation in functional and photodamaged photosystem II centres. Dephosphorylation is a prerequisite for degradation of damaged D1* J. Biol. Chem. 1996 271 14870-14875.
80. O. Kruse D. Zheleva J. Barber Stabilization of photosystem two dimers by phosphorylation: Implication for the regulation of the turnover of D1 protein FEBS Lett. 1997 408 276-280.
81. E. Baena-Gonzalez R. Barbato E.-M. Aro Role of PSII phosphorylation in the PSII repair cycle and oligomeric structure Planta 1999 208 196-204.
82. R. Kettunen S. Pursiheimo E. Rintamäki K. J. van Wijk E.-M. Aro Transcriptional and translational adjustments of psbA gene expression in mature chloroplasts during photoinhibition and subsequent repair of photosystem II Eur. J. Biochem. 1997 247 441-448.
83. V. Bonardi P. Pesaresi T. Becker E. Schleiff R. Wagner T. Pfannschmidt P. Jahns D. Leister Photosystem II core phosphorylation and photosynthetic acclimation require two different protein kinases Nature 2005 437 1179-1182.
84. M. Lindahl C. Spetea T. Hundal A. B. Oppenheim Z. Adam B. Andersson The thylakoid FtsH protease plays a role in the light-induced turnover of the photosystem II D1 protein Plant Cell 2000 12 419-431.
85. E. Kanervo C. Spetea Y. Nishiyama N. Murata B. Andersson E.-M. Aro Dissecting cyanobacterial proteolytic system: efficiency in inducing degradation of the D1 protein of photosystem II in cyanobacteria and plants Biochim. Biophys. Acta 2003 1607 131-140.
86. P. Silva E. Thompson S. Bailey O. Kruse C. W. Mullineaux C. Robinson N. H. Mann P. J. Nixon FtsH is involved in the early stages of repair of photosystem II in Synechocystis sp PCC 6803 Plant Cell 2003 15 2152-2164.
87. P. J. Nixon M. Barker M. Boehm R. de Vries J. Komenda FtsH-mediated repair of the photosystem II complex in response to light stress J. Exp. Bot. 2005 56 357-363.
88. Z. Adam A. Zaltsman G. Sinvany-Villalobo W. Sakamoto FtsH proteases in chloroplasts and cyanobacteria Physiol. Plant. 2005 123 386-390.
89. P. F. Huesgen H. Schuhmann I. Adamska The family of Deg proteases in cyanobacteria and chloroplasts of higher plants Physiol. Plant. 2005 123 413-420.
90. S. Bailey E. Thompson P. J. Nixon P. Horton C. W. Mullineaux C. Robinson N. H. Mann A critical role for the Var2 FtsH homologue of Arabidopsis thaliana in the photosystem II repair cycle in vivo J. Biol. Chem. 2002 277 2006-2011.
91. L. Zhang V. Paakkarinen K. J. van Wijk E.-M. Aro Co-translational assembly of the D1 protein into photosystem II J. Biol. Chem. 1999 274 16062-16067.
92. R. Nilsson J. Brunner N. E. Hoffman K. J. van Wijk Interactions of ribosome nascent chain complexes of the chloroplast-encoded D1 thylakoid membrane protein with cpSRP54 EMBO J. 1999 18 733-742.
93. L. Zhang V. Paakkarinen M. Suorsa E.-M. Aro A SecY homologue is involved in chloroplast-encoded D1 protein biogenesis J. Biol. Chem. 2001 276 37809-37814.
94. L. Zhang V. Paakkarinen K. J. van Wijk E.-M. Aro Biogenesis of the chloroplast-encoded D1 protein: regulation of translation elongation, insertion, and assembly into photosystem II Plant Cell 2000 12 1769-1781.
95. J. R. Bowyer J. C. L. Packer B. A. McCormack J. P. Whitelegge C. Robinson M. Taylor Carboxyl-terminal processing of the D1 protein and photoactivation of water splitting in photosystem II J. Biol. Chem. 1992 267 5424-5433.
96. M. Hager M. Hermann K. Biehler A. Krieger-Liszkay R. Bock Lack of the small plastid-encoded PsbJ polypeptide results in a defective water-splitting apparatus of photosystem II, reduced photosystem I levels and hypersensitivity to light J. Biol. Chem. 2002 277 14031-14039.
97. M. Suorsa R. E. Regel V. Paakkarinen N. Battchikova R. G. Herrmann E.-M. Aro Protein assembly of photosystem II and accumulation of subcomplexes in the absence of low molecular mass subunits PsbL and PsbJ Eur. J. Biochem. 2004 271 96-107.
98. L. G. Nijtmans L. de Jong M. Artal Sanz P. J. Coates J. A. Berden J. W. Back A. O. Muijsers H. van der Spek L. A. Grivell Prohibitins act as a membrane-bound chaperone for the stabilization of mitochondrial proteins EMBO J. 2000 19 2444-2451.
99. A. H. Mehler Studies on reactivities of illuminated chloroplasts. I. Mechanism of the reaction of oxygen and other Hill reagents Arch. Biochem. Biophys. 1951 33 65-77.
100. C. P. Osmond S. C. Grace Perspectives on photoinhibition and photorespiration in the field: quintessential inefficiencies of the light and dark reactions of photosynthesis? J. Exp. Bot. 1995 46 1351-1362.
101. U. Heber Irrungen, wirrungen? The Mehler reaction in relation to cyclic electron transport in leaves Photosynth. Res. 2002 73 223-231.
102. M. R. Badger S. von Caemerer S. Ruuska H. Nakano Electron flow to oxygen in higher plants and algae: rates and control of direct photoreduction (Mehler reaction) and rubisco oxygenase Philos. Trans. R. Soc. London, Ser. B 2000 355 1433-1446.
103. L. Rizhsky H. Liang R. Mittler The water–water cycle is essential for chloroplast protection in the absence of stress J. Biol. Chem. 2003 278 38921-38925.
104. D. C. Fork S. K. Herbert Electron transport and photophosphorylation by photosystem I in vivo in plants and cyanobacteria Photosynth. Res. 1993 36 149-168.
105. P. Barth B. Lagoutte P. Sétif Ferredoxin reduction by photosystem I from Synechocystis sp. PCC 6803: Toward an understanding of the respective roles of subunits PsaD and PsaE in ferredoxin binding Biochemistry 1998 37 16233-16241.
106. Y. Munekage M. Hojo J. Meurer T. Endo M. Tasaka T. Shikanai PGR5 is involved in cyclic electron flow around photosystem I and is essential for photoprotection in Arabidopsis Cell 2002 110 361-371.
107. H. M. Zhang J. P. Whitelegge W. A. Cramer Ferredoxin:NADP(+) oxidoreductase is a subunit of the chloroplast cytochrome b(6)f complex J. Biol. Chem. 2001 276 38159-38165.
108. D. Stroebel Y. Choquet J.-L. Popot D. Picot An atypical haem in the cytochrome b6f complex Nature 2003 426 413-418.
109. T. Shikanai T. Endo T. Hashimoto Y. Yamada K. Asada A. Yokota Directed disruption of the tobacco ndhB gene impairs cyclic electron flow around photosystem I Proc. Natl. Acad. Sci. U. S. A. 1998 95 9705-9709.
110. E. M. Horváth S. O. Peter T. Joet D. Rumeau L. Cournac G. V. Horváth T. A. Kavanagh C. Schäfer G. Peltier P. Medgyesy Targeted inactivation of the plastid ndhB gene in tobacco results in an enhanced sensitivity of photosynthesis to moderate stomatal closure Plant Physiol. 2000 123 1337-1349.
111. T. Joet L. Cournac G. Peltier M. Havaux Cyclic electron flow around photosystem I in C3 plants. In vivo control by the redox state of chloroplasts and involvement of the NDH-dehydrogenase complex Plant Physiol. 2002 128 760-769.
112. D. Rumeau N. Bécuwe-Linka A. Beyly M. Louwagie J. Garin G. Peltier New subunits NDH-M, -N, and -O, encoded by nuclear genes, are essential for plastid Ndh complex functioning in higher plants Plant Cell 2005 17 219-232.
113. Y. Munekage M. Hashimoto C. Miyake K.-I. Tomizawa T. Endo M. Tasaka T. Shikanai Cyclic electron flow around photosystem I is essential for photosynthesis Nature 2004 429 579-582.
114. S. Berry D. Schneider W. F. J. Vermaas M. Rögner Electron transport routes in whole cells of Synechocystis sp. strain PCC 6803: the role of the cytochrome bd-type oxidase Biochemistry 2002 41 3422-3429.
115. S. Berry Y. V. Bolychevtseva M. Rögner N. V. Karapetyan Photosynthetic and respiratory electron transport in the alkaliphilic cyanobacterium Arthrospira (Spirulina) platensis Photosynth. Res. 2003 78 67-76.
116. P. Bennoun Chlororespiration and the process of carotenoid biosynthesis Biochim. Biophys. Acta 2001 1506 133-142.
117. P. J. Nixon P. Maliga Reply…Chlororespiration: only half a story Trends Plant Sci. 1999 4 51.
118. P. J. Nixon Chlororespiration Philos. Trans. R. Soc. London, Ser. B 2000 355 1541-1547.
119. M. R. Aluru S. R. Rodermel Control of chloroplast redox by the IMMUTANS terminal oxidase Physiol. Plant. 2004 120 4-11.
120. G. Peltier L. Cournac Chlororespiration Annu. Rev. Plant Physiol. Plant Mol. Biol. 2002 53 523-550.
121. P. Carol D. Stevenson C. Bisanz J. Breitenbach G. Sandmann R. Mache G. Coupland M. Kunz Mutations in the Arabidopsis gene IMMUTANS cause a variegated phenotype by inactivating a chloroplast terminal oxidase associated with phytoene desaturation Plant Cell 1999 11 57-68.
122. D. Wu D. A. Wright C. Wetzel D. F. Voytas S. Rodermel The IMMUTANS variegation locus of Arabidopsis defines a mitochondrial alternative oxidase homolog that functions during early chloroplast biogenesis Plant Cell 1999 11 43-55.
123. L. Cournac K. Redding J. Ravenel D. Rumeau E. Josse M. Kuntz G. Peltier Electron flow between photosystem II and oxygen in chloroplasts of photosystem I-deficient algae is mediated by a quinol oxidase involved in chlororespiration J. Biol. Chem. 2000 275 17256-17262.
124. T. Joet B. Genty E. M. Josse M. Kuntz L. Cournac G. Peltier Involvement of a plastid terminal oxidase in plastoquinone oxidation as evidenced by expression of the Arabidopsis thaliana enzyme in tobacco J. Biol. Chem. 2002 277 31623-31630.
125. J. N. Baerr J. D. Thomas B. G. Taylor S. R. Rodermel G. R. Gray Differential photosynthetic compensatory mechanisms exist in the immutans mutant of Arabidopsis thaliana Physiol. Plant. 2005 124 390-402.
126. E. Baena-González Y. Allahverdiyeva Z. Svab P. Maliga E.-M. Josse M. Kuntz P. Mäenpää E.-M. Aro Deletion of the tobacco plastid psbA gene triggers an upregulation of the thylakoid-associated NAD(P)H dehydrogenase complex and the plastid terminal oxidase (PTOX) Plant J. 2003 35 704-716.
127. 559 mediates the oxidation of reduced plastoquinone in the dark J. Biol. Chem. 2003 278 13554-13560.
128. T. Ogawa A gene homologous to the subunit-2 gene of NADH dehydrogenase is essential to inorganic carbon transport of Synechocystis PCC 6803 Proc. Natl. Acad. Sci. U. S. A. 1991 88 4275-4278.
129. H. Mi T. Endo U. Schreiber T. Ogawa K. Asada Electron donation from cyclic and respiratory flows to the photosynthetic intersystem chain is mediated by pyridine nucleotide dehydrogenase in the cyanobacterium Synechocystis PCC 6803 Plant Cell Physiol. 1992 33 1233-1237.
130. G. Schmetterer, in The Molecular Biology of Cyanobacteria, ed. D. A. Bryant, Kluwer Academic Publishers, Dordrecht, The Netherlands, 1994, pp. 409–435.
131. H. Mi T. Endo T. Ogawa K. Asada Thylakoid membrane-bound, NADPH-specific pyridine nucleotide dehydrogenase complex mediated cyclic electron transport in the cyanobacterium Synechocystis sp. PCC 6803 Plant Cell Physiol. 1995 36 661-668.
132. 2 concentrating mechanisms in cyanobacteria: molecular components, their diversity and evolution J. Exp. Bot. 2003 54 609-622.
133. M. Herranen N. Battchikova P. Zhang A. Graf S. Sirpiö V. Paakkarinen E.-M. Aro Towards functional proteomics of membrane protein complexes in Synechocystis sp. PCC 6803 Plant Physiol. 2004 134 470-481.
134. P. Zhang N. Battchikova T. Jansen J. Appel T. Ogawa E.-M. Aro Expression and functional roles of the two distinct NDH-1 complexes and the carbon acquisition complex NdhD3/NdhF3/CupA/Sll1735 in Synechocystis sp PCC 6803 Plant Cell 2004 16 3326-3340.
135. P. Zhang N. Battchikova V. Paakkarinen H. Katoh M. Iwai M. Ikeuchi H. B. Pakrasi T. Ogawa E.-M. Aro Isolation, subunit composition and interaction of the NDH-1 complexes from Thermosynechococcus elongatus BP-1 Biochem. J. 2005 390 513-520.
136. P. Prommeenate A. M. Lennon C. Markert M. Hippler P. J. Nixon Subunit composition of NDH-1 complexes of Synechocystis sp PCC 6803-Identification of two new ndh gene products with nuclear-encoded homologues in the chloroplast Ndh complex J. Biol. Chem. 2004 279 28165-28173.
137. N. Battchikova P. Zhang S. Rudd T. Ogawa E.-M. Aro Identification of NdhL and Ssl1690 (NdhO) in NDH-1L and NDH-1M complexes of Synechocystis sp. PCC 6803 J. Biol. Chem. 2005 280 2587-2595.
138. 2-concentrating mechanism in the cyanobacterium Synechocystis sp. PCC 6803 Plant Physiol. 2003 132 218-229.
139. H.-L. Wang B. L. Postier R. L. Burnap Alterations in global patterns of gene expression in Synechocystis sp. PCC 6803 in response to inorganic carbon limitation and the inactivation of ndhR, a LysR family regulator J. Biol. Chem. 2004 279 5739-5751.
140. 3- uptake in Synechocystis sp. strain PCC 6803 J. Bacteriol. 2000 182 2591-2596.
141. 2 uptake systems in cyanobacteria: genes involved and their phylogenetic relationship with homologous genes in other organisms Proc. Natl. Acad. Sci. U. S. A. 2001 98 11789-11794.