Chlororespiration and cyclic electron flow around PSI during photosynthesis and plant stress response

Plant, Cell and Environment

Volumn 30, Issue 9, 2007, Pages 1041-1051

  Rumeau, Dominique ^a   Peltier, Gilles ^a   Cournac, Laurent ^a  

^a IRFM   (France)

Author keywords

Chloroplast; FQR; NADH dehydrogenase; PGR5; Photosystem; PTOX

Indexed keywords

OXIDOREDUCTASE; PLASTOQUINONE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE DEHYDROGENASE; WATER;

CHLOROPLAST; ELECTRON; ENVIRONMENTAL STRESS; PHENOTYPE; PHOTOSYNTHESIS;

CHLOROPLAST; ELECTRON TRANSPORT; HEAT; LIGHT; METABOLISM; OXIDATION REDUCTION REACTION; PHOTOSYNTHESIS; PHOTOSYSTEM I; PHYSIOLOGY; PLANT; REVIEW; THYLAKOID;

CHLOROPLASTS; ELECTRON TRANSPORT; HEAT; LIGHT; NADPH DEHYDROGENASE; OXIDATION-REDUCTION; OXIDOREDUCTASES; PHOTOSYNTHESIS; PHOTOSYNTHETIC REACTION CENTER COMPLEX PROTEINS; PHOTOSYSTEM I PROTEIN COMPLEX; PLANTS; PLASTOQUINONE; THYLAKOIDS; WATER;

EMBRYOPHYTA;

EID: 34547546173     PISSN: 01407791     EISSN: 13653040     Source Type: Journal    
DOI: 10.1111/j.1365-3040.2007.01675.x     Document Type: Review

References (104)

1. Aluru M.R., Bae H., Wu D. Rodermel S.R. (2001) The Arabidopsis immutans mutation affects plastid differentiation and the morphogenesis of white and green sectors in variegated plants. Plant Physiology 127, 67 77.
2. Aluru M.R., Yu F., Fu A.G. Rodermel S. (2006) Arabidopsis variegation mutants: new insights into chloroplast biogenesis. Journal of Experimental Botany 57, 1871 1881.
3. Amann K., Lezhneva L., Wanner G., Herrmann R.G. Meurer J. (2004) ACCUMULATION OF PHOTOSYSTEM ONE1, a member of a novel gene family, is required for accumulation of [4Fe-4S] cluster-containing chloroplast complexes and antenna proteins. Plant Cell 16, 3084 3097.
4. Baena-Gonzalez E., Allahverdiyeva Y., Svab Z., Maliga P., Josse E.M., Kuntz M., Maenpaa P. Aro E.M. (2003) 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). The Plant Journal 35, 704 716.
5. Barkan A. Goldschmidt-Clermont M. (2000) Participation of nuclear genes in chloroplast gene expression. Biochimie 82, 559 572.
6. Barth C. Krause G.H. (2002) Study of tobacco transformants to assess the role of chloroplastic NAD(P)H dehydrogenase in photoprotection of photosystems I and II. Planta 216, 273 279.
7. Battchikova N., Zhang P.P., Rudd S., Ogawa T. Aro E.M. (2005) Identification of NdhL and Ssl1690 (NdhO) in NDH-1L, and NDH-1M complexes of Synechocystis sp PCC 6803. Journal of Biological Chemistry 280, 2587 2595.
8. Bendall D.S. Manasse R.S. (1995) Cyclic photophosphorylation and electron transport. Biochimica et Biophysica Acta 1229, 23 38.
9. Bennoun P. (1982) Evidence for a respiratory chain in the chloroplast. Proceedings of the National Academy of Sciences of the USA 79, 4352 4356.
10. Bock R. (2000) Sense from nonsense: how the genetic information of chloroplasts is altered by RNA editing. Biochimie 82, 549 557.
11. Bojko M., Kruk J. Wieckowski S. (2003) Plastoquinones are effectively reduced by ferredoxin : NADP+ oxidoreductase in the presence of sodium cholate micelles. Significance for cyclic electron transport and chlororespiration. Phytochemistry 64, 1055 1060.
12. Bondarava N., De Pascalis L., Al-Babili S., Goussias C., Golecki J.R., Beyer P., Bock R. Krieger-Liszkay A. (2003) Evidence that cytochrome b559 mediates the oxidation of reduced plastoquinone in the dark. Journal of Biological Chemistry 278, 13554 13560.
13. Breyton C., Nandha B., Johnson G.N., Joliot P. Finazzi G. (2006) Redox modulation of cyclic electron flow around photosystem I in C3 plants. Biochemistry 45, 13465 13475.
14. Bukhov N. Carpentier R. (2004) Alternative photosystem I-driven electron transport routes: mechanisms and functions. Photosynthesis Research 82, 17 33.
15. Bukhov N.G., Samson G. Carpentier R. (2000) Nonphotosynthetic reduction of the intersystem electron transport chain of chloroplasts following heat stress. Steady-state rate. Photochemistry and Photobiology 72, 351 357.
16. Burrows P.A., Sazanov L.A., Svab Z., Maliga P. Nixon P.J. (1998) Identification of a functional respiratory complex in chloroplasts through analysis of tobacco mutants containing disrupted plastid ndh genes. EMBO Journal 17, 868 876.
17. del Campo E.M., Sabater B. Martin M. (2000) Transcripts of the ndhH-D operon of barley plastids: possible role of unedited site III in splicing of the ndhA intron. Nucleic Acids Research 28, 1092 1098.
18. del Campo E.M., Sabater B. Martin M. (2002) Post-transcriptional control of chloroplast gene expression - accumulation of stable psaC mRNA is due to downstream RNA cleavages in the ndhD gene. Journal of Biological Chemistry 277, 36457 36464.
19. Carol P., Stevenson D., Bisanz C., Breitenbach J., Sandmann G., Mache R., Coupland G. Kuntz M. (1999) Mutations in the Arabidopsis gene immutans cause a variegated phenotype by inactivating a chloroplast terminal oxidase associated with phytoene desaturation. Plant Cell 11, 57 68.
20. Casano L.M., Zapata J.M., Martin M. Sabater B. (2000) Chlororespiration and poising of cyclic electron transport - plastoquinone as electron transporter between thylakoid NADH dehydrogenase and peroxidase. Journal of Biological Chemistry 275, 942 948.
21. Casano L.M., Martin M. Sabater B. (2001) Hydrogen peroxide mediates the induction of chloroplastic Ndh complex under photooxidative stress in barley. Plant Physiology 125, 1450 1458.
22. Chateigner-Boutin A.L. Hanson M.R. (2003) Developmental co-variation of RNA editing extent of plastid editing sites exhibiting similar cis-elements. Nucleic Acids Research 31, 2586 2594.
23. Corneille S., Cournac L., Guedeney G., Havaux M. Peltier G. (1998) Reduction of the plastoquinone pool by exogenous NADH and NADPH in higher plant chloroplasts - characterization of a NAD(P)H-plastoquinone oxidoreductase activity. Biochimica et Biophysica Acta 1363, 59 69.
24. Cournac L., Redding K., Ravenel J., Rumeau D., Josse E.M., Kuntz M. Peltier G. (2000) Electron flow between photosystem II and oxygen in chloroplasts of photosystem I-deficient algae is mediated by a quinol oxidase involved in chlororespiration. Journal of Biological Chemistry 275, 17256 17262.
25. Cournac L., Latouche G., Cerovic Z., Redding K., Ravenel J. Peltier G. (2002) In vivo interactions between photosynthesis, mitorespiration, and chlororespiration in Chlamydomonas reinhardtii. Plant Physiology 129, 1921 1928.
26. Darie C.C., De Pascalis L., Mutschler B. Haehnel W. (2006) Studies of the Ndh complex and photosystem II from mesophyll and bundle sheath chloroplasts of the C-4-type plant Zea mays. Journal of Plant Physiology 163, 800 808.
27. Endo T., Shikanai T., Takabayashi A., Asada K. Sato F. (1999) The role of chloroplastic NAD(P)H dehydrogenase in photoprotection. FEBS Letters 457, 5 8.
28. Favory J.-J., Kobayshi M., Tanaka K., Peltier G., Kreis M., Valay J.-G. Lerbs-Mache S. (2005) Specific function of a plastid sigma factor for ndhF gene transcription. Nucleic Acids Research 33, 5991 5999.
29. Fischer M., Funk E. Steinmüller K. (1997) The expression of subunits of the mitochondrial complex I-homologous NAD(P)H-plastoquinone-oxidoreductase during plastid development. Zeitschrift für Naturforschung Section C Journal of Biosciences 52, 481 486.
30. Fork D.C. Herbert S.K. (1993) Electron transport and photophosphorylation by photosystem I in vivo in plants and cyanobacteria. Photosynthesis Research 36, 149 168.
31. Funk E., Schafer E. Steinmuller K. (1999) Characterization of the complex I-homologous NAD(P)H-plastoquinone-oxidoreductase (NDH-complex) of maize chloroplasts. Journal of Plant Physiology 154, 16 23.
32. Golding A.J., Finazzi G. Johnson G.N. (2004) Reduction of the thylakoid electron transport chain by stromal reductants - evidence for activation of cyclic electron transport upon dark adaptation or under drought. Planta 220, 356 363.
33. Guedeney G., Corneille S., Cuine S. Peltier G. (1996) Evidence for an association of ndh B, ndh J gene products and ferredoxin-NADP-reductase as components of a chloroplastic NAD(P)H dehydrogenase complex. FEBS Letters 378, 277 280.
34. Guera A., de Nova P.G. Sabater B. (2000) Identification of the Ndh (NAD(P)H-plastoquinone-oxidoreductase) complex in etioplast membranes of barley: changes during photomorphogenesis of chloroplasts. Plant and Cell Physiology 41, 49 59.
35. Guera A., Calatayud A., Sabater B. Barreno E. (2005) Involvement of the thylakoidal NADH-plastoquinoneoxidoreductase complex in the early responses to ozone exposure of barley (Hordeum vulgare L.) seedlings. Journal of Experimental Botany 56, 205 218.
36. Harbinson J. Foyer C.H. (1991) Relationships between the efficiencies of photosystems I and II and stromal redox state in CO2-free air - evidence for cyclic electron flow in vivo. Plant Physiology 97, 41 49.
37. Hashimoto M., Endo T., Peltier G., Tasaka M. Shikanai T. (2003) A nucleus-encoded factor, CRR2, is essential for the expression of chloroplast ndhB in Arabidopsis. The Plant Journal 36, 541 549.
38. Havaux M. (1996) Short-term responses of photosystem I to heat stress. Induction of a PS Il-independent electron transport through PS I fed by stromal components. Photosynthesis Research 47, 85 97.
39. Havaux M., Greppin H. Strasser R.J. (1991) Functioning of photosystem I and photosystem II in pea leaves exposed to heat stress in the presence or absence of light. Analysis using in vivo fluorescence, absorbance, oxygen and photoacoustic measurements. Planta 186, 88 98.
40. Havaux M., Rumeau D. Ducruet J.M. (2005) Probing the FQR and NDH activities involved in cyclic electron transport aroundphotosystem I by the 'afterglow' luminescence. Biochimica et Biophysica Acta 1709, 203 213.
41. Heber U. Walker D. (1992) Concerning a dual function of coupled cyclic electron transport in leaves. Plant Physiology 100, 1621 1626.
42. Hirose T. Sugiura M. (1997) Both RNA editing and RNA cleavage are required for translation of tobacco chloroplast ndhD mRNA: a possible regulatory mechanism for the expression of a chloroplast operon consisting of functionally unrelated genes. The EMBO Journal 16, 6804 6811.
43. Hoefnagel M.H.N., Atkin O.K. Wiskich J.T. (1998) Interdependence between chloroplasts and mitochondria in the light and the dark. Biochimica et Biophysica Acta 1366, 235 255.
44. Horvath E.M., Peter S.O., Joet T., Rumeau D., Cournac L., Horvath G.V., Kavanagh T.A., Schafer C., Peltier G. Medgyesy P. (2000) Targeted inactivation of the plastid ndhB gene in tobacco results in an enhanced sensitivity of photosynthesis to moderate stomatal closure. Plant Physiology 123, 1337 1349.
45. Joet T., Cournac L., Horvath E.M., Medgyesy P. Peltier G. (2001) Increased sensitivity of photosynthesis to antimycin a induced by inactivation of the chloroplast ndhB gene. Evidence for a participation of the NADH-dehydrogenase complex to cyclic electron flow around photosystem I. Plant Physiology 125, 1919 1929.
46. Joet T., Cournac L., Peltier G. Havaux M. (2002a) Cyclic electron flow around photosystem I in C-3 plants. In vivo control by the redox state of chloroplasts and involvement of the NADH-dehydrogenase complex. Plant Physiology 128, 760 769.
47. Joet T., Genty B., Josse E.M., Kuntz M., Cournac L. Peltier G. (2002b) Involvement of a plastid terminal oxidase in plastoquinone oxidation as evidenced by expression of the Arabidopsis thaliana enzyme in tobacco. Journal of Biological Chemistry 277, 31623 31630.
48. Johnson G.N. (2005) Cyclic electron transport in C3 plants: fact or artefact? Journal of Experimental Botany 56, 407 416.
49. Joliot P. Joliot A. (2005) Quantification of cyclic and linear flows in plants. Proceedings of the National Academy of Sciences of the USA 102, 4913 4918.
50. Jordan D.B. Ogren W. (1984) The CO2/O2 specificity of ribulose-1,5-biphosphate carboxylase/oxygenase. Planta 161, 308 313.
51. Khorobrykh S.A. Ivanov B.N. (2002) Oxygen reduction in a plastoquinone pool of isolated pea thylakoids. Photosynthesis Research 71, 209 219.
52. Kofer W., Koop H.U., Wanner G. Steinmuller K. (1998) Mutagenesis of the genes encoding subunits A, C, H, I, J and K of the plastid NAD(P)H- plastoquinone-oxidoreductase in tobacco by polyethylene glycol-mediated plastome transformation. Molecular & General Genetics 258, 166 173.
53. Kotera E., Tasaka M. Shikanai T. (2005) A pentatricopeptide repeat protein is essential for RNA editing in chloroplasts. 433, 326 330.
54. Kruk J. Strzalka K. (2001) Redox changes of cytochrome b559 in the presence of plastoquinones. Journal of Biological Chemistry 276, 86 91.
55. Kubicki A., Funk E., Westhoff P. Steinmuller K. (1996) Differential expression of plastome-encoded ndh genes in mesophyll and bundle-sheath chloroplasts of the C-4 plant Sorghum bicolor indicates that the complex I-homologous NAD(P)H-plastoquinone oxidoreductase is involved in cyclic electron transport. Planta 199, 276 281.
56. Lascano H.R., Casano L.M., Martin M. Sabater B. (2003) The activity of the chloroplastic Ndh complex is regulated by phosphorylation of the NDH-F subunit. Plant Physiology 132, 256 262.
57. Lennon A.M., Prommeenate P. Nixon P.J. (2003) Location, expression and orientation of the putative chlororespiratory enzymes, Ndh and IMMUTANS, in higher-plant plastids. Planta 218, 254 260.
58. Lintala M., Allahverdiyeva Y., Kidron H., Piippo M., Battchikova N., Suorsa M., Rintamaki E., Salminen T.A., Aro E.-M. Mulo P. (2007) Structural and functional characterization of ferredoxin-NADP+-oxidoreductase using knock-out mutants of Ara1bidopsis. The Plant Journal 49, 1041 1052.
59. Loschelder H., Schweer J., Link B. Link G. (2006) Dual temporal role of plastid Sigma factor 6 in Arabidopsis development. Plant Physiology 142, 642 650.
60. Maier R.M., Zeltz P., Kässel H., Bonnard G., Gualberto J.M. Grienenberger J.M. (1996) RNA editing in plant mitochondria and chloroplasts. Plant Molecular Biology 32, 343 365.
61. McDonald A.E. Vanlerberghe G.C. (2006) Origins, evolutionary history, and taxonomic distribution of alternative oxidase and plastoquinol terminal oxidase Comparative Biochemistry and Physiology D-Genomics & Proteomics 1, 357 364.
62. Meurer J., Berger A. Westhoff P. (1996) A nuclear mutant of Arabidopsis with impaired stability on distinct transcripts of the plastid psbB, psbD/C, ndhH, and ndhC operons. Plant Cell 8, 1193 1207.
63. Miyake C., Miyata M., Shinzaki Y. Tomizawa K.-i. (2005) CO2 response of cyclic electron flow around PSI (CEF-PSI) in tobacco leaves - relative electron fluxes through PSI and PSII determine the magnitude of non-photochemical quenching (NPQ) of Chl fluorescence. Plant and Cell Physiology 46, 629 637.
64. Monde R.A., Schuster G. Stern D.B. (2000) Processing and degradation of chloroplast mRNA. Biochimie 82, 573 582.
65. Mubarakshina M., Khorobrykh S. Ivanov B. (2006) Oxygen reduction in chloroplast thylakoids results in production of hydrogen peroxide inside the membrane. Biochimica et Biophysica Acta 1757, 1496 1503.
66. Munekage Y., Hojo M., Meurer J., Endo T., Tasaka M. Shikanai T. (2002) PGR5 is involved in cyclic electron flow around photosystem I and is essential for photoprotection in Arabidopsis. Cell 110, 361 371.
67. Munekage Y., Hashimoto M., Miyake C., Tomizawa K., Endo T., Tasaka M. Shikanai T. (2004) Cyclic electron flow around photosystem I is essential for photosynthesis. Nature 429, 579 582.
68. Munshi M.K., Kobayashi Y. Shikanai T. (2005) Identification of a novel protein, CRR7, required for the stabilization of the chloroplast NAD(P)H dehydrogenase complex in Arabidopsis. The Plant Journal 44, 1036 1044.
69. Munshi M.K., Kobayashi Y. Shikanai T. (2006) CHLORORESPIRATORY REDUCTION 6 is a novel factor required for accumulation of the chloroplast NAD(P)H dehydrogenase complex in Arabidopsis. Plant Physiology 141, 737 744.
70. Muraoka R., Okuda K., Kobayashi Y. Shikanai T. (2006) A eukaryotic factor required for accumulation of the chloroplast NAD(P)H dehydrogenase complex in Arabidopsis. Plant Physiology 142, 1683 1689.
71. Mus F., Cournac L., Cardettini W., Caruana A. Peltier G. (2005) Inhibitor studies on non-photochemical plastoquinone reduction and H-2 photoproduction in Chlamydomonas reinhardtii. Biochimica et Biophysica Acta-Bioenergetics 1708, 322 332.
72. Nagashima A., Hanaoka M., Motohashi R., Seki M., Shinozaki K., Kanamaru K., Takahashi H. Tanaka K. (2004) DNA microarray analysis of plastid gene expression in an Arabidopsis mutant deficient in a plastid transcription factor sigma, SIG2. Bioscience, Biotechnology and Biochemistry 68, 694 704.
73. Nixon P.J. (2000) Chlororespiration. Philosophical Transactions of the Royal Society of London Series B-Biological Sciences 355, 1541 1547.
74. Niyogi K.K. (2000) Safety valves for photosynthesis. Current Opinion in Plant Biology 3, 455 460.
75. Okutani S., Hanke G.T., Satomi Y., Takao T., Kurisu G., Suzuki A. Hase T. (2005) Three maize leaf ferredoxin : NADPH oxidoreductases vary in subchloroplast location, expression, and interaction with ferredoxin. Plant Physiology 139, 1451 1459.
76. Osmond C.B. (1981) Photorespiration and photoinhibition. Some implications for the energetics of photosynthesis. Biochimica et Biophysica Acta 639, 77 98.
77. Peltier G. Cournac L. (2002) Chlororespiration. Annual Review of Plant Biology 53, 523 550.
78. Prommeenate P., Lennon A.M., Markert C., Hippler M. Nixon P.J. (2004) 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. Journal of Biological Chemistry 279, 28165 28173.
79. Quiles M.J. (2006) Stimulation of chlororespiration by heat and high light intensity in oat plants. Plant, Cell & Environment 29, 1463 1470.
80. Quiles M.J. Cuello J. (1998) Association of Ferredoxin-NADP oxidoreductase with the chloroplastic pyridine nucleotide dehydrogenase complex in barley leaves. Plant Physiology 117, 235 244.
81. Quiles M.J. Lopez N.I. (2004) Photoinhibition of photosystems I and II induced by exposure to high light intensity during oat plant growth - effects on the chloroplast NADH dehydrogenase complex. Plant Science 166, 815 823.
82. Rizhsky L., Hallak-Herr E., Van Breusegem F., Rachmilevitch S., Barr J.E., Rodermel S., Inze D. Mittler R. (2002) Double antisense plants lacking ascorbate peroxidase and catalase are less sensitive to oxidative stress than single antisense plants lacking ascorbate peroxidase or catalase. The Plant Journal 32, 329 342.
83. Rodriguez R.E., Lodeyro A., Poli H.O., et al 2007) Transgenic tobacco plants overexpressing chloroplastic ferredoxin-NADP(H) reductase display normal nates of photosynthesis and increased tolerance to oxidative stress. Plant Physiology 143, 639 649.
84. Rosso D., Ivanov A.G., Fu A., et al 2006) IMMUTANS does not act as a stress-induced safety valve in the protection of the photosynthetic apparatus of Arabidopsis during steady-state photosynthesis. Plant Physiology 142, 574 585.
85. Rumeau D., Becuwe-Linka N., Beyly A., Louwagie M., Garin J. Peltier G. (2005) New subunits NDH-M, -N, and -O, encoded by nuclear genes, are essential for plastid Ndh complex functioning in higher plants. Plant Cell 17, 219 232.
86. Salvucci M.E. Crafts-Brandner S.J. (2004a) Inhibition of photosynthesis by heat stress: the activation state of Rubisco as a limiting factor in photosynthesis. Physiologia Plantarum 120, 179 186.
87. Salvucci M.E. Crafts-Brandner S.J. (2004b) Relationship between the heat tolerance of photosynthesis and the thermal stability of rubisco activase in plants from contrasting thermal environments. Plant Physiology 134, 1460 1470.
88. Sazanov L.A., Burrows P.A. Nixon P.J. (1998a) The chloroplast Ndh complex mediates the dark reduction of the plastoquinone pool in response to heat stress in tobacco leaves. FEBS Letters 429, 115 118.
89. Sazanov L.A., Burrows P.A. Nixon P.J. (1998b) The plastid ndh genes code for an NADH-specific dehydrogenase: isolation of a complex I analogue from pea thylakoid membranes. Proceedings of the National Academy of Sciences of the USA 95, 1319 1324.
90. Shikanai T. (2007) Cyclic electron transport around photosystem I: genetic approaches. Annual Review of Plant Biology 58, Epub ahead of print doi:10.1146/annurev.arplant.58.091406.110525.
91. Shikanai T., Endo T., Hashimoto T., Yamada Y., Asada K. Yokota A. (1998) Directed disruption of the tobacco ndhB gene impairs cyclic electron flow around photosystem I. Proceedings of the National Academy of Sciences of the USA 95, 9705 9709.
92. Sonoike K. (1996) Photoinhibition of photosystem I: its physiological significance in the chilling sensitivity of plants. Plant and Cell Physiology 37, 239 247.
93. Stegemann S., Hartmann S., Ruf S. Bock R. (2003) High-frequency gene transfer from the chloroplast genome to the nucleus. Proceedings of the National Academy of Sciences of the USA 100, 8828 8833.
94. Streb P., Josse E.-M., Gallouet E., Baptist F., Kuntz M. Cornic G. (2005) Evidence for alternative electron sinks to photosynthetic carbon assimilation in the high mountain plant species Ranunculus glacialis. Plant, Cell & Environment 28, 1123 1135.
95. Sugita M. Sugiura M. (1996) Regulation of gene expression in chloroplasts of higher plants. Plant Molecular Biology 32, 315 326.
96. Takabayashi A., Kishine M., Asada K., Endo T. Sato F. (2005) Differential use of two cyclic electron flows around photosystem I for driving CO2-concentration mechanism in C-4 photosynthesis. Proceedings of the National Academy of Sciences of the USA 102, 16898 16903.
97. Teicher H.B. Scheller H.V. (1998) The NAD(P)H dehydrogenase in barley thylakoids is photoactivatable and uses NADPH as well as NADH. Plant Physiology 117, 525 532.
98. Tsudzuki T., Wakasugi T. Sugiura M. (2001) Comparative analysis of RNA editing sites in higher plant chloroplasts. Journal of Molecular Evolution 53, 327 332.
99. Wang P., Duan W., Takabayashi A., Endo T., Shikanai T., Ye J.Y. Mi H.L. (2006) Chloroplastic NAD(P)H dehydrogenase in tobacco leaves functions in alleviation of oxidative damage caused by temperature stress. Plant Physiology 141, 465 474.
100. Wu D.Y., Wright D.A., Wetzel C., Voytas D.F. Rodermel S. (1999) The immutans variegation locus of Arabidopsis defines a mitochondrial alternative oxidase homolog that functions during early chloroplast biogenesis. Plant Cell 11, 43 55.
101. Yamamoto H., Kato H., Shinzaki Y., et al 2006) Ferredoxin limits cyclic electron flow around PSI (CEF-PSI) in higher plants - stimulation of CEF-PSI enhances non-photochemical quenching of Chl fluorescence in transplastomic tobacco. Plant and Cell Physiology 47, 1355 1371.
102. Yamane Y., Shikanai T., Kashino Y., Koike H. Satoh K. (2000) Reduction of Q(A) in the dark: another cause of fluorescence F-o increases by high temperatures in higher plants. Photosynthesis Research 63, 23 34.
103. Zapata J.M., Guera A., Esteban-Carrasco A., Martin M. Sabater B. (2005) Chloroplasts regulate leaf senescence: delayed senescence in transgenic ndhF-defective tobacco. Cell Death and Differentiation 12, 1277 1284.
104. Zhang H., Whitelegge J.P. Cramer W.A. (2001) Ferredoxin:NADP+ oxidoreductase is a subunit of the chloroplast cytochrome b6f complex. Journal of Biological Chemistry 276, 38159 38165.