Chloroplasts as source and target of cellular redox regulation: A discussion on chloroplast redox signals in the context of plant physiology

Journal of Experimental Botany

Volumn 56, Issue 416, 2005, Pages 1449-1462

  Baier, Margarete ^a   Dietz, Karl Josef ^a  

^a BIELEFELD UNIVERSITY   (Germany)

Author keywords

Abscisic acid; Antioxidants; Chloroplast; Gene expression; Oxolipin; Peroxiredoxin; Photosynthesis; Redox regulation; Signalling; Stress

Indexed keywords

BIOSYNTHESIS; CELLS; ENZYMES; GENES; METABOLISM; MOLECULAR WEIGHT; ORGANIC ACIDS; PATHOLOGY; REDOX REACTIONS;

CELLULAR REDOX REGULATION; CHLOROPLASTS; PHOTO-OXIDATIVE DAMAGE; SIGNAL TRANSMISSION;

PLANTS (BOTANY);

VEGETABLE PROTEIN;

CELL NUCLEUS; CHLOROPLAST; METABOLISM; OXIDATION REDUCTION REACTION; PHOTOSYNTHESIS; PHYSIOLOGY; PLANT; REVIEW; SIGNAL TRANSDUCTION;

CELL NUCLEUS; CHLOROPLASTS; OXIDATION-REDUCTION; PHOTOSYNTHESIS; PLANT PROTEINS; PLANTS; SIGNAL TRANSDUCTION;

EID: 20044391613     PISSN: 00220957     EISSN: None     Source Type: Journal    
DOI: 10.1093/jxb/eri161     Document Type: Review

References (138)

1. Ahlfors R, Land S, Overmyer K, et al. 2004. Arabidopsis RADICAL-INDUCED CELL DEATH1 belongs to the WWE protein-protein interaction domain protein family and modulates abscisic acid, ethylene, and methyljasmonate responses. The Plant Cell 16, 1925-1937.
2. Allen JF. 1992. Protein phosphorylation in regulation of photosynthesis. Biochimica et Biophysica Acta 1098, 275-335.
3. Asada K. 2000. The water-water cycle as alternative photon and electron sink. Philosophical Transactions of the Royal Society London B 355, 1419-1431.
4. Asai T, Tena G, Plotnikova J, Willmann MR, Chiu W-L, Gomez-Gomez L, Boller T, Ausubel FM, Sheen J. 2002. MAP kinase signalling cascade in Arabidopsis innate immunity. Nature 415, 977-983.
5. 2. Plant Physiology 135, 1685-1696.
6. Baier M, Dietz K-J. 1996. Primary structure and expression of plant homologues of animal and fungal thioredoxin-dependent peroxide reductases and bacterial alkyl hydroperoxide reductases. Plant Molecular Biology 31, 553-564.
7. Baier M, Dietz K-J. 1997. The plant 2-Cys peroxiredoxin BAS1 is a nuclear-encoded chloroplast protein: its expressional regulation, phylogenetic origin, and implications for its specific physiological function in plants. The Plant Journal 60, 282-314.
8. Baier M, Dietz K-J. 1998. The costs and benefits of oxygen for photosynthesizing cells. Progress in Botany 60, 282-314.
9. Baier M, Dietz K-J. 1999a. Alkyl hydroperoxide reductases: the way out of the oxidative breakdown of lipids in chloroplasts. Trends in Plant Science 4, 166-168.
10. Baier M, Dietz K-J. 1999b. Protective function of chloroplast 2-cysteine peroxiredoxin in photosynthesis. Evidence from transgenic Arabidopsis. Plant Physiology 119, 1407-1414.
11. Baier M, Noctor G, Foyer CH, Dietz KJ. 2000. Antisense suppression of 2-Cys peroxiredoxin in Arabidopsis specifically enhanced activities and expression of enzymes associated with ascorbate metabolism but not glutathione metabolism. Plant Physiology 124, 823-832.
12. Baier M, Ströher E, Dietz KJ. 2004. The acceptor availability at photosystem I and ABA control nuclear expression of 2-Cys peroxiredoxin-A in Arabidopsis thaliana. Plant and Cell Physiology 45, 997-1006.
13. Ball L, Accotto G-P, Bechtold U, et al. 2004. Evidence for a direct link between glutathione biosynthesis and stress defense gene expression in Arabidopsis. The Plant Cell 16, 2448-2462.
14. Barnes D, Mayfield SP. 2003. Redox control of post-transcriptional processes in the chloroplast. Antioxidants and Redox Signaling 5, 89-94.
15. Beale SJ. 1999. Enzymes in chlorophyll biosynthesis. Photosynthesis Research 60, 43-73.
16. Berger S, Bell E, Mullet JE. 1996. Two methyl jasmonate-insensitive mutants show altered expression of AtVsp in response to methyl jasmonate and wounding. Plant Physiology 111, 525-531.
17. Blankenship RE. 2002. Molecular mechanisms of photosynthesis. London: Blackwell.
18. Blée E, Joyard J. 1996. Envelope membranes from spinach chloroplasts are a site of metabolism of PUFA hydroperoxides. Plant Physiology 110, 445-454.
19. Bolle C, Sopory SL, Lübberstedt T, Klösgen R, Herrmann RG, Oelmüller R. 1994. The role of plastids in the expression of nuclear genes for thylakoid proteins studied with chemirc β-glucuronidase gene fusions. Plant Physiology 105, 1355-1364.
20. Bratt CE, Arvidsson P-O, Carlsson M, Åkerlund H-E. 1995. Regulation of violaxanthin de-epoxidase activity by pH and ascorbate concentration. Photosynthesis Research 45, 169-175.
21. Chang CC-C, Ball L, Fryer MJ, Baker NR, Karpinski S, Mullineaux PM. 2004. Induction of ASCORBATE PEROXIDASE 2 expression in wounded Arabidopsis leaves does not involve known wound-signalling pathways but is associated with changes in photosynthesis. The Plant Journal 38, 499-511.
22. Chen YB, Durnford DG, Koblizek M, Falkowski PG. 2004. Plastid regulation of Lhcb1 transcription in the chlorophyte alga Dunaliella tertiolecta. Plant Physiology 136, 3737-3750.
23. Chen W, Provart NJ, Glazebrook J, et al. 2002. Expression profile matrix of Arabidopsis transcription factor genes suggests their putative functions in response to environmental stresses. The Plant Cell 14, 559-574.
24. Cheong YH, Chang H-S, Gupta R, Wang X, Zhu T, Luan S. 2002. Transcriptional profiling reveals novel interactions between wounding, pathogen, abiotic stress, and hormonal responses in Arabidopsis. Plant Physiology 129, 661-677.
25. Chew O, Whelan J, Millar AH. 2003. Molecular definition of the ascorbate-glutathione cycle in Arabidopsis mitochondria reveals dual targeting of antioxidant defenses in plants. Journal of Biological Chemistry 278, 46869-46877.
26. Collin V, Lamkemeyer P, Miginiac-Maslow M, Hirasawa M, Knaff DB, Dietz K-J, Issakidis-Bourguet E. 2004. Characterization of plastidial thioredoxins from Arabidopsis belonging to the new y-type. Plant Physiology 136, 4088-4095.
27. Conklin PL, Pallanca JE, Last RL, Smirnoff N. 1997. L-Ascorbic acid metabolism in the ascorbate-deficient Arabidopsis mutant vtc1. Plant Physiology 115, 1227-1285.
28. Davletova S, Rizhsky L, Liang H, Shengquiang Z, Oliver DJ, Coutu J, Shulaev V, Schlauch K, Mittler R. 2005. Cytosolic ascorbate peroxidase I is a central component of the reactive oxygen gene network of Arabidopsis. The Plant Cell 17, 268-281.
29. deLeon IP, Sanz A, Hamberg M, Castresana C. 2002. Involvement of the Arabidopsis alpha-DOX1 fatty acid dioxygenase against oxidative stress and cell death. The Plant Journal 29, 61-72.
30. Desikan R, AH-Mackerness S, Hancock JT, Neill SJ. 2001. Regulation of the Arabidopsis transcriptome by oxidative stress. Plant Physiology 127, 159-172.
31. Després C, Chubak C, Rochon A, Clark R, Bethune T, Desveaux D, Fobert PR. 2003. The Arabidopsis NPR1 disease resistance protein is a novel cofactor that confers redox regulation of DNA binding activity to the basic domain/leucine zipper transcription factor TGA1. The Plant Cell 15, 2181-2191.
32. Dietz KJ. 2003. Redox control, redox signaling, and redox homeostasis in plant cells. International Reviews in Cytology 228, 141-193.
33. Dietz KJ, Horling F, König J, Baier M. 2002. The function of the chloroplast 2-cysteine peroxiredoxin in peroxide detoxification and its regulation. Journal of Experimental Botany 53, 1321-1329.
34. Dijkwel PP, Huijser C, Weisbeek PJ, Smeekens SCM. 1997. Sucrose control of phytochrome A signaling in Arabidopsis. The Plant Cell 9, 583-595.
35. Elstner EF. 1990. Der Sauerstoff: Biochemie, Biologie, Medizin. Mannheim: BI Wissenschaftsverlag.
36. Escoubas J-M, Lomas M, LaRoche S, Stutios LM, Angell NA, Mindrinos M, Cho RJ, Oefner PJ, Davis RW, Ausubel FM. 1995. Light intensity regulation of cab gene transcription is signalled by the redox state of the plastoquinone pool. Proceedings of the National Academy of Sciences, USA 92, 10237-10241.
37. Eskling M, Arvidsson P-O, Åkerlund H-E. 1997. The xanthophylls cycle, its regulation and components. Physiologia Plantarum 100, 806-816.
38. Euglem T, Rushton PJ, Robatzek S, Somssich IE. 2000. The WRKY superfamily of plant transcription factors. Trends in Plant Science 5, 199-206.
39. Farmer EE, Weber H, Vollweider S. 1998. Fatty acid signalling in Arabidopsis. Planta 206, 167-174.
40. Feussner I, Wasternack C. 2002. The lipoxygenase pathway. Annual Reviews in Plant Biology 53, 275-297.
41. Fey V, Wagner R, Bräutigam K, Wirtz M, Hell R, Dietzmann A, Leister D, Oelmüller R, Pfannschmidt T. 2005. Retrograde plastid redox signals in the expression of nuclear genes for chloroplast proteins of Arabidopsis thaliana. Journal of Biological Chemistry (online Manuscript M406358200).
42. Finkelstein RR, Rock CD. 2002. Ascorbic acid biosynthesis and response. In: The Arabidopsis book. American Society of Plant Biologists.
43. Fortis G, Elli G. 1996. Stimulation of photophosphorylation by ascorbate as a function of light intensity. Plant Physiology 112, 1509-1511.
44. Foyer CH, Halliwell B. 1977. Presence of glutathione and glutathione reductase in chloroplasts - proposed role in ascorbic acid metabolism. Planta 133, 21-25.
45. Foyer CH, Lelandais M. 1996. A comparison of the relative rates of transport of ascorbate and glucose across the thylakoid, chloroplast and plasmalemma membranes of pea mesophyll cells. Journal of Plant Physiology 148, 391-398.
46. Foyer CH, Lelandais M, Kunert K-J. 1997. Photo-oxidative stress in plants. Physiologia Plantarum 92, 696-717.
47. Fridlyand LE, Scheibe R. 1999. Controlled distribution of electrons between acceptors in chloroplasts: a theoretical consideration. Biochimica et Biophysica Acta 1413, 31-42.
48. Gardeström P, Igamberdiev AU, Raghavendra AS. 2002. Mitochondrial functions in light and significance to carbon-nitrogen interactions. In: Foyer CH, Noctor G, eds. Advances in photosynthesis and respiration: photosynthetic nitrogen assimilation and associated carbon metabolism, Vol. 12. Dortrecht: Kluwer Academic Press, 151-172.
49. Goslings D, Meskauskien R, Kim C, Lee KP, Nater M, Apel K. 2004. Concurrent interactions of haem and FLU with Glut RNA reductase (HEMA1), the target of metabolic feedback inhibition of tetrapyrrole biosynthesis, in dark- and light-grown Arabidopsis plants. The Plant Journal 40, 957-967.
50. Gray JC, Sornarajah R, Zabron AA, Duckett CM, Khan MS. 1995. Chloroplast control of nuclear gene expression. In: Mathis P, ed. Photosynthesis: from light to biosphere, Vol. 3. Dordrecht: Kluwer Academic Press, 543-550.
51. Haehnel W. 1984. Photosynthetic electron transport in higher plants. Annual Review of Plant Physiology 35, 659-693.
52. Halford NG, Hey S, Jhurreea D, Laurie S, McKibbin RS, Paul M, Zhang Y. 2003. Metabolic signalling and carbon partitioning: role of Snf1-related (SnRK1) protein kinase. Journal of Experimental Botany 54, 467-475.
53. Halliwell B, Gutteridge JMC. 1999. Free radicals in biology and medicine. Oxford: Oxford Science Pulications.
54. Hamberg M, Sanz A, Rodriguez MJ, Calvo AP, Castresana C. 2003. Activation of the PUFA α-dioxygenase pathway during bacterial infection of tobacco leaves; formation of oxolipins protecting against cell death. Journal of Biological Chemistry 278, 51796-51805.
55. Harpster MH, Mayfield SP, Taylor WC. 1984. Effects of pigment-deficient mutants on the accumulation of photosynthetic proteins in maize. Plant Molecular Biology 3, 59-71.
56. 3 plants. Photosynthesis Research 73, 223-231.
57. Heineke D, Riens B, Grosse H, Hoferichter P, Peter U, Flügge U-I, Heldt HW. 1991. Redox transfer across the inner chloroplast envelope membrane. Plant Physiology 95, 1131-1137.
58. Holley SR, Yalamanchili RD, Moura DS, Ryan CA, Stratmann JW. 2003. Convergence of signalling pathways induced by systemin, oligosaccharide elicitors, and ultraviolet-B radiation at the level of mitogen-activated protein kinases in Lycopersicon peruvianum suspension-cultured cells. Plant Physiology 132, 1728-1738.
59. Horling F, Baier M, Dietz K-J. 2001. Redox-regulation of the expression of the peroxide-detoxifying chloroplast 2-Cys peroxiredoxin in the liverwort Riccia fluitans. Planta 214, 304-313.
60. Horling F, Lamkemeyer P, König J, Finkemeier I, Kandlbinder A, Baier M, Dietz K-J. 2003. Divergent light-, ascorbate-, and oxidative stress-dependent regulation of expression of the peroxiredoxin gene family in Arabidopsis. Plant Physiology 131, 317-325.
61. Huijser C, Kortstee A, Pego J, Weisbeek P, Smeekens S. 2000. The Arabidopsis SUCROSE UNCOUPLED-6 gene is identical to ABSCISIC ACID INSENSITIVE-4: involvement of abscisic acid in sugar responses. The Plant Journal 23, 577-585.
62. Ichimura K, Mizoguchi T, Yoshida R, Shinozaki K. 2000. Various abiotic stresses rapidly activate Arabidopsis MAP kinases ATMPK4 and ATMPK6. The Plant Journal 24, 655-665.
63. Jang J-C, Léon P, Zhou L, Sheen J. 1997. Hexokinase as a sugar sensor in higher plants. The Plant Cell 9, 5-19.
64. Kanna M, Tamaoki M, Kubo A, et al. 2003. Isolation of an ozone-insensitive and jasmonate-semi-insensitive Arabidopsis mutant (oji1). Plant and Cell Physiology 44, 1301-1310.
65. Karpinski S, Escobar C, Karpinska B, Creissen G, Mullineaux PM. 1997. Photosynthetic electron transport regulates expression of cytosolic ascorbate peroxidase genes in Arabidopsis during excess light stress. The Plant Cell 9, 627-640.
66. Keetman U, Mock HP, Grimm B. 2002. Kinetics of antioxidative defense responses to photosensitization in porphyrin-accumulating tobacco plants. Plant Physiology and Biochemistry 40, 697-707.
67. Keryer E, Collin V, Lavergne D, Lemaire S, Issakidis-Bourguet E. 2004. Characterization of Arabidopsis mutants for the variable subunit of ferredoxin:thioredoxin reductase. Photosynthesis Research 79, 265-274.
68. Kimura M, Yamamoto YY, Seti M, Sakurai T, Sato M, Abe T, Yoshida S, Manabe K, Shinozaki K, Matsui M. 2003. Identification of Arabidopsis genes regulated by high light-stress using cDNA microarray. Photochemistry and Photobiology 77, 226-233.
69. Kliebenstein DJ, Monde R-A, Last RL. 1998. Superoxide dismutase in Arabidopsis: an eclectic enzyme family with disperate regulation and protein localization. Plant Physiology 118, 637-650.
70. König J, Baier M, Horling F, Kahmann U, Schürmann P, Dietz K-J. 2002. The plant-specific function of 2-Cys peroxiredoxin-mediated detoxification of peroxides in the redox-hierarchy of photosynthetic electron flux. Proceedings of the National Academy of Sciences, USA 99, 5738-5743.
71. König J, Lotte K, Plessow R, Brockhinke A, Baier M, Dietz K-J. 2003. Reaction mechanism of plant 2-Cys peroxiredoxin: role of the C-terminus and the quaternary structure. Journal of Biological Chemistry 278, 24409-24420.
72. Kovtun Y, Chiu WL, Tena G, Sheen J. 2000. Functional analysis of oxidative stress-activated mitogen-activated protein kinase cascades in plants. Proceedings of the National Academy of Sciences, USA 97, 2940-2945.
73. Larkin RM, Alonso JM, Ecker JR, Chory J. 2003. GUN4, a regulator of chlorophyll synthesis and intracellular signaling. Science 299, 902-906.
74. Lebel E, Heifetz P, Thorne L, Uknes S, Ryals J, Ward E. 1998. Functional analysis of regulatory sequences controlling PR-1 gene expression in Arabidopsis. The Plant Journal 16, 223-233.
75. Lorenzo O, Chico JM, Sanchez-Serrano JJ, Solano R. 2004. Jasmonate-insensitive1 encodes a MYC transcription factor essential to discriminate between different jasmonate-regulated defense responses in Arabidopsis. The Plant Cell 16, 1938-1950.
76. Maeo K, Hayashi S, Kojima-Suzuki H, Morikami A, Nakamura K. 2001. The role of conserved residues of the WRKY domain in the DNA-binding of tobacco WRKY family proteins. Bioscience, Biotechnology and Biochemistry 65, 2428-2436.
77. Mahalingam R, Gomez-Buitrago AM, Eckardt N, Shah N, Guevara-Garcia A, Day P, Raina R, Fedoroff NV. 2003. Characterizing the stress/defense transcriptome of Arabidopsis. Genome 4, R20.
78. Martin C, Paz-Ares J. 1997. MYB transcription factors in plants. Trends in Genetics 13, 67-73,
79. Mauch F, Mauch-Mani B, Gaille C, Kull B, Haas D, Reimann C. 2001. Manipulation of salicylate content in Arabidopsis thaliana by the expression of an engineered bacterial salicylate synthase. The Plant Journal 25, 67-77.
80. Mayfield SP, Taylor WC. 1984. Carotenoid-deficient maize seedlings fail to accumulate light-harvesting chlorophyll a/b binding protein (LHCP) mRNA. European Journal of Biochemistry 144, 79-84.
81. Maxwell DP, Laudenbach DE, Huner NPA. 1995. Redox regulation of light-harvesting complex II and cab mRNA abundance in Dunaliella salina. Plant Physiology 109, 787-795.
82. Mehler A. 1951. Studies on the reaction of illuminated chloroplasts. I. Mechanisms of the reduction of oxygen and other Hill reagents. Archives in Biochemistry and Biophysics 33, 65-77.
83. Meinhard M, Grill E. 2001. Hydrogen peroxide is a regulator of ABI1, a protein phosphatase 2C from Arabidopsis. FEBS Letters 508, 443-446.
84. Meinhard M, Rodriguez PL, Grill E. 2002. The sensitivity of ABI2 to hydrogen peroxide links abscisic acid-response regulator to redox signalling. Planta 214, 775-782.
85. Meskauskien R, Nater M, Goslings D, Kessler F, op den Camp R, Apel K. 2001. FLU: a negative regulator of chlorophyll biosynthesis in Arabidopsis thaliana. Proceedings of the National Academy of Sciences, USA 98, 12826-12831.
86. Milla MAR, Marer A, Huete AR, Gustafson JP. 2003. Glutathione peroxidase genes in Arabidopsis are ubiquitous and regulated by abiotic stresses through diverse signalling pathways. The Plant Journal 36, 602-615.
87. Mittler R, Vanderauwera S, Gollery M, Van Breusegem F. 2004. The reactive oxygen gene network of plants. Trends in Plant Science 9, 490-498.
88. Miyake C, Asada K. 1996, Inactivation mechanisms of ascorbate peroxidase at low concentrations of ascorbate: hydrogen peroxide decomposes compound I of ascorbate peroxidase. Plant and Cell Physiology 37, 423-430.
89. Mochizuki N, Brusslan JA, Larkin R, Nagatani A, Chory J. 2001. Arabidopsis genomes uncoupled .5 (gun5) mutant reveals the involvement of Mg-chelatase H subunit in plastid-to-nucleus signal transduction. Proceedings of the National Academy of Sciences, USA 98, 2053-2058.
90. Montillet J-L, Cacas J-L, Garnier L, et al. 2004. The upstream oxylipins profile of Arabidopsis thaliana: a tool to scan for oxidative stress. The Plant Journal 40, 439-451.
91. Moon H, Lee B, Choi G, et al. 2003. NDP kinase 2 interacts with two oxidative stress-activated MAPKs to regulate cellular redox state and enhances multiple stress tolerance in transgenic plants. Proceedings of the National Academy of Sciences, USA 100, 358-363.
92. Moore B, Zhou L, Rolland F, Hall Q, Cheng W-H, Liu Y-X, Hwang I, Jones T, Sheen J. 2003. Role of the Arabidopsis glucose sensor HXK1 in nutrient, light, and hormonal signalling. Science 300, 332-336.
93. Motohashi K, Kondoh A, Stumpp MT, Hisabori T. 2001. A comprehensive survey of proteins targeted by chloroplast thioredoxins. Proceedings of the National Academy of Sciences, USA 98, 11224-11229.
94. Mullineaux PM, Karpinski S, Jimenez A, Cleary SP, Robinson C, Creissen GP. 1998. Identification of cDNAs encoding plastid-targeted glutathione- peroxidase. The Plant Journal 13, 375-379.
95. Noctor G, Veljovic-Jovanovic S, Foyer C. 2000. Peroxide processing in photosynthesis: antioxidant coupling and redox signalling. Philosophical Transactions of the Royal Society London, Series B 355, 1465-1475.
96. Oswald O, Martin T, Dominy PJ, Graham IA. 2001, Plastid redox state and sugars: interactive regulators of nuclear-encoded photosynthetic gene expression. Proceedings of the National Academy of Sciences, USA 98, 2047-2052.
97. Pastori GM, Kiddle G, Antoniw J, Bernard S, Veljovic-Jovanovic S, Verrier PJ, Noctor G, Foyer CH. 2003. Leaf vitamin C contents modulate plant defense transcripts and regulate genes that control development through hormone signaling. The Plant Cell 15, 939-951.
98. Padmasree K, Padmavathi L, Raghavendra AS. 2002. Essentiality of mitochondrial oxidative metabolism for photosynthesis: optimization of carbon assimilation and protection against photoinhibition. Critical Reviews in Biochemistry and Molecular Biology 37, 71-119.
99. Palenchar PM, Kouranov A, Lejay LV, Coruzzi GM. 2004. Genome-wide patterns of carbon and nitrogen regulation of gene expression validate the combined carbon and nitrogen (CN)-signalling hypothesis in plants. Genome Biology 5, R91.
100. Panchuk II, Volkov RA, Schöffl F. 2002. Heat stress- and heat shock transcription factor-dependent expression and activity of ascorbate peroxidase in Arabidopsis. Plant Physiology 129, 838-853.
101. Peltier G, Cournac L. 2002. Chlororespiration. Annual Review of Plant Biology 53, 523-550.
102. Pfannschmidt T, Milsson A, Allen JF. 1999. Photosynthetic control of chloroplast gene expression. Nature 397, 625-628.
103. Pfannschmidt T, Allen JE, Oelmüller R. 2001a. Principles of redox control in photosynthetic gene expression. Physiologia Plantarum 112, 1-9.
104. Pfannschmidt T, Schütze K, Brost M, Oelmüller R. 2001b. A novel mechanism of nuclear photosynthesis gene regulation by redox signals from the chloroplast during photosystem stoichiometry adjustment. Journal of Biological Chemistry 276, 36125-36130.
105. Pfannschmidt T, Schütze K, Fey V, Sherameti I, Oelmüller R. 2003. Chloroplast redox control of nuclear gene expression - a new class of plastid signals in interorganellar communication. Antioxidants and Redox Signaling 5, 95-101.
106. Pursiheimo S, Mulo P, Rintamaki E, Aro EM. 2001. Coregulation of light-harvesting complex II phosphorylation and lhcb mRNA accumulation in winter rye. The Plant Journal 26, 317-327.
107. Rao MV, Lee HI, Creelman RA, Raskin I, Mullet JE, Davis KR. 2000. Jasmonic acid signalling modulates ozone-induced hype-senitive cell death. The Plant Cell 12, 1633-1646.
108. Rizhsky L, Davletova S, Liang H, Mittler R. 2004. The zinc finger protein Zatl2 is required for cytosolic ascorbate peroxidase 1 expression during oxidative stress in Arabidopsis. Journal of Biological Chemistry 279, 11736-11743.
109. Romano PGN, Horton P, Gray JE. 2004. The Arabidopsis cyclophilins gene family. Plant Physiology 134, 1268-1282.
110. Rook F, Corke F, Card R, Munz G, Smith C, Bevan MW. 2001. Impaired sucrose-induction mutants reveal the modulation of sugar-inducible starch biosynthetic gene expression by abscisic acid signalling. The Plant Journal 26, 421-433.
111. Rouhier N, Gelhaye E, Jacquot JP. 2004. Plant glutaredoxins: still mysterious reducing systems. Cell and Molecular Life Science 61, 1266-1277.
112. Rushton PJ, Somssich IE. 1998. Transcriptional control of plant genes responsive to pathogens. Current Opinion in Plant Biology 1, 311-315.
113. Saradadevi K, Raghavendra AS. 1992. Dark respiration protects phtosynthesis against photoinhibition in mesophyll protoplasts od pea (Pisum sativum). Plant Physiology 99, 1232-1237.
114. Schafer FQ, Buettner GR. 2001. Redox environment of the cell as viewed through the redox state of the glutathione disulfide/glutathione couple. Free Radicals in Biology and Medicine 30, 1191-1212.
115. Schindler U, Beckmann H, Cashmore AR. 1992. TGA1 and G-box binding factors: two distinct classes of Arabidopsis leucine zipper proteins compete for the G-box-like element TGACGTGG. The Plant Cell 4, 1309-1319.
116. Schmidt M, Dehne S, Feierabend J. 2002. Post-transcriptional mechanisms control catalase synthesis during ist light-induced turnover in rye leaves through the availability of the hemin cofactor and reversible changes of the translation efficiency of mRNA. The Plant Journal 31, 601-613.
117. Schürmann P. 2003. Redox signaling in the chloroplast: the ferredoxin/thioredoxin system. Antioxidants and Redox Signaling 5, 69-78.
118. Scott IM, Clarke SM, Wood JE, Mur LAJ. 2004. Salicylate accumulation inhibits growth at chilling temperature in Arabidopsis. Plant Physiology 135, 1040-1049.
119. Shinozaki K, Yamaguchi-Shinozaki K. 2000. Molecular responses to dehydration and low temperature: differences and cross-talk between two stress signalling pathways. Current Opinion in Plant Biology 3, 217-223.
120. 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.
121. Staswick PE, Tiryaki I. 2004. The oxolipin signal jasmonic acid is activated by an enzyme that conjugates it to isoleucine in Arabidopsis. The Plant Cell 16, 2117-2127.
122. Staswick PE, Tiryaki I, Rowe ML. 2002. Jasmonate response locus jar1 and several related Arabidopsis genes encode enzymes of the firefly luciferase superfamily that show activity on jasmonic, salicylic, and indole-3-acetic acids in an assay for adenylation. The Plant Cell 14, 1405-1415.
123. Strand A. 2004. Plastid-to-nucleus signalling. Current Opinion in Plant Biology 7, 621-625.
124. Strand A, Asami T, Alonso J, Ecker JR, Chory J. 2003. Chloroplast to nucleus communication by accumulation of Mg-protoporphyrin IX. Nature 421, 79-83.
125. Sullivan JA, Gray JC. 2002. Multiple plastid signals regulate the expression of the pea plastocyanin gene in pea and transgenic tobacco plants. The Plant Journal 32, 763-774.
126. Sun Y, Oberley LW. 1996. Redox regulation of transcriptional activators. Free Radicals in Biology and Medicine 21, 335-348.
127. Susek RE, Ausubel FM, Chory J. 1993. Signal transduction mutants of Arabidopsis uncouple nuclear CAB and RBCS gene expression from chloroplast development. Cell 74, 787-799.
128. Taylor WC. 1989. Regulatory interactions between nuclear and plastid genomes. Annual Review of Plant Physiology and Plant Molecular Biology 40, 211-233.
129. Vandenabeele S, Vanderauwera S, Vuylsteke M, Rombauts S, Langebartels C, Seidlitz HK, Zaheau M, Van Montagu M, Inzé D, Van Breusegem F. 2004. Catalase deficiency drastically affects gene expression induced by high light in Arabidopsis thaliana. The Plant Journal 39, 45-58.
130. GLU reductase: mutations affecting haem inhibition and enzyme activity. Phytochemistry 47, 513-519.
131. Weatherwax SC, Ong MS, Degenhardt J, Bray EA, Tobin EM. 1996. The interaction of light and abscisic acid in the regulation of plant gene expression. Plant Physiology 111, 363-370.
132. 3 plants. The EMBO Jounal 16, 4806-4816.
133. Wood ZA, Schröder E, Harris JR, Poole LB. 2003. Structure, mechanism and regulation of peroxiredoxins. Trends in Biochemical Sciences 28, 32-40.
134. Xie D-X, Feys BF, James S, Nieto-Rostro M, Turner JG. 1998. CO11: an Arabidopsis gene required for jasmonate-regulated defense and fertility. Science 280, 1091-1094.
135. Yabuta Y, Murata T, Yoshimura K, Ishikawa T, Shigeoka S. 2004. Two distinct redox signalling pathways for cytosoloc APX induction under photo-oxidative stress. Plant Cell Physiology 45, 1586-1594.
136. Yeh CM, Hsiao LJ, Huang HJ. 2004. Cadmium activates a mitogen-activated protein kinase gene and MBP kinases in rice. Plant and Cell Physiology 45, 1306-1312.
137. Yoshimura K, Yabuta Y, Ishikawa T, Shigeoka S. 2000. Expression of spinach ascorbate peroxidase isoenzymes in response to oxidative stress. Plant Physiology 123, 223-233.
138. 6f complexes controls the activation of LHCII kinase. EMBO Journal 18, 2961-2969.