Oxidant and antioxidant signalling in plants: A re-evaluation of the concept of oxidative stress in a physiological context

Plant, Cell and Environment

Volumn 28, Issue 8, 2005, Pages 1056-1071

  Foyer, Christine H ^a   Noctor, Graham ^b  

^a ROTHAMSTED RESEARCH   (United Kingdom)

^b INSTITUTE OF PLANT SCIENCES PARIS SACLAY IPS2   (France)

Author keywords

Ascorbate; Glutathione; Ozone; Programmed cell death; Reactive oxygen species; Redox signalling; Thioldisulphide interactions

Indexed keywords

PHYSIOLOGY; SIGNALING;

EID: 26844496737     PISSN: 01407791     EISSN: 13653040     Source Type: Journal    
DOI: 10.1111/j.1365-3040.2005.01327.x     Document Type: Review

References (163)

1. Apel K. & Hirt H. (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annual Review of Plant Biology 55, 373-399.
2. 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. Plant Journal 12, 179-190.
3. Baier M., Noctor G., Foyer C.H. & Dietz K.J. (2000) Antisense suppression of 2-cys peroxiredoxin in Arabidopsis thaliana specifically enhances the activities and expression of enzymes associated with ascorbate metabolism, but not glutathione metabolism. Plant Physiology 124, 823-832.
4. Baier M., Kandlbinder A., Golldack D & Dietz K.-J. (2005) Oxidative stress and ozone: perception, signalling and response. Plant, Cell and Environment 28, in press.
5. Ball L., Accotto G., Bechtold U., et al. (2004) Evidence for a direct link between glutathione biosynthesis and stress defense gene expression in Arabidopsis. Plant Cell 16, 2448-2462.
6. Baluska F., Samaj J., Wojtaszek P., Volkmann D. & Menzel D. (2003) Cytoskeleton-plasma membrane-cell wall continuum in plants. Emerging links revisited. Plant Physiology 133, 482-491.
7. Barth C., Moeder W., Klessig D.F. & Conklin P.L. (2004) The timing of senescence and response to pathogens is altered in the ascorbate-deficient muttant vitamin C-1. Plant Physiology 134, 178-192.
8. Baudouin E., Frendo P., Le Gleuher M. & Puppo A. (2004) A Medicago saliva haem oxygenase gene is preferentially expressed in root nodules. Journal of Experimental Botany 55, 43-47.
9. Becana M., Dalton D.A., Moran J.F., Iturbe-Ormaetxe I., Matamoros M.A. & Rubio M.C. (2000) Reactive oxygen species and antioxidants in legume nodules. Physiologia Plantarum 109, 372-381.
10. Berczi A. & Møller I.M. (1998) NADH-monodehydroascorbate oxidoreductase is one of the redox enzymes in spinach leaf plasma membranes. Plant Physiology 116, 1029-1036.
11. Bick J.A., Setterdahl A.T., Knaff D.B., Chen Y., Pitcher L.H., Zilinskas B.A. & Leustek T. (2001) Regulation of the plant-type 5′- adenylylsulfate reductase by oxidative stress. Biochemistry 40, 9040-9048.
12. Biteau B., Labarre J. & Toledano M.B. (2003) ATP-dependent reduction of cysteine-sulphinic acid by S. cerevisiae sulphiredoxin. Nature 425, 980-984.
13. Broin M., Cuiné S., Eymery F. & Rey P. (2002) The plastidic 2-cysteine peroxiredoxin is a target for a thioredoxin involved in the protection of the photosynthetic apparatus against oxidative damage. Plant Cell 14, 1417-1432.
14. Burkey K.O., Eason G. & Fiscus E.L. (2003) Factors that affect leaf extracellular ascorbic acid content and redox status. Physiologia Plantarum 117, 51-57.
15. Cagnac O., Bourbouloux A., Chakrabarty D., Zhang M.Y. & Delrot S. (2004) AtOPT6 transports glutathione derivatives and is induced by primisulfuron. Plant Physiology 135, 1378-1387.
16. Canut H., Carrasco A., Galaud J.P., Cassan C., Bouyssou H., Vita N., Ferrara P. & Pont-Lezica R. (1998) High affinity RGD-binding sites at the plasma membrane of Arabidopsis thaliana links the cell wall. Plant Journal 16, 63-71.
17. Cao H., Bowling S.A., Gordon A.S. & Dong X.N. (1994) Characterization of an Arabidopsis mutant that is nonresponsive to inducers of systemic acquired-resistance. Plant Cell 6, 1583-1592.
18. Chamnongpol S., Willekens H., Langebartels C., Van Montagu M., Inze D. & Van Camp W. (1996) Transgenic tobacco with a reduced catalase activity develops necrotic lesions and induces pathogenesis-related expression under high light. Plant Journal 10, 491-503.
19. Chang T.S., Jeong W., Ae Woo H., Lee S.M., Park S. & Ree S.G. (2004) Characterization of mammalian sulphiredoxin and its reactivation by hyperoxidized peroxiredoxin through reduction of cysteine sulfinic acid in the active site to cysteine. Journal of Biological Chemistry 279, 50994-51001.
20. Chen C. & Dickman M.B. (2004) Bcl-2 family members localize to tobacco chloroplasts and inhibit programmed cell death induced by chloroplast-targeted herbicides. Journal of Experimental Botany 55, 2617-2623.
21. Chen Z. & Gallie D.R. (2004) The ascorbic acid redox state controls guard cell signaling and stomatal movement. Plant Cell 16, 1143-1162.
22. Chen Z., Young T.E., Ling J., Chang S.C. & Gallie D.R. (2003) Increasing vitamin C content of plants through enhanced ascorbate recycling. Proceedings of the National Academy of Sciences of the USA 100, 3525-3530.
23. Cheng J.C., Seeley K.A. & Sung Z.R. (1995) RML1 and RML2, Arabidopsis genes required for cell proliferation at the root tip. Plant Physiology 107, 365-376.
24. Cobbett C.S., May M.J., Howden R. & Rolls B. (1998) The glutathione-deficient, cadmium-sensitive mutant, cad2-1, of Arabidopsis thaliana is deficient in γ-glutamylcysteine synthetase. Plant Journal 16, 73-78.
25. Collin V., Lankemeyer P., Miginiac-Maslow M., Hirasawa M., Knaff D.B., Dietz K.J. & Issakidis-Bourguet E. (2004) Characterization of plastidial thioredoxins belonging to the new y-type. Plant Physiology 136, 4088-4095.
26. Conklin P.L. & Earth C. (2004) Ascorbic acid, a familiar small molecule intertwined in the response of plants to ozone, pathogens and the onset of senescence. Plant, Cell and Environment 27, 959-970.
27. Conklin P.L. & Last R.L. (1995) Differential accumulation of antioxidant mRNAs in Arabidopsis thaliana exposed to ozone. Plant Physiology 109, 203-212.
28. Conklin P.L., Williams E.H. & Last R.L. (1996) Environmental stress sensitivity of an ascorbic acid-deficient Arabidopsis mutant. Proceedings of the National Academy of Sciences of the USA 93, 9970-9974.
29. Creissen G., Firmin J., Fryer M., et al. (1999) Elevated glutathione biosynthetic capacity in the chloroplasts of transgenic tobacco plants paradoxically causes increased oxidative stress. Plant Cell 11, 1277-1291.
30. Cummins I., Cole D.J. & Edwards R. (1999) A role for glutathione transferases functioning as glutathione peroxidases in resistance to multiple herbicides in black grass. Plant Journal 18, 285-292.
31. Dat J., Vandenabeele S., Vranova E., Van Montagu M., Inzé D. & Van Breusegem F. (2000) Dual action of the active oxygen species during plant stress responses. Cellular and Molecular Life Sciences 57, 779-795.
32. De Block M., Verduyn C., De Brouwer D. & Cornelissen M. (2004) Generating stress tolerant crops by economizing energy consumption. Pflanzenschutz-Nachrichten Bayer 57, 105-110.
33. Delaney T.P., Friedrich I. & Ryals J.A. (1995) Arabidopsis signal-transduction mutant defective in chemically and biologically induced disease resistance. Proceedings of the National Academy of Sciences of the USA 92, 6602-6606.
34. Desikan R., Mackerness S.A.H., Hancock J.T. & Neill S.J. (2001) Regulation of the Arabidopsis transcriptome by oxidative stress. Plant Physiology 127, 159-172.
35. Després C., Chubak C., Rochon A., Clark R., Bethune T., Desveaux D. & Fobert P.R. (2003) The Arabidopsis NPR1 disease resistance protein is a novel cofactor that confers redox regulation of DNA binding activity to the basis domain/leucine zipper transcription factor TGA1. Plant Cell 15, 2181-2191.
36. Dewitte W. & Murray J.A.H. (2003) The plant cell cycle. Annual Review of Plant Biology 54, 235-264.
37. Dixon D.P., Davis B.G. & Edwards R. (2002) Functional divergence in the glutathione transferase superfamily in plants. Identification of two classes with putative functions in redox homeostasis in Arabidopsis thaliana. Journal of Biological Chemistry 277, 30859-30869.
38. Doke N., Miura. Y., Sanchez L. & Kawakita K. (1994) Involvement of superoxide in signal transduction: Responses to attack by pathogens, physical and chemical shocks, and UV irradiation. In Causes of Photooxidative Stresses and Amelioration of Defense Systems in Plants (eds C.H. Foyer & P. Mullineaux), pp. 177-198. CRC Press, Boca Raton, FL, USA.
39. Dröge W. (2002) Free radicals in the physiological control of cell function. Physiological Reviews 82, 47-95.
40. Droux M. (2004) Sulfur assimilation and the role of sulfur in plant metabolism: a survey. Photosynthesis Research 79, 331-348.
41. Dutilleul C., Garmier M., Noctor G., Mathieu C.D., Chétrit P., Foyer C.H. & De Paepe R. (2003) Leaf mitochondria modulate whole cell redox homeostasis, set antioxidant capacity and determine stress resistance through altered signaling and diurnal regulation. Plant Cell 15, 1212-1226.
42. Ermak G. & Davies K.J. (2002) Calcium and oxidative stress: from cell signalling to cell death. Molecular Immunology 38, 713-721.
43. Falkowski P.G., Katz M.E., Knoll A.H., Quigg A., Raven J.A., Schofield O. & Taylor F.J.R. (2004) The evolution of modern eukaryotic phytoplankton. Science 305, 354-360.
44. Foreman J., Demidchik V., Bothwell J.H., et al. (2003) Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature 27, 442-446.
45. Foyer C.H. (2004) The role of ascorbic acid in defence networks and signalling in plants. In Vitamin C Functions and Biochemistry in Animals and Plants (eds H. Asard, J.M. May & N. Smirnoff), Chapter 4. pp. 65-82. Bios Scientific Publishers, Oxford UK.
46. Foyer C.H. & Noctor G. (2000) Oxygen processing in photosynthesis: regulation and signalling. New Phytology 146, 359-388.
47. Foyer C.H. & Noctor G. (2003) Redox sensing and signaling associated with reactive oxygen in chloroplasts, peroxisomes and mitochondria. Physiologia Plantarum 119, 355-364.
48. Foyer C.H., Theodoulou F.L. & Delrot S. (2001) The functions of intercellular and intracellular glutathione transport systems in plants. Trends in Plant Science 6, 486-492.
49. Foyer C.H., Trebst A. & Noctor G. (2005) Signaling and integration of defense functions of tocopherol, ascorbate, and glutathione. In Photoprotection, Photoinhibition, Gene Regulation, and Environment (eds B. Demmig-Adams & W. W. Adams), pp. 00-00. Kluwer Academic Publishers, Dordrecht, The Netherlands, in press.
50. Frendo P., Harrison J., Norman C., Herandez-Jimenez M.-J., Van de Sype G., Gilabert A. & Puppo A. (2005) Glutathione and homoglutathione play a critical role in the nodulation process of Medicago truncatula. Molecular Plant-Microbe Interactions, in press.
51. Fridovich I. (1998) Oxygen toxicity: a radical explanation. Journal of Experimental Biology 201, 1203-1209.
52. Frova C. (2003) The glutathione transferase gene family: genomic structure, functions, expression and evolution. Physiologia Plantarum 119, 469-479.
53. Gomez L.D., Noctor G., Knight M. & Foyer C.H. (2004a) Regulation of calcium signaling and gene expression by glutathione. Journal of Experimental Botany 55, 1851-1859.
54. Gomez L., Vanacker H., Buchner P., Noctor G. & Foyer C.H. (2004b) The intercellular distribution of glutathione synthesis and its response to chilling in maize. Plant Physiology 134, 1662-1671.
55. Gorman A.A. & Rodgers M.A.J. (1992) Current perspectives of singlet oxygen detection in biological environments. Journal of Photochemistry and Photobiology B 14, 159-176.
56. Gozalbo D., Gil-Navarro I., Azorin I., Renau-Piqueras J., Martinez J.P. & Gil M.L. (1998) The cell wall-associated glyceraldehyde-3-phosphate dehydrogenase of Candida albicans is also a fibronectin and laminin binding protein. Infection and Immunity 66, 2052-2059.
57. Green R. & Fluhr R. (1995) UV-B-induced PR-1 accumulation is mediated by active oxygen species. Plant Cell 7, 203-212.
58. Green M.A. & Fry S.C. (2005) Degradation of vitamin C in plant cells via enzymic hydrolysis of 4-O-oxalyl-1-threonate. Nature 433, 83-87.
59. Halliwell B. (1981) Toxic effects of oxygen on plant tissues. In Chloroplast Metabolism: the Structure and Function of Chloroplasts in Green Leaf Cells, pp. 179-205. Clarenden Press, Oxford, UK
60. Harada E., Kusano T. & Sano H. (2000) Differential expression of genes encoding enzymes envolved in sulfur assimilation pathways in response to wounding and jasmonate in Arabidopsis thaliana. Journal of Plant Physiology 156, 272-276.
61. Harms K., Von Ballmoos P., Brunold C., Höfgen R. & Hesse H. (2000) Expression of a bacterial serine acetyltransferase in transgenic potato plants leads to increased levels of cysteine and glutathione. Plant Journal 22, 335-343.
62. Hell R. & Bergmann L. (1990) γ-Glutamylcysteine synthetase in higher plants: catalytic properties and subcellular localization. Planta 180, 603-612.
63. Herbette S., Lenne C., Leblanc N., Julien J.-L., Drevet J.R. & Roeckel-Drevet P. (2002) Two GPX-like proteins from Lycopersicon esculentum and Helianthus annuus are antioxidant enzymes with phospholipid hydroperoxide glutathione peroxidase and thioredoxin peroxidase activities. European Journal of Biochemistry 269, 2414-2420.
64. Hérouart D., Van Montagu M. & Inzé D. (1993) Redox-activated expression of the cytosolic copper/zinc superoxide dismutase gene in Nicotiana. Proceedings of the National Academy of Sciences of the USA 90, 3108-3112.
65. 35S-sulphur in 3-year-old beech trees (Fagus sylvatica). Physiologia Plantarum 95, 379-386.
66. Hirai M.Y., Fujiwara T., Awazuhara M., Kimura T., Noji M. & Saito K. (2003) Global expression profiling of sulfur-starved Arabidopsis by DNA macroarray reveals the role of O-acetyl-L-serine as a general regulator of gene expression in response to sulfur nutrition. Plant Journal 33, 651-663.
67. Horemans N., Foyer C.H. & Asard H. (2000) Transport and action of ascorbate at the plant plasma membrane. Trends in Plant Science 5, 263-267.
68. Horling F., Lamkemeyer P., Konig 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.
69. Howden R., Andersen C.R., Goldsbrough P.B. & Cobbett C.S. (1995) A cadmium-sensitive, glutathione-deficient mutant of Arabidopsis thaliana. Plant Physiology 107, 1067-1073.
70. Huang C.S., Chang L.S., Anderson M.E. & Meister A. (1993) Catalytic and regulatiory properties of the heavy subunit of rat kidney γ-glutamylcysteine synthetase. Journal of Biological Chemistry 268, 19675-19680.
71. Hwang D., Chen H.C. & Sheen J. (2002) Two-component signal transduction pathways in Arabidopsis. Plant Physiology 129, 500-515.
72. Hynes R.O. (2002) A re-evaluation of integrins as regulators of angiogenesis. Nature Medicine 8, 918-921.
73. Ito H., Iwabuchi M. & Ogawa K. (2003) The sugar-metabolic enzymes aldolase and triose-phosphate isomerase are targets of glutathionylation in Arabidopsis thaliana: detection using biotinylated glutathione. Plant and Cell Physiology 44, 655-660.
74. Jez J.M., Cahoon R.E. & Chen S. (2004) Arabidopsis thaliana glutamate-cysteine ligase. Functional properties, kinetic mechanism, and regulation of activity. Journal of Biological Chemistry 279, 33463-33470.
75. Johansson C., Lillig C.H. & Holmgren A. (2004) Human mitochondrial glutaredoxin reduces S-glutathionylated proteins with high affinity accepting electrons from either glutathione or thioredoxin reductase. Journal of Biological Chemistry 279, 7537-7543.
76. Kaiser W.M. (1979) Reversible inhibition of the Calvin cycle and activation of oxidative pentose phosphate cycle in isolated intact chloroplasts by hydrogen peroxide. Planta 145, 377-382.
77. Kangasjärvi J., Jaspers P. & Kollist H. (2005) Signalling and cell death in ozone-exposed plants. Plant, Cell and Environment 28, in press.
78. Kato N. & Esaka M. (1999) Changes in ascorbate oxidase gene expression and ascorbate levels in cell division and cell elongation in tobacco cells. Physiologia Plantarum 105, 321-329.
79. Kendall A.C., Keys A.J., Turner J.C., Lea P.J. & Miflin B.J. (1983) The isolation and characterisation of a catalase-deficient mutant of barley (Hordeum vulgare L.). Planta 159, 505-511.
80. Kiddle G., Pastori G.M., Bernard S., Pignocchi C., Antoniw J., Verrier P.J. & Foyer C.H. (2003) Effects of ascorbate signaling on defense and photosynthesis genes. Antioxidants and Redox Signaling 5, 23-32.
81. Kimura M., Yoshizumi T., Manabe K., Yamamoto Y.Y. & Matsui M. (2001) Arabidopsis transcriptional regulation by light stress via hydrogen peroxide-dependent and - independent pathways. Genes to Cells 6, 607-617.
82. Kisu Y., Ono T., Shimofurutani N., Suzuki M. & Esaka M. (1998) Characterisation and expression of a new class of zinc finger protein that binds to silencer region of ascorbate oxidase gene. Plant Cell Physiology 39, 1054-1064.
83. Köhler B., Hills A. & Blatt M.R. (2003) Control of guard cell ion channels by hydrogen peroxide and abscisic acid indicates their action through alternate signaling pathways. Plant Physiology 131, 385-388.
84. Kopriva S. & Rennenberg H. (2004) Control of sulphate assimilation by glutathione synthesis: interactions with N and C metabolism. Journal of Experimental Botany 55, 1831-1842.
85. Kristensen B.K., Askerlund P., Bykova N.V., Egsgaard H. & Møller I.M. (2004) Identification of oxidised proteins in the matrix of rice leaf mitochondria by immunoprecipitation and two-demensional liquid chromatography-tandem mass spectrometry. Phytochemistry 65, 1839-1851.
86. Kwak J.M., Mori I.C., Pei Z.M., et al. (2003) NADPH oxidase AtrbohD and AtrbohF genes function in ROS-dependent ABA signaling in Arabidopsis. EMBO Journal 22, 2623-2633.
87. Laloi C., Mestres-Ortega D., Marco Y., Meyer Y. & Reichheld J.P. (2004) The Arabidopsis cytosolic thioredoxin h5 gene induction by oxidative stress and its W-Box-mediated response to pathogen elicitor. Plant Physiology 134, 1006-1016.
88. Lederer B. & Boger P. (2003) Binding and protection of porphyrins by glutathione-S-transferases of Zea mays L. Biochimica et Biophysica Acta 1621, 226-233.
89. Lee K.P., Kim C., Lee D.W. & Apel K. (2003) TIGRINA d, required for regulating the biosynthesis of tetrapyrroles in barley, is an ortholog of the FLU gene of Arabidopsis thaliana. FEBS Letters 553, 119-124.
90. Leisinger U., Rufenacht K., Fischer B., Pesaro M., Spengler A., Zehnder A.J.B. & Eggen R.I.L. (2001) The glutathione peroxidase homologous gene from Chlamydomonas reinhardtii is transcriptionally up-regulated by singlet oxygen. Plant Molecular Biology 46, 395-408.
91. Lemaire S.D. (2004) The glutaredoxin family in oxygenic photosynthetic organisms. Photosynthesis Research 79, 305-318.
92. Levine R.L., Berlett B.S., Moskovitz J., Mosoni L. & Stadtman E.R. (1999) Methionine residues may protect proteins from critical oxidative damage. Mechanisms of Ageing and Development 107, 323-332.
93. 2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response. Cell 79, 583-593.
94. Maddison J., Lyons T., Plochl M. & Barnes J. (2002) Hydroponically cultivated radish fed 1-galactono-1,4-lactone exhibits increased tolerance to ozone. Planta 214, 383-391.
95. Mahalingam R. & Federoff N. (2003) Stress response, cell death, and signalling: the many faces of reactive oxygen species. Physiologia Plantarum 119, 56-68.
96. Matsumura H., Nirasawa S., Kiba A., Urasaki N., Saitoh H., Ito M., Kawai-Yamada M., Uchimiya H. & Terauchi R. (2003) Overexpression of Bax inhibitor suppresses the fungal elicitor-induced cell death in rice (Oryza saliva L.) cells. Plant Journal 33, 425-437.
97. May M.J. & Leaver C.J. (1994) Arabidopsis thaliana γ-glutamylcysteine synthetase is structurally unrelated to mammalian, yeast and E. coli homologues. Proceedings of the National Academy of Sciences of the USA 91, 10059-10063.
98. May M.J., Vernoux T., Leaver C., van Montagu M. & Inzé D. (1998) Glutathione homeostasis in plants: implications for environmental sensing and plant development. Journal of Experimental Botany 49, 649-667.
99. Meijer M. & Murray J.A.H. (2001) Cell cycle controls and the development of plant form. Current Opinion in Plant Biology 4, 44-49.
100. Meinhardt S.W., Cheng W.J., Kwon C.Y., Donohue C.M. & Rasmussen J.B. (2002) Role of the arginyl-glycyl-aspartic motif in the action of Ptr ToxA produced by Pyrenophora tritici-repentis. Plant Physiology 130, 1545-1551.
101. Meskauskiene 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 of the USA 98, 12826-12831.
102. Mittler R. (2002) Oxidative stress, antioxidants and stress tolerance. Trends in Plant Science 7, 405-410.
103. Mittler R., Vanderauwera S., Gollery M. & Van Breusegem F. (2004) Reactive oxygen gene network of plants. Trends in Plant Science 9, 490-498.
104. Mittova V., Kiddle G., Theodoulou F.L., Gomez L., Volokita M., Tal M., Foyer C.H. & Guy M. (2003) Co-ordinate induction of glutathione biosynthesis and glutathione-metabolising enzymes is correlated with salt tolerance in tomato. FEBS Letters 554, 417-421.
105. Møller I.M. & Kristensen B.K. (2004) Protein oxidation in plant mitochondria as a stress indicator. Photochemical and Photobiological Sciences 3, 730-735.
106. Mou Z., Fan W. & Dong X. (2003) Inducers of plant systemic acquired resistance regulate NPR1 function through redox changes. Cell 27, 935-944.
107. Neill S., Desikan R. & Hancock J. (2002) Hydrogen peroxide signalling. Current Opinion in Plant Biology 5, 388-395.
108. Noctor G. & Foyer C.H. (1998) Ascorbate and glutathione: keeping active oxygen under control. Annual Review of Plant Physiology and Plant Molecular Biology 49, 249-279.
109. Noctor G., Arisi A.C.M., Jouanin L., Valadier M.H., Roux Y. & Foyer C.H. (1997) The role of glycine in determining the rate of glutathione synthesis in poplar. Possible implications for glutathione production during stress. Physiologia Plantarum 100, 255-263.
110. Noctor G., Gomez L., Vanacker H. & Foyer C.H. (2002b) Glutathione homeostasis and signaling: the influence of biosynthesis, compartmentation and transport. Journal of Experimental Botany 53, 1283-1304.
111. Noctor G., Strohm M., Jouanin L., Kunert K.J., Foyer C.H. & Rennenberg H. (1996) Synthesis of glutathione in leaves of transgenic poplar (Populus tremula x P. alba) overexpressing γ-glutamylcysteine synthetase. Plant Physiology 112, 1071-1078.
112. Noctor G., Veljovic-Jovanovic S., Driscoll S., Novitskaya L. & Foyer C.H. (2002a) Drought and oxidative load in wheat leaves: a predominant role for photorespiration? Annals of Botany 89, 841-850.
113. Ogawa K., Tasaka Y., Mino M., Tanaka Y. & Iwabuchi M. (2002) Association of glutathione with flowering in Arabidopsis thaliana. Plant Cell Physiology 42, 524-530.
114. Op den Camp R.G., Przybyla D., Ochsenbein C., et al. (2003) Rapid induction of distinct stress responses after the release of singlet oxygen in Arabidopsis. Plant Cell 15, 2320-2332.
115. Pastori G.M., kiddle G., Antoniw J., Bernard S., Veljovic-Jovanovic S., Verrier P.J., Noctor G. & Foyer C.H. (2003) Leaf vitamin C contents modulate plant defense transcripts and regulate genes that control development through hormone signalling. Plant Cell 15, 939-951.
116. Piffanelli P., Zhou F., Casais C., Orme J., Jarosch B., Schaffrath U., Collins N.C., Panstruga R. & Schulze-Lefert P. (2002) The barley MLO modulator of defence and cell death is responsive to biotic and abiotic stimuli. Plant Physiology 129, 1076-1085.
117. Pignocchi C. & Foyer C.H. (2003) Apoplastic ascorbate metabolism and its role in the regulation of cell signalling. Current Opinion in Plant Biology 6, 379-389.
118. Pignocchi C., Fletcher J.M., Wilkinson J.E., Barnes J.D. & Foyer C.H. (2003) The function of ascorbate oxidase in tobacco. Plant Physiology 132, 1631-1641.
119. Polte T. & Tyrrell R.M. (2004) Involvement of lipid peroxidation and organic peroxides in UVA-induced matrix metalloproteinase-1 expression. Free Radical Biology and Medicine 36, 1566-1574.
120. Porta H. & Rocha-Sosa M. (2002) Plant lipoxygenases. Physiological and molecular features. Plant Physiology 130, 15-21.
121. Potters G., De Gara L., Asard H. & Horemans N. (2002) Ascorbate and glutathione: guardians of the cell cycle, partners in crime? Plant Physiology and Biochemistry 40, 537-548.
122. Potters G., Horemans N., Bellone S., Caubergs J., Trost P., Guisez Y. & Asard H. (2004) Dehydroascorbate influences the plant cell cycle through a glutathione-independent reduction mechanism. Plant Physiology 134, 1479-1487.
123. Rentel M.C. & Knight M.R. (2004) Oxidative stress-induced calcium signaling in Arabidopsis. Plant Physiology 135, 1471-1479.
124. Rentel M.C., Lecourieux D., Ouaked F., et al. (2004) OX Kinase is necessary for oxidative burst-mediated signalling in Arabidopsis. Nature 427, 858-861.
125. Rey P., Cuiné S., Eymery F., Garin J., Court M., Jacquot J.P., Rouhier N. & Broin M. (2005) Analysis of the proteins targeted by CDSP32, a plastidic thioredoxin participating in oxidative stress responses. Plant Journal in press.
126. Rodermel S. (2001) Pathways of plastid-to-nucleus signalling. Trends in Plant Science 6, 471-478.
127. Romero H.M., Berlett B.S., Jensen P.J., Pell E.V. & Tien M. (2004) Investigations into the role of the plastidial peptide methionine sulfoxide reductase in response to oxidative stress in Arabidopsis. Plant Physiology 136, 3784-3994.
128. Rouhier N., Gelhaye E., Sautiere P.E., Brun A., Laurent P., Tagu D., Gerard J., De Fay E., Meyer Y. & Jacquot J.P. (2001) Isolation and characterization of a new peroxiredoxin from poplar sieve tubes that uses either glutaredoxin or thioredoxin as a proton donor. Plant Physiology 127, 1299-1309.
129. Sadanandom A., Poghosyan Z., Fairbairn D.J. & Murphy D.J. (2000) Differential regulation of plastidial and cytosolic isoforms of peptide methionine sulfoxide reductase in Arabidopsis. Plant Physiology 123, 255-263.
130. Sandermann H. (2000) Active oxygen species as mediators of plant immunity: three case studies. Biological Chemistry 381, 649-653.
131. Sanmartin M., Drogouti P.D., Lyons T., Barnes J. & Kanellis A.K. (2003) Overexpression of ascorbate oxidase in the apoplast of transgenic tobacco results in altered ascorbate and glutathione redox states and increased sensitivity to ozone. Planta 216, 918-928.
132. Schäfer H.J., Haag-Kerwer A. & Rausch T. (1998) cDNA cloning and expression analysis of genes encoding GSH synthesis in roots of the heavy-metal accumulator Brassica juncea L.: evidence for Cd-induction of a putative mitochondrial γ-glutamylcysteine synthetase isoform. Plant Molecular Biology 37, 87-97.
133. Schroeder J.I., Allen G.J., Hugouvieux V., Kwak J.M. & Waner D. (2001b) Guard cell signal transduction. Annual Review of Plant Physiology and Plant Molecular Biology 52, 627-658.
134. Schroeder J.I., Kwak J.M. & Allen G.J. (2001a) Guard cell abscisic acid signalling and engineering drought hardiness in plants. Nature 410, 327-330.
135. Schürmann P. & Jacquot J.P. (2000) Plant thioredoxin systems revisited. Annual Review of Plant Physiology and Plant Molecular Biology 51, 371-400.
136. Sen Gupta A., Alscher R.G. & McCune D. (1991) Response of photosynthesis and cellular antioxidants to ozone in Populus leaves. Plant Physiology 96, 650-655.
137. Shirasu K., Nakajima H., Rajasekhar V.K., Dixon R.A. & Lamb C. (1997) Salicylic acid potentiates an agonist-dependent gain control that amplifies pathogen signals in the activation of defense mechanisms. Plant Cell 9, 261-270.
138. Smirnoff N., Running J.A. & Gatzek S. (2004) Ascorbate metabolism in relation to oxidative stress. In: Vitamin C Functions and Biochemistry in Animals and Plants (eds H. Asard, J.M. May & N. Smirnoff), pp. 1-30. Bios Scientific Publishers, London, UK.
139. Smith I.K., Kendall A.C., Keys A.J., Turner J.C. & Lea P.J. (1984) Increased levels of glutathione in a catalase-deficient mutant of barley (Hordeum vulgare L.). Plant Science Letters 37, 29-33.
140. Strand A., Asami T., Alonso J., Ecker J.R. & Chory J. (2003) Chloroplast to nucleus communication triggered by accumulation of Mg-protoporphyrin IX. Nature 421, 79-83.
141. Suharsono U., Fujisawa Y., Kawasaki T., Iwasaki Y., Satoh H. & Shimamoto K. (2002) The heterotrimeric G protein alpha subunit acts upstream of the small GTPase Rac in disease resistance of rice. Proceedings of the National Academy of Sciences of the USA 99, 13307-13312.
142. Sun W.M., Huang Z.Z. & Lu S.C. (1996) Regulation of γ-glutamylcysteine synthetase by protein phosphorylation. Biochemical Journal 320, 321-328.
143. Sweetlove L., Heazlewood J.L., Herald V., Holtzapffil R., Day D.A., Leaver C.J. & Millar A.H. (2002) The impact of oxidative stress on Arabidopsis mitochondria. Plant Journal 32, 891-904.
144. Takahama U. & Oniki T. (1994) The association of ascorbate and ascorbate oxidase in the apoplast with IAA-enhanced elongation of epicotyls from Vigna angularis. Plant Cell Physiology 35, 257-266.
145. Taylor N.L., Day D.A. & Millar A.H. (2002) Environmental stress causes oxidative damage to plant mitochondria leading to inhibition of glycine decarboxylase. Journal of Biological Chemistry 277, 42663-42668.
146. Thom R., Dixon D.P., Edwards R., Cole D.J. & Lapthorn A.J. (2001) The structure of a zeta class glutathione S-transferase from Arabidopsis thaliana: Characterisation of a GST with novel active-site architecture and a putative role in tyrosine catabolism. Journal of Molecular Biology 308, 949-962.
147. Ursini F., Mariorino M., Brigelius-Flohé R., Aumann K.D., Roveri A., Schomburg D. & Flohé L. (1995) Diversity of glutathione peroxidase. Methods in Enzymology 252, 38-53.
148. 2 accumulation in mesophyll cells leads to induction of glutathione during the hypersensitive response in the barley-powdery mildew interaction. Plant Physiology 123, 1289-1300.
149. Vandenabeele S., Van Der Kelen K., Dat J., et al. (2002) A comprehensive analysis of hydrogen peroxide-induced gene expression in tobacco. Proceedings of the National Academy of Sciences of the USA 100, 16113-16118.
150. Vavilin D.V. & Vermaas W.F.J. (2002) Regulation of the tetrapyrrole biosynthetic pathway leading to heme and chlorophyll in plants and cyanobacteria. Physiologia Plantarum 115, 9-24.
151. Veljovic-Jovanovic S.D., Pignocchi C., Noctor G. & Foyer C.H. (2001) Low ascorbic acid in the vtc1 mutant of Arabidopsis is associated with decreased growth and intracellular redistribution of the antioxidant system. Plant Physiology 127, 426-435.
152. Vernoux T., Wilson R.C., Seeley K.A., et al. (2000) The ROOT MERISTEMLESS1/CADMIUM SENSITIVE2 gene defines a glutathione-dependent pathway involved in initiation and maintenance of cell division during postembryonic root development. Plant Cell 12, 97-110.
153. Vranova E., Atichartpongkul S., Villarroel R., Van Montagu M., Inzé D. & Van Camp W. (2002) Comprehensive analysis of gene expression in Nicotiana tabacum leaves acclimated to oxidative stress. Proceedings of the National Academy of Sciences of the USA 99, 10870-10875.
154. Wachter A., Wolf S., Steiniger H., Bogs J. & Rausch T. (2005) Differential targeting of GSH1 and GSH2 is achieved by multiple transcription initiation: implications for the compartmentation of glutathione biosynthesis in the Brassicaceae. Plant Journal 41, 15-30.
155. Wagner D., Przybyla D., Op den Camp R., et al. (2004) The genetic basis of singlet oxygen-induced stress responses of Arabidopsis thaliana. Science 306, 1183-1185.
156. 3 plants. EMBO Journal 16, 4806-4816.
157. Wingsle G. & Karpinski S. (1996) Differential redox regulation by glutathione of glutathione reductase and CuZn-superoxide dismutase gene expression in Pinus sylvestris L. needles. Planta 198, 151-157.
158. Xiang C. & Bertrand D. (2000) Glutathione synthesis in Arabidopsis: multilevel controls coordinate responses to stress. In Sulfur Nutrition and Sulphur Assimilation in Higher Plants (eds C. Brunold, H. Rennenberg, L.J. De Kok, I. Stulen & J.C. Davidian), pp. 409-412. Paul Haupt, Bern, Switzerland.
159. Xiang C. & Oliver D.J. (1998) Glutathione metabolic genes coordinately respond to heavy metals and jasmonic acid in Arabidopsis. Plant Cell 10, 1539-1550.
160. Xiang C., Werner B.L., Christensen E.M. & Oliver D.J. (2001) The biological functions of glutathione revisited in Arabidopsis transgenic plants with altered glutathione levels. Plant Physiology 126, 564-574.
161. 2-induced cell death via coordinated regulation of stress kinases. Cancer Research 60, 4053-4057.
162. Yoshimura K., Miyao K., Gaber A., Takeda T., Kanaboshi H., Miyasaka H. & Shigeoka S. (2004) Enhancement of stress tolerance in transgenic tobacco plants overexpressing Chlamydomonas glutathione peroxidase in chloroplasts or cytosol. Plant Journal 37, 21-33.
163. Zhang W., Zhang L., Dong F., Gao J., Galbraith D.W. & Song C.P. (2001) Hydrogen peroxide is involved in abscisic acid-induced stomatal closure in Vicia faba. Plant Physiology 126, 1438-1448.