Metabolic signalling in defence and stress: The central roles of soluble redox couples

Plant, Cell and Environment

Volumn 29, Issue 3, 2006, Pages 409-425

  Noctor, Graham ^a  

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

Author keywords

Antioxidant; Ascorbate; Calcium; Glutathione; NAD; NADP; Pyridine nucleotides; Reductant

Indexed keywords

ASCORBIC ACID; GLUTATHIONE; NICOTINAMIDE ADENINE DINUCLEOTIDE; NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE;

METABOLISM;

ADAPTATION; BIOSYNTHESIS; CELL COMPARTMENTALIZATION; ENVIRONMENT; METABOLISM; OXIDATION REDUCTION REACTION; PHYSIOLOGY; PLANT; REVIEW; SIGNAL TRANSDUCTION;

ADAPTATION, PHYSIOLOGICAL; ASCORBIC ACID; CELL COMPARTMENTATION; ENVIRONMENT; GLUTATHIONE; NAD; NADP; OXIDATION-REDUCTION; PLANTS; SIGNAL TRANSDUCTION;

EID: 33645038450     PISSN: 01407791     EISSN: 13653040     Source Type: Journal    
DOI: 10.1111/j.1365-3040.2005.01476.x     Document Type: Review

References (171)

1. Agius F. González-Lamothe R. Caballero JL. Muňòoz- Blanco J. Botella MA. Valpuesta V. 2003 Engineering increased vitamin C levels in plants by overexpression of a d -galacturonic acid reductase Nature Biotechnology 21 177 181
2. Allen JF. 2002 Plastoquinone redox control of chloroplast thylakoid protein phosphorylation and distribution of excitation energy between photosystems: discovery, background, implications Photosynthesis Research 73 139 148
3. Anderson LE. Wang X. Gibbons JT. 1995 Three enzymes of carbon metabolism or their antigenic analogs in pea leaf nuclei Plant Physiology 108 659 667
4. Apel K. Hirt H. 2004 Reactive oxygen species: metabolism, oxidative stress, and signal transduction Annual Review of Plant Biology 55 373 399
5. Arisi ACM. Noctor G. Foyer CH. Jouanin L. 1997 Modification of thiol contents in poplars (Populus tremula×P. alba) overexpressing enzymes involved in glutathione synthesis Planta 203 362 372
6. Asada K. 1999 The water-water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons Annual Review of Plant Physiology and Plant Molecular Biology 50 601 639
7. Baerson SR. Sánchez-Moreiras A. Pedrol-Bonjoch N. Schulz M. Kagan IA. Agarwal AK. Reigosa MJ. Duke SO. 2005 Detoxification and transcriptome response in Arabidopsis seedlings exposed to the allelochemical benzoxazolin-2-(3H)-one Journal of Biological Chemistry 280 21867 21881
8. Baier M. Dietz K-J. 2005 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 56 1449 1462
9. 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
10. Bartoli CG. Guiamet JJ. Kiddle G. Pastori GM. Di Cagno R. Theodoulou F. Foyer CH. 2005 Ascorbate content of wheat leaves is not determined by maximal l -galactono-1,4-lactone dehydrogenase (GalLDH) activity under drought stress Plant, Cell and Environment 28 1073 1081
11. Bechtold U. Karpinski S. Mullineaux PM. 2005 The influence of the light environment and photosynthesis on oxidative signalling responses in plant-biotrophic pathogen interactions Plant, Cell and Environment 28 1046 1055
12. Beer SM. Taylor ER. Brown SE. Dahm CC. Costa NJ. Runswick MJ. Murphy MP. 2004 Glutaredoxin 2 catalyzes the reversible oxidation and glutathionylation of mitochondrial membrane thiol proteins Journal of Biological Chemistry 279 47939 47951
13. Belmonte MF. Donald G. Reid DM. Yeung EC. Stasolia C. 2005 Alterations of the glutathione redox state improve apical meristem structure and somatic embryo quality in white spruce (Picea glauca) Journal of Experimental Botany 56 2355 2364
14. Bérczi A. Møller IM. 2000 Redox enzymes in the plant plasma membrane and their possible roles Plant, Cell and Environment 23 1287 1302
15. Berglund TL. Kalbin G. Strid A. Rydström J. Ohlsson AB. 1996 UV-B- and oxidative stress-induced increase in nicotinamide and trigonelline and inhibition of defensive metabolism induction by poly (ADP-ribose) polymerase inhibitor in plant tissue FEBS Letters 380 188 193
16. Bick JA. Setterdahl AT. Knaff DB. Chen Y. Pitcher LH. Zilinskas BA. Leustek T. 2001 Regulation of the plant-type 5′-adenylylsulfate reductase by oxidative stress Biochemistry 40 9040 9048
17. Bolwell GP. Bindschedler LV. Blee KA. Butt VS. Davies DR. Gardner SL. Gerrish C. Minibayeva F. 2002 The apoplastic oxidative burst in response to biotic stress in plants: a three-component system Journal of Experimental Botany 53 1367 1376
18. Bouché N. Yellin A. Snedden WA. Fromm H. 2005 Plant-specific calmodulin-binding proteins Annual Review of Plant Biology 56 435 466
19. Brandizzi F. Fricker M. Hawes C. 2002 A greener world: the revolution in plant bioimaging Nature Reviews Molecular Cell Biology 3 520 529
20. Broadbent P. Creissen GP. Kular B. Wellburn AR. Mullineaux P. 1995 Oxidative stress responses in transgenic tobacco containing altered levels of glutathione reductase activity Plant Journal 8 247 255
21. Buchanan BB. Balmer Y. 2005 Redox regulation: a broadening horizon Annual Review of Plant Biology 56 187 220
22. Cagnac O. Bourbouloux A. Chakrabarty D. Zhang MY. Delrot S. 2004 AtOPT6 transports glutathione derivatives and is induced by primisulfuron Plant Physiology 135 1378 1387
23. Chen Z. Gallie DR. 2004 The ascorbic acid redox state controls guard cell signalling and stomatal movement Plant Cell 16 1143 1162
24. Chen Z. Gallie DR. 2005 Increasing tolerance to ozone by elevating foliar ascorbic acid confers greater protection against ozone than increasing avoidance Plant Physiology 138 1673 1689
25. Cheng NH. Hirschi KD. 2003 Cloning and characterization of CXIP1, a novel PICOT domain-containing Arabidopsis protein that associates with CAX1 Journal of Biological Chemistry 278 6503 6509
26. 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
27. Cobbett CS. Goldsborough P. 2002 Phytochelatins and metallothioneins: roles in heavy metal detoxification and homeostasis Annual Review of Plant Biology 53 159 182
28. Cobbett CS. May MJ. 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
29. Conklin PL. Barth 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
30. Conklin PL. Williams EH. Last RL. 1996 Environmental stress sensitivity of an ascorbic acid-deficient Arabidopsis mutant Proceedings of the National Academy of Sciences of the USA 93 9970 9974
31. Conklin PL. Norris SR. Wheeler GL. Williams EH. Smirnoff N. Last RL. 1999 Genetic evidence for the role of GDP-mannose in plant ascorbic acid (vitamin C) biosynthesis Proceedings of the National Academy of Sciences of the USA 96 4198 4203
32. Conklin PL. Saracco SA. Norris SR. Last RL. 2000 Identification of ascorbic acid-deficient Arabidopsis thaliana mutants Genetics 154 847 856
33. Corpas FJ. Barroso JB. Sandalio LM. Distefano S. Palma JM. Lupianez JA. Del Rio LA. 1998 A dehydrogenase-mediated recycling system of NADPH in plant peroxisomes Biochemical Journal 330 777 784
34. Crawford NM. Guo FQ. 2005 New insights in nitric oxide metabolism and regulatory functions Trends in Plant Science 10 195 200
35. Creissen G. Reynolds H. Xue YB. Mullineaux P. 1995 Simultaneous targeting of pea glutathione reductase and of a bacterial fusion protein to chloroplasts and mitochondria Plant Journal 8 167 175
36. Creissen G. Firmin J. Fryer M. et al. 1999 Elevated glutathione biosynthetic capacity in the chloroplasts of transgenic tobacco paradoxically causes increased oxidative stress Plant Cell 11 1277 1291
37. 2+ signaling in T-lymphocytes Journal of Biological Chemistry 280 21394 21399
38. Davletova S. Rizhsky L. Liang H. Shengqiang Z. Oliver DJ. Coutu J. Shulaev V. Schlauch K. Mittler R. 2005 Cytosolic ascorbate peroxidase 1 is a central component of the reactive oxygen gene network of Arabidopsis Plant Cell 17 268 281
39. De Pinto MC. De Gara L. 2004 Changes in the ascorbate metabolism of apoplastic and symplastic spaces are associated with cell differentiation Journal of Experimental Botany 55 2559 2569
40. De Tullio MC. Arrigoni O. 2004 Hopes, disillusions and more hopes from vitamin C Cellular and Molecular Life Sciences 61 209 219
41. Debnam PM. Fernie AR. Leisse A. Golding A. Bowsher CG. Grimshaw C. Knight JS. Emes MJ. 2004 Altered activity of the P2 isoform of plastidic glucose 6-phosphate dehydrogenase in tobacco (Nicotiana tabacum cv. Samsun) causes changes in carbohydrate metabolism and response to oxidative stress in leaves Plant Journal 38 49 59
42. 2 receptor and redox-transducer in gene activation Cell 111 1 11
43. Delumeau O. Renard M. Montrichard F. 2000 Characterization and possible redox regulation of the purified calmodulin-dependent NAD kinase from Lycopersicon pimpinellifolium Plant, Cell and Environment 23 1267 1273
44. Demmig-Adams B. 1990 Carotenoids and photoprotection in plants: a role for the xanthophyll zeaxanthin Biochimica et Biophysica Acta 1020 1 24
45. Desikan R. Mackerness SAH. Hancock JT. Neill SJ. 2001 Regulation of the Arabidopsis transcriptome by oxidative stress Plant Physiology 127 159 172
46. Desikan R. Hancock JT. Bright J. Harrison J. Weir I. Hooley R. Neill SJ. 2005 A role for ETR1 in hydrogen peroxide signaling in stomatal guard cells Plant Physiology 137 831 834
47. 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 Plant Cell 15 2181 2191
48. D'Haese D. Vandermeiren K. Asard H. Horemans N. 2005 Other factors than apoplastic ascorbate contribute to the differential ozone tolerance of two clones of Trifolium repens L Plant, Cell and Environment 28 623 632
49. Díaz M. Achkor H. Titarenko E. Martínez MC. 2003 The gene encoding glutathione-dependent formaldehyde dehydrogenase/GSNO reductase is responsive to wounding, jasmonic acid and salicylic acid FEBS Letters 543 136 139
50. Dietz K-J. 2003 Plant peroxiredoxins Annual Review of Plant Biology 54 93 107
51. Dixon DP. Davis BG. 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 30 859 30 869
52. Dixon DP. Fordham-Skelton AP. Edwards R. 2005 Redox regulation of a soybean tyrosine-specific protein phosphatase Biochemistry 44 7696 7703
53. Dixon DP. Skipsey M. Grundy NM. Edwards R. 2005 Stress-induced protein S-glutathionylation in Arabidopsis Plant Physiology 138 2233 2244
54. Dizengremel P. 2001 Effects of ozone on the carbon metabolism of forest trees Plant Physiology and Biochemistry 39 729 742
55. Douce R. Neuburger M. 1989 The uniqueness of plant mitochondria Annual Review of Plant Physiology and Plant Molecular Biology 40 371 414
56. Droux M. 2004 Sulfur assimilation and the role of sulfur in plant metabolism: a survey Photosynthesis Research 79 331 348
57. Dutilleul C. Driscoll S. Cornic G. De Paepe R. Foyer CH. Noctor G. 2003a Functional mitochondrial complex I is required for optimal photosynthetic performance in photorespiratory conditions and during transients Plant Physiology 131 264 275
58. Dutilleul C. Garmier M. Noctor G. Mathieu CD. Chétrit P. Foyer CH. De Paepe R. 2003b 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
59. Dutilleul C. Lelarge C. Prioul JL. De Paepe R. Foyer CH. Noctor G. 2005 Mitochondria-driven changes in leaf NAD status exert a crucial influence on the control of nitrate assimilation and the integration of carbon and nitrogen metabolism Plant Physiology 139 64 78
60. Edwards R. Blount JW. Dixon RA. 1991 Glutathione and elicitation of the phytoalexin response in legume cell cultures Planta 184 403 409
61. Edwards R. Dixon DP. Walbot V. 2000 Plant glutathione S-transferases: enzymes with multiple functions in sickness and in health Trends in Plant Sciences 5 193 198
62. Evans NH. McAinsh MR. Hetherington AM. Knight MR. 2005 ROS perception in Arabidopsis thaliana: the ozone-induced calcium response Plant Journal 41 615 626
63. Fey V. Wagner R. Bräutigam K. Pfannschmidt T. 2005 Photosynthetic redox control of nuclear gene expression Journal of Experimental Botany 56 1491 1498
64. + and NADH allows the transcriptional corepressor carboxyl-terminal binding protein to serve as a metabolic sensor Proceedings of the National Academy of Sciences of the USA 100 9202 9207
65. Foreman J. Demidchik V. Bothwell JH. et al. 2003 Reactive oxygen species produced by NADPH oxidase regulate plant cell growth Nature 27 442 446
66. Foyer CH. Noctor G. 2005 Redox homeostasis and antioxidant signaling: a metabolic interface between stress perception and physiological responses Plant Cell 17 1866 1875
67. Foyer CH. Lelandais M. Harbinson J. 1992 Control of the quantum efficiencies of photosystem I and II, electron flow, and enzyme activation following dark-to-light transitions in pea leaves Plant Physiology 99 979 986
68. Foyer CH. Souriau N. Perret S. Lelandais M. Kunert KJ. Pruvost C. Jouanin L. 1995 Overexpression of glutathione reductase but not glutathione synthetase leads to increases in antioxidant capacity and resistance to photoinhibition in poplar trees Plant Physiology 109 1047 1057
69. Franceschi VR. Nakata PA. 2005 Calcium oxalate in plants: formation and function Annual Review of Plant Biology 56 41 71
70. Franceschi VR. Tarlyn NM. 2002 l -Ascorbic acid is accumulated in source leaf phloem and transported to sink tissues in plants Plant Physiology 130 649 656
71. Frendo P. Gallesi D. Turnbull R. Van de Sype G. Hérouart D. Puppo A. 1999 Localisation of glutathione and homoglutathione in Medicago truncatula is correlated to a differential expression of genes involved in their synthesis Plant Journal 17 215 219
72. Frendo P. Harrison J. Norman C. Hernandez-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 18 254 259
73. Gao Z. Loescher WH. 2000 NADPH supply and mannitol biosynthesis. Characterization, cloning, and regulation of the non-reversible glyceraldehyde-3-phosphate dehydrogenase in celery leaves Plant Physiology 124 321 330
74. Gatzek S. Wheeler GL. Smirnoff N. 2002 Antisense suppression of l -galactose dehydrogenase in Arabidopsis thaliana provides evidence for its role in ascorbate synthesis and reveals light-modulated l -galactose synthesis Plant Journal 30 541 553
75. Gelhaye E. Rouhier N. Gérard J. et al. 2004 A specific form of thioredoxin h occurs in plant mitochondria and regulates the alternative oxidase Proceedings of the National Academy of Sciences of the USA 101 14545 14550
76. Giegé P. Heazlewood JL. Roessner-Tunali U. Millar AH. Fernie AR. Leaver CJ. Sweetlove LJ. 2003 Enzymes of glycolysis are functionally associated with the mitochondrion in Arabidopsis cells Plant Cell 15 2140 2151
77. Gomez L. Vanacker H. Buchner P. Noctor G. Foyer CH. 2004 The intercellular distribution of glutathione synthesis and its response to chilling in maize Plant Physiology 134 1662 1671
78. Grace SC. Logan BA. 1996 Acclimation of foliar antioxidant systems to growth irradiance in three broad-leaved evergreen species Plant Physiology 112 1631 1640
79. Green MA. Fry SC. 2005 Vitamin C degradation in plant cells via enzymatic hydrolysis of 4-O-oxalyl- l -threonate Nature 433 83 87
80. Hanson GT. Aggeler R. Oglesbee D. Cannon M. Capaldi RA. Tsien RY. Remington SJ. 2004 Investigating mitochondrial redox potential with redox-sensitive green fluorescent protein indicators Journal of Biological Chemistry 279 13044 13053
81. Harding SA. Oh SH. Roberts DA. 1997 Transgenic tobacco expressing a foreign calmodulin gene shows an enhanced production of active oxygen species EMBO Journal 16 1137 1144
82. 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
83. Hartmann TN. Fricker MD. Rennenberg H. Meyer AJ. 2003 Cell-specific measurement of cytosolic glutathione in poplar leaves Plant, Cell and Environment 26 965 975
84. Hayashi M. Takahashi H. Tamura K. Huang J. Yu LH. Kawai-Yamada M. Tezuka T. Uchimiya H. 2005 Enhanced dihydroflavonol-4-reductase activity and NAD homeostasis leading to cell death tolerance in transgenic rice Proceedings of the National Academy of Sciences of the USA 102 7020 7025
85. Heineke D. Riens B. Grosse H. Hoferichter P. Peter U. Flügge UI. Heldt HW. 1991 Redox transfer across the inner chloroplast envelope membrane Plant Physiology 95 1131 1137
86. 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
87. Hu X. Neill SJ. Tang Z. Cai W. 2005 Nitric oxide mediates gravitropic bending in soybean roots Plant Physiology 137 663 670
88. Hunt L. Lerner F. Ziegler M. 2004 NAD - new roles in signalling and gene regulation in plants New Phytologist 163 31 44
89. Igamberdiev AU. Gardeström P. 2003 Regulation of NAD- and NADP-dependent isocitrate dehydrogenases by reduction levels of pyridine nucleotides in mitochondria and cytosol of pea leaves Biochimica et Biophysica Acta 1606 117 125
90. 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
91. Jamaï A. Tommasini R. Martinoia E. Delrot S. 1996 Characterization of glutathione uptake in broad bean leaf protoplasts Plant Physiology 111 1145 1152
92. Jez JM. Cahoon RE. Chen S. 2004 Arabidopsis thaliana glutamate-cysteine ligase. Functional properties, kinetic mechanism, and regulation of activity Journal of Biological Chemistry 279 33463 33470
93. Kiddle G. Pastori GM. Bernard S. Pignocchi C. Antoniw J. Verrier PJ. Foyer CH. 2003 Effects of leaf ascorbate on defense and photosynthesis gene expression in Arabidopsis thaliana Antioxidants and Redox Signaling 5 23 32
94. Kocsy G. Von Ballmoos S. Suter M. Ruegsegger A. Galli U. Szalai G. Galiba G. Brunold C. 2000 Inhibition of glutathione synthesis reduces chilling tolerance in maize Planta 211 528 536
95. 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
96. Kranner I. Beckett RP. Wornik S. Zorn M. Pfeifhofer HW. 2002 Revival of a resurrection plant correlates with its antioxidant status Plant Journal 31 13 24
97. Kushnir S. Babiychuk E. Kampfenkel K. Belles-Boix E. Van Montagu M. Inzé D. 1995 Characterization of Arabidopsis thaliana cDNAs that render yeasts tolerant toward the thiol-oxidizing drug diamide Proceedings of the National Academy of Sciences of the USA 92 10580 10584
98. Kwak JM. Mori IC. Pei ZM. Leonhardt N. Torres MA. Dangl JL. Bloom RE. Bodde S. Jones JD. Schroeder JI. 2003 NADPH oxidase AtrbohD and AtrbohF genes function in ROS-dependent ABA signaling in Arabidopsis EMBO Journal 22 2623 2633
99. Laing WA. Bulley S. Wright M. Cooney J. Jensen D. Barraclough D. MacRae E. 2004 A highly specific l -galactose-1-phosphate phosphatase on the path to ascorbate biosynthesis Proceedings of the National Academy of Sciences of the USA 101 16976 16981
100. Laloi C. Mestres-Ortega D. Marco Y. Meyer Y. Reichheld JP. 2004 The Arabidopsis cytosolic thioredoxin h5 gene induction by oxidative stress and is W-Box-mediated response to pathogen elicitor Plant Physiology 134 1006 1016
101. Lemaire SD. 2004 The glutaredoxin family in oxygenic photosynthetic organisms Photosynthesis Research 79 305 318
102. Leterrier M. Corpas FJ. Barroso JB. Sandalio LM. Del Rio LA. 2005 Peroxisomal monodehydroascorbate reductase. Genomic clone characterization and functional analysis under environmental stress conditions Plant Physiology 138 2111 2113
103. Lindermayr C. Saalbach G. Durner J. 2005 Proteomic identification of S-nitrosylated proteins in Arabidopsis Plant Physiology 137 921 930
104. Loewus FA. 1999 Biosynthesis and metabolism of ascorbic acid in plants and of analogs of ascorbic acid in fungi Phytochemistry 52 193 210
105. Looger LL. Lalonde S. Frommer WB. 2005 Genetically encoded FRET sensors for visualizing metabolites with subcellular resolution in living cells Plant Physiology 138 555 557
106. Lorence A. Chevone BI. Mendes P. Nessler CL. 2004 myo-Inositol oxygenase offers a possible entry point into plant ascorbate biosynthesis Plant Physiology 134 1200 1205
107. Maddison J. Lyons T. Plochl M. Barnes J. 2002 Hydroponically cultivated radish fed l -galactono-1,4-lactone exhibits increased tolerance to ozone Planta 214 383 391
108. Mano J. Belles-Boix E. Babiychuk E. Inzé D. Torii Y. Hiraoka E. Takimoto K. Slooten L. Asada K. Kushnir S. 2005 Protection against photooxidative injury of tobacco leaves by 2-alkenal reductase. Detoxification of lipid peroxide-derived reactive carbonyls Plant Physiology 139 1773 1783
109. May MJ. Vernoux T. Sanchez-Fernandez R. Van Montagu M. Inzé D. 1998 Evidence for post-transcriptional activation of γ-glutamylcysteine synthetase during plant stress responses Proceedings of the National Academy of Sciences of the USA 95 12049 12054
110. Meyer AJ. May MJ. Fricker M. 2001 Quantitative in vivo measurement of glutathione in Arabidopsis cells Plant Journal 27 67 78
111. Mezzari M. Walters K. Jelinkova M. Shih MC. Just CL. Schnoor JL. 2005 Gene expression and microscopic analysis of Arabidopsis exposed to chloroacetanilide herbicides and explosive compounds. A phytoremediation approach Plant Physiology 138 858 869
112. Michelet L. Zaffagnini M. Marchand C. et al. 2005 Glutathionylation of chloroplast thioredoxin f is a redox signaling mechanism in plants Proceedings of the National Academy of Sciences of the USA 102 16478 16483
113. Millar AH. Mittova V. Kiddle G. Heazlewood JL. Bartoli CG. Theodoulou FL. Foyer CH. 2003 Control of ascorbate synthesis by respiration and its implications for stress responses Plant Physiology 133 443 447
114. Mittler R. Vanderauwera S. Gollery M. Van Breusegem F. 2004 Reactive oxygen gene network of plants Trends in Plant Science 9 490 498
115. Møller IM. 2001 Plant mitochondria and oxidative stress: electron transport, NADPH turnover, and metabolism of reactive oxygen species Annual Review of Plant Physiology and Plant Molecular Biology 52 561 591
116. Møller IM. Rasmusson AG. 1998 The role of NADP in the mitochondrial matrix Trends in Plant Science 3 21 27
117. Mou Z. Fan W. Dong X. 2003 Inducers of plant systemic acquired resistance regulate NPR1 function through redox changes Cell 27 935 944
118. Müller-Moulé P. Conklin PL. Niyogi KK. 2002 Ascorbate deficiency can limit violaxanthin de-epoxidase activity in vivo Plant Physiology 128 970 977
119. Müller-Moulé P. Golan T. Niyogi KK. 2004 Ascorbate-deficient mutants of Arabidopsis grow in high light despite chronic photooxidative stress Plant Physiology 134 1163 1172
120. Navazio L. Bewell MA. Siddiqua A. Dickinson G. Galione A. Sanders D. 2000 Calcium release from the endoplasmic reticulum of higher plants elicited by the NADP metabolite nicotinic acid adenine dinucleotide phosphate Proceedings of the National Academy of Sciences of the USA 97 8693 8698
121. Noctor G. Gomez L. Vanacker H. Foyer CH. 2002 Interactions between biosynthesis, compartmentation and transport in the control of glutathione homeostasis and signalling Journal of Experimental Botany 53 1283 1304
122. Nunes-Nesi A. Carrari F. Lytovchenko A. Smith AMO. Loureiro ME. Ratcliffe RG. Sweetlove LJ. Fernie AR. 2005 Enhanced photosynthetic performance and growth as a consequence of decreasing mitochondrial malate dehydrogenase activity in transgenic tomato plants Plant Physiology 137 611 622
123. Ortega A. Ferrer P. Carretero J. Obrador E. Asensi M. Pellicer JA. Estrela JM. 2003 Down-regulation of glutathione and Bcl-2 synthesis in mouse B16 melanoma cells avoids their survival during interaction with the vascular endothelium Journal of Biological Chemistry 278 39591 39599
124. 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 signalling Plant Cell 15 939 951
125. Pignocchi C. Foyer CH. 2003 Apoplastic ascorbate metabolism and its role in the regulation of cell signalling Current Opinion in Plant Biology 6 379 389
126. Planchet E. Gupta KJ. Sonoda M. Kaiser WM. 2005 Nitric oxide emission from tobacco leaves: rate-limiting factors and evidence for the involvement of mitochondrial electron transport Plant Journal 41 732 743
127. Polle A. 2001 Dissecting the superoxide dismutase-ascorbate-glutathione pathway in chloroplasts by metabolic modeling. Computer simulations as a step towards flux analysis Plant Physiology 126 445 462
128. 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
129. Preger V. Scagliarini S. Pupillo P. Trost P. 2004 Identification of an ascorbate-dependent cytochrome b of the tonoplast membrane sharing biochemical features with members of the cytochrome b561 family Planta 220 365 375
130. Pugin A. Frachisse JM. Tavernier E. Bligny R. Gout E. Douce R. Guern J. 1997 Early events induced by the elicitor cryptogein in tobacco cells: involvement of a plasma membrane NADPH oxidase and activation of glycolysis and the pentose phosphate pathway Plant Cell 9 2077 2091
131. Raghavendra AS. Padmasree K. 2003 Beneficial interactions of mitochondrial metabolism with photosynthetic carbon assimilation Trends in Plant Science 8 546 553
132. Rasmusson AG. Soole KL. Elthon TE. 2004 Alternative NAD(P)H dehydrogenases of plant mitochondria Annual Review of Plant Biology 55 23 39
133. Reid ME. 1941 Relation of vitamin C to cell size in the growing region of the primary root of cowpea seedlings American Journal of Botany 28 410 415
134. Rizhsky L. Hallak-Herr E. Van Breusegem F. Rachmilevitch S. Barr JE. Rodermel S. Inzé 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 Plant Journal 32 329 342
135. Sabar M. De Paepe R. De Kouchkovsky Y. 2000 Complex I impairment, respiratory compensations, and photosynthetic decrease in nuclear and mitochondrial male sterile mutants of Nicotiana sylvestris Plant Physiology 124 1239 1249
136. Saito K. 2004 Sulfur assimilatory metabolism: the long and smelling road Plant Physiology 136 2443 2450
137. Sanders D. Pelloux J. Brownlee C. Harper JF. 2002 Calcium at the crossroads of signaling Plant Cell 14 S401 S417
138. Sanmartin M. Drogouti PD. Lyons T. Barnes J. Kanellis AK. 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
139. Scheibe R. Backhausen JE. Emmerlich V. Holtgrefe S. 2005 Strategies to maintain redox homeostasis during photosynthesis under changing conditions Journal of Experimental Botany 56 1481 1489
140. Sen Gupta A. Alscher RG. McCune D. 1991 Response of photosynthesis and cellular antioxidants to ozone in Populus leaves Plant Physiology 96 650 655
141. Setterdahl AT. Chivers PT. Hirasawa M. et al. 2003 Effect of pH on the oxidation-reduction properties of thioredoxins Biochemistry 42 14877 14884
142. Shimaoka T. Miyake C. Yokota A. 2003 Mechanism of the reaction catalyzed by dehydroascorbate reductase from spinach chloroplasts European Journal of Biochemistry 270 921 928
143. Singh SP. Wishnok JS. Keshive M. Deen WM. Tannenbaum SR. 1996 The chemistry of the S-nitrosoglutathione/glutathione system Proceedings of the National Academy of Sciences of the USA 100 14672 14677
144. Singla-Pareek SL. Reddy MK. Sopory SK. 2003 Genetic engineering of the glyoxalase pathway in tobacco leads to enhanced salinity tolerance Proceedings of the National Academy of Sciences of the USA 100 14672 14677
145. Skipsey M. Andrews CJ. Townson JK. Jepson I. Edwards R. 2000 Cloning and characterization of glyoxalase I from soybean Archives of Biochemistry and Biophysics 374 261 268
146. Smith IK. Kendall AC. Keys AJ. Turner JC. Lea PJ. 1985 The regulation of the biosynthesis of glutathione in leaves of barley (Hordeum vulgare L.) Plant Science 41 11 17
147. Sparla F. Zaffagnini M. Wedel N. Scheibe R. Pupillo P. Trost P. 2005 Regulation of photosynthetic GAPDH dissected by mutants Plant Physiology 138 2210 2219
148. Starke DW. Chock PB. Mieyal JJ. 2003 Glutathione-thiyl radical scavenging and transferase properties of human glutaredoxin (thioltransferase). Potential role in redox signal transduction Journal of Biological Chemistry 278 14607 14613
149. Steinkamp R. Schweihofen B. Rennenberg H. 1987 γ- Glutamylcyclotransferase in tobacco suspension cultures: catalytic properties and subcellular localization Physiologia Plantarum 69 499 503
150. Storozhenko S. Belles-Boix E. Babiychuk E. Hérouart D. Davey MR. Slooten L. Van Montagu M. Inzé D. Kushnir S. 2002 γ-Glutamyl transpeptidase in transgenic tobacco plants. Cellular localization, processing, and biochemical properties Plant Physiology 128 1109 1119
151. Streb P. Aubert S. Gout E. Bligny R. 2003 Cold- and light-induced changes of metabolite and antioxidant levels in two high mountain plant species Soldanella alpina and Ranunculus glacialis and a lowland species Pisum sativum Physiologia Plantarum 118 96 104
152. Sun J. Xu L. Eu JP. Stamler JS. Meissner G. 2003 Nitric oxide, NOC-12, and S-nitrosoglutathione modulate the skeletal muscle calcium release channel/ryanodine receptor by different mechanisms Journal of Biological Chemistry 278 8184 8189
153. Sunkar R. Bartels D. Kirch HH. 2003 Overexpression of a stress-inducible aldehyde dehydrogenase gene from Arabidopsis thaliana in transgenic plants improves stress tolerance Plant Journal 35 452 464
154. Tausz M. Šircelj H. Grill D. 2004 The glutathione system as a stress marker in plant ecophysiology: is a stress-response concept valid? Journal of Experimental Botany 55 1955 1962
155. +-ATPase activity is related to disulfide bridge formation in subunit E as well as subunit A Plant Journal 28 512 559
156. Turner WL. Waller JC. Vanderbeld B. Snedden WA. 2004 Cloning and characterization of two NAD kinases from Arabidopsis. Identification of a calmodulin-binding isoform Plant Physiology 135 1243 1255
157. 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
158. Veljovic-Jovanovic SD. Pignocchi C. Noctor G. Foyer CH. 2001 Low ascorbic acid in the vtc-1 mutant of Arabidopsis is associated with decreased growth and intracellular redistribution of the antioxidant system Plant Physiology 127 426 435
159. Verelst W. Asard H. 2004 Analysis of an Arabidopsis thaliana protein family, structurally related to cytochromes b561 and potentially involved in catecholamine biochemistry in plants Journal of Plant Physiology 161 175 181
160. Vernoux T. Wilson RC. Seeley KA. et al. 2000 The ROOT MERISTEMLESS1/CADMIUM SENSITIVE2 gene defines a glutathione-dependent pathway
161. Voehringer DW. McConkey DJ. McDonnell TJ. Brisbay S. Meyn RE. 1998 Bcl-2 expression causes redistribution of glutathione to the nucleus Proceedings of the National Academy of Sciences of the USA 95 2956 2960
162. 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
163. Wheeler GL. Jones MA. Smirnoff N. 1998 The biosynthetic pathway of vitamin C in higher plants Nature 303 365 369
164. Wolf AE. Dietz K-J. Schröder P. 1996 Degradation of glutathione S-conjugates by a carboxypeptidase in the plant vacuole FEBS Letters 384 31 34
165. Wolucka BA. Van Montagu M. 2003 GDP-mannose 3′,5′-epimerase forms GDP- l -gulose, a putative intermediate for the de novo biosynthesis of vitamin C in plants Journal of Biological Chemistry 278 47483 47490
166. Wolucka BA. Persiau G. Van Doorsselaere J. Davey MW. Demol H. Vandekerckhove J. Van Montagu M. Zabeau M. Boerjan W. 2001 Partial purification and identification of GDP-mannose 3′,5′-epimerase of Arabidopsis thaliana, a key enzyme of the plant vitamin C pathway Proceedings of the National Academy of Sciences of the USA 98 14843 14848
167. Wu Y. Sanchez JP. Lopez-Molina L. Himmelbach A. Grill E. Chua NH. 2003 The abi1-1 mutation blocks ABA signalling downstream of cAPR action Plant Journal 34 307 315
168. Xiang C. Oliver DJ. 1998 Glutathione metabolic genes coordinately respond to heavy metals and jasmonic acid in Arabidopsis Plant Cell 10 1539 1550
169. Yanagida M. Mino M. Iwabuchi M. Ogawa K. 2004 Reduced glutathione is a novel regulator of vernalization-induced bolting in the rosette plant Eustoma grandiflorum Plant and Cell Physiology 45 129 137
170. Yoshimura K. Ishikawa T. Nakamura Y. Tamoi M. Takeda T. Tada T. Nishimura K. Shigeoka S. 1998 Comparative study on recombinant chloroplastic and cytosolic ascorbate peroxidase isozymes of spinach Archives of Biochemistry and Biophysics 353 55 63
171. Zeier J. Delledonne M. Mishina T. Severi E. Sonoda M. Lamb C. 2004 Genetic elucidation of nitric oxide signaling in incompatible plant-pathogen interactions Plant Physiology 136 2875 2886