Reactive oxygen species: Metabolism, oxidative stress, and signal transduction

Annual Review of Plant Biology

Volumn 55, Issue , 2004, Pages 373-399

  Apel, Klaus ^a   Hirt, Heribert ^b  

^a ETH ZURICH   (Switzerland)

^b UNIVERSITY OF VIENNA   (Austria)

Author keywords

Abiotic stress; Pathogen defense; Programmed cell death

Indexed keywords

REACTIVE OXYGEN METABOLITE;

AEROBIC METABOLISM; GENE EXPRESSION REGULATION; METABOLISM; OXIDATIVE STRESS; PHYSIOLOGY; PLANT; PLANT DISEASE; PLANT PHYSIOLOGY; REVIEW; SIGNAL TRANSDUCTION;

AEROBIOSIS; GENE EXPRESSION REGULATION, PLANT; OXIDATIVE STRESS; PLANT DISEASES; PLANT PHYSIOLOGY; PLANTS; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION;

ANIMALIA;

EID: 3242715114     PISSN: 15435008     EISSN: None     Source Type: Book Series    
DOI: 10.1146/annurev.arplant.55.031903.141701     Document Type: Review

References (134)

1. Allan AC, Fluhr R. 1997. Two distinct sources of elicited reactive oxygen species in tobacco epidermal cells. Plant Cell. 9:1559-72
2. Allen RD. 1995. Dissection of oxidative stress tolerance using transgenic plants. Plant Physiol. 107:1049-54
3. Alscher RG, Donahue JH, Cramer CL. 1997. Reactive oxygen species and anti-oxidants: relationships in green cells. Physiol. Plantarum. 100:224-33
4. Alvarez ME, Pennell RI, Meijer P-J, Ishikawa A, Dixon RA, Lamb C. 1998. Reactive oxygen intermediates mediate a systemic signal network in the establishment of plant immunity. Cell 92:773-84
5. Apostol I, Heinstein PF, Low PS. 1989. Rapid stimulation of an oxidative burst during elicidation of cultured plant cells. Role in defense and signal transduction. Plant Physiol. 90:106-16
6. Asada K, Takahashi M. 1987. Production and scavenging of active oxygen in photosynthesis. In Photoinhibition, eds. DJ Kyle, CB Osborne, CJ Arntzen, pp. 227-87, Amsterdam: Elsevier
7. Asada K. 1999. The water-water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons. Annu. Rev. Plant Physiol. Plant Mol. Biol. 50:601-39
8. Babior BM. 1999. NADPH oxidase: an update. Blood 93:1464-76
9. Baker MA, Orlandi EW. 1995. Active oxygen in plant pathogenesis. Annu. Rev. Phytopathol. 33:299-321
10. Barber J. 1998. Photosystem two. Biochim. Biophys. Acta. 1365:269-77
11. Bennoun P. 1982. Evidence for a respiratory chain in the chloroplast. Proc. Natl. Acad. Sci. USA 79:4352-56
12. Bi JL, Felton GW. 1995. Foliar oxidative stress and insect herbivory: primary compounds, secondary metabolites and reactive oxygen species as components of induced resistance. J. Chem. Ecol. 1511-30
13. Bolwell GP, Bindschedler LV, Blee KA, Butt VS, Davies DR, et al. 2002. The apoplastic oxidative burst in response to biotic stress in plants: a three-component system. J. Exp. Bot. 53:1367-76
14. Bolwell GP, Davies DR, Gerrish C, Auh CK, Murphy TM. 1998. Comparative biochemistry of the oxidative burst produced by rose and french bean cells reveals two distinct mechanisms. Plant Physiol. 116:1379-85
15. Bolwell GP. 1999. Role of active oxygen species and NO in plant defense responses. Curr. Opin. Plant Biol. 2:287-94
16. Bradley DJ, Kjellbom P, Lamb CJ. 1992. Elicitor- and wound-induced oxidative cross-linking of a proline-rich plant cell-wall protein: A novel, rapid defense response. Cell 70:21-30
17. Bray EA, Bailey-Serres J, Weretilnyk E. 2000. Responses to abiotic stresses. In Biochemistry and Molecular Biology of Plants, eds. BB Buchanan, W Gruissem and RL Jones, pp. 1158-203. Rockville, MD: Am. Soc. Plant Physiol.
18. Cadenas E. 1989. Biochemistry of oxygen toxicity. Annu. Rev. Biochem. 58:79-110
19. Causton HC, Ren B, Koh SS, Harbison CT, Kanin E, et al. 2001. Remodeling of yeast genome expression in response to environmental changes. Mol. Biol. Cell 12:323-37
20. 2 in transgenic tobacco. Proc. Natl. Acad. Sci. USA 95:5818-23
21. Chen D, Toone WM, Mata J, Lyne R, Burns G, et al. 2003. Global transcriptional responses of fission yeast to environmental stress. Mol. Biol. Cell 14:214-29
22. Chen SX, Schopfer P. 1999. Hydroxylradical production in physiological reactions. A novel function of peroxidase. Eur. J. Biochem. 260:726-35
23. Conklin PL, Williams EH, Last RL. 1996. Environmental stress sensitivity of an ascorbic acid-deficient Arabidopsis mutant. Proc. Natl. Acad. Sci. USA 93:9970-74
24. Creissen G, Firmin J, Fryer M, Kular B, Leyland N, et al. 1999. Elevated glutathione biosynthetic capacity in the chloroplasts of transgenic tobacco plants paradoxically causes increased oxidative stress. Plant Cell 11:1277-92
25. Dalton TP, Shertzer HG, Puga A. 1999. Regulation of gene expression by reactive oxygen. Annu. Rev. Pharmacol. Toxicol. 39:67-101
26. Dangl JL, Jones JDG. 2001. Plant pathogens and integrated defense responses to infection. Nature 411:826-33
27. Davison PA, Hunter CN, Horton P. 2002. Overexpression of β-carotene hydroxylase enhances stress tolerance in Arabidopsis. Nature 418:203-6
28. 2 sensing through oxidation of the Yap2 transcription factor. EMBO J. 19:5157-66
29. 2 receptor and redox-transducer in gene activation. Cell 111:471-81
30. Delledonne M, Zeier J, Marocco A, Lamb C. 2001. Signal interactions between nitric oxide and reactive oxygen intermediates in the plant hypersensitive disease resistance response. Proc. Natl. Acad. Sci. USA 98:13454-59
31. Desikan R, A-H Mackerness S, Hancock JT, Neill SJ. 2001. Regulation of the Arabidopsis transcriptome by oxidative stress. Plant Physiol. 127:159-72
32. Desikan R, Hancock JT, Coffey MJ, Neill SJ. 1996. Generation of active oxygen in elicited cells of Arabidopsis thaliana is mediated by a NADPH oxidase-like enzyme. FEBS Lett. 382:213-17
33. Desikan R, Neill SJ, Hancock JT. 2000. Hydrogen peroxide-induced gene expression in Arabidopsis thaliana. Free Rad. Biol. Med. 28:773-78
34. Desikan R, Reynolds A, Hancock JT, Neill SJ. 1998. Harpin and hydrogen peroxide both initiate programmed cell death but have differential effects on gene expression in Arabidopsis suspension cultures. Biochem. J. 330:115-20
35. 2-generation in membrane fractions isolated from wounded potato tubers inoculated with Phytophtora infestans. Physiol. Plant Pathol. 27:311-22
36. Elstner EF. 1991. Mechanisms of oxygen activation in different compartments of plant cells. In Active Oxygen/Oxidative Stress in Plant Metabolis, eds. EJ Pelland, KL Steffen. pp. 13-25. Rockville, MD: Am. Soc. Plant Physiol.
37. Feild TS, Nedbal L, Ort DR. 1998. Nonphotochemical reduction of the plastoquinone pool in sunflower leaves originates from chlororespiration. Plant Physiol. 116:1209-18
38. Foyer CH, Harbinson JC. 1994. Oxygen metabolism and the regulation of photosynthetic electron transport. In Causes of Photooxidative Stress and Amelioration of Defense Systems in Plant, eds. CH Foyer, PM Mullineaux. pp. 1-42. Boca Raton, Fla.: CRC
39. Foyer CH, Noctor G. 2000. Oxygen processing in photosynthesis: regulation and signaling. New Phytol. 146:359-88
40. 2-reducing activity of horseradish peroxidase by diphenyleneiodonium. Phytochemistry 48:223-27
41. Frahry G, Schopfer P. 2001. NADH-stimulated, cyanide-resistant superoxide production in maize coleoptiles analyzed with a tetrazolium-based assay. Planta 212:175-83
42. Fryer MJ, Oxborough K, Mullineaux PM, Baker NR. 2002. Imaging of photo-oxidative stress responses in leaves. J. Exp. Bot. 53:1249-54
43. Garreton V, Carpinelli J, Jordana X, Holuigue L. 2002. The as-1 promoter element is an oxidative stress-responsive element and salicylic acid activates it via oxidative species. Plant Physiol. 130:1516-26
44. Gasch A, Spellman P, Kao C, Harel O, Eisen M, et al. 2000. Genomic expression programs in the response of yeast cells to environmental changes. Mol. Biol. Cell 11:4241-57
45. Georgiou G. 2002. How to flip the (redox) switch. Cell 111:607-10
46. Girotti AW. 2001. Photosensitized oxidation of membrane lipids: reaction pathways, cytotoxic effects and cytoprotective mechanisms. J. Photochem. Photobiol. 63:103-13
47. Glazener JA, Orlandi EW, Baker CJ. 1996. The active oxygen response of cell suspensions to incompatible bacteria is not sufficient to cause hypersensitive cell death. Plant Physiol. 110:759-63
48. Grant JJ, Loake GJ. 2000. Role of reactive oxygen intermediates and cognate redox signaling in disease resistance. Plant Physiol. 124:21-29
49. Grether-Beck S, Bonizzi G, Schmitt-Brenden H, Felsner I, Timmer A, et al. 2000. Non-enzymatic triggering of the ceramide signaling cascade by solar UVA radiation. EMBO J. 19:5793-800
50. Gupta R, Luan S. 2003. Redox control of protein tyrosine phosphatases and mitogen-activated protein kinases in plants. Plant Physiol. 132:1149-52
51. Gustin MC, Albertyn J, Alexander M, Davenport K. 1998. MAP kinase pathways in the yeast Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev. 62:1264-300
52. Halliwell B, Gutteridge JMC. 1989. Free Radicals in Biology and Medicine, 2nd ed., Oxford: Clarendon
53. Hammond-Kosack K, Jones JDG. 2000. Responses to plant pathogens. In Biochemistry and Molecular Biology of Plants, eds. BB Buchanan, W Gruissem, RL Jones. pp. 1102-156. Rockville, MD: Am. Soc. Plant Physiol.
54. Hideg É, Barta C, Kalai T, Vass I, Hideg K, Asada K. 2002. Detection of singlet oxygen and superoxide with fluorescent sensors in leaves under stress by photo inhibition or UV radiation. Plant Cell Physiol. 43:1154-64
55. Hideg É, Kalai T, Hideg K, Vass I. 1998. Photoinhibition of photosynthesis in vivo results in singlet oxygen production. Detection via nitroxide-induced fluorescence quenching in broad bean leaves. Biochemistry 37:11405-11
56. Hu G, Yalpani N, Briggs SP, Johal GS. 1998. A porphyrin pathway impairment is responsible for the phenotype of a dominant disease lesion mimic mutant of maize. Plant Cell 10:1095-105
57. Hwang I, Chen H-C, Sheen J. 2002. Two-component signal transduction pathways in Arabidopsis. Plant Physiol. 129:500-15
58. Ichinose Y, Andi S, Doi R, Tanaka R, Taguchi F, et al. 2001. Generation of hydrogen peroxide is not required for harpin-induced apoptotic cell death in tobacco BY-2 cell suspension cultures. Plant Physiol. Biochem. 39:771-76
59. Jabs T, Dietrich RA, Dangl JL. 1996. Initiation of runaway cell death in an Arabidopsis mutant by extracellular superoxide. Science 273:1853-56
60. Jonak C, Ökresz L, Bögre L, Hirt H. 2002. Complexity, cross talk and integration of plant MAP kinase signaling. Curr. Opin. Plant Biol. 5:415-24
61. Joo JH, Bae YS, Lee JS. 2001. Role of auxin-induced reactive oxygen species in root gravitropism. Plant Physiol. 126:1055-60
62. Karin M, Liu Z, Zandi E. 1997. AP-1 function and regulation. Curr. Opin. Cell Biol. 9:240-46
63. Karpinski S, Reynolds H, Karpinska B, Wingsle G, Creissen J, Mullineaux PC. 1999. Systemic signaling and acclimation in response to excess excitation energy in Arabidopsis. Science 284:654-57
64. Kawasaki T, Henmi K, Ono E, Hatakeyama S, Iwano M, et al. 1999. The small GTP-binding protein Rac is a regulator of cell death in plants. Proc. Natl. Acad. Sci. USA 96:10922-26
65. Keller T, Danude HG, Werner D, Doerner P, Dixon RA, Lamb C. 1998. A plant homolog of the neutrophil NADPH oxidase gp91phox subunit gene encodes a plasma membrane protein with Ca2+ binding motifs. Plant Cell. 10:255-66
66. Klessig DF, Durner J, Noad R, Navarre DA, Wendehenne D, et al. 2000. Nitric oxide and salicylic acid signaling in plant defense. Proc. Natl. Acad. Sci. USA 97:8849-55
67. Klotz L-O. 2002. Oxidant-induced signaling: effects of peroxynitrite and singlet oxygen. Biol. Chem. 383:443-56
68. Kovtun Y, Chiu W-L, Tena G, Sheen J. 2000. Functional analysis of oxidative stress-activated mitogen-activated protein kinase cascade in plants. Proc. Natl. Acad. Sci. USA 97:2940-45
69. Lee S, Choi H, Suh S, Doo I-S, Oh K-Y, et al. 1999. Oligogalacturonic acid and chitosan reduce stomatal aperture by inducing the evolution of reactive oxygen species from guard cells of tomato and Commelina communis. Plant Physiol. 121:147-52
70. Leisinger U, Rufenacht K, Fischer B, Pesaro M, Spengler A, et al. 2001. The glutathione peroxidase homologous gene from Chlamydomonas reinhardtii is transcriptionally up-regulated by singlet oxygen. Plant Mol. Biol. 46:395-408
71. 2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response. Cell 79:583-93
72. Low PS, Merida JR. 1996. The oxidative burst in plant defense: function and signal transduction. Physiol. Plant. 96:533-42
73. Mach JM, Castillo AR, Hoogstraten R, Greenberg JT. 2001. The Arabidopsis-accelerated cell death gene ACD2 encodes red chlorophyll catabolite reductase and suppresses the spread of disease symptoms. Proc. Natl. Acad. Sci. USA 98:771-76
74. Macpherson AN, Telfer A, Barber J, Truscott TG. 1993. Direct detection of singlet oxygen from isolated photosystem II reaction centres. Biochim. Biophys. Acta 1143:301-9
75. Malan C, Gregling MM, Gressel J. 1990. Correlation between CuZn superoxide dismutase and glutathione reductase and environmental and xenobiotic stress tolerance in maize inbreds. Plant Sci. 69:157-66
76. Matringe M, Camadro JM, Labbe P, Scalla R. 1989. Protoporphyrinogen oxidase as a molecular target for diphenylether herbicides. Biochem. J. 260:231-35
77. Maxwell DP, Nickels R, McIntosh L. 2002. Evidence of mitochondrial involvement in the transduction of signals required for the induction of genes associated with pathogen attack and senescence. Plant J. 29:269-79
78. Maxwell DP, Wang Y, McIntosh L. 1999. The alternative oxidase lowers mitochondrial reactive oxygen production in plant cells. Proc. Natl. Acad. Sci. USA 96:8271-76
79. McAinsh MR, Clayton H, Mansfield TA, Hetherington AM. 1996. Changes in stomatal behaviour and guard cell cytosolic free calcium in response to oxidative stress. Plant Physiol. 111:1031-42
80. Mehler AH. 1951. Studies on reactions of illuminated chloroplasts. II Stimulation and inhibition of the reaction with molecular oxygen. Arch. Biochem. Biophys. 33:339-51
81. Meinhard M, Grill E. 2001. Hydrogen peroxide is a regulator of ABI1, a protein phosphatase 2C from Arabidopsis. FEBS Lett. 508:443-46
82. Meinhard M, Rodriguez PL, Grill E. 2002. The sensitivity of AB12 to hydrogen peroxide links the abscisic acid-response regulator to redox signaling. Planta 214:775-82
83. L and Ced-9 inhibit cell death in tobacco plants. Curr. Biol. 9:775-78
84. Mittler R, Herr EH, Orvar BL, van Camp W, Willekens H, et al. 1999. Transgenic tobacco plants with reduced capability to detoxify reactive oxygen intermediates are hyperresponsive to pathogen infection. Proc. Natl. Acad. Sci. USA 96:14165-14170
85. Mock HP, Heller W, Molina A, Neubohn B, Sandermnann H, Grimm B. 1999. Expression of uroporphyrinogen decarboxylase or coproporphyrinogen oxidase anti-sense RNA in tobacco induces pathogen defense responses conferring increased resistance to tobacco mosaic virus. J. Biol. Chem. 274:4231-38
86. Moon H, Lee B, Choi G, Shin D, Prasad T, 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. Proc. Natl. Acad. Sci. USA 100:358-63
87. Moseyko N, Zhu T, Chang HS, Wang X, Feldman LJ. 2002. Transcription profiling of the early gravitropic response in Arabidopsis using high-density oligonucleotide probe microarrays. Plant Physiol. 130:720-28
88. Mou Z, Fan W, Dong X. 2003. Inducers of plant systemic acquired resistance regulate NPR1 function through redox changes. Cell 113:935-44
89. Mullineaux P, Karpinski S. 2002. Signal transduction in response to excess light: getting out of the chloroplast. Curr. Opin. Plant Biol. 5:43-48
90. 2+ channels in guard cells requires cytosolic NAD(P)H and is differentially disrupted upstream and downstream of reactive oxygen species production in abi1-1 and abi2-1 protein phosphatase 2C mutants. Plant Cell. 13:2513-23
91. Mustilli A-C, Merlot S, Vavasseur A, Fenzi F, Giraudat J. 2002. Arabidopsis OST1 protein kinase mediates the regulation of stomatal aperture by abscisic acid and acts upstream of reactive oxygen species production. Plant Cell 14:3089-99
92. Neill N, Desikan R, Hancock J. 2002. Hydrogen peroxide signaling. Curr. Opin. Plant Biol. 5:388-95
93. Nixon PJ. 2000. Chlororespiration. Philos. Trans. R. Soc. London B 355:1541-47
94. Noctor G, Gomez L, Vanacker H, Foyer CH. 2002. Interactions between biosynthesis, compartmentation and transport in the control of glutathione homeostasis and signaling. J. Exp. Bot. 53:1283-304
95. Ogawa K, Kanematsu S, Asada K. 1997. Generation of superoxide anion and localization of CuZn-superoxide dismutase in the vascular tissue of spinach hypocotyls: their association with lignification. Plant Cell Physiol. 38:1118-26
96. op den Camp RG, Przybyla D, Ochsenbein C, Laloi C, Kim C, et al. 2003. Rapid induction of distinct stress responses following the release of singlet oxygen in Arabidopsis thaliana. Plant Cell 15:2320-32
97. Orozco-Cardenas ML, Narvaez-Vasquez J, Ryan CA. 2001. Hydrogen peroxide acts as a second messenger for the induction of defense genes in tomato plants in response to wounding, systemin, and methyl jasmonate. Plant Cell. 13:179-91
98. Orozco-Cardenas ML, Ryan C. 1999. Hydrogen peroxide is generated systemically in plant leaves by wounding and systemin via the octadecanoid pathway. Proc. Natl. Acad. Sci. USA 96:6553-57
99. Ort RD, Baker NR. 2002. A photoprotective role for O2 as an alternative electronic sink in photosynthesis? Curr. Opin. Plant Biol. 5:193-98
100. Pei Z-M, Murata Y, Benning G, Thomine S, Klusener B, et al. 2000. Calcium channels activated by hydrogen peroxide mediate abscisic signaling in guard cells. Nature 406:731-34
101. Petit J-M, Briat J-F, Lobréaux S. 2001. Structure and differential expression of the four members of the Arabidopsis thaliana ferritin gene family. Biochem. J. 359:575-82
102. Polidoros AN, Mylona PV, Scandalios JG. 2001. Transgenic tobacco plants expressing the maize Cat2 gene have altered catalase levels that affect plant-pathogen interactions and resistance to oxidative stress. Transgenic Res. 10:555-69
103. Prasad TK, Anderson MD, Martin BA, Stewart CR. 1994. Evidence for chilling-induced oxidative stress in maize seedlings and a regulatory role for hydrogen peroxide. Plant Cell. 6:65-74
104. Purvis AC. 1997. Role of the alternative oxidase in limiting superoxide production by plant mitochondria. Physiol. Plant. 100:165-70
105. Quinn J, Findlay VJ, Dawson K, Millar JB, Jones N, et al. 2002. Distinct regulatory proteins control the graded transcriptional response to increasing H(2)O(2) levels in fission yeast Schizosaccharomyces pombe. Mol. Biol. Cell. 13:805-16
106. Rebeiz CA, Montazer-Zouhoor A, Mayasich JM, Tripathy BC, Wu S-M, Rebeiz C. 1988. Photodynamic herbicides. Recent developments and molecular basis of selectivity. CRC Crit. Rev. Plant Sci. 6:385-436
107. Rizhsky L, Hallak-Herr E, Van Breusegem F, Rachmilevitch S, Barr JE, et al. 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 J. 32:329-42
108. Roxas VP, Smith RK, Allen ER, Allen RD. 1997. Overexpression of glutathione S-transferase/glutathione peroxidase enhances the growth of transgenic tobacco seedlings during stress. Nat. Biotechnol. 15:988-91
109. Sagi M, Fluhr R. 2001. Superoxide production by plant homologues of the gp91phox NADPH oxidase. Modulation of activity by calcium and by tobacco mosaic virus infection. Plant Physiol. 126:1281-90
110. Schopfer P, Plachy C, Frahry G. 2001. Release of reactive oxygen intermediates (superoxide radicals, hydrogen peroxide, and hydroxyl radicals) and peroxidase in germinating radish seeds controlled by light, gibberellin and abscisic acid. Plant Physiol. 125:1591-602
111. Schopfer P. 2001. Hydroxyl radical-induced cell-wall loosening in vitro and in vivo: implications for the control of elongation growth. Plant J. 28:679-88
112. Singh KK. 2000. The Saccharomyces cerevisiae SLN1P-SSK1P two component system mediates response to oxidative stress and in an oxidant-specific fashion. Free Rad. Biol. Med. 29:1043-50
113. Solomon M, Belenghi B, Delledonne M, Menachem E, Levine A. 1999. The involvement of cysteine proteases and protease inhibitor genes in the regulation of programmed cell death in plants. Plant Cell 11:431-43
114. Steinbeck MJ, Khan AU, Karnovsky MJ. 1992. Intracellular singlet oxygen generation by phagocytosing neutrophils in response to particles coated with a chemical trap. J. Biol. Chem. 267:13425-33
115. Sweetlove LJ, Heazlewood JL, Herald V, Holtzapffel R, Day DA, et al. 2002. The impact of oxidative stress on Arabidopsis mitochondria. Plant J. 32:891-904
116. Takeda T, Toda T, Kominami K, Kohnosu A, Yanagida M, Jones N. 1995. Schizosaccharomyces pombe atf1+ encodes a transcription factor required for sexual development and entry into stationary phase. EMBO J. 14:6193-208
117. Tenhaken R, Levine A, Brisson LF, Dixon RA, Lamb C. 1995. Function of the oxidative burst in hypersensitive disease resistance. Proc. Natl. Acad. Sci. USA 92:4158-63
118. Tiwari BS, Belenghi B, Levine A. 2002. Oxidative stress increased respiration and generation of reactive oxygen species, resulting in ATP depletion, opening of mitochondrial permeability transition, and programmed cell death. Plant Physiol. 128:1271-81
119. phox homologues AtrbohD and AtrbohF are required for accumulation of reactive oxygen intermediates in the plant defense response. Proc. Natl. Acad. Sci. USA 99:517-22
120. Torres MA, Onouchi H, Hamada S, Machida C, Hammond-Kossack KE, Jones JDG. 1998. Six Arabidopsis thaliana homologues of the human respiratory burst oxidase (gp91phox). Plant J. 14:365-70
121. Tsugane K, Kobayashi K, Niwa Y, Ohba Y, Wada K, Kobayashi H. 1999. A recessive Arabidopsis mutant that grows enhanced active oxygen detoxification. Plant Cell. 11:1195-206
122. van Breusegem F, Slooten L, Stassart JM, Moens T, Botterman J, et al. 1999. Overproduction of Arabidopsis thaliana Fe-SOD confers oxidative stress tolerance to transgenic maize. Plant Cell Physiol. 40:515-23
123. van Montfort RL, Congreve M, Tisi D, Carr R, Jhoti H. 2003. Oxidation state of the active-site cysteine in protein tyrosine phosphatase 1B. Nature 423:773-77
124. 2 accumulation in mesophyll cells leads to induction of glutathione during the hypersensitive response in the barley-powdery mildew interaction. Plant Physiol. 123:1289-300
125. Vera-Estrella R, Blumwald E, Higgins VJ. 1992. Effect of specific elicitors of Cladosporium fulvum on tomato suspension cells. Evidence for the involvement of active oxygen species. Plant Physiol. 99:1208-15
126. Vernoux T, Sanchez-Fernandez R, May M. 2002. Glutathione biosynthesis in plants. In Oxidative Stress in Plants, eds. D Inze, MV Montagu. pp. 297-311. London: Taylor and Francis
127. Vianello A, Macri F. 1991. Generation of superoxide anion and hydrogen peroxide at the surface of plant cells. J. Bioenerg. Biomembr. 23:409-23
128. Vranova E, Atichartpongkul S, Villarroel R, Van Montagu M, Inze D, Van Camp W. 2002. Comprehensive analysis of gene expression in Nicotiana tabacum leaves acclimated to oxidative stress. Proc. Natl. Acad. Sci. USA 99:10870-75
129. Wagner AM. 1995. A role for active oxygen species as second messengers in the induction of alternative oxidase gene expression in Petunia hybrida cells. FEBS Lett. 368:339-12
130. Whistler CA, Corbell NA, Sarniguet A, Ream W, Loper JE. 1998. The two-component regulators GacS and GacA influence accumulation of the stationary-phase sigma factor sigmaS and the stress response in Pseudomonas fluorescens Pf-5. J. Bacteriol. 180:6635-11
131. 2 and is indispensable for stress defense in C3 plants. EMBO J. 16:4806-16
132. Wohlgemuth H, Mittelstrass K, Kschieschan S, Bender J, Weigel H-J, et al. 2002. Activation of an oxidative burst is a general feature of sensitive plants exposed to the air pollutant ozone. Plant Cell Environ. 25:717-26
133. Zhang X, Zhang L, Dong F, Gao J, Galbraith DW, Song C-P. 2001. Hydrogen peroxide is involved in abscisic acid-induced stomatal closure in Vicia faba. Plant Physiol. 126:1438-48
134. Zheng M, Aslund F, Storz G. 1998. Activation of the OxyR transcription factor by reversible disulflde bond formation. Science 279:1718-21