Antioxidants, oxidative damage and oxygen deprivation stress: A review

Annals of Botany

Volumn 91, Issue , 2003, Pages 179-194

  Blokhina, Olga ^a   Virolainen, Eija ^a   Fagerstedt, Kurt V ^a  

^a UNIVERSITY OF HELSINKI   (Finland)

Author keywords

Adaptation; Anoxia; Antioxidant; Hypoxia; Lipid peroxidation; Oxygen deprivation stress; Reactive oxygen species; Review

Indexed keywords

ANTIOXIDANT; ASCORBIC ACID; GLUTATHIONE; OXYGEN; REACTIVE OXYGEN METABOLITE; TOCOPHEROL;

ADAPTATION; ANOXIA; ANTIOXIDANT; HYPOXIA; ENVIRONMENTAL STRESS; PHYSIOLOGICAL RESPONSE;

ADAPTATION; METABOLISM; OXIDATION REDUCTION REACTION; PHYSIOLOGY; PLANT PHYSIOLOGY; REVIEW;

ADAPTATION, PHYSIOLOGICAL; ANTIOXIDANTS; ASCORBIC ACID; GLUTATHIONE; OXIDATION-REDUCTION; OXYGEN; PLANT PHYSIOLOGY; REACTIVE OXYGEN SPECIES; TOCOPHEROLS;

EID: 0037237973     PISSN: 03057364     EISSN: None     Source Type: Journal    
DOI: 10.1093/aob/mcf118     Document Type: Review

References (162)

1. Alin P, Jensson H, Guthenberg C, Danielson UH, Tahir MK, Mannervik B. 1985. Purification of major basic glutathione transferase isoenzymes from rat liver by use of affinity chromatography and fast protein liquid chromatofocusing. Analytical Biochemistry 146: 313-320.
2. Alscher RG. 1989. Biosynthesis and antioxidant function of glutathione in plants. Physiologia Plantarum 77: 457-464.
3. 2-induced cell death: possible involvement of peroxidases and of alternative oxidase. FEBS Letters 477: 175-180.
4. Arora A, Byrem TM, Nair MG, Strasburg GM. 2000. Modulation of liposomal membrane fluidity by flavonoids and isoflavonoids. Archives of Biochemistry and Biophysics 373: 102-109.
5. Arrigoni O, De Tullio MC. 2000. The role of ascorbic acid in cell metabolism: between gene-directed functions and unpredictable chemical reactions. Journal of Plant Physiology 157: 481-488.
6. Asada K. 1999. The 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. Avsian-Kretchmer O, Eshdat Y, Gueta-Dahan Y, Ben-Hayyim G. 1999. Regulation of stress-induced phospholipid hydroperoxide glutathione peroxidase expression in citrus. Planta 209: 469-477.
8. Azzi A, Stocker A. 2000. Vitamin E: non-antioxidant roles. Progress in Lipid Research 39: 231-255.
9. Bannister JV, Bannister WH, Rotilio G. 1987. Aspects of the structure, function and applications of superoxide dismutase. Critical Reviews in Biochemistry 22: 111-180
10. Bartoli CG, Pastori GM, Foyer CH. 2000. Ascorbate biosynthesis in mitochondria is linked to the electron transport chain between complexes III and IV. Plant Physiology 123: 335-343.
11. Berglund AH, Nilsson R, Liljenberg C. 1999. Permeability of large unilamellar digalactosyldiacylglycerol vesicles for protons and glucose - influence of a-tocopherol, �-carotene, zeaxanthin and cholesterol. Plant Physiology and Biochemistry 37: 179-186.
12. Biemelt S, Keetman U Albrecht G. 1998. Re-aeration following hypoxia or anoxia leads to activation of the antioxidative defense system in roots of wheat seedlings. Plant Physiology 116: 651-658.
13. Biemelt S, Keetman U, Mock H-P, Grimm B. 2000. Expression and activity of isoenzymes of superoxide dismutase in wheat roots in response to hypoxia and anoxia. Plant Cell and Environment 23: 135-144.
14. Blokhina OB, Fagerstedt KV, Chirkova TV. 1999. Relationships between lipid peroxidation and anoxia tolerance in a range of species during post-anoxic reaeration. Physiologia Plantarum 105: 625-632.
15. Blokhina OB, Virolainen E, Fagerstedt KV, Hoikkala A, Wa�ha�la� K, Chirkova TV. 2000. Antioxidant status of anoxia-tolerant and -intolerant plant species under anoxia and reaeration. Physiologia Plantarum 109: 396-403.
16. Blokhina OB, Chirkova TV, Fagerstedt KV. 2001. Anoxic stress leads to hydrogen peroxide formation in plant cells. Journal of Experimental Botany 52: 1-12.
17. Bolwell GP, Wojtaszek P. 1997. Mechanisms for generation of reactive oxygen species in plant defence - a broad perspective. Physiological and Molecular Plant Pathology 51: 347-366.
18. Boo YC, Jung J. 1999. Water deficit-induced oxidative stress and antioxidafive defenses in rice plants. Journal of Plant Physiology 155: 255-261.
19. Bourbouloux A, Shahi P, Chakladar A, Delrot S, Bachhawat AH. 2000. Hgt1p, a high affinity glutathione transporter from the yeast Saccharomyces cerevisiae. Journal of Biological Chemistry 275: 13259-13265.
20. Bowler C, Van Montagu M, Inze D. 1992. Superoxide dismutase and stress tolerance. Annual Review of Plant Physiology and Plant Molecular Biology 43: 83-116.
21. Braidot E, Petrussa E, Vianello A, Macri F. 1999. Hydrogen peroxide generation by higher plant mitochondria oxidizing complex I of complex II substrates. FEBS Letters 451: 347-350.
22. Buettner GR. 1993. The pecking order of free radicals and antioxidants: lipid peroxidation, a-tocopherol, and ascorbate. Archives of Biochemistry and Biophysics 300: 535-543.
23. Chakraborti T, Das S, Mondal M, Roychoudhury S, Chakraborti S. 1999. Oxidant, mitochondria and calcium: an overview. Cellular Signalling 11: 77-85.
24. Chang WWP, Huang L, Shen M, Webster C, Burlingame AL, Roberts JKM. 2000. Patterns of protein synthesis and tolerance of anoxia in root tips of maize seedlings acclimated to a low-oxygen environment, and identification of proteins by mass spectrometry. Plant Physiology 122: 295-317.
25. Cheng Z, Putt DA, Lash LH. 2000. Enrichment and functional reconstitution of glutathione transport activity from rabbit kidney mitochondria: further evidence for the role of dicarboxylate and 2-oxoglutarate carriers in mitochondrial glutathione transport. Archives of Biochemistry and Biophysics 373: 193-202.
26. Chirkova TV. 1988. Plant adaptation to hypoxia and anoxia. Leningrad: Leningrad State University Press.
27. Chirkova TV, Voltzekovskaya SA. 1999. Plant protein synthesis under hypoxia and anoxia. Uspekhi Sovremennoi Biologii 119: 178-189.
28. Chirkova TV, Zhukova TM. Tretiakov AL. 1984. Adenine nucleotides in wheat and rice seedlings under aeration and anoxia. Vestnik LGU 15: 74-81 (in Russian).
29. Chirkova TV, Sinyutina NF, Blyudzin YA, Barsky IE, Smetannikova SV. 1989. Phospholipid fatty acids of root mitochondria and microsomes from rice and wheat seedlings exposed to aeration or anaerobiosis. Russian Journal of Plant Physiology 36: 126-134.
30. Chirkova TV, Zhukova TM, Goncharova NN. 1991a. Method of determination of plant resistance to oxygen shortage. Russian Journal of Plant Physiology 38: 359-364.
31. Chirkova TV, Zhukova TM, Goncharova NN. 1991b. Specificity of membrane permeability in wheat and rice seedlings under anoxia. Fiziologia i Biokhimia Kulturnux Rastenii 23: 541-546 (in Russian).
32. Chirkova TV, Zhukova TM, Bugrova MP. 1992. Redox reactions of plant cells in response to short-term anaerobiosis. Vestnik SPBGU 3: 82-86 (in Russian).
33. Chirkova TV, Novitskaya LO, Blokhina OB. 1998. Lipid peroxidation and antioxidant systems under anoxia in plants differing in their tolerance to oxygen deficiency. Russian Journal of Plant Physiology 45: 55-62.
34. Conklin PL. 2001. Recent advances in the role and biosynthesis of ascorbic acid in plants. Plant Cell and Environment 24: 383-394.
35. 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.
36. Crawford RMM, Braendle R. 1996. Oxygen deprivation stress in a changing environment. Journal of Experimental Botany 47: 145-159.
37. Crawford RMM, Walton JC, Wollenweber-Ratzer B. 1994. Similarities between post-ischaemic injury to animal tissues and post anoxic injury in plants. Proceedings of the Royal Society of Edinburgh 102B, 325-332.
38. Cummings BS, Angeles R, McCauley RB, Lash LH. 2000. Role of voltage-dependent channels in glutathione transport into yeast mitochondria. Biochemical and Biophysical Research Communications 276: 990-944.
39. Davey MW, Gilot C, Persiau G, �stergaard J, Hart Y, Bauw GC, Van Montagu M. 1999. Ascorbate biosynthesis in Arabidopsis cell suspension culture. Plant Physiology 121: 535-543.
40. Dean JV, Devarenne TP. 1997. Peroxidase-mediated conjugation of glutathione to unsaturated phenylpropanoids - evidence against glutathione S-transferase involvement. Physiologia Plantarum 99: 271-278.
41. DeLong JM, Steffen KL. 1998. Lipid peroxidation and a-tocopherol content in a-tocopherol-supplemented thylakoid membranes during UV-B exposure. Environmental and Experimental Botany 39: 177-185.
42. De Tullio MC, Paciolla C, Dalla Vecchia F, Rascio N, D'Emerico S, De Gara L, Liso R, Arrigoni O. 1999. Changes in onion root development induced by the inhibition of peptidyl-prolyl hydroxylase and influence of the ascorbate system on cell division and elongation. Planta 209: 424-434.
43. Dixon DP, Cummins I, Cole DJ, Edwards R. 1998. Glutathione-mediated detoxification systems in plants. Current Opinion in Plant Biology 1: 258-266.
44. Drew MC. 1997. Oxygen deficiency and root metabolism: injury and acclimation under hypoxia and anoxia. Annual Review of Plant Physiology and Plant Molecular Biology 48: 223-250.
45. Ellis MH, Setter TL. 1999. Hypoxia induces anoxia tolerance in completely submerged rice seedlings. Journal of Plant Physiology 154: 219-230.
46. Ellis MH, Dennis ES, Peacock WL. 1999. Arabidopsis roots and shoots have different mechanisms for hypoxic stress tolerance. Plant Physiology 119: 57-64.
47. Elstner EF. 1987. Metabolism of activated oxygen species. In: Davies DD, ed. Biochemistry of plants. Vol. 11. London: Academic Press, 253-315.
48. Elstner EF, Osswald W. 1994. Mechanisms of oxygen activation during plant stress. Proceedings of the Royal Society of Edinburgh 102B: 131-154.
49. Foyer CH, Halliwell B. 1976. The presence of glutathione and glutathione reductase in chloroplasts: a proposed role in ascorbic acid metabolism. Planta 133: 21-25.
50. Foyer CH, Lelandais MA. 1996. A comparison of the relative rates of transport of ascorbate and glucose across the thylakoid, chloroplast and plasmalemma membranes of pea leaves mesophyll cells. Journal of Plant Physiology 148: 391-398.
51. Foyer CH, Lelandais M, Edwards EA, Mullineaux PM. 1991. The role of ascorbate in plants, interactions with photosynthesis, and regulatory significance, In: Pell E, Steffen K, eds. Active Oxygen/Oxidative Stress and Plant Metabolism: Proceedings of the 6th Annual Penn State Symposium in Plant Physiology, 23-25 May 1991. Rockville, MD: American Society of Plant Physiologists, 131-144.
52. Frenkel C. 1991. Disruption of macromolecular hydration - a possible origin of chilling destabilisation of biopolymers. Trends in Food Science and Technology 2: 39-41.
53. Fryer MJ. 1992. The antioxidant effects of thylakoid vitamin E (atocopherol). Plant Cell and Environment 15: 381-392.
54. Garci�a-Plazaola JI, Becerril JM. 2000. Effects of drought on photoprotective mechanisms in European beech (Fagus sylvatica L.) seedlings from different provenances. Trees 14: 485-490.
55. Gardner HW, Eskins K, Grams GW, Inglett GE. 1972. Radical addition of linoleic hydroperoxides to a-tocopherol or the analogous hydroxychroman. Lipids 7: 324-334.
56. Generosova IP, Krasavina MS, Polyakova LI., Burmistrova NA, Lyubomilova MV, Vartapetian BB. 1998. On some molecular aspects of adaptation of Oryza sativa seedlings to anoxia. Russian Journal of Plant Physiology 45: 227-233.
57. 1 redox couple regulates mitochondrial oxygen radical formation. Archives of Biochemistry and Biophysics 388: 34-38.
58. Gout E, Boisson AM, Aubert S, Douce R, Bligny R. 2001. Origin of the cytoplasmic pH changes during anaerobic stress in higher plant cells. Carbon-13 and phosphorus-31 nuclear magnetic resonance studies. Plant Physiology 125: 912-925.
59. Grace S, Logan BA. 2000. Energy dissipation and radical scavenging by the plant phenylpropanoid pathway. Philosophical Transactions of the Royal Society of London B 355: 1499-1510.
60. Hanhija�rvi AM, Fagerstedt KV. 1994. Comparison of the effect of natural and experimental anoxia on carbohydrate and energy metabolism in Iris pseudacorus rhizomes. Physiologia Plantarum 90: 437-444.
61. Hanhija�rvi AM, Fagerstedt KV. 1995. Comparison of carbohydrate utilization and energy charge in the yellow flag iris (Iris pseudacorus) and garden iris (Iris germanica) under anoxia. Physiologia Plantarum 93: 493-497.
62. Henzi T, Braendle R. 1993. Long term survival of rhizomatous species under oxygen deprivation. In: Jackson MB, Black CR, eds. Interacting stresses on plants in a changing climate, NATO ASI Series, Vol. I 16. Berlin, Heidelberg: Springer-Verlag, 305-314.
63. Hetherington AM, Hunter MI, Crawford RMM. 1982. Contrasting effects of anoxia on rhizome lipids of Iris species. Phytochemistry 21: 1275-1278.
64. Horemans N, Asard H, Van Gestelen P, Caubergs RJ. 1998a. Facilitated diffusion drives transport of oxidised ascorbate molecules into purified plasma membrane vesicles of Phaseolus vulgaris. Physiologia Plantarum 104: 783-789.
65. Horemans N, Potters G, Caubergs RJ, Asard H. 1998b. Transport of ascorbate into protoplasts of Nicotiana tabacum Bright Yellow-2 cell line. Protoplasma 205: 114-121.
66. Horemans N, Foyer CH, Asard H. 2000a. Transport and action of ascorbate at the plant plasma membrane. Trends in Plant Sciences 5: 263-267.
67. Horemans N, Foyer CH, Potters G, Asard H. 2000b. Ascorbate function and associated transport systems in plants. Plant Physiology and Biochemistry 38: 531-540.
68. Hunter MIS, Hetherington AM, Crawford RMM. 1983. Lipid peroxidation - a factor in anoxia intolerance in Iris species? Phytochemistry 22: 1145-1147.
69. Janiszowska W, Korczak G. 1980. The intracellular distribution of tocopherols in Calendula officinalis leaves. Phytochemistry 19: 1391-1392.
70. Janiszowska W, Pennock JF. 1976. The biochemistry of vitamin E in plants. Vitamins and Hormones 34: 77-105.
71. Jimenez A, Hernandez JA, Pastori G, del Rio LA, Sevilla F. 1998. Role of the ascorbate-glutathione cycle of mitochondria and peroxisomes in the senescence of pea leaves. Plant Physiology 118: 1327-1335.
72. Kagan VE. 1989. Tocopherol stabilizes membrane against phospholipase A, free fatty acids, and lysophospholipids. In: Diplock AT, Machlin J, Packer L, Pryor WA, eds. Vitamin E: biochemistry and health implications. Vol. 570. New York, NY: Annals of the New York Academy of Sciences, 121-135.
73. Kagan VE, Fabisiak JP, Quinn PJ. 2000. Coenzyme Q and vitamin E need each other as antioxidants. Protoplasma 214: 11-18.
74. Kaiser S, Di Mascio P, Murphy ME, Sies H. 1990. Physical and chemical scavenging of singlet molecular oxygen by tocopherols. Archives of Biochemistry and Biophysics 277: 101-108.
75. Kalashnikov JuE, Balakhnina TI, Zakrzhevsky DA. 1994. Effect of soil hypoxia on activation of oxygen and the system of protection from oxidative destruction in roots and leaves of Hordeum vulgare. Russian Journal of Plant Physiology 41: 583-588.
76. Kamal-Eldin A, Appelqvist L-A�. 1996. The chemistry and antioxidant properties of tocopherols and tocotrienols. Lipids 31: 671-701.
77. Kanofsky JR, Axelrod B. 1986. Singlet oxygen production by soybean lipoxygenase isozymes. Journal of Biological Chemistry 261: 1099-1104.
78. Kato-Noguchi H. 2000. Abscisic acid and hypoxic induction of anoxia tolerance in roots of lettuce seedlings. Journal of Experimental Botany 51: 1939-1944.
79. Kim FJ, Kim HP, Hah YC, Roe JH. 1996. Differential expression of superoxide dismutases containing Ni and Fe/Zn in Streptomyces coelicolor. European Journal of Biochemistry 241: 178-185.
80. Kruk J, Jemiola-Rzeminska M, Strzalka K. 1997. Plastoquinol and a-tocopherol quinol are more active than ubiquinol and a-tocopherol in inhibition of lipid peroxidation. Chemistry and Physics of Lipids 87: 73-80.
81. Kruk J, Schmid GH, Strzalka K. 2000. Interaction of a-tocopherol quinone, a-tocopherol and other prenyllipids with photosystem. II. Plant Physiology and Biochemistry 38: 271-277.
82. Lal SK, Lee C, Sachs MM. 1998. Differential regulation of enolase during anaerobiosis in maize. Plant Physiology 118: 1285-1293.
83. Lamb C, Dixon RA. 1997. The oxidative burst in plant disease resistance. Annual Review of Plant Physiology and Plant Molecular Biology 48: 251-275.
84. Lander HM. 1997. An essential role for free radicals and derived species in signal transduction. FASEB Journal 11: 118-124.
85. Larson RA. 1988. The antioxidants of higher plants. Phytochemistry 27: 969-978.
86. Lee TM, Lin YN. 1995. Changes in soluble and cell wall-bound peroxidase activities with growth in anoxia-treated rice (Oryza sativa L.) coleoptiles and roots. Plant Science 106: 1-7.
87. Leipner J, Fracheboud Y, Stamp P. 1999. Effect of growing season on the photosynthetic apparatus and leaf antioxidative defenses in two maize genotypes of different chilling tolerance. Environmental and Experimental Botany 42: 129-139.
88. Leipner J, Stamp P, Fracheboud Y. 2000. Artificially increased ascorbate content affects zeaxanthin formation but not thermal energy dissipation or degradation of antioxidants during cold-induced photooxidative stress in maize leaves. Planta 210: 964-969.
89. Liso R, Innocenti AM, Bitonti MB, Arrigoni O. 1988. Ascorbic acid-induced progression of quiescent centre cells from G1 to S phase. New Phytologist 110: 469-471.
90. Loewus FA. 1980. L-ascorbic acid: metabolism, biosynthesis, function. In: Preiss J, ed. Carbohydrates, structure and function. The biochemistry of plants. Vol. 3. New York: Academic Press, 77-79.
91. Loewus MW, Bedgar DR, Saito K, Loewus FA. 1990. Conversion of L-sorbosone to L-ascorbic acid by a NADP-dependent dehydrogenase in bean and spinach leaf. Plant Physiology 94: 1492-1495.
92. Lynch DV, Thompson JE. 1984. Lipoxygenase-mediated production of superoxide anion in senescing plant tissue. FEBS Letters 173: 251-254.
93. Marrs KA. 1996. The functions and regulation of glutathione S-transferases in plants. Annual Review of Plant Physiology and Plant Molecular Biology 47: 127-158.
94. May MJ, Vernoux T, Leaver C, Van Montagu M, Inze D. 1998. Glutathione homeostasis in plants: implications for environmental sensing and plant development. Journal of Experimental Botany 49: 649-667.
95. Mehlhorn H, Lelandais M, Korth HG, Foyer CH. 1996. Ascorbate is the natural substrate for plant peroxidases? FEBS Letters 378: 203-206.
96. Merzlyak MN. 1989. Activated oxygen and oxidative processes in plant cell membranes. Itogi Nauki Tekhhiki Ser. Plant Physiology 6: 1-167.
97. Moldau H, Bichele I, Huve K. 1998. Dark-induced ascorbate deficiency in leaf cell walls increases plasmalemma injury under ozone. Planta 207: 60-66.
98. Mo�ller 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: 561-91.
99. Monk LS, Fagerstedt KV, Crawford RMM. 1987. Superoxide dismutase as an anaerobic polypeptide - a key factor in recovery from oxygen deprivation in Iris pseudacorus? Plant Physiology 85: 1016-1020.
100. Monk LS, Fagerstedt KV, Crawford RMM. 1989. Oxygen toxicity and superoxide dismutase as an antioxidant in physiological stress. Physiologia Plantarum 76: 456-459.
101. Munne�-Bosch S, Alegre L. 2000a. Changes in carotenoids, tocopherols and diterpenes during drought and recovery, and the biological significance of chlorophyll loss in Rosmarinus officinalis plants. Planta 210: 925-931.
102. Munne�-Bosch S, Alegre L. 2000b. The significance of �-carotene, a-tocopherol and the xanthophyll cycle in droughted Melissa officinalis plants. Australian Journal of Plant Physiology 27: 139-146.
103. Munne�-Bosch S, Alegre L. 2001. Subcellular compartmentation of the diterpene carnosic acid and its derivatives in the leaves of rosemary. Plant Physiology 125: 1094-1102.
104. Munne�-Bosch S, Schwarz K, Alegre L. 1999. Enhanced formation of a-tocopherol and highly oxidized abietane diterpenes in water-stressed rosemary plants. Plant Physiology 121: 1047-1052.
105. Noctor G, Foyer CH. 1998. Ascorbate and glutathione: keeping active oxygen under control. Annual Review of Plant Physiology and Plant Molecular Biology 49: 249-279.
106. Noctor G, Arisi ACM, Jouanin L, Foyer CH. 1998a. Manipulation of glutathione and amino acid biosynthesis in the chloroplast. Plant Physiology 118: 471-482.
107. Noctor G, Arisi ACM, Jouanin L, Kunert KJ, Rennenberg H, Foyer CH. 1998b. Glutathione: biosynthesis, metabolism and relationship to stress tolerance explored in transformed plants. Journal of Experimental Botany 49: 623-647.
108. Ostergaard J, Persiau G, Davey MW, Bauw G, Van Montagu M. 1997. Isolation of a cDNA coding for L-galactono-gamma-lactone dehydrogenase, an enzyme involved in the biosynthesis of ascorbic acid in plants. Purification, characterization, cDNA cloning, and expression in yeast. Journal of Biological Chemistry 272: 30009-30016.
109. Packer L, Weber SU, Rimhach G. 2001. Molecular aspects of a-tocotrienol antioxidant action and cell signalling. Journal of Nutrition 131: 369S-373S.
110. Pavelic D, Arpagaus S, Rawyler A, Braendle R. 2000. Impact of post-anoxia stress on membrane lipids of anoxia pretreated potato cells. A re-appraisal. Plant Physiology 124: 1285-1292.
111. Pfister-Sieber M, Braendle R. 1994. Aspects of plant behavior under anoxia and post-anoxia. Proceedings of the Royal Society of Edinburgh 102B: 313-324.
112. Price AH, Hendry GAF. 1989. Stress and the role of activated oxygen scavengers and protective enzymes in plants subjected to drought. Biochemical Society Transactions 17: 493-494.
113. Ratcliffe RG. 1995. Metabolic aspects of the anoxic response in plant tissue. In: Smirnoff N, ed. Environment and plant metabolism: flexibility and acclimation. Oxford: BIOS Scientific Publishers, 111-127.
114. Rawyler A, Pavelic D, Gianiazzi C, Oberson J, Braendle R. 1999. Membrane lipid integrity relies on a threshold of ATP production rate in potato cell cultures submitted to anoxia. Plant Physiology 120: 293-300.
115. Rea PA. 1999. MRP subfamily ABC transporters from plants and yeast. Journal of Experimental Botany 50: 895-913.
116. Recknagel RO, Glende EA, Jr. 1984. Spectrophotometric detection of lipid conjugated dienes. Methods in Enzymology 105: 331-337.
117. Reggiani R, Bertani A. 1989. Effect of decreasing oxygen concentration on polyamine metabolism in rice and wheat shoots. Journal of Plant Physiology 135: 375-377.
118. Rice-Evans CA, Miller NJ, Paganga G. 1997. Antioxidant properties of phenolic compounds. Trends in Plant Sciences 2: 152-159.
119. Richard B, Couce I, Raymond P, Saglio PH, Saint-Ges V, Pradet A. 1994. Plant metabolism under hypoxia and anoxia. Plant Physiology and Biochemistry 32: 1-10.
120. Rickauer M, Brodschelm W, Bottin A, Veronesi C, Grimal H, Esquerretugaye MT. 1997. The jasmonate pathway is involved differentially in the regulation of different defense responses in tobacco cells. Planta 202: 155-162.
121. Rosahl S. 1996. Lipoxygenases in plants - their role in development and stress response. Zeitschrift fur Naturforschung 51c: 123-138.
122. Russel DA, Sachs MM. 1991. The maize cytosolic glyceraldehyde-3-phosphate dehydrogenase gene family: organ specific expression and genetic analysis. Molecular and General Genetics 229: 219-228.
123. Sairam RK, Deshmukh PS, Saxena DC. 1998. Role of antioxidant systems in wheat genotype tolerance to water stress. Biologia Plantarum 41: 387-394.
124. Sanchez-Fernandez R, Fricker M, Corben LB, White NS, Sheard N, Leaver CJ, Van Montagu M, Inze D, May MJ. 1997. Cell proliferation and hair tip growth in the Arabidopsis root are under mechanistically different forms of redox control. Proceedings of the National Academy of Sciences of the USA 94: 2745-50.
125. Scebba F, Sebastiani L, Vitagliano C. 1998. Changes in activity of antioxidative enzymes in wheat (Triticum aestivum) seedlings under cold acclimation. Physiologia Plantarum 104: 747-752.
126. Schultz G, Heintze A, Hoppe P, Hagelstein P, Go�rlach J, Meereis K, Schwanke U, Preiss M. 1991. Tocopherol and carotenoid synthesis in chloroplasts: tight linkage to plastidic carbon metabolism in developing chloroplasts. In: Pell E, Steffen K, eds. Active Oxygen/Oxidative Stress and Plant Metabolism: Proceedings of the 6th Annual Penn State Symposium in Plant Physiology 23-25 May 1991. Rockville, MD: American Society of Plant Physiologists, 156-170.
127. Semenza GL. 1999. Perspectives on oxygen sensing. Cell 98: 281-284.
128. Serbinova EA, Packer L. 1994. Antioxidant properties of a-tocopherol and a-tocotrienol. Methods in Enzymology 234: 354-366.
129. Shewfelt RL, Purvis AC. 1995. Toward a comprehensive model for lipid peroxidation in plant tissue disorders. HortScience 30: 213-218.
130. Skoneczny M, Rytka J. 2000. Oxygen and haem regulate the synthesis of peroxisomal proteins: catalase A, acyl-CoA oxidase and Pex 1p in the yeast Saccharomyces cerevisiae; the regulation of these proteins by oxygen is not mediated by haem. Biochemical Journal 350: 313-319.
131. Skulachev VP. 1997. Membrane-linked systems preventing superoxide formation. Bioscience Reports 17: 347-366.
132. Skulachev VP. 1998. Cytochrome c in the apoptotic and antioxidant cascades. FEBS Letters 423: 275-280.
133. Smirnoff N. 1995. Antioxidant systems and plant response to the environment. In: Smirnoff N, ed. Environment and plant metabolism: flexibility and acclimation. Oxford: BIOS Scientific Publishers, 217-243.
134. Smirnoff N. 1996. The function and metabolism of ascorbic acid in plants. Annals of Botany 78: 661-669.
135. Smirnoff N. 2000. Ascorbic acid: metabolism and functions of a multi-facetted molecule. Current Opinion in Plant Biology 3: 229-235.
136. Smirnoff N, Conklin PL, Loewus FA. 2001. Biosynthesis of ascorbic acid in plants: a renaissance. Annual Review of Plant Physiology and Plant Molecular Biology 52: 437-467.
137. Sugimoto M, Furui S, Suzuki Y. 1997. Molecular cloning and characterisation of a cDNA encoding putative phospholipid hydroperoxide glutathione peroxidase from spinach. Bioscience, Biotechnology and Biochemistry 61: 1379-1381.
138. Tadege M, Dupuis I, Kuhlemeier C. 1999. Ethanolic fermentation: new functions for an old pathway. Trends in Plant Sciences 4: 320-325.
139. Takahama U, Oniki T. 1997. A peroxide/phenolics/ascorbate system can scavenge hydrogen peroxide in plant cells. Physiologia Plantarum 101: 845-852.
140. Tarchevskii IA. 1992. Regulatory role of degradation of biopolymers and lipids. Fiziologiya Rastenii 39: 1215-1223.
141. Thomas CE, McLean LR, Parker RA, Ohlweiler DF. 1992. Ascorbate and phenolic antioxidant interactions in prevention of liposomal oxidation. Lipids 27: 543-550.
142. Thomas SM, Gebi�cki JM, Dean RT. 1989. Radical initiated a-tocopherol depletion and lipid peroxidation in mitochondrial membranes. Biochimica et Biophysica Acta 1002: 189-197.
143. Threlfall DR, Whistance GR. 1977. Dehydrophylloquinone, a-hydrotocopherolquinone and dehydrotocopherols from etiolated maize and barley shoots. Phytochemistry 16: 1903-1907.
144. Tommasini R, Martinoia E, Grill E, Dietz KJ, Amrhein N. 1993. Transport of oxidized glutathione into barley vacuoles: evidence for the involvement of the glutathione-S-conjugate ATPase. Zeitschrift fu�r Naturforschung. C. 48c: 867-871.
145. Upston JM, Terentis AC, Stocker R. 1999. Tocopherol-mediated peroxidation of lipoproteins: implications for vitamin E as a potential antiatherogenic supplement. FASEB Journal 13: 977-994.
146. Ushimaru T, Shibazaka M, Tsuji H. 1994. Resistance to oxidative injury in submerged rice seedlings after exposure to air. Plant Cell Physiology 35: 211-218.
147. Ushimaru T, Maki Y, Sano S, Koshiba K, Asada K, Tsuji H. 1997. Induction of enzymes involved in the ascorbate-dependent antioxidative system, namely ascorbate peroxidase, monodehydroascorbate reductase and dehydroascorbate reductase, after exposure to air of rice (Oryza sativa) seedlings germinated under water. Plant and Cell Physiology 38: 541-549.
148. Ushimaru T, Kanematsu S, Shibasaka M, Tsuji H. 1999. Effect of hypoxia on the antioxidative enzymes in aerobically grown rice (Oryza sativa) seedlings. Physiologia Plantarum 107: 181-187.
149. Ushimaru T, Kanematsu S, Katayama M, Tsuji H. 2001. Antioxidative enzymes in seedlings of Nelumbo nucifera germinated under water. Physiologia Plantarum 112: 39-46.
150. Van Toai TT, Bolles CS. 1991. Postanoxic injury in soybean (Glycine max) seedlings. Plant Physiology 97: 588-592.
151. Vartapetian BB, Jackson MB. 1997. Plant adaptations to anaerobic stress. Annals of Botany 79 (Suppl. A): 3-20.
152. 2 supply prior to anoxia on tolerance to anoxia, alcoholic fermentation, and sugar levels. Journal of Experimental Botany 42: 1437-1447.
153. Wheeler GL, Jones MA, Smirnoff N. 1998. The biosynthetic pathway of vitamin C in higher plants. Nature 393: 365-369.
154. Willekens H, Inze D, Van Montagu M, Van Camp W. 1995. Catalase in plants. Molecular Breeding 1: 207-228.
155. Wingate VPM, Lawton MA, Lamb CJ. 1988. Glutathione causes a massive and selective induction of plant defence genes. Plant Physiology 87: 206-210.
156. Wollenweher-Ratzer B, Crawford RMM. 1994. Enzymatic defence against post-anoxic injury in higher plants. Proceedings of the Royal Society of Edinburgh 102B: 381-390.
157. Xia JH, Roberts JKM. 1994. Improved cytoplasmic pH regulation, increased lactate efflux, and reduced cytoplasmic lactate levels are biochemical traits expressed in root tips of whole maize seedlings acclimated to low oxygen environment. Plant Physiology 105: 651-657
158. Yabuta Y, Yoshimura K, Takeda T, Shigeoka S. 2000. Molecular characterization of tobacco mitochondrial L-galactono-gammalactone dehydrogenase and its expression in Escherichia coli. Plant and Cell Physiology 41: 666-675.
159. 2-peroxidase system. FEBS Letters 422: 377-380.
160. Yan B. Dai Q, Liu X, Huang S, Wang Z. 1996. Flooding-induced membrane damage, lipid oxidation and activated oxygen generation in corn leaves. Plant and Soil 179: 261-268.
161. Yu Q, Rengel Z. 1999a. Drought and salinity differentially influence activities of superoxide dismutase in narrow-leafed lupins. Plant Science 142: 1-11.
162. Yu Q, Rengel Z. 1999b. Waterlogging influences plant growth and activities of superoxide dismutases in narrow-leafed lupin and transgenic tobacco plants. Journal of Plant Physiology 155: 431-438.