Ozone-induced oxidative stress: Mechanisms of action and reaction

Physiologia Plantarum

Volumn 100, Issue 2, 1997, Pages 264-273

  Pell, Eva J ^a   Schlagnhaufer, Carl D ^b   Arteca, Richard N ^b  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

^b NONE

Author keywords

Active oxygen species; Antioxidants; Ethylene; Oxidative stress; Ozone; Programmed cell death; Rubisco; Senescence

Indexed keywords

EID: 0030974273     PISSN: 00319317     EISSN: None     Source Type: Journal    
DOI: 10.1034/j.1399-3054.1997.1000207.x     Document Type: Article

References (94)

1. Adams, D. O. & Yang, S. F. 1979. Ethylene biosynthesis: Identification of 1-aminocyclopropane-1-carboxylic acid as an intermediate in the conversion of methionine to ethylene. - Proc. Natl. Acad. Sci. USA 76: 170-174.
2. Bae, G. Y., Nakajima, N., Ishizuka, K. & Kondo, N. 1996. The role of phytotoxicity of the evolution of ethylene upon induction of 1-aminocyclopropane-1-carboxylate synthase by ozone fumigation in tomato plants. - Plant Cell Physiol. 37: 129-134.
3. Bahl, A. & Kahl, G. 1995. Air pollutant stress changes the steady-state transcript levels of three photosynthesis genes. - Environ. Pollut. 88: 57-65.
4. Bleecker, A. B., Estelle, M. A., Somerville, C. & Kende, H. 1988. Insensitivity to ethylene conferred by a dominant mutation in Arabidopsis thaliana. - Science 241: 1086-1089.
5. Botella, J. R., Arteca, J. M., Schlagnhaufer, C. D., Arteca, R. N. & Phillips, A. T. 1992. Identification and characterization of a full length cDNA encoding an auxin-induced 1-aminocyclopropane-1-carboxylate synthase from etiolated mung bean hypocotyl segments and expression of its mRNA in response to indole-3-acetic acid. - Plant Mol. Biol. 20: 425-436.
6. _ , Schlagnhaufer, C. D., Arteca, J. M., Arteca, R. M. & Phillips, A. T. 1993. Identification of two new members of the 1-aminocyclopropane-1-carboxylate synthase-encoding multigene family in mung bean. - Gene 123: 249-253.
7. Brendley, B. W. 1996. Ozone-induced changes in the status of Rubisco in aging foliage of Populus and Quercus and the role of Rubisco in stress compensation. Ph. D. Thesis, The Pennsylvania State Univ., University Park, PA. DAI-B 57/04. p. 2400.
8. Byvoet, P., Balis, J. U., Shelley, S. A., Montgomery, M. R. & Barber, M. J. 1995. Detection of hydroxyl radicals upon interaction of ozone with aqueous media or extracellular surfactant: The role of trace iron. - Arch. Biochem. Biophys. 319: 464-469.
9. Casano, L. M., Martin, M. & Sabater, B. 1994. Sensitivity of superoxide dismutase transcript levels and activities of oxidative stress is lower in mature-senescent than in young barley leaves. - Plant Physiol. 106: 1033-1039.
10. 2+ transport in membrane vesicles from pinto bean leaves and its alteration after ozone exposure. - Plant Physiol. 94: 788-795.
11. Conklin, P. L. & Last, R. L. 1995. Differential accumulation of antioxidant mRNAs in Arabidopsis thaliana exposed to ozone. - Plant Physiol. 109: 203-212.
12. Dalling, M. J. 1987. Proteolytic enzymes and plant senescence. - In Plant Senescence: Its Biochemistry and Physiology (W. W. Thomson, E. A. Nothnagel and R. C. Huffaker, eds), pp. 54-70. The American Society of Plant Physiology, Rockville, MD. ISBN 0-943088-10-0.
13. Dann, M. S. & Pell, E. J. 1989. Decline of activity and quantity of ribulose bisphosphate carboxylase/oxygenase and net photosynthesis in ozone-treated foliage. - Plant Physiol. 91: 427-432.
14. Davies, K. M. & Grierson, D. 1989. Identification of cDNA clones for tomato (Lycopersicon esculentum Mill.) mRNAs that accumulate during ripening and leaf senescence. - Planta 179: 73-80.
15. +-stimulated ATPase of the plasmalemma of pinto bean leaves by ozone. - Plant Physiol. 77: 43-45.
16. 3-induced degradation of Rubisco protein and loss of Rubisco mRNA in relation to leaf age in potato. - New Phytol. 127: 741-748.
17. _ & Pell, E. J. 1995. Oxidative modification of Rubisco from potato foliage in response to ozone. - Plant Physiol. Biochem. 33: 273-282.
18. _ , Landry, L. G. & Pell, E. J. 1991. Ozone-induced changes in RuBPCase from potato and hybrid poplar. - In Active Oxygen/Oxidative Stress and Plant Metabolism (E. J. Pell and K. L. Steffen, eds), pp. 233-237. Current Topics in Plant Physiology: An American Society of Plant Physiologists Series, Vol. 6. Rockville, MD. ISBN 0-943088-22-4.
19. Elstner, E. F., Oswald, W. & Youngman, R. J. 1985. Basic mechanism of pigment bleaching and loss of structural resistance in spruce (Picea abies) needles: Advances in phytomedical diagnostics. - Experientia 41: 571-591.
20. Ernst, D., Schraudner, M., Langebartels, C. & Sandermann, H. 1992. Ozone-induced changes of mRNA levels of β-1,3-glucanase, chitinase and 'pathogenesis-related' protein 1b in tobacco plants. - Plant Mol. Biol. 20: 673-682.
21. _ , Bodemann, A., Schmelzer, E., Langebartels, C. & Sandermann, H. 1996. β-1,3-glucanase mRNA is locally, but not systemically induced in Nicotiana tabacum L. cv. BEL W3 after ozone fumigation. - J. Plant Physiol. 148: 215-221.
22. Eyal, Y., Meller, Y., Lev-Yadun, S. & Fluhr, R. 1993. A basic-type PR-1 promoter directs ethylene responsiveness, vascular and abscission zone-specific expression. - Plant J. 4: 225-234.
23. Galliano, H., Cabané, M., Eckerskorn, C., Lottspeich, F., Sandermann, H. Jr & Ernst, D. 1993. Molecular cloning, sequence analysis and elicitor-/ozone-induced accumulation of cinnamyl alcohol dehydrogenase from Norway spruce (Picea abies L.). - Plant Mol. Biol. 23: 145-156.
24. Glick, R. E., Schlagnhaufer, C. D., Arteca, R. N. & Pell, E. J. 1995. Ozone-induced ethylene emission accelerates the loss of ribulose-1,5-bisphosphate carboxylate/oxygenase and nuclear-encoded mRNAs in senescing potato leaves. - Plant Physiol. 109: 891-898.
25. Greenberg, J. T., Guo, A., Klessig, D. F. & Ausubel, F. M. 1994. Programmed cell death in plants: A pathogen-triggered response activated coordinately with multiple defense functions. - Cell 77: 551-563.
26. Gribć, V. & Bleecker, A. B. 1995. Ethylene regulates the timing of leaf senescence in Arabidopsis. - Plant J. 8: 595-602.
27. Grimes, H. D., Perkins, K. K. & Boss, W. F. 1983. Ozone degrades into hydroxyl radical under physiological conditions. A spin trapping study. - Plant Physiol. 72: 1016-1020.
28. Hahn, G. H., Bucheli, P., Cervone, F., Doares, S. H., O'Neill, R. A., Darvill, A. & Albersheim, P. 1989. Role of cell wall constituents in plant-pathogen interactions. - In Plant-Microbe Interactions, Vol. 3 (T. Kosuge and E. W. Nester, eds), pp. 131-181. McGraw Hill, New York, NY. ISBN 0-07-046281-X.
29. Hart, C. M., Nagy, F. & Meins, F. Jr. 1993. A 61 bp enhancer element of the tobacco β-1,3-glucanase B gene interacts with one or more regulated nuclear proteins. - Plant Mol. Biol. 21: 121-131.
30. Heath, R. L. 1987. The biochemistry of ozone attack on the plasma membrane of plant cells. - Adv. Phytochem. 21: 29-54.
31. Hensel, L., Grbić, V., Baumgarten, D. A. & Bleecker, A. B. 1993. Developmental and age-related processes that influence the longevity and senescence of photosynthetic tissues in Arabidopsis. - Plant Cell 5: 553-564.
32. Huang, P. L., Parks, J. E., Rottmann, W. H. & Theologis, A. 1991. Two genes encoding 1-aminocyclopropane-1-carboxylate synthase in zucchini (Cucurbita pepo) are clustered and similar but differentially regulated. - Proc. Natl. Acad. Sci. USA 88: 7021-7025.
33. Huffaker, R. C. 1990. Proteolytic activity during senescence of plants. Tansley Rev. No. 25. - New Phytol. 116: 199-213.
34. John, I., Drake, R., Farrell, A., Cooper, W., Lee, P., Horton, P. & Grierson, D. 1995. Delayed leaf senescence in ethylene-deficient ACC-oxidase antisense tomato plants: Molecular and physiological analysis. - Plant J. 7: 483-490.
35. Kampfenkel, K., Van Montagu, M. & Inzé, D. 1995. Effects of iron excess on Nicotiana plumbaginifolia plants. - Plant Physiol. 107: 725-735.
36. Kangasjärvi, J., Talvinen, J., Utrianien, M. & Karjalainen, R. 1994. Plant defense systems induced by ozone. - Plant Cell Environ. 17: 783-794.
37. Kende, H. 1993. Ethylene biosynthesis. - Annu. Rev. Plant Physiol. Plant Mol. Biol. 44: 283-307.
38. Laisk, A., Kull, O. & Moldau, H. 1989. Ozone concentration in leaf intercellular air spaces is close to zero. - Plant Physiol. 90: 1163-1167.
39. Lanahan, M. B., Yen, H. C., Giovannoni, J. J. & Klee, H. J. 1994. The never ripe mutation blocks ethylene perception in tomato. - Plant Cell 6: 521-530.
40. 3-stressed hybrid poplar. - Plant Physiol. 101: 1355-1362.
41. Langebartels, C., Kerner, K., Leonardi, S., Schraudner, M., Trost, M., Heller, W. & Sandermann, H. Jr. 1991. Biochemical plant response to ozone. I. Differential induction of polyamine and ethylene biosynthesis in tobacco. - Plant Physiol. 95: 882-889.
42. Liang, X., Abel, S., Keller, J. A., Shen, N. F. & Theologis, A. 1992. The 1-aminocyclopropane-1-carboxylate synthase gene family of Arabidopsis thaliana. - Proc. Natl. Acad. Sci. USA 89: 11046-11050.
43. Low, P. S. & Merida, J. R. 1996. The oxidative burst in plant defense: Function and signal transduction. - Physiol. Plant. 96: 533-542.
44. Maccarrone, M., Veldink, G. A. & Vliegenthart, J. F. G. 1992. Thermal injury and ozone stress affect soybean lipoxygenases expression. - FEBS Lett. 309: 225-230.
45. Mayak, S. & Adam, Z. 1984. Accelerated ethylene production by a microsomal membrane fraction from carnation petals in vitro. - Plant Sci. Lett. 33: 345-352.
46. Mehlhorn, H. & Wellburn, A. R. 1987. Stress ethylene formation determines plant sensitivity to ozone. - Nature 327: 417-418.
47. _ , Tabner, B. J. & Wellburn, A. R. 1990. Electron spin resonance evidence for the formation of free radicals in plants exposed to ozone. - Physiol. Plant. 79: 377-383
48. Mehta, R. A., Fawcett, T. W., Porath, D. & Mattoo, A. K. 1992. Oxidative stress causes rapid membrane translocation and in vivo degradation of ribulose-1,5-bisphosphate carboxylase/oxygenase. - J. Biol. Chem. 267: 2810-2816.
49. Mudd, J. B., Banerjee, S. K., Dooley, M. M. & Knight, K. L. 1984. Pollutants and plant cells: Effects on membranes. - In Gaseous Air Pollutants and Plant Metabolism (M. J. Koziol and F. R. Whatley, eds), pp. 105-116. Butterworths, London. ISBN 0-408-11152-6.
50. Nakagawa, N., Mori, H., Yamazaki, K. & Imaseki, H. 1991. Cloning of a complementary DNA for auxin-induced 1-aminocyclopropane-1-carboxylate synthase and differential expression of the gene by auxin and wounding. - Plant Cell Physiol. 32: 1153-1163.
51. Ohme-Takagi, M. & Shinshi, H. 1990. Structure and expression of a β-1,3-glucanase gene. - Plant Mol. Biol. 15: 941-946.
52. Olson, D. C., White, J. A., Edelman, L., Harkins, R. N. & Kende, H. 1991. Differential expression of two genes for 1-aminocyclopropane-1-carboxylate synthase in tomato fruits. - Proc. Natl. Acad. Sci. USA 88: 5340-5344.
53. Park, K. Y., Drory, A. & Woodson, W. R. 1992. Molecular cloning of an 1-aminocyclopropane-1-carboxylate synthase from senescing carnation flower petals. - Plant Mol. Biol. 18: 377-386.
54. Paulin, A., Droillard, M. & Bureau, J. M. 1986. Effect of a free radical scavenger 3,4,5-trichlorophenol, on ethylene production and on changes in lipids and membrane integrity during senescence of petals of cut carnations (Dianthus caryophyllus). - Physiol. Plant. 67: 465-471.
55. Pell, E. J. & Dann, M. S. 1991 Multiple stress-induced foliar senescence and implications for whole-plant longevity. - In Response of Plants to Multiple Stresses (H. A. Mooney, W. E. Winner and E. J. Pell, eds), pp. 189-204. Academic Press, San Diego, CA. ISBN 0-12-505355-X.
56. _ , Enyedi, A., Eckardt, N. & Landry, L. 1990. Ozone-induced alterations in quantity and activity of Rubisco: Implications for foliar senescence. - In Proceedings of the International Symposium on Biological Oxidation Systems (C. C. Reddy, G. A. Hamilton and K. M. Madyastha, eds), pp. 389-403. Academic Press, San Diego, CA. ISBN 0-12-584551-0.
57. _ , Eckardt, N. A. & Enyedi, A. J. 1992. Timing of ozone stress and resulting status of ribulose bisphosphate carboxylase/oxygenase and associated net photosynthesis. - New Phytol. 120: 397-405.
58. _ , Eckardt, N. A. & Glick, R. E. 1994. Biochemical and molecular basis for impairment of photosynthetic potential. - Photosynth. Res. 39: 453-462.
59. Picton, S., Barton, S., Bouzayen, M., Hamilton, A. & Grierson, D. 1993. Altered fruit ripening and leaf senescence in tomatoes expressing an antisense ethylene-forming enzyme transgene. - Plant J. 3: 469-481.
60. Price, A., Lucas, P. W. & Lea, P. J. 1990. Age dependent damage and glutathione metabolism in ozone fumigated barley: A leaf section approach. - J. Exp. Bot. 41: 1309-1317.
61. Pryor, W. A. & Church, D. F. 1991. Aldehydes, hydrogen peroxide, and organic radicals as mediators of ozone toxicity. - Free Radic. Biol. Med. 11: 41-46.
62. Ranieri, A., D'urso, G., Nali, C., Lorenzini, G. & Soldatini, G. F. 1996. Ozone stimulates apoplastic antioxidant systems in pumpkin leaves. - Physiol. Plant. 97: 381-387.
63. 3 on the oxygen free radical scavenging system in Arabidopsis thaliana genotypes differing in flavonoid biosynthesis. - Photochem. Photobiol. 62: 719-726.
64. _ , Paliyath, G. & Ormrod, D. P. 1995. Differential response of photosynthetic pigments, Rubisco activity and Rubisco protein of Arabidopsis thaliana exposed to UVB and ozone. - Photochem. Photobiol. 62: 727-735.
65. 3-stressed potato foliage. - Plant Cell Environ. 16: 819-826.
66. Richards, B. L., Middleton, J. T. & Hewitt, W. B. 1958. Air pollution with relation to agronomic crops. V. Oxidant stipple of grape. - Agron. J. 50: 559-561.
67. Rottmann, W. R., Peter, G. F., Oeller, P. W., Keller, J. A., Shen, N. F., Nagy, B. P., Taylor, L. P., Campbell, A. D. & Theologis, A. 1991. 1-aminocyclopropane-1-carboxylate synthase in tomato is encoded by a multigene family whose transcription is induced during fruit and floral senescence. - J. Mol. Biol. 222: 937-961.
68. Sakaki, T., Tanaka, K. & Yamada, M. 1994. General metabolic changes in leaf lipids in response to ozone. - Plant Cell Physiol. 35: 53-62.
69. Schlagnhaufer, C. D., Glick, R. E., Arteca, R. N. & Pell, E. J. 1995. Molecular cloning of an ozone-induced 1-aminocyclopropane-1-carboxylate synthase cDNA and its relationship with a loss of rbcS in potato (Solanum tuberosum L.) plants. - Plant Mol. Biol. 28: 93-103.
70. _ , Arteca, R. N. & Pell, E. J. 1996. Differential expression of ACC synthase genes in response to stress. - HortScience 31: 287.
71. Schneiderbauer, A., Back, E., Sandermann, H. Jr & Ernst, D. 1995. Ozone induction of extensin mRNA in Scots pine, Norway spruce and European beech. - New Phytol. 130: 225-230.
72. Schraudner, M., Ernst, D., Langebartels, C. & Sandermann, H. Jr. 1992. Biochemical plant responses to ozone. III. Activation of the defense-related proteins β-1,3-glucanase and chitinase in tobacco leaves. - Plant Physiol. 99: 1321-1328.
73. Sgherri, C. L. M. & Navari-Izzo, F. 1995. Sunflower seedlings subjected to increasing water deficit stress: Oxidative stress and defence mechanisms. - Physiol. Plant. 93: 25-30.
74. Sharma, Y. K. & Davis, K. R. 1994. Ozone-induced expression of stress-related genes in Arabidopsis thaliana. - Plant Physiol. 105: 1089-1096.
75. _ , León, J., Raskin, I. & Davis, K. R. 1996. Ozone-induced responses in Arabidopsis thaliana: The role of salicylic acid in the accumulation of defense-related transcripts and induced resistance. - Proc. Natl. Acad. Sci. USA 93: 5099-5104.
76. Slakeski, N. & Fincher, G. B. 1992. Developmental regulation of (1→3, 1→4)-β-glucanase gene expression in barley. - Plant Physiol. 99: 1226-1231.
77. Sohal, R. S. & Weindruch, R. 1996. Oxidative stress, caloric restriction, and aging. - Science 273: 59-63.
78. Spanu, P., Boller, T. & Kende, H. 1993. Differential accumulation of transcripts of 1-aminocyclopropane-1-carboxylate synthase genes in tomato plants infected with Phytophthora infestans and in elicitor-treated tomato cell suspensions. - J. Plant Physiol. 141: 557-562.
79. Stadtman, E. R. 1992. Protein oxidation and aging. - Science 257: 1220-1224.
80. 3 on foliar gas exchange in Glycine max L. Merr.: A potential role for exogenous stress ethylene. - New Phytol. 110: 301-307.
81. Thalmair, M., Bauw, G., Thiel, S., Döhring, T., Langebartels, C. & Sandermann, H. Jr. 1996. Ozone and ultraviolet B effects on the defense-related proteins β-1,3-glucanase and chitinase in tobacco. - J. Plant Physiol. 148: 222-228.
82. Ting, I. P. & Heath, R. L. 1975. Responses of plants to air pollutant oxidants. - Adv. Agron. 27: 89-121.
83. Tingey, D. T., Standley, C. & Field, R. W. 1976. Stress ethylene evolution: A measure of ozone effects on plants. - Atmos. Environ. 10: 964-974.
84. Tobin, E. M. & Silverthorne, J. 1985. Light regulation of gene expression. - Ann. Rev. Plant Physiol. 36: 569-593.
85. Van der Straeten, D., Rodrigues-Pousada, R. A., Villarroel, R., Hanley, S., Goodman, H. M. & Van Montagu, M. 1992. Cloning, genetic mapping and expression analysis of an Arabidopsis thaliana gene that encodes 1-aminocyclopropane-1-carboxylate synthase. - Proc. Natl. Acad. Sci. USA 89: 9969-9973.
86. _ , Djudzman, A., Van Caeneghem, W., Smalle, J. & Van Montagu, M. 1993. Genetic and physiological analysis of a new locus in Arabidopsis that confers resistance to 1-aminocyclopropane-1-carboxylic acid and ethylene and specifically affects the ethylene signal transduction pathway. - Plant Physiol. 102: 401-408.
87. Vierstra, R. D. 1987. Ubiquitin, a key component in the degradation of plant proteins. - Physiol. Plant. 70: 103-106.
88. Wang, T. & Arteca, R. N. 1995. Identification and characterization of cDNAs encoding ethylene biosynthetic enzymes from Pelargonium x hortorum cv. Snow Mass leaves. - Plant Physiol. 109: 627-636.
89. 9 fatty acids in autumnal lipids of Norway spruce [Picea abies (L.) Karst]. - New Phytol. 127: 355-361.
90. 3. - Physiol. Plant. 80: 286-293.
91. Yip, W. K., Moore, T. & Yang, S. F. 1992. Differential accumulation of transcripts for four tomato 1-aminocyclopropane-1-carboxylate synthase homologs under various conditions. - Proc. Natl. Acad. Sci. USA 89: 2475-2479.
92. Yu, Y.-B. & Yang, S. F. 1980. Biosynthesis of wound ethylene. - Plant Physiol. 66: 281-285.
93. Zacarias, L. & Reid, M. S. 1990. Role of growth regulators in the senescence of Arabidopsis thaliana leaves. - Physiol. Plant. 80: 549-554.
94. Zarembinski, T. I. & Theologis, A. 1993. Anaerobiosis and plant growth hormones induce two genes encoding 1-aminocyclopropane-1-carboxylate synthase in rice (Oryza sativa L.). - Mol. Biol. Cell 4: 363-373.