Abstract
To evaluate the feasibility of using engineered antioxidant enzymes as an approach to improve the tolerance of plants to ambient stress, we have constructed transgenlc tobacco plants that overproduce superoxide dismutase (SOD), an enzyme which converts superoxide radicals into hydrogen peroxide and oxygen, and is believed to play a crucial role in antioxidant defense. We have targeted the MnSOD from Nicotiana plumbaginifolia either to the chloroplasts or to the mitochondria, and evaluated the ozone tolerance of transgenic and control plants. Enhanced SOD activity in the mitochondria had only a minor effect on ozone tolerance. However, overproduction of SOD in the chloroplasts resulted in a 3–4 fold reduction of visible ozone injury.
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Tarczynski, M.C., Jensen, R.G. and Bohnert, H.J. 1993. Stress protection of transgenic tobacco by production of the osmolyte mannitol. Science 259: 508–510.
Murata, N., Ishizaki-Nishizawa, O., Higashi, S., Hayashi, H., Tasaka, Y. and Nishida, I. 1992. Genetically engineered alteration in the chilling sensitivity of plants. Nature 356: 710–713.
Bowler, C., Van Montagu, M. and Inzé, D. 1992. Superoxide dismutase and stress tolerance. Ann. Rev. Plant Physiol. Plant Mol. Biol. 43: 83–116.
Bowler, C., Van Camp, W., Van Montagu, M. and Inzé, D. 1994. Superoxide dismutase in plants. CRC Crit. Rev. Plant Sci. In press.
Asada, K. and Takahashi, M. 1987. Production and scavenging of active oxygen in photosynthesis, p. 227–287. In: Photoinhibition. Kyle, D.J., Osmond, C.B. and Arntzen, C.J. (Eds.). Elsevier Science Publishers B.V., Amsterdam, The Netherlands.
Halliwell, B. and Gutteridge, J.M.C., 1989. Free Radicals in Biology and Medicine. Clarendon Press, Oxford, U.K.
Van Camp, W., Van Montagu, M. and Inzé, D. 1993. Superoxide dismutases, in press In: Causes of Photooxidative Stress and Amelioration of Defense Systems in Plants. Foyer, C.H. and Mullineaux, P.M. (Eds.). CRC Press, Boca Raton, FL.
Sen Gupta, A., Heinen, J.L., Holaday, A.S., Burke, J.J. and Alien, R.D. 1993. Increased resistance to oxidative stress in transgenic plants that overexpress chloroplastic Cu/Zn superoxide dismutase. Proc. Natl. Acad. Sci. USA 90: 1629–1633.
Guderian, R. 1985. Air Pollution by Photochemical Oxidants. Springer-Verlag, Berlin, FRG.
Heck, W.W., Taylor, O.C. and Tingey, D.T. 1988. Assessment of Crop Loss from Air Pollutants Elsevier, London, U.K.
Bowler, C., Slooten, L., Vandenbranden, S., De Rycke, R., Botterman, J., Sybesma, C., Van Montagu, M. and Inzé, D. 1991. Manganese superoxide dismutase can reduce cellular damage mediated by oxygen radicals in transgenic plants. EMBO J. 10: 1723–1732.
Lefohn, A.S. 1992. Surface Level Ozone Exposures and their Effects on Vegetation. Lewis Publishers, Chelsea, U.K.
Guderian, R., 1977. Air Pollution. Springer-Verlag, New York, USA.
Seckmayer, G. and Payer, H.D. 1993. A new sunlight simulator for ecological research on plants. J. Photobiochem. Photobiol. In press.
Darrall, N.M. 1989. The effect of air pollutants on physiological processes in plants. Plant, Cell & Environm. 12: 1–30.
Heath, R.L. 1988. Biochemical mechanisms of pollutant stress, p. 259–286 In: Assessment of Corp Loss from Air Pollutants. Heck, W.W., Taylor, O.C. and Tingey, D.T. (Eds). Elsevier, London, U.K.
Floyd, R.A., West, M.S., Hogsett, W.E. and Tingey, D.T. 1989. Increased 8-hydroxyguanine content of chloroplast DNA from ozone-treated plants. Plant Physiol. 91: 644–647.
Sakaki, T., Kondo, N. and Sugahara, K. 1983. Breakdown of photosynthetic pigments and lipids in spinach leaves with ozone fumigation: role of active oxygens. Physiol. Plant. 59: 28–34.
Pitcher, L.H., Brennan, E., Hurley, A., Dunsmuir, P., Tepperman, J.M. and Zilinskas, B.A. 1991. Overproduction of petunia chloroplastic copper/zinc superoxide dismutase does not confer ozone tolerance in transgenic tobacco. Plant Physiol. 97: 452–455.
Tepperman, J.M. and Dunsmuir, P. 1990. Transformed plants with elevated levels of chloroplastic SOD are not more resistant to superoxide toxicity. Plant Mol. Biol. 14: 501–511.
Elroy-Stein, O., Bernstein, Y. and Groner, Y. 1986. Overproduction of human Cu/Zn-superoxide dismutase in transfected cells: extenuation of paraquat-mediated cytotoxicity and enhancement of lipid peroxidation. EMBO J. 5: 615–622.
Ceballos, I., Delabar, J.M., Nicole, A., Lynch, R.E., Hallewell, R.A., Kamoun, P. and Sinet, P.M. 1988. Expression of transfected human CuZn-superoxide dismutase gene in mouse L cells and NS20Y neuroblastoma cells induces enhancement of glutathione peroxidase activity. Biochem. Biophys. Acta 949: 58–64.
Kelner, M.J. and Bagnell, R. 1990. Alteration of endogenous glutathione peroxidase, manganese superoxide dismutase, and glutathione transferase activity in cells transfected with a copper-zinc superoxide dismutase expression vector. Explanation for variations in paraquat resistance. J. Biol. Chem. 265: 10872–10875.
Pitcher, L.H., Brennan, E. and Zilinskas, B.A. 1992. The antiozonant ethyl-enediurea does not act via superoxide dismutase induction in bean. Plant Physiol. 99: 1388–1392.
Scandalios, J.G. 1990. Response of plant antioxidant defense genes to environmental stress. Adv. Genet. 28: 1–41.
Tsang, E.W.T., Bowler, C., Hérouart, D., Van Camp, W., Villarroel, R., Genetello, C., Van Montagu, M. and Inzé, D. 1991. Differential regulation of superoxide dismutase in plants exposed to environmental stress. Plant Cell 3: 783–792.
Perl-Treves, R. and Galun, E. 1991. The tomato Cu,Zn superoxide dismutase genes are developmentally regulated and respond to light and stress. Plant Mol. Biol. 17: 745–760.
Payer, H.D., Blank, L.W., Gnatz, G., Schmolke, W., Schramel, P. and Bosch, C. 1986. Simultaneous exposure of forest trees to pollutants and climatic stress. Water Air Soil Pollut. 31: 485–491.
Langebartels, C., Kerner, K., Leonardi, S., Schraudner, M., Trost, M., Heller, W. and Sanderaiann, H. Jr. 1991. Biochemical plant responses to ozone. I. Differential induction of polyamine and ethylene biosynthesis in tobacco. Plant Physiol. 95: 882–889.
Bradford, M.M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72: 248–254.
Beauchamp, C.O. and Fridovich, I. 1973. Isozymes of superoxide dismutase from wheat germ. Biochim. Biophys. Acta 317: 50–64.
Sandalio, L.M. and del Río, L.A. 1987. Localization of superoxide dismutase in glyoxysomes from Citrullus vulgaris. Functional implications in cellular metabolism. J. Plant Physiol. 127: 395–409.
Cerović, Z.G. and Plesničar, M. 1984. An improved procedure for the isolation of intact chloroplasts of high photosynthetic capacity. Biochem. J. 223: 543–545.
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Camp, W., Willekens, H., Bowler, C. et al. Elevated Levels of Superoxide Dismutase Protect Transgenic Plants Against Ozone Damage. Nat Biotechnol 12, 165–168 (1994). https://doi.org/10.1038/nbt0294-165
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DOI: https://doi.org/10.1038/nbt0294-165
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