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. 1996 Dec;112(4):1703–1714. doi: 10.1104/pp.112.4.1703

Enhancement of oxidative stress tolerance in transgenic tobacco plants overproducing Fe-superoxide dismutase in chloroplasts.

W Van Camp 1, K Capiau 1, M Van Montagu 1, D Inzé 1, L Slooten 1
PMCID: PMC158104  PMID: 8972606

Abstract

A chimeric gene consisting of the coding sequence for chloroplastic Fe superoxide dismutase (FeSOD) from Arabidopsis thaliana, coupled to the chloroplast targeting sequence from the pea ribulose-1,5-bisphosphate carboxylase/oxygenase small subunit, was expressed in Nicotiana tabacum cv Petit Havana SR1. Expression of the transgenic FeSOD protected both the plasmalemma and photosystem II against superoxide generated during illumination of leaf discs impregnated with methyl viologen. By contrast, overproduction of a mitochondrial MnSOD from Nicotiana plumbaginifolia in the chloroplasts of cv SR1 protected only the plasmalemma, but not photosystem II, against methyl viologen (L. Slooten, K. Capiau, W. Van Camp, M. Van Montagu, C. Sybesma, D. Inzé [1995] Plant Physiol 107: 737-750). The difference in effectiveness correlates with different membrane affinities of the transgenic FeSOD and MnSOD. Overproduction of FeSOD does not confer tolerance to H2O2, singlet oxygen, chilling-induced photoinhibition in leaf disc assays, or to salt stress at the whole plant level. In nontransgenic plants, salt stress led to a 2- to 3-fold increase in activity, on a protein basis, of FeSOD, cytosolic and chloroplastic Cu/ZnSOD, ascorbate peroxidase, dehydroascorbate reductase, and glutathione reductase. In FeSOD-overproducing plants under salt stress, the induction of cytosolic and chloroplastic Cu/ZnSOD was suppressed, whereas induction of a water-soluble chloroplastic ascorbate peroxidase isozyme was promoted.

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Selected References

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  1. Allen R. D. Dissection of Oxidative Stress Tolerance Using Transgenic Plants. Plant Physiol. 1995 Apr;107(4):1049–1054. doi: 10.1104/pp.107.4.1049. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Aro E. M., Virgin I., Andersson B. Photoinhibition of Photosystem II. Inactivation, protein damage and turnover. Biochim Biophys Acta. 1993 Jul 5;1143(2):113–134. doi: 10.1016/0005-2728(93)90134-2. [DOI] [PubMed] [Google Scholar]
  3. Block M. D., Botterman J., Vandewiele M., Dockx J., Thoen C., Gosselé V., Movva N. R., Thompson C., Montagu M. V., Leemans J. Engineering herbicide resistance in plants by expression of a detoxifying enzyme. EMBO J. 1987 Sep;6(9):2513–2518. doi: 10.1002/j.1460-2075.1987.tb02537.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bowler C., Slooten L., Vandenbranden S., De Rycke R., Botterman J., Sybesma C., Van Montagu M., Inzé D. Manganese superoxide dismutase can reduce cellular damage mediated by oxygen radicals in transgenic plants. EMBO J. 1991 Jul;10(7):1723–1732. doi: 10.1002/j.1460-2075.1991.tb07696.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Buchanan B. B. Regulation of CO2 assimilation in oxygenic photosynthesis: the ferredoxin/thioredoxin system. Perspective on its discovery, present status, and future development. Arch Biochem Biophys. 1991 Jul;288(1):1–9. doi: 10.1016/0003-9861(91)90157-e. [DOI] [PubMed] [Google Scholar]
  6. Cerović Z. G., Plesnicar M. An improved procedure for the isolation of intact chloroplasts of high photosynthetic capacity. Biochem J. 1984 Oct 15;223(2):543–545. doi: 10.1042/bj2230543. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Cheeseman J. M. Mechanisms of salinity tolerance in plants. Plant Physiol. 1988 Jul;87(3):547–550. doi: 10.1104/pp.87.3.547. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Chen G. X., Blubaugh D. J., Homann P. H., Golbeck J. H., Cheniae G. M. Superoxide contributes to the rapid inactivation of specific secondary donors of the photosystem II reaction center during photodamage of manganese-depleted photosystem II membranes. Biochemistry. 1995 Feb 21;34(7):2317–2332. doi: 10.1021/bi00007a028. [DOI] [PubMed] [Google Scholar]
  9. Chen Z., Silva H., Klessig D. F. Active oxygen species in the induction of plant systemic acquired resistance by salicylic acid. Science. 1993 Dec 17;262(5141):1883–1886. doi: 10.1126/science.8266079. [DOI] [PubMed] [Google Scholar]
  10. Geller B. L., Winge D. R. Subcellular distribution of superoxide dismutases in rat liver. Methods Enzymol. 1984;105:105–114. doi: 10.1016/s0076-6879(84)05014-x. [DOI] [PubMed] [Google Scholar]
  11. Gupta A. S., Heinen J. L., Holaday A. S., Burke J. J., Allen R. D. Increased resistance to oxidative stress in transgenic plants that overexpress chloroplastic Cu/Zn superoxide dismutase. Proc Natl Acad Sci U S A. 1993 Feb 15;90(4):1629–1633. doi: 10.1073/pnas.90.4.1629. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Gupta A. S., Webb R. P., Holaday A. S., Allen R. D. Overexpression of Superoxide Dismutase Protects Plants from Oxidative Stress (Induction of Ascorbate Peroxidase in Superoxide Dismutase-Overexpressing Plants). Plant Physiol. 1993 Dec;103(4):1067–1073. doi: 10.1104/pp.103.4.1067. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Havir E. A. The in Vivo and in Vitro Inhibition of Catalase from Leaves of Nicotiana sylvestris by 3-Amino-1,2,4-Triazole. Plant Physiol. 1992 Jun;99(2):533–537. doi: 10.1104/pp.99.2.533. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Hopkin K. A., Papazian M. A., Steinman H. M. Functional differences between manganese and iron superoxide dismutases in Escherichia coli K-12. J Biol Chem. 1992 Dec 5;267(34):24253–24258. [PubMed] [Google Scholar]
  15. MARGOLIASH E., NOVOGRODSKY A., SCHEJTER A. Irreversible reaction of 3-amino-1:2:4-triazole and related inhibitors with the protein of catalase. Biochem J. 1960 Feb;74:339–348. doi: 10.1042/bj0740339. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. McKersie B. D., Chen Y., de Beus M., Bowley S. R., Bowler C., Inzé D., D'Halluin K., Botterman J. Superoxide dismutase enhances tolerance of freezing stress in transgenic alfalfa (Medicago sativa L.). Plant Physiol. 1993 Dec;103(4):1155–1163. doi: 10.1104/pp.103.4.1155. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Mittler R., Zilinskas B. A. Detection of ascorbate peroxidase activity in native gels by inhibition of the ascorbate-dependent reduction of nitroblue tetrazolium. Anal Biochem. 1993 Aug 1;212(2):540–546. doi: 10.1006/abio.1993.1366. [DOI] [PubMed] [Google Scholar]
  18. Miyao M. Involvement of active oxygen species in degradation of the D1 protein under strong illumination in isolated subcomplexes of photosystem II. Biochemistry. 1994 Aug 16;33(32):9722–9730. doi: 10.1021/bi00198a043. [DOI] [PubMed] [Google Scholar]
  19. Okada K., Satoh K., Katoh S. Chloramphenicol is an inhibitor of photosynthesis. FEBS Lett. 1991 Dec 16;295(1-3):155–158. doi: 10.1016/0014-5793(91)81407-y. [DOI] [PubMed] [Google Scholar]
  20. Tepperman J. M., Dunsmuir P. Transformed plants with elevated levels of chloroplastic SOD are not more resistant to superoxide toxicity. Plant Mol Biol. 1990 Apr;14(4):501–511. doi: 10.1007/BF00027496. [DOI] [PubMed] [Google Scholar]
  21. Van Camp W., Bowler C., Villarroel R., Tsang E. W., Van Montagu M., Inzé D. Characterization of iron superoxide dismutase cDNAs from plants obtained by genetic complementation in Escherichia coli. Proc Natl Acad Sci U S A. 1990 Dec;87(24):9903–9907. doi: 10.1073/pnas.87.24.9903. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Wang W. Q., Chapman D. J., Barber J. Effect of Cold Treatments on the Binding Stability of Photosystem II Extrinsic Proteins and an Associated Increase in Susceptibility to Photoinhibition. Plant Physiol. 1992 May;99(1):21–25. doi: 10.1104/pp.99.1.21. [DOI] [PMC free article] [PubMed] [Google Scholar]

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