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

Plant Physiology

Volumn 112, Issue 4, 1996, Pages 1703-1714

  Van Camp, Wim ^a   Capiau, Katelijne ^c   Van Montagu, Marc ^a   Inzé, Dirk ^a,b   Slooten, Luit ^c  

^a GHENT UNIVERSITY   (Belgium)

^b Inst Natl de la Rech Agronomique   (France)

^c VRIJE UNIVERSITEIT BRUSSEL   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 0030452648     PISSN: 00320889     EISSN: None     Source Type: Journal    
DOI: 10.1104/pp.112.4.1703     Document Type: Article

References (68)

1. Allen RD (1995) Dissection of oxidative stress tolerance using transgenic plants. Plant Physiol 107: 1049-1054
2. Ananyev G, Renger G, Wacker U, Klimov V (1994) The production of superoxide radicals and the superoxide dismutase activity of photosystem II. The possible involvement of cytochrome b559. Photosynth Res 41: 327-338
3. Aro E-M, Virgin I, Andersson B (1993) Photoinhibition of photosystem II: inactivation, protein damage and turnover. Biochim Biophys Acta 1143: 113-134
4. Asada K (1994) Production and action of active oxygen species in photosynthetic tissues. In CH Foyer, PM Mullineaux, eds, Causes of Photooxidative Stress and Amelioration of Defense Systems in Plants. CRC Press, Boca Raton, FL, pp 77-104
5. Asada K, Takahashi M (1987) Production and scavenging of active oxygen in photosynthesis. In DJ Kyle, CB Osmond, CJ Arntzen, eds, Photoinhibition (Topics in Photosynthesis, Vol 9). Elsevier, Amsterdam, pp 227-287
6. Badger MR (1985) Photosynthetic oxygen exchange. Annu Rev Plant Physiol 36: 27-53
7. Barber J (1994) Molecular basis of the vulnerability of photosystem II to damage by light. Aust J Plant Physiol 22: 201-208
8. Bowler C, Slooten L, Vandenbranden S, De Rycke R, Botterman J, Sybesma C, Van Montagu M, Inzé D (1991) Manganese Superoxide dismutase can reduce cellular damage mediated by oxygen radicals in transgenic plants. EMBO J 10: 1723-1732
9. Bowler C, Van Montagu M, Inzé D (1992) Superoxide dismutase and stress tolerance. Annu Rev Plant Physiol Plant Mol Biol 43: 83-116
10. Bradford MM (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248-254
11. Buchanan BB (1980) Role of light in the regulation of chloroplast enzymes. Annu Rev Plant Physiol 31: 341-374
12. 2 assimilation in oxygenic photosynthesis: the ferredoxin/thioredoxin system. Arch Biochem Biophys 288: 1-9
13. Cerovic ZG, Plesnicar M (1984) An improved method for the isolation of intact chloroplasts of high photosynthetic capacity. Biochem J 223: 543-545
14. Cheeseman JM (1988) Mechanism of salt tolerance in plants. Plant Physiol 87: 547-550
15. Chen G-X, Asada K (1989) Ascorbate peroxidase in tea leaves: occurrence of two isozymes and the differences in their enzymatic and molecular properties. Plant Cell Physiol 30: 987-998
16. Chen G-X, Blubaugh DJ, Homann PH, Golbeck JH, Cheniae GM (1995) 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 34: 2317-2332
17. Chen Z, Silva H, Klessig DF (1993) Active oxygen species in the induction of plant systemic acquired resistance by salicylic acid. Science 262: 1883-1886
18. De Block M, Botterman J, Vandewiele M, Dockx J, Thoen C, Gosselé V, Movva R, Thompson C, Van Montagu M, Leemans J (1987) Engineering herbicide resistance in plants by expression of a detoxifying enzyme. EMBO J 6: 2513-2518
19. Eckert H-J, Geiken B, Bernarding J, Napiwotzki A, Eichler H-J, Renger G (1991) Two sites of photoinhibition of the electron transfer in oxygen evolving and Tris-treated PSII membranes from spinach. Photosynth Res 27: 97-108
20. Foyer CH, Descourvières P, Kunert KJ (1994) Protection against oxygen radicals: an important defense mechanism studied in transgenic plants. Plant Cell Environ 17: 507-523
21. 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
22. Fujii T, Yokoyama E-i, Inoue K, Sakurai H (1990) The sites of electron donation of photosystem I to methyl viologen. Biochim Biophys Acta 1015: 41-48
23. Furbank RT, Badger MA (1982) Oxygen exchange associated with electron transport and photophosphorylation in spinach chloroplasts. Biochim Biophys Acta 723: 400-409
24. Geller BL, Winge DR (1984) Subcellular distribution of superoxide dismutases in rat liver. Methods Enzymol 105: 105-114
25. Genty B, Briantais J-M, Baker NR (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim Biophys Acta 990: 87-92
26. Gossett DG, Millhollon EP, Lucas MC (1994) Antioxidant response to NaCl stress in salt-tolerant and salt-sensitive cultivars of cotton. Crop Sci 34: 706-714
27. Greenway H, Munns R (1980) Mechanism of salt tolerance in non-halophytes. Annu Rev Plant Physiol 31: 149-190
28. Greer DH, Berry JA, Björkman O (1986) Photoinhibition of photosynthesis in intact bean leaves: role of light and temperature, and requirement for chloroplast-protein synthesis during recovery. Planta 168: 253-260
29. Halliwell B (1984) Chloroplast Metabolism: The Structure and Function of Chloroplasts in Green Leaf Cells. Clarendon Press, Oxford, UK
30. Halliwell B (1987) Oxidative damage, lipid peroxidation and antioxidant protection in chloroplasts. Chem Phys Lipids 44: 327-340
31. Havir EA (1992) The in vivo and in vitro inhibition of catalase from leaves of Nicotiana sylvestris by 3-amino-1,2,4-triazole. Plant Physiol 99: 533-537
32. Hernandez JA, Olmos E, Corpas FJ, Sevilla F, Del Rio LA (1995) Salt-induced oxidative stress in chloroplasts of pea plants. Plant Sci 105: 151-167
33. Hideg E, Spetea C, Vass I (1994) Singlet oxygen production in thylakoid membranes during photoinhibition as detected by EPR spectroscopy. Photosynth Res 39: 191-199
34. Hopkin KA, Papazian MA, Steinman HM (1992) Functional differences between manganese and iron Superoxide dismutases in Escherichia coli K-12. J Biol Chem 267: 24253-24258
35. Hosein B, Palmer G (1983) The kinetics and mechanism of oxidation of reduced spinach ferredoxin by molecular oxygen and its reduced products. Biochim Biophys Acta 723: 383-390
36. Kaiser WM (1979) Reversible inhibition of the Calvin cycle and activation of oxidative pentose phosphate cycle in isolated intact chloroplasts by hydrogen peroxide. Planta 145: 377-382
37. Knox JP, Dodge AD (1985) The photodynamic action of eosin, a singlet-oxygen generator: some effects on leaf tissue of Pisum sativum L. Planta 164: 22-29
38. Landgraf P, Doege M, Ohmann E, Tschiersch H (1995) Light stress and reactive oxygen species: consequences for photosynthesis in Euglena gracilis. In P Mathis, ed, Photosynthesis: From Light to Biosphere, Vol IV. Kluwer Academic Publishers, Dordrecht, The Netherlands, pp 465-468
39. Margoliash E, Novogrodsky A, Schejter A (1960) Irreversible reaction of 3-amino-1:2:4-triazole and related inhibitors with the protein of catalase. Biochem J 74: 339-350
40. McKersie BD, Chen Y, de Beus M, Bowley SR, Bowler C, Inzé D, D'Halluin K, Botterman J (1993) Superoxide dismutase enhances tolerance of freezing stress in transgenic alalfa (Medicago sativa L.). Plant Physiol 103: 1155-1163
41. Mittler R, Zilinskas BA (1993) Detection of ascorbate peroxidase activity in native gels by inhibition of ascorbate-dependent reduction of nitroblue tetrazolium. Anal Biochem 212: 540-546
42. Miyake C, Asada K (1992) Thylakoid-bound ascorbate peroxidase in spinach chloroplasts and photoreduction of its primary oxidation product monodehydroascorbate radicals in thylakoids. Plant Cell Physiol 33: 541-553
43. Miyake C, Asada K (1994) Ferredoxin-dependent photoreducion of the monodehydroascorbate radical in spinach thylakoids. Plant Cell Physiol 35: 539-549
44. Miyao M (1994) Involvement of active oxygen species in degradation of the D1 protein under strong illumination in isolated subcomplexes of photosystem II. Biochemistry 33: 9722-9730
45. Miyao-Tokutomi M, Okada K, Yamamoto N (1995) Specific cleavage of the D1 protein of PSII by exogenous active oxygen species. In P Mathis, ed, Photosynthesis: From Light to Biosphere, Vol IV. Kluwer Academic Publishers, Dordrecht, The Netherlands, pp 243-246
46. Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22: 867-880
47. Ogawa K, Kanematsu S, Asada K (1995a) Spinach chloroplastic and cytosolic CuZnSODs are localized at the sites of superoxide generation. In P Mathis, ed, Photosynthesis: From Light to Biosphere, Vol IV. Kluwer Academic Publishers, Dordrecht, The Netherlands, pp 339-342
48. Ogawa K, Kanematsu S, Takabe K, Asada K (1995b) Attachment of CuZn-superoxide dismutase to thylakoid membranes at the site of superoxide generation (PSI) in spinach chloroplasts: detection by immunogold labeling after rapid freezing and substitution method. Plant Cell Physiol 36: 565-573
49. Okada K, Satoh K, Katoh S (1991) Chloramphenicol is an inhibitor of photosynthesis. FEBS Lett 295: 155-158
50. Olmos E, Hernandez JA, Sevilla F, Hellin E (1994) Induction of several antioxidant enzymes in the selection of a salt-tolerant cell line of Pisum sativum. J Plant Physiol 144: 594-598
51. Perl A, Perl-Treves R, Galili S, Aviv D, Shalgi E, Malkin S, Galun E (1993) Enhanced oxidative-stress defense in transgenic potato overexpressing tomato Cu,Zn superoxide dismutases. Theor Appl Genet 85: 568-576
52. Pitcher LH, Brennan E, Hurley A, Dunsmuir P, Tepperman JM, Zilinskas BA (1991) Overproduction of petunia chloroplastic copper/zinc Superoxide dismutase does not confer ozone tolerance in transgenic tobacco. Plant Physiol 97: 452-455
53. Prasil O, Adir N, Ohad I (1992) Dynamics of photosystem II: mechanism of photoinhibition and recovery processes. In J Barber, ed, Topics in Photosynthesis, Vol 11. The Photosystems: Structure, Function and Molecular Biology. Elsevier, Amsterdam, pp 295-348
54. Sehmer L, Alaoui-Sosse B, Dizengremel P (1995) Effect of salt stress on growth and on the detoxifying pathway of pedunculate oak seedlings (Quercus robur L.). J Plant Physiol 147: 144-151
55. Sen Gupta A, Heinen JL, Holaday AS, Burke JJ, Allen RD (1993a) Increased resistance to oxidative stress in transgenic plants that overexpress chloroplastic Cu/Zn Superoxide dismutase. Proc Natl Acad Sci USA 90: 1629-1633
56. Sen Gupta A, Webb RP, Holaday AS, Allen RD (1993b) Overexpression of superoxide dimutase protects plants from oxidative stress. Plant Physiol 103: 1067-1073
57. 2 metabolism in Vigna and Oryza seedlings. Biochem Physiol Pflanz 186: 69-74
58. Slooten L, Capiau K, Van Camp W, Van Montagu M, Sybesma C, Inzé D (1995) Factors affecting the enhancement of oxidative stress tolerance in transgenic tobacco overexpressing manganese Superoxide dismutase in the chloroplasts. Plant Physiol 107: 737-750
59. Stitt M, McC Lilley R, Gerhardt R, Heldt HW (1989) Metabolite levels in specific cells and subcellular compartments of plant leaves. Methods Enzymol 174: 518-552
60. Takahashi M, Asada K (1988) Superoxide production in the aprotic interior of thylakoid membranes. Arch Biochem Biophys 267: 714-722
61. Takeda T, Yokota A, Shigeoka S (1995) Resistance of photosynthesis to hydrogen peroxide in algae. Plant Cell Physiol 36: 1089-1095
62. Tepperman JM, Dunsmuir P (1990) Transformed plants with elevated levels of chloroplastic SOD are not more resistant to Superoxide toxicity. Plant Mol Biol 14: 501-511
63. Thiele A, Winter K, Krause GH (1995) Photoinhibition of photosynthesis related to xanthophyll cycle and D1 protein turnover in higher plants. In P Mathis, ed, Photosynthesis: From Light to Biosphere, Vol IV. Kluwer Academic Publishers, Dordrecht, The Netherlands, pp 437-440
64. Van Camp W, Bowler C, Villarroel R, Tsang EWT, Van Montagu M, Inzé D (1990) Characterization of iron Superoxide dismutase cDNAs from plants obtained by genetic complementation in Escherichia coli. Proc Natl Acad Sci USA 87: 9903-9907
65. Van Camp W, Van Montagu M, Inzé D (1994a) Superoxide dismutases. In CH Foyer, PM Mullineaux, eds, Causes of Photooxidative Stress in Plants and Amelioration of Defense Systems. CRC Press, Boca Raton, FL, pp 317-341
66. Van Camp W, Willekens H, Bowler C, Van Montagu M, Inzé D, Reupold-Popp R, Sandermann H Jr, Langebartels C (1994b) Elevated levels of Superoxide dismutase protect transgenic plants against ozone damage. Bio/Technology 12: 165-168
67. A species promote chlorophyll triplet formation. Proc Natl Acad Sci USA 89: 1408-1412
68. Wang WS, Chapman DJ, Barber J (1992) Effect of cold treatments on the binding stability of photosystem two extrinsic proteins and associated increase in susceptibility to photoinhibition. Plant Physiol 99: 21-25