Elevated glutathione biosynthetic capacity in the chloroplasts of transgenic tobacco plants paradoxically causes increased oxidative stress

Plant Cell

Volumn 11, Issue 7, 1999, Pages 1277-1291

  Creissen, Gary ^a   Firmin, John ^a   Fryer, Michael ^a   Kular, Baldeep ^a   Leyland, Nicola ^a   Reynolds, Helen ^b   Pastori, Gabriela ^b   Wellburn, Florence ^b   Baker, Neil ^c   Wellburn, Alan ^c   Mullineaux, Philip ^c  

^a NORWICH RESEARCH PARK   (United Kingdom)

^b UNIVERSITY OF ESSEX   (United Kingdom)

^c LANCASTER UNIVERSITY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BIOSYNTHESIS; CHLOROPLAST; GLUTAMATE CYSTEINE LIGASE; GLUTATHIONE; TRANSGENIC PLANT;

NICOTIANA OBTUSIFOLIA; NICOTIANA TABACUM; TRIXIS;

EID: 0032696323     PISSN: 10404651     EISSN: None     Source Type: Journal    
DOI: 10.1105/tpc.11.7.1277     Document Type: Article

References (65)

1. Aebi, H. (1984). Catalase In vitro. Methods Enzymol. 105, 121-126.
2. Allen, A.C., and Fluhr, R. (1997). Two distinct sources of elicited reactive oxygen species in tobacco epidermal cells. Plant Cell 9, 1559-1572.
3. Alting-Mees, M.A., and Short, Ü.M. (1989). pBluescript II, gene mapping vectors. Nucleic Acids Res. 17, 9494.
4. Anderson, S., and Smith, S.M. (1986). Synthesis of the small subunit of ribulose-bisphosphate carboxylase from genes cloned into plasmids containing the SP6 promoter. Biochem. J. 240, 709-715.
5. Apontoweil, P., and Berends, W. (1975). Isolation and initial characterization of glutathione-deficient mutants of Escherichia coli K12. Biochim. Biophys. Acta 399, 10-22.
6. Arisi, A.-C.M., Noctor, G., Foyer, C.H., and Jouanin, L. (1997). Modification of thiol contents in poplars (Populus tremula x P. alba) overexpressing enzymes involved in glutathione synthesis. Planta 203, 362-372.
7. Asada, K. (1994). Production and action of active oxygen species in photosynthetic tissues. In Causes of Photooxidative Stress and Amelioration of Defense Systems in Plants, C.H. Foyer and P.M. Mullineaux, eds (Boca Raton, FL: CRC Press), pp. 77-104.
8. Baker, C.J., and Orlandi, E.W. (1995). Active oxygen in plant pathogenesis. Annu. Rev. Phytopathol. 33, 299-321.
9. Baker, N.R. (1994). Chilling stress and photosynthesis. In Causes of Photooxidative Stress and Amelioration of Defense Systems in Plants, C.H. Foyer and P.M. Mullineaux, eds (Boca Raton, FL: CRC Press), pp. 127-154.
10. Bevan, M. (1984). Binary Agrobacterium vectors for plant transformation. Nucleic Acids Res. 12, 8711-8721.
11. Bielawski, W., and Joy, K.W. (1986). Reduced and oxidised glutathione and glutathione-reductase activity in tissues of Pisum sativum. Planta 169, 267-272.
12. Bongi, G., and Long, S.P. (1987). Light dependent damage to photosynthesis in olive leaves during chilling and high-temperature stress. Plant Cell Environ. 10, 241-249.
13. Bowler, C., Alliotte, T., De Loose, M., Van Montagu, M., and Inzé, D. (1989). The induction of manganese Superoxide dismutase in response to stress in Nicotians plumbaginifolia. EMBO J. 8, 31-38.
14. Broadbent, P., Creissen, G.P., Kular, B., Wellburn, A.R., and Mullineaux, P.M. (1995). Oxidative stress responses in transgenic tobacco containing altered levels of glutathione reductase activity. Plant J. 8, 247-255.
15. Chamnongpol, S., Willekens, H., Langebartels, C., Van Montagu, M., Inzé, D., and Van Camp, W. (1996). Transgenic tobacco with a reduced catalase activity develops necrotic lesions and induces pathogenesis-related expression under high light. Plant J. 10, 491-503.
16. Conklin, P.L., and Last, R.L. (1995). Differential accumulation of antioxidant mRNAs in Arabidopsis thaliana exposed to ozone. Plant Physiol. 109, 203-212.
17. Creissen, G.P., and Mullineaux, P.M. (1995). Cloning and characterisation of glutathione reductase cDNAs and identification of two genes encoding the tobacco enzyme. Planta 197, 422-425.
18. Creissen, G., Reynolds, H., Xue, Y., and Mullineaux, P. (1995). Simultaneous targeting of pea glutathione reductase and of a bacterial fusion protein to chloroplasts and mitochondria in transgenic tobacco. Plant J. 8, 167-175.
19. Criqui, M.C., Jamet, E., Parmentier, Y., Marbach, J., Durr, A., and Flack, J. (1992). Isolation and characterization of a plant cDNA showing homology to animal glutathione peroxidases. Plant Mol. Biol. 18, 623-627.
20. Deitrich, R.A., Delaney, T.P., Uknes, S.J., Ward, E.R., Ryals, J.A., and Dangl, J.L. (1994). Arabidopsis mutants simulating disease resistance response. Cell 77, 565-577.
21. Ditta, G., Stanfield, S., Corbin, D., and Helinski, D.R. (1980). Broad host range DNA cloning system for Gram-negative bacteria: Construction of a gene bank of Rhizoblum meliloti. Proc. Natl. Acad. Sci. USA 77, 7347-7351.
22. Doehlert, D.C., Kuo, T.M., and Felker, F.C. (1988). Enzymes of sucrose and hexose metabolism in developing kernels of two inbreds of maize. Plant Physiol. 86, 1013-1019.
23. Foyer, C.H., and Halliwell, B. (1976). The presence of glutathione and glutathione reductase in chloroplasts: A proposed role in ascorbate metabolism. Planta 133, 21-25.
24. Foyer, C.H., and Harbinson, J. (1994). Oxygen metabolism and the regulation of photosynthetic electron transport. In Causes of Photooxidative Stress and Amelioration of Defense Systems in Plants, C.H. Foyer and P.M. Mullineaux, eds (Boca Raton, FL: CRC Press), pp. 1-42.
25. Foyer, C.H., Lopez-Delgado, H., Dat, J.F., and Scott, I.M. (1997). Hydrogen peroxide- and glutathione-associated mechanisms of acclimatory stress tolerance and signaling. Physiol. Plant. 100, 241-254.
26. Fryer, M. (1993). The antioxidant effects of thylakoid vitamin E (atocopherol). Plant Cell Environ. 15, 381-392.
27. Grantz, A.A., Brummell, D.A., and Bennett, A.B. (1995). Ascorbate free radical reductase mRNA levels are induced by wounding. Plant Physiol. 108, 411-418.
28. Greenberg, J.T., Quo, A., Klessig, D.F., and Ausübe), F.M. (1994). Programmed cell death in plants: A pathogen-triggered response activated coordinately with multiple defense functions. Cell 77, 551-563.
29. Guerineau, F., Woolston, S., Brooks, L., and Mullineaux, P. (1988). An expression cassette for targeting foreign proteins into chloroplasts. Nucleic Acids Res. 16, 11380.
30. Guilbault, G.G., Kramer, D.N., and Hackley, E. (1967). A new substrate for fluorometric determination of oxidative enzymes. Anal. Chem.39, 271.
31. Gushima, H., Yasuda, S., Soeda, E., Yokota, M., Kondo, M., and Kimura, A. (1984). Complete nucleotide sequence of the E coli glutathione synthetase gsh-ll. Nucleic Acids Res. 12, 9299-9307.
32. Hell, R., and Bergmann, L. (1990). γ-Glutamylcysteine synthetase in higher plants: Catalytic properties and subcellular localization. Planta 180, 603-612.
33. Hérouart, D., Van Montagu, M., and Inzé, D. (1993). Redox-activated expression of the cytosolic copper/zinc Superoxide dismutase gene in Nicotians. Proc. Natl. Acad. Sci. USA 90, 3108-3112.
34. Jabs, T., Dietrich, R.A., and Dangl, J.L. (1996). Initiation of runaway cell death in an Arabidopsis mutant by extracellular superoxide. Science 273, 1853-1856.
35. Journal, E.-P., and Douce, R. (1985). Enzymatic capacities of purified cauliflower bud plastids for lipid synthesis and carbohydrate metabolism. Plant Physiol. 79, 458-467.
36. Karpinski, S., Escobar, C., Karpinska, B., Creissen, G., and Mullineaux, P.M. (1997). Photosynthetic electron transport regulates the expression of cytosolic ascorbate peroxidase genes in Arabidopsis during excess light stress. Plant Cell 9, 627-640.
37. Law, M.Y., Charles, S.A., and Halliwell, B. (1983). Glutathione and ascorbic acid in spinach (Sp/nac/a o/eracea) chloroplasts. Biochem J. 210, 899-903.
38. Levine, A., Tenhaken, Ft., Dixon, Ft., and Lamb, C.J. (1994). H2O2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response. Cell 79, 583-593.
39. Link, G. (1996). Green life: Control of chloroplast gene transcription. Bioessays 18, 465-471.
40. May, M., Hammond-Kosack, K.E., and Jones, J.D.G. (1996). Involvement of reactive oxygen species, glutathione metabolism, and lipid peroxidation in the Cf-gene-dependent defense response of tomato cotyledons induced by race-specific elicitors of Cladosporium fulvum. Plant Physiol. 110, 1367-1379.
41. 2 and antioxidants have opposite effects on activation of NF-KB and AP-1 in intact cells: AP-1 as secondary antioxidant-responsive factor. EMBOJ. 12, 2005-2015.
42. Mittler, R., Shulaev, V., Seskar, M., and Lam, E. (1996). Inhibition of programmed cell death in tobacco plants during a pathogeninduced hypersensitive response at low oxygen pressure. Plant CellB, 1991-2001.
43. Mullineaux, P., and Creissen, G. (1996). Opportunities for the genetic manipulation of antioxidants in plant foods. Biochem. Soc. Trans. 24, 829-835.
44. Mullineaux, P.M., and Creissen, G.P. (1997). Glutathione reductase: Regulation and role in oxidative stress. In Oxidative Stress and the Molecular Biology of Antioxidant Defenses, J. Scandalios, ed (Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press), pp. 667-713.
45. Mullineaux, P.M., Karpinski, S., Jiménez, A., Cleary, S.P., Robinson, C., and Creissen, G.P. (1998). Identification of cDNAs encoding plastid-targeted glutathione peroxidase. Plant J. 13, 375-379.
46. Newton, G.L., Dorian, R., and Fahey, R.C. (1981). Analysis of biological thiols: Derivitization with monobromobimane and separation by reverse-phase high performance liquid chromatography. Anal. Biochem. 114, 383-387.
47. Noctor, G., Strohm, M., Jouanin, L., Kunert, K.-J., Foyer, C.H., and Rennenberg, H. (1996). Synthesis of glutathione in leaves of transgenic poplar overexpressing γ-glutamylcysteine synthetase. Plant Physiol. 112, 1071-1078.
48. Noctor, G., Arisi, A.-C.M., Jouanin, L., Valadier, M.-H., Roux, Y., and Foyer, C.H. (1997). The role of glycine in determining the rate of glutathione synthesis in poplar: Possible implications for glutathione production during stress. Physiol. Plant. 100, 255-263.
49. Noctor, G., Arisi, A.-C.M., Jouanin, L., Kunert, K.J., Rennenberg, H., and Foyer, C.H. (1998). Glutathione: Biosynthesis, metabolism and relationship to stress tolerance in transformed plants. J. Exp. Bot. 49, 623-647.
50. Penneil, R.I., and Lamb, C. (1997). Programmed cell death in plants. Plant Cell 9, 1157-1168.
51. Polie, A. (1996). Developmental changes of antioxidative systems in tobacco leaves as affected by limited sucrose export in transgenic plants expressing yeast-invertase in the apoplastic space. Planta 198, 253-262.
52. Ruegsegger, A., and Brunold, C. (1993). Localization of γ-glutamylcysteine synthetase and glutathione synthetase activity in maize seedlings. Plant Physiol. 101, 561-566.
53. Sambrook, J., Fritsch, E.F., and Maniatis, T. (1989). Molecular Cloning: A Laboratory Manual, 2nd ed. (Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press).
54. Smith, I.K., Vierhaller, T.L., and Thorne, C.A. (1989). Properties and functions of glutathione reductase in plants. Physiol. Plant. 77, 449-456.
55. Stevens, R.G., Creissen, G.P., and Mullineaux, P.M. (1997). Cloning and characterisation of a cytosolic glutathione reductase cDNA from pea (Pisum sativum L.) and its expression in response to stress. Plant Mol. Biol. 35, 641-654.
56. Strohm, M., Jouanin, L., Kunert, K.-J., Pruvost, C., Polle, A., Foyer, C.H., and Rennenberg, H. (1995). Regulation of glutathione synthesis in leaves of transgenic poplar (Populus tremula x P. alba) overexpressing glutathione synthetase. Plant J. 7, 141-145.
57. Tsang, E.W.T., Bowler, C., Herouart, D., Van Camp, W., Villarroel, R., Genetello, C., Van Montagu, M., and Inzé, D. (1991). Differential regulation of Superoxide dismutases in plants exposed to environmental stress. Plant Cell 3, 783-792.
58. Von Caemmerer, S., and Farquar, G.D. (1981). Some relationships between the biochemistry of photosynthesis and the gas exchange of leaves. Planta 156, 199-206.
59. Watanabe, K., Yamano, Y., Murata, K., and Kimura, A. (1986). The nucleotide sequence of the gene for -y-glutamylcysteine synthetase of Escherichia coli. Nucleic Acids Res. 14, 4393-4400.
60. Wellburn, F.A.M., and Wellburn, A.R. (1994). Atmospheric ozone affects carbohydrate allocation and winter hardiness of Pinus halpensis (Mill.). J. Exp. Bot. 45, 607-614.
61. Wellburn, F.A.M, Creissen, G.P., Lake, J.A., Mullineaux, P.M., and Wellburn, A.R. (1998). Tolerance to atmospheric ozone in transgenic tobacco over-expressing glutathione synthetase in plastids. Physiol. Plant. 104, 623-629.
62. Willekens, H., Van Camp, W., Van Montagu, M., Inzé, D., Langebartels, C., and Sandermann, H. (1995). Ozone, sulfur dioxide and ultraviolet B have similar effects on mRNA accumulation of antioxidant genes in Nicotiana plumbaginifolia L. Plant Physiol. 106, 1007-1014.
63. 3 plants. EMBO J. 16, 4806-4816.
64. Wingate, V.P.M., Lawton, MA., and Lamb, C.J. (1989). Glutathione causes a massive and selective induction of plant defense genes. Plant Physiol. 87, 206-210.
65. Wingsle, G., and Karpinski, S. (1996). Differential redox regulation by glutathione of glutathione reductase and CuZn-superoxide dismutase gene expression in Pinus sylvestris L needles. Planta 198, 151-157.