Transgenic tobacco (Nicotiana tabacum L.) plants with increased expression levels of mitochondrial NADP+-dependent isocitrate dehydrogenase: Evidence implicating this enzyme in the redox activation of the alternative oxidase

Plant and Cell Physiology

Volumn 45, Issue 10, 2004, Pages 1413-1425

  Gray, Gordon R ^a   Villarimo, Alicia R ^b   Whitehead, Carmen L ^a   McIntosh, Lee ^b,c  

^a UNIVERSITY OF SASKATCHEWAN   (Canada)

^b MICHIGAN STATE UNIVERSITY   (United States)

^c Michigan State University   (United States)

Author keywords

Alternative oxidase; Isocitrate dehydrogenase; Mitochondria; Nicotiana tabacum L.; Sauromatum guttatum Schott; Tricarboxylic acid cycle

Indexed keywords

LILIUM; NICOTIANA; NICOTIANA OBTUSIFOLIA; NICOTIANA TABACUM; SAUROMATUM GUTTATUM;

EID: 9244254317     PISSN: 00320781     EISSN: None     Source Type: Journal    
DOI: 10.1093/pcp/pch162     Document Type: Article

References (71)

1. Altschul, S.F., Madden, T.L., Schaffer, A.A., Zhang, J., Zhang, Z., Miller, W. and Lipman, D.J. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25: 3389-3402.
2. An, G., Eben, P.R., Mitra, A. and Ha, S.B. (1988) Binary vectors. In Plant Molecular Biology Manual. Edited by Gelvin, S.B. and Schilperoort, R.A. pp. A3, 1-19. Kluwer Academic Publishers, Dordrecht.
3. Attucci, S., Rivoal, J., Brouquisse, R., Carde, J.-P., Pradet, A. and Raymond, P. (1994) Characterization of a mitochondrial NADP-dependent isocitrate dehydrogenase in axes of germinating sunflower seeds. Plant Sci. 102: 49-59.
4. Ausubel, F.M., Brent, R., Kingston, R.E., Moore, D.D., Seidman, J.G., Smith, J.A. and Struhl, K. (1987) Current Protocols in Molecular Biology. John Wiley & Sons, New York.
5. Balmer, Y., Vensel, W.H., Tanaka, C.K., Hurkman, W.J., Gelhaye, E., Rouhier, N., Jacquot, J.-P., Manieri, W., Schürmann, P., Droux, M. and Buchanan, B.B. (2004) Thioredoxin links redox to the regulation of fundamental processes of plant mitochondria. Proc. Natl Acad. Sci. USA 101: 2642-2647.
6. Banze, M. and Follmann, H. (2000) Organelle-specific NADPH thioredoxin reductase in plant mitochondria. J. Plant Physiol. 156: 126-129.
7. Boutry, M., Faber, A.-M., Charbonnier, M. and Briquet, M. (1984) Microanalysis of plant mitochondrial protein synthesis products: Detection of variant polypeptides associated with cytoplasmic male sterility. Plant Mol. Biol. 3: 445-452.
8. 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.
9. Chen, R.D. and Gadal, P. (1990) Structure, functions and regulation of NAD and NADP dependent isocitrate dehydrogenases in higher plants and other organisms. Plant Physiol. Biochem. 28: 411-427.
10. Chivasa, S., Berry, J.O., ap Rees, T. and Carr, J.P. (1999) Changes in gene expression during development and thermogenesis in Arum. Aust. J. Plant Physiol. 26: 391-399.
11. Cooper, T.G. and Beavers, H. (1969) Mitochondria and glyoxysomes from castor bean endosperm. Enzyme constituents and catalytic capacity. J. Biol. Chem. 244: 3507-3513.
12. +-dependent isocitrate dehydrogenases in mitochondria purified from Picea abies seedlings. Physiol. Plant. 96: 312-318.
13. Cox, G.F. and Davies, D.D. (1967) Nicotinamide-adenine dinucleotide-specific isocitrate dehydrogenase from pea mitochondria. Biochem. J. 105: 729-734.
14. Curry, R.A. and Ting, T.P. (1976) Purification, properties and kinetic observation on the isoenzymes of NADP-isocitrate dehydrogenase. Arch. Biochem. Biophys. 176: 501-509.
15. Douce, R., Christensen, E.L. and Bonner, W.D. Jr. (1972) Preparation of intact plant mitochondria. Biochim. Biophys. Acta 275: 148-160.
16. Douce, R. and Neuburger, M. (1989) The uniqueness of plant mitochondria. Annu. Rev. Plant Physiol. 40: 371-414.
17. Elthon, T.E. and McIntosh, L. (1987) Identification of the alternative terminal oxidase of higher plant mitochondria. Proc. Natl Acad. Sci. USA 84: 8399-8403.
18. Elthon, T.E., Nickels, R.L. and McIntosh, L. (1989) Mitochondrial events during development of thermogenesis in Sauromatum guttatum (Schott). Planta 180: 82-89.
19. +-dependent isocitrate dehydrogenase versus fumarase. Plant Physiol. 117: 473-481.
20. Feinberg, A.P. and Vogelstein, B. (1983) A technique for radiolabelling DNA restriction endonuclease fragments to high specific activity. Anal. Biochem. 132: 6-13.
21. +-dependent isocitrate dehydrogenase from potato. Implications for nitrogen metabolism. Plant Physiol. 107: 905-913.
22. Gálvez, S., Bismuth, E., Sarda, C. and Gadal, P. (1994) Purification and characterization of chloroplastic NADP-isocitrate dehydrogenase from mixotrophic tobacco cells. Comparison with the cytosolic isoenzyme. Plant Physiol. 105: 593-600.
23. Gálvez, S. and Gadal, P. (1995) On the function of the NADP-dependent isocitrate dehydrogenase isoenzymes in living organisms. Plant Sci. 105: 1-14.
24. Gálvez, S., Hodges, M., Decottignies, P., Bismuth, E., Lancien, M., Sangwan, R.S., Dubois, F., LeMaréchal, P., Crétin, C. and Gadal, P. (1996) Identification of a tobacco cDNA encoding a cytosolic NADP-isocitrate dehydrogenase. Plant Mol. Biol. 30: 307-320.
25. Gálvez, S., Roche, O., Bismuth, E., Brown, S., Gadal, P. and Hodges, M. (1998) Mitochondrial localization of a NADP-dependent isocitrate dehydrogenase isoenzyme by using the green fluorescent protein as a marker. Proc. Natl. Acad. Sci. USA 95: 7813-7818.
26. Gamborg, O.L., Miller, R.A. and Ojima, K. (1968) Nutrient requirements of suspension cultures of soybean root cells. Exp. Cell Res. 50: 151-158.
27. Hayes, M.K., Luethy, M.H. and Elthon, T.E. (1991) Mitochondrial malate dehydrogenase from corn. Purification of multiple forms. Plant Physiol. 97: 1381-1387.
28. Hill, S.A., Grof, C.P.L., Bryce, J.H. and Leaver, C.J. (1992) Regulation of mitochondrial function and biogenesis in cucumber (Cucumis sativus L.) cotyledons during early seedling growth. Plant Physiol. 99: 60-66.
29. +-dependem isocitrale dehydrogenases, ammonium assimilation and NADPH production. Plant Physiol. Biochem. 41: 577-585.
30. Horsch, R.B., Fry, J., Hoffmann, N., Neidermeyer, J., Rogers, S.G. and Fraley, R.T. (1988) Leaf disc transformation. In Plant Molecular Biology Manual. Edited by Gelvin, S.B. and Schilperoort, R.A. pp. A5, 1-9. Kluwer Academic Publishers, Dordrecht.
31. Konrad, A., Banze, M. and Follmann, H. (1996) Mitochondria of plant leaves contain two thioredoxins. Completion of the thioredoxin profile of higher plants. J. Plant Physiol. 149: 317-321.
32. Laemmli, U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685.
33. Laloi, C., Rayapuram, N., Chattier, Y., Grienenberger, J.-M., Bonnard, G. and Meyer, Y. (2001) Identification and characterization of a mitochondrial thioredoxin system in plants. Proc. Natl Acad. Sci. USA 98: 14144-14149.
34. Lumbers, H. (1982) Cyanide-resistant respiration: a nonphosphorylating electron transport pathway acting as an energy overflow. Physiol. Plant. 55: 478-485.
35. Lancien, M., Ferrario-Méry, S., Roux, Y., Bismuth, E., Masclaux, C., Hirel, B., Gadal, P. and Hodges, M. (1999) Simultaneous expression of NAD-dependent isocitrate dehydrogenase and other Krebs cycle genes after nitrate resupply to short-term nitrogen-starved tobacco. Plant Physiol. 120: 717-725.
36. Lancien, M., Gadal, P. and Hodges, M. (1998) Molecular characterization of higher plant NAD-dependent isocitrate dehydrogenase: evidence for a heteromeric structure by the complementation of yeast mutants. Plant J. 16: 325-333.
37. Landschütze, V., Müller-Röber, B. and Willmitzer, L. (1995a) Mitochondrial citrate synthase from potato: predominant expression in mature leaves and young flower buds. Planta 196: 756-764.
38. Landschütze, V., Willmitzer, L. and Müller-Röber, B. (1995b) Inhibition of flower formation by antisense repression of mitochondrial citrate synthase in transgenic potato plants leads to a specific disintegration of the ovary tissues of flowers. EMBO J. 14: 660-666.
39. Levings, C.S. III and Siedow, J.N. (1995) Regulation by redox poise in chloroplasts. Science 268: 695-696.
40. Lowry, O.H., Rosebrough, N.J., Farr, A.L. and Randall, R.J. (1951) Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193: 265-275.
41. MacDougall, A.J. and ap Rees, T. (1991) Control of the Krebs cycle in Arum spadix. J. Plant Physiol. 137: 683-690.
42. Mackenzie, S. and McIntosh, L. (1999) Higher plant mitochondria. Plant Cell 11: 571-585.
43. Maxwell, D.P., Wang, Y. and McIntosh, L. (1999) The alternative oxidase lowers mitochondrial reactive oxygen production in plant cells. Proc. Natl Acad. Sci. USA 96: 8271-8276.
44. McIntosh, L., Eichler, T., Gray, G.R., Maxwell, D., Nickels, R. and Wang, Y. (1998) Biochemical and genetic controls exerted by plant mitochondria. Biochim. Biophys. Acta 1365: 278-284.
45. Millar, A.H., Atkin, O.K., Menz, R.I., Henry, B., Farquhar, G. and Day, D.A. (1998) Analysis of respiratory chain regulation in roots of soybean seedlings. Plant Physiol. 117: 1083-1093.
46. Millenaar, F.F., Gonzàlez-Meler, M.A., Fiorani, F., Welschen, R., Ribas-Carbo, M., Siedow, J.N., Wagner, A.M. and Lambers, H. (2001) Regulation of alternative oxidase activity in six wild monocotyledonous species. An in vivo study at the whole root level. Plant Physiol. 126: 376-387.
47. Millenaar, F.F., Gonzalez-Meler, M.A., Siedow, J.N., Wagner, A.M. and Lambers, H. (2002) Role of sugars and organic acids in regulating the concentration and activity of the alternative oxidase in Poa annua roots. J. Exp. Bot. 53: 1081-1088.
48. Møller, I.M. (2001) Plant mitochondria and oxidative stress: Electron transport, NADPH turnover, and metabolism of reactive oxygen species. Annu. Rev. Plant Physiol. Plant Mol. Biol. 52: 561-591.
49. Møller, I.M. and Rasmusson, A.G. (1998) The role of NADP in the mitochondrial matrix. Trends Plant Sci. 3: 21-27.
50. Oliver, D.J. and McIntosh, C.A. (1995) The biochemistry of the mitochondrial matrix. In The Molecular Biology of Plant Mitochondria. Edited by Levings, C.S. III and Vasil, I.K. pp. 237-280. Kluwer Academic Publishers, Dordrecht.
51. Omran, R.G. and Dennis, D.T. (1971) Nicotinamide adenine dinucleotide phosphate-specific isocitrate dehydrogenase from a higher plant. Plant Physiol. 47: 43-47.
52. Popova, T.N. and de Carvalho, M.A.A.P. (1998) Citrate and isocitrate in plant metabolism. Biochim. Biophys. Acta 1364: 307-325.
53. Rasmusson, A.G. and Møller, I.M. (1990) NADP-utilizing enzymes in the matrix of plant mitochondria. Plant Physiol. 94: 1012-1018.
54. Sambrook, J., Fritsch, E.F. and Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual, 2nd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, U.S.A.
55. Siedow, J.N. and Umbach, A.L. (1995) Plant mitochondrial electron transfer and molecular biology. Plant Cell 7: 821-831.
56. Simons, B.H., Millenaar, F.F., Mulder, L., Van Loon, L.C. and Lambers, H. (1999) Enhanced expression and activation of the alternative oxidase during infection of Arabidopsis with Pseudomonas syringae pv tomato. Plant Physiol. 120: 529-538.
57. Towbin, H., Staehelin, T. and Gordon, J. (1979) Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc. Natl Acad. Sci. USA 76: 4350-4354.
58. Umbach, A.L. and Siedow, J.N. (1993) Covalent and noncovalent dimers of the cyanide-resistant alternative oxidase protein in higher plant mitochondria and their relationship to enzyme activity. Plant Physiol. 103: 845-854.
59. Umbach, A.L. and Siedow, J.N. (1997) Changes in the redox state of the alternative oxidase regulatory sulfhydryl/disulfide system during mitochondrial isolation: implications for inferences of activity in vivo. Plant Sci. 123: 19-28.
60. Vanlerberghe, G.C., Day, D.A., Wiskich, J.T., Vanlerberghe, A.E. and McIntosh, L. (1995) Alternative oxidase activity in tobacco leaf mitochondria. Dependence on tricarboxylic acid cycle-mediated redox regulation and pyruvate activation. Plant Physiol. 109: 353-361.
61. Vanlerberghe, G.C. and McIntosh, L. (1992a) Lower growth temperature increases alternative pathway capacity and alternative oxidase protein in tobacco. Plant Physiol. 100: 115-119.
62. Vanlerberghe, G.C. and McIntosh, L. (1992b) Coordinate regulation of cytochrome and alternative pathway respiration in tobacco. Plant Physiol. 100: 1846-1851.
63. Vanlerberghe, G.C. and McIntosh, L. (1994) Mitochondrial electron transport regulation of nuclear gene expression. Studies with the alternative oxidase gene of tobacco. Plant Physiol. 105: 867-874.
64. Vanlerberghe, G.C. and McIntosh, L. (1996) Signals regulating the expression of the nuclear gene encoding alternative oxidase of plant mitochondria. Plant Physiol. 111: 589-595.
65. Vanlerberghe, G.C. and McIntosh, L. (1997) Alternative oxidase: from gene to function. Annu. Rev. Plant Physiol. Plant Mol. Biol. 48: 703-734.
66. Vanlerberghe, G.C., McIntosh, L. and Yip, J.Y.H. (1998) Molecular localization of a redox-modulated process regulating plant mitochondrial electron transport. Plant Cell 10: 1551-1560.
67. Vanlerberghe, G.C., Vanlerberghe, A.E. and McIntosh, L. (1994) Molecular genetic alteration of plant respiration. Silencing and overexpression of alternative oxidase in transgenic tobacco. Plant Physiol. 106: 1503-1510.
68. Vanlerberghe, G.C., Vanlerberghe, A.E. and McIntosh, L. (1997) Molecular genetic evidence of the ability of alternative oxidase to support respiratory carbon metabolism. Plant Physiol. 113: 657-661.
69. Vanlerberghe, G.C., Yip, J.Y.H. and Parsons, H.L. (1999) In organello and in vivo evidence of the importance of the regulatory sulfhydryl/disulfide system and pyruvate for alternative oxidase activity in tobacco. Plant Physiol. 121: 793-803.
70. Verwoerd, T.C., Dekker, B.M.M. and Hoekema, A. (1989) A small scale procedure for the rapid isolation of plant RNAs. Nucleic Acids Res. 17: 2362.
71. Wiskich, J.T. and Dry, I.B. (1985) The tricarboxylic acid cycle in plant mitochondria: Its operation and regulation. In Encyclopedia of Plant Physiology, New Series, vol. 18, Higher Plant Cell Respiration. Edited by Douce, R. and Day, D.A. pp. 281-313. Springer-Verlag, Berlin.