Nitrate acts as a signal to induce organic acid metabolism and repress starch metabolism in tobacco

Plant Cell

Volumn 9, Issue 5, 1997, Pages 783-798

  Scheible, Wolf Rüdiger ^a   González Fontes, Agustin ^a,e   Lauerer, Marianne ^b   Müller Röber, Bernd ^c   Caboche, Michel ^d   Stitt, Mark ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b UNIVERSITY OF BAYREUTH   (Germany)

^c MAX PLANCK INSTITUTE OF MOLECULAR PLANT PHYSIOLOGY   (Germany)

^d CEMAGREF   (France)

^e UNIVERSITY OF CÓRDOBA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

NICOTIANA TABACUM;

EID: 2642677675     PISSN: 10404651     EISSN: None     Source Type: Journal    
DOI: 10.1105/tpc.9.5.783     Document Type: Article

References (77)

1. Bergmeyer, H.U. (1989). Citrate. In Methods of Enzymatic Analysis, Vol. 7 (Weinheim, Germany: Verlag Chemie), pp. 2-24.
2. Bernier, G., Havelange, A., Houssa, C., Petitjean, A., and Lejeune, P. (1993). Physiological signals that induce flowering. Plant Cell 5, 1147-1155.
3. Champigny, M.L., and Foyer, C.H. (1992). Nitrate activation of cytosolic protein kinases diverts photosynthetic carbon from sucrose to amino acid biosynthesis. Basis for a new concept. Plant Physiol. 100, 7-12.
4. + assimilation on sucrose synthesis in leaves. J. Plant Physiol. 139, 361-368.
5. Cheng, C.L., Acedo, G.N., Dewdney, J., Goodman, H.M., and Conkling, M.A. (1991). Differential expression of two Arabidopsis nitrate reductase genes. Plant Physiol. 96, 275-279.
6. Chollet, R., Vidal, J., and O'Leary, M.H. (1996). Phosphoenolpyruvate carboxylase: A ubiquitous, highly regulated enzyme in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 47, 273-298.
7. Crawford, N.M. (1994). Metabolic and genetic control of nitrate, phosphate and iron assimilation in plants. In Arabidopsis, E.M. Meyerowitz and C.R. Somerville, eds (Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press), pp. 1119-1146.
8. Crawford, N.M. (1995). Nitrate: Nutrient and signal for plant growth. Plant Cell 7, 859-868.
9. Crawford, N.M., and Arst, H.N., Jr. (1993). The molecular genetics of nitrate assimilation in fungi and plants. Annu. Rev. Genet. 27,115-146.
10. Drew, M.C., and Saker, L.R. (1975). Nutrient supply and the growth of the seminal root system in barley. II. Localized compensatory changes in lateral root growth and the rates of nitrate uptake when nitrate is restricted to only one part of the root system. J. Exp. Bot. 26, 79-90.
11. Dubois, F., Brugière, N., Sangwan, R.S., and Hirel, B. (1996). Localization of tobacco cytosolic glutamine synthetase enzymes and the corresponding transcripts show organ- and cell-specific patterns of protein synthesis and gene expression. Plant Mol. Biol. 31, 803-817.
12. Duff, S.M.G., and Chollet, R. (1995). In vivo regulation of wheat-leaf phosphoenolpyruvate carboxylase by reversible phosphorylation. Plant Physiol. 107, 775-782.
13. Fernandez, E., and Cardenas, J. (1989). Genetics and regulatory aspects of nitrate assimilation in algae. In Molecular and Genetic Aspects of Nitrate Assimilation, J.L. Wray and J.L. Kinghorn, eds (Oxford, UK: Oxford Science Publications), pp. 101-124.
14. Fichtner, K., and Schulze, E.-D. (1992). The effect of nitrogen nutrition on annuals originating from habitats of different nitrogen availability. Oecologia 92, 236-241.
15. +-dependent isocitrate dehydrogenase from potato. Plant Physiol. 107, 905-913.
16. Foyer, C.H., and Ferrario, S. (1994). Modulation of carbon and nitrogen metabolism in transgenic plants with a view to improved biomass production. Biochem. Soc. Trans. 22, 909-915.
17. Foyer, C.H., Champigny, M.L., Valadier, M.H., and Ferrario, S. (1996). Partitioning of photosynthetic carbon: The role of nitrate activation of protein kinases. In Proceedings of the Phytochemical Society of Europe, P. Shewry, N. Halford, and R. Hooley, eds (Oxford, UK: Clarendon Press), pp. 35-51.
18. Galangau, F., Daniel-Vedèle, F., Moureaux, T., Dorbe, M.F. Leydecker, M.T., and Caboche, M. (1988). Expression of leaf nitrate reductase genes from tomato and tobacco in relation to light dark regimes and nitrate supply. Plant Physiol. 88, 383-388.
19. Gebauer, G., Melzer, A., and Rehder, H. (1984). Nitrate content and nitrate reductase activity in Rumex obtusifolia L. I. Differences in organs and diurnal changes. Oecologia 92, 236-241.
20. Geigenberger, P., Lerchl, J., Stitt, M., and Sonnewald, U. (1996). Phloem-specific expression of pyrophosphatase inhibits long-distance transport of carbohydrates and amino acids in tobacco plants. Plant Cell Environ. 19, 43-55.
21. Gowri, G., Ingemarsson, B., Redinbaugh, M.G., and Campbell, W.H. (1992). Nitrate reductase transcript is expressed in the primary response of maize to environmental nitrate. Plant Mol. Biol. 18, 55-64.
22. Granato, T.C., and Raper, C.D., Jr. (1989). Proliferation of maize roots in response to localized supply of nitrate. J. Exp. Bot. 40, 263-275.
23. Hanning, I., and Heldt, H.W. (1993). On the function of mitochondrial metabolism during photosynthesis in spinach (Spinacia oleracea L.) leaves. Plant Physiol. 103, 1147-1154.
24. Hayakawa, T., Yamaya, T., Kamachi, K., and Ojima, K. (1992). Purification, characterization and immunological properties of NADH-dependent glutamate synthase from rice cell cultures. Plant Physiol. 98, 1317-1322.
25. Hecht, U., Oelmüller, R., Schmidt, S., and Mohr, H. (1988). Action of light, nitrate and ammonium on the levels of NADH- and ferredoxin-dependent glutamate synthase in the cotelydons of mustard seedlings. Planta 175, 130-138.
26. Hehl, G., and Mengel, K. (1972). Der Einfluss einer variierten Kalium- und Stickstoffdüngung auf den Kohlenhydratgehalt verschiedener Futterpflanzen. Landwirtsch. Forsch. Sonderh. 27, 117-129.
27. Hoff, T., Truong, H.-N., and Caboche, M. (1994). The use of mutants and transgenic plants to study nitrate assimilation. Plant Cell Environ. 17, 489-506.
28. Hofstra, R., Lanting, L., and De Visser, R. (1985). Metabolism of Urtica dioica as dependent on the supply of mineral nutrients. Physiol. Plant. 63, 13-18.
29. Huber, S.C., and Huber, J.L. (1996). Role and regulation of sucrose-phosphate-synthase in higher plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 47, 431-444.
30. Huppe, H.C., and Turpin, D.H. (1994). Integration of carbon and nitrogen metabolism in plant and algal cells. Annu. Rev. Plant Physiol. Plant Mol. Biol. 45, 577-607.
31. Imsande, J., and Touraine, B. (1994). Nitrogen demand and the regulation of nitrate uptake. Plant Physiol. 105, 3-7.
32. Jackson, W.A., Flesher, D., and Hageman, R.H. (1973). Nitrate uptake by dark-grown corn seedlings: Some characteristics of apparent induction. Plant Physiol. 51, 120-127.
33. Kaiser, W.M., and Huber, S.C. (1994). Posttranslational regulation of nitrate reductase in higher plants. Plant Physiol. 106, 817-821.
34. Koch, K.E. (1996). Carbohydrate modulated gene expression in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 47, 509-540.
35. Krapp, A., Hofmann, B., Schäfer, C., and Stitt, M. (1993). Regulation of the expression of rbcS and other photosynthetic genes by carbohydrates: A mechanism for the "sink-regulation" of photosynthesis? Plant J. 3, 817-828.
36. Kronenberger, J., Lepingle, A., Caboche, M., and Vaucheret, H. (1993). Cloning and expression of distinct nitrite reductases in tobacco leaves and roots. Mol. Gen. Genet. 236, 203-208.
37. Lainé, P., Ourry, A., and Boucaud, J. (1995). Shoot control of nitrate uptake rates by roots of Brassica napus L.: Effects of localized nitrate supply. Planta 196, 77-83.
38. Lam, H.M., Coshigano, K., Oliveira, I., Melo-Oliveira, R., and Coruzzi, G. (1996). The molecular genetics of nitrogen assimilation into amino acids in higher plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 47, 569-593.
39. Lambers, H., Cambridge, M.L., Konings, H., and Pons, T.L. (1990). Causes and Consequences of Variation in Growth Rate and Productivity of Higher Plants. (The Hague, The Netherlands: SPB Academic Publishing bv).
40. Lauerer, M. (1996). Wachstum, Kohlenstoff- und Stickstoffhaushalt von Nicotiana tabacum mit reduzierter Nitratreduktaseaktivität. In Bayreuther Forum Ökologie, Vol. 31 (Bayreuth, Germany: Bayreuther Institut für Terrestrische Ökosystemforschung), pp. 1-177.
41. Lea, P.J., Blackwell, R.D., Chen, F.-L., and Hecht, U. (1990). Enzymes of ammonia assimilation. In Methods in Plant Biochemistry, Vol. 3, P.J. Lea, ed (London: Academic Press Limited), pp. 257-276.
42. Li, B., Zhang, X.-Q., and Chollet, R. (1996). Phosphoenolpyruvate carboxylase kinase in tobacco leaves is activated by light in a similar but not identical way as in maize. Plant Physiol. 111, 497-505.
43. Lin, Y., Hwang, C.-F., Brown, J.B., and Cheng, C.L. (1994). 5′ Proximal regions of Arabidopsis nitrate reductase genes direct nitrate-induced transcription in transgenic tobacco. Plant Physiol. 106, 477-484.
44. Marschner, M. (1995). Mineral Nutrition of Higher Plants, 2nd ed. (London: Academic Press Limited).
45. Marzluf, G.A. (1993). Regulation of sulfur and nitrogen metabolism in filamentous fungi. Annu. Rev. Microbiol. 47, 31-55.
46. Moorhead, G., Douglas, P., and MacKintosh, C. (1996). Phosphorylated nitrate reductase from spinach leaves is inhibited by 14-3-3 proteins and activated by fusicoccin. Curr. Biol. 6, 1104-1113.
47. Müller, A., and Mendel, R. (1989). Biochemical and somatic cell genetics of nitrate reduction in Nicotiana. In Molecular and Genetic Aspects of Nitrate Assimilation, J.L. Wray and J.L. Kinghorn, eds (Oxford, UK: Oxford Science Publications), pp. 166-185.
48. Müller-Röber, B.T., Kossmann, J., Hannah, C.L., Willmitzer, L., and Sonnewald, U. (1990). One of the two ADP-glucose pyrophosphorylase genes from potato responds strongly to elevated levels of sucrose. Mol. Gen. Genet. 224, 136-146.
49. Pouteau, S., Chérel, I., Vaucheret, H., and Caboche, M. (1989). Nitrate reductase mRNA regulation in Nicotiana plumbaginifolia nitrate reductase-deficient mutants. Plant Cell 1, 1111-1120.
50. Preiss, J., Ball, K., Smith-White, B., Inglesias, A., Kakefuda, G., and Li, L. (1991). Starch biosynthesis and its regulation. Biochem. Soc. Trans. 19, 539-547.
51. Quesada, A., Krapp, A., Daniel-Vedèle, F., Fernández, E., Forde, B., and Caboche, M. (1997). A general strategy to identify nitrate transporters from Chlamydomonas reinhardtii: Cloning of ntr2:1 Np from Nicotiana plumbaginifolia. Plant Mol. Biol., in press.
52. Radin, J.W., and Eidenbock, M.P. (1986). Carbon accumulation during photosynthesis in leaves of nitrogen- and phosphorus-stressed cotton. Plant Physiol. 82, 869-871.
53. Rastogi, R., Back, E., Schneiderbauer, A., Bowsher, C.G., Moffatt, B., and Rothstein, S.J. (1993). A 330-bp region of the spinach nitrite reductase gene promoter directs nitrate-inducible tissue-specific expression in transgenic tobacco. Plant J. 4, 317-326.
54. Redinbaugh, M.G., and Campbell, W.H. (1991). Higher plant responses to environmental nitrate. Physiol. Plant. 82, 640-650.
55. Redinbaugh, M.G., and Campbell, W.H. (1993). Glutamine synthetase and ferredoxin-dependent glutamate synthase expression in the maize (Zea mays) root: Primary response to nitrate. Plant Physiol. 101, 1249-1255.
56. Reimholz, R., Krause, K.P., Geiger, M., Haake, V., Deiting, U., Sonnewald, U., and Stitt, M. (1997). Potato plants contain multiple forms of sucrose-phosphate synthase, that show differences in their tissue distribution, their response during development, and their response to low temperature. Plant Cell Environ. 20, 291-305.
57. Ritchie, S.W., Redinbaugh, M.G., Shiraishi, N., Verba, J.M., and Campbell, W.H. (1994). Identification of a maize root transcript expressed in the primary response to nitrate: Characterization of a cDNA with homology to ferredoxin-NADP(+) oxidoreductase. Plant Mol. Biol. 26, 679-690.
58. Rufty, T.W., Huber, S.C., and Volk, R.J. (1988). Alterations in leaf carbohydrate metabolism in response to nitrogen stress. Plant Physiol. 88, 725-730.
59. Sakakibara, H., Watanabe, M., Hase, T., and Sugiyama, T. (1991). Molecular cloning and characterization of complementary DNA encoding ferredoxin-dependent glutamate synthase in maize leaf. J. Biol. Chem. 266, 2028-2035.
60. Scheible, W.-R., Lauerer, M., Schulze, E.-D., Caboche, M., and Stitt, M. (1997a). Accumulation of nitrate in the shoot acts as a signal to regulate shoot-root allocation in tobacco. Plant J., in press.
61. Scheible, W.-R., González-Fontes, A., Morcuende, R., Lauerer, M., Geiger, M., Glaab, J., Gojon, A., Schulze, E.-D., Caboche, M., and Stitt, M. (1997b). Tobacco mutants with a decreased number of functional nia-genes compensate by modifying the diurnal regulation of transcription, post-translational modification and turnover of nitrate reductase. Planta, in press.
62. Shaner, D.L., and Boyer, J.S. (1976). Nitrate reductase activity in maize (Zea mays L.) leaves. I. Regulation by nitrate flux. Plant Physiol. 58, 499-504.
63. Siddiqi, M.Y., Glass, A.D.M., Ruth, T.J., and Rufty, T.W. (1990). Studies of the uptake of nitrate in barley. Plant Physiol. 93, 1426-1432.
64. Smith, A.M. (1990). Enzymes of starch synthesis. In Methods in Plant Biochemistry, Vol. 3, P.J. Lea, ed (London: Academic Press Limited), pp. 93-102.
65. Stitt, M., and Schulze, E.-D. (1994). Does Rubisco control the rate of photosynthesis and plant growth? An exercise in molecular ecophysiology. Plant Cell Environ. 17, 465-487.
66. Stitt, M., Lilley, R.M., Gerhardt, R., and Heldt, H.W. (1989). Metabolite levels in specific cells and subcellular compartments of plant leaves. Methods Enzymol. 174, 518-552.
67. Sugiharto, B., and Sugiyama, T. (1992). Effects of nitrate and ammonium on gene expression of phosphoenolpyruvate carboxylase and nitrogen metabolism in maize leaf tissue during recovery from nitrogen stress. Plant Physiol. 98, 1403-1408.
68. Sugiharto, B., Suzuki, I., Burnell, J.N., and Sugiyama, T. (1992). Glutamine induces the nitrogen-dependent accumulation of mRNAs encoding phosphoenolpyruvate carboxylase and carbonic anhydrase in detached maize leaf tissue. Plant Physiol. 100, 2066-2070.
69. Sukanya, R., Li, M.G., and Snustad, D.P. (1994). Root- and shoot-specific responses of individual glutamine synthetase genes of maize to nitrate and ammonia. Plant Mol. Biol. 26, 1935-1946.
70. Trueman, L.J., Richardson, A., and Forde, B.G. (1996). Molecular cloning of higher plant homologues of the high affinity nitrate transporters of Chlamydomonas reinhardtii and Aspergillus nidulans. Gene 175, 223-231.
71. - enhances the kinase activity for phosphorylation of phosphoenolpyruvate carboxylase and sucrose phosphate synthase proteins in wheat leaves. Plant Physiol. 99, 344-347.
72. Vaucheret, H., and Caboche, M. (1995). Induction of nitrate reductase host gene expression has a negative effect on the expression of transgenes driven by the nitrate reductase promotor. Plant Sci. 107, 95-104.
73. Vaucheret, H., Chabaud, M., Kronenberger, J., and Caboche, M. (1990). Functional complementation of tobacco and Nicotiana plumbaginifolia nitrate reductase deficient mutants by transformation with the wild-type alleles of the tobacco structural genes Mol. Gen. Genet. 220, 468-474.
74. - in barley root cells using triple-barraled, ion-selective microelectrodes. Plant Physiol. 108, 743-751.
75. Waring, R.H., McDonald, A.J.S., Larsson, S., Ericsson, T., Wiren, A., Arwidsson, E., Ericsson, A., and Lohammar, T. (1985). Differences in chemical composition of plants grown at constant relative growth rates with stable mineral nutrition. Oecologia 66, 157-160.
76. Wray, J.L. (1993). Molecular biology, genetics and regulation of nitrite reduction in higher plants. Physiol. Plant. 89, 607-612.
77. Wray, J.L., and Fido, R.J. (1990). Nitrate reductase and nitrite reductase. In Methods in Plant Biochemistry, Vol. 3, P.J. Lea, ed (London: Academic Press Limited), pp. 241-256.