Antisense inhibition of NADH glutamate synthase impairs carbon/nitrogen assimilation in nodules of alfalfa (Medicago sativa L.)

Plant Journal

Volumn 33, Issue 6, 2003, Pages 1037-1049

  Cordoba, Elizabeth ^a   Shishkova, Svetlana ^a   Vance, Carroll P ^b,c   Hernández, Georgina ^a  

^a INSTITUTO DE CIENCIAS FÍSICAS   (Mexico)

^b UNIVERSITY OF MINNESOTA   (United States)

^c AGRICULTURAL RESEARCH SERVICE   (United States)

Author keywords

Antisense transgenic alfalfa; C N metabolism in nodules; NADH glutamate synthase; S. meliloti alfalfa symbiosis; Symbiotic N fixation

Indexed keywords

CATALYSIS; GROWTH KINETICS; METABOLISM; NITROGEN FIXATION; PHOTOSYNTHESIS; RNA;

NITROGEN ASSIMILATION;

ENZYMES;

AMINO ACID OXIDOREDUCTASES; ANTISENSE ELEMENTS (GENETICS); CARBON; GENE EXPRESSION REGULATION, PLANT; GLUTAMATE SYNTHASE (NADH); MEDICAGO SATIVA; MYCORRHIZAE; NITROGEN; PHENOTYPE; PLANTS, GENETICALLY MODIFIED; SYMBIOSIS;

EMBRYOPHYTA; FUNGI; GLYCINE MAX; MEDICAGO; MEDICAGO SATIVA; SINORHIZOBIUM; SINORHIZOBIUM MELILOTI;

EID: 0037355214     PISSN: 09607412     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-313X.2003.01686.x     Document Type: Article

References (59)

1. Allaway, D., Lodwig, E.M., Crompton, L.A., Wood, M., Parsons, R., Wheeler, T.R. and Poole, P.S. (2000) Identification of alanine dehydrogenase and its role in mixed secretion of ammonium and alanine by pea bacteroids. Mol. Microbiol. 36, 508-515.
2. Anderson, M.P., Vance, C.P., Heichel, G.H. and Miller, S.S. (1989) Purification and characterization of NADH-glutamate synthase from alfalfa root nodules. Plant Physiol. 90, 351-358.
3. Appleby, C.A. (1984) Leghemoglobin and Rhizobium respiration. Annu. Rev. Plant Physiol. 35, 443-478.
4. Arrese-Igor, C., Minchin, F.R., Gordon, A.J. and Nath, A.K. (1997) Possible causes of the decline in soybean nitrogen fixation in the presence of nitrate. J. Exp. Bot. 48, 905-914.
5. Austin, S., Bingham, E.T., Matthews, D.E., Shahan, M.N., Will, J. and Burgess, R.R. (1995) Production and field performance of transgenic alfalfa (Medicago sativa L.) expressing alpha-amylase and manganese-dependent lignin peroxidase. Euphytica, 85, 381-393.
6. Avila, C., Marquez, A.J., Pajuelo, P., Cannell, M.E., Wallsgrove, R.M. and Forde, B.G. (1993) Cloning and sequence analysis of a cDNA for barley ferredoxin-dependent glutamate synthase and molecular analysis of photorespiratory mutants deficient in the enzyme. Planta, 189, 475-483.
7. Bevan, M. (1984) Binary Agrobacterium vectors for plant transformation. Nucl. Acids Res. 12, 8711-8721.
8. Blake, N.R., Ditterline, R.L. and Stout, R.G. (1991) Polymerase chain reaction used for monitoring multiple gene integration in Agrobacterium-mediated transformation. Crop Sci. 31, 1686-1688.
9. 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.
10. Brosius, J. (1989) Laboratory methods. Superpolylinkers in cloning and expression vectors. DNA, 8, 759-777.
11. Broughton, W.J. and Dilworth, M. (1971) Control of leghemoglobin synthesis in snake beans. Biochem. J. 125, 1075-1080.
12. de Brujin, F.J., Felix, G., Grunenberg, B., Hoffmann, H.J., Mets, B., Rater, P., Simons-Schreier, A., Szabados, L., Welters, P. and Schell, J. (1989) Regulation of plant genes specifically induced in nitrogen-fixing nodules: role of cis-acting elements and transacting factors in leghemoglobin gene expression. Plant Mol. Biol. 13, 319-325.
13. Cevallos, M.A., Encarnación, S., Leija, A., Mora, Y. and Mora, J. (1996) Genetic and physiological characterization of a Rhizobium etli mutant strain unable to synthesize poly-β-hydroxybutyrate. J. Bacteriol. 178, 1646-1654.
14. Christensen, T., Sandal, N.N., Stougaard, J. and Marcker, K.A. (1989) 5′ Flanking sequence of the soybean leghemoglobin Ibc3 gene. Nucl. Acids Res. 17, 4383.
15. Coruzzi, G.M. and Zhou, L. (2001) Carbon and nitrogen sensing and signalling in plants: emerging 'matrix effects'. Curr. Opin. Plant Biol. 4, 247-253.
16. Deroche, M.E., Carrayol, E. and Jolivet, E. (1983) Phosphoenolpyruvate carboxylase in legume nodules. Physiol. Veg. 21, 1075-1081.
17. Egli, M.A., Griffith, S.M., Miller, S.S., Anderson, M.P. and Vance, C.P. (1989) Nitrogen assimilating enzyme activities and enzyme protein during development and senescence of effective and plants gene-controlled ineffective alfalfa nodules. Plant Physiol. 91, 898-904.
18. Fedorova, M., Tikhonovich, I.A. and Vance, C.P. (1999) Expression of C-assimilating enzymes in pea (Pisum sativum L.) root nodules. In situ localization in effective nodules. Plant Cell Environ. 22, 1249-1262.
19. Ferguson, A.R. and Sims, A.P. (1971) Inactivation in vivo of glutamine synthetase and NAD-specific glutamate dehydrogenase: its role in the regulation of glutamine synthesis in yeasts. J. Gen. Microbiol. 69, 423-427.
20. Ferrario-Méry, S., Suzuki, A., Kunz, C., Valadier, M.H., Roux, V., Hirel, B. and Foyer, C.H. (2000) Modulation of amino acid metabolism in transformed tobacco plants deficient in Fd-GOGAT. Plant Soil, 221, 67-79.
21. 2 enrichment of plants grown in pots and in hydroponic culture. Planta, 202, 510-521.
22. Gordon, A.J. (1992) Carbon metabolism in the legume nodule. In Carbon Partitioning within and between Organisms. (Pollock, C.J., Farrar, J.F., Gordon, A.J., eds), Oxford: Bios Scientific Publishers, pp. 133-162.
23. Gordon, A.J. and Kessler, W. (1990) Defoliation-induced stress in nodules of white clover. Immunological and enzymic measurements of key proteins. J. Exp. Bot. 41, 1255-1262.
24. Gordon, A.J., Minchin, F.R., James, C.L. and Komina, O. (1999) Sucrose synthase in legume nodules is essential for nitrogen fixation. Plant Physiol. 120, 867-877.
25. 2 fixation are related to nodule sucrose synthase activity. Plant Physiol. 114, 937-946.
26. Graan, T. and Ort, D.O. (1984) Quantitation of the rapid electron donors to P700 the functional plastiquinone pool and the ratio of the photosystems in spinach chloroplasts. J. Biol. Chem. 250, 1403-1410.
27. Gregerson, R.G., Miller, S.S., Twary, S.N., Gantt, J.S. and Vance, C.P. (1993) Molecular characterization of NADH-dependent glutamate synthase from alfalfa nodules. Plant Cell, 5, 215-226.
28. Griffith, S.M. and Vance, C.P. (1989) Aspartate aminotransferase in alfalfa root nodules. Purification and partial characterization. Plant Physiol. 90, 1622-1629.
29. Groat, G.R. and Vance, C.P. (1981) Root and nodule enzymes of ammonia assimilation in alfalfa (Medicago sativa L.). Plant Physiol. 67, 1198-1205.
30. Harrison, J., Brugière, N., Phillipson, B., Ferrario-Méry, S., Becker, T., Limami, A. and Hirel, B. (2000) Manipulating the pathway of ammonia assimilation through genetic engineering and breeding: consequences to plant physiology and plant development. Plant Soil, 221, 81-93.
31. Jefferson, R.A., Kavanagh, T.A. and Bevan, M.W. (1987) GUS fusions: β-glucoronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J. 6, 3901-3907.
32. Lam, H.M., Coschigano, K.T., Oliveira, I.C., Melo-Oliveira, R. and Coruzzi, G.M. (1996) The molecular-genetics of nitrogen assimilation into amino acids in higher plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 47, 569-593.
33. Lea, P.J. and Forde, B.G. (1994) The use of mutants and transgenic plants to study amino acid metabolism. Plant Cell Environ. 17, 541-556.
34. Lee, N.G., Stein, B., Suzuki, H. and Verma, D.P.S. (1993) Expression of antisense nodulin-35 RNA in Vigna aconitifolia transgenic roots nodules retards peroxisome development and affects nitrogen availability to the plant. Plant J. 3, 599-606.
35. 2. Transgenic Res. 5, 105-113.
36. Miller, S.S., Boylan, K.L.M. and Vance, C.P. (1987) Alfalfa root nodule carbon dioxide fixation. Immunological studies of nodule phosphoenol pyruvate carboxylase. Plant Physiol. 84, 501-508.
37. Morrell, M. and Copeland, L. (1985) Sucrose synthase of soybean nodules. Plant Physiol. 78, 149-164.
38. 2 diffusion in legume nodules. Plant Physiol. 113, 259-267.
39. Nogués, S., Allen, D.J., Morrison, J.I.L. and Baker, N.R. (1998) Ultraviolet-B radiation effects on water relations, leaf development and photosynthesis in droughted pea plants. Plant Physiol. 117, 173-181.
40. Oliveira, I.C., Lam, H.M., Coschigano, K., Melo-Oliveira, R. and Coruzzi, G. (1997) Molecular-genetic dissection of ammonium assimilation in Arabidopsis thaliana. Plant Physiol. Biochem. 35, 185-198.
41. Pladys, D. and Vance, C.P. (1993) Proteolysis during development and senescence of effective and plant gene-controlled ineffective alfalfa nodules. Plant Physiol. 103, 379-384.
42. Ramlov, K.B., Laursen, N.B., Stougaard, J. and Marcker, K.A. (1993) Site-directed mutagenesis of the organ-specific element in the soybean leghemoglobin lbc3 gene promoter. Plant J. 4, 577-580.
43. Schoenbeck, M.A., Temple, S.J., Trepp, G.B., Blumenthal, J.M., Samac, D.A., Gantt, J.S., Hernández, G. and Vance, C.P. (2000) Decreased NADH glutamate synthase activity in nodules and flowers of alfalfa (Medicago sativa L.) transformed with antisense glutamate synthase transgene. J. Exp. Bot. 51, 29-39.
44. Schulze, J., Shi, L., Blumenthal, J., Samac, D.A., Gantt, J.S. and Vance, C.P. (1998) Inhibition of alfalfa root nodule phosphoenolpyruvate carboxylase through an antisense strategy impacts nitrogen fixation and plant growth. Phytochemistry, 49, 341-346.
45. Sijen, T. and Kooter, J.M. (2000) Post-transcriptional gene-silencing: RNAs on the attack or on the defense? Bioessays, 22, 520-531.
46. Somerville, C.R. and Ogren, W.L. (1980) Inhibition of photosynthesis in Arabidopsis mutants lacking leaf glutamate synthase activity. Nature, 286, 257-259.
47. 2-fixation gene expression within the alfalfa root nodule. Proc. Natl. Acad. Sci. USA, 92, 3759-3763.
48. Stougaard, J., Marcker, K.A., Otten, L. and Schell, J. (1986) Nodule-specific expression of a chimeric soybean leghaemoglobin gene in transgenic Lotus corniculatus. Nature, 321, 669-674.
49. Temple, S.J., Bagga, S. and Sengupta-Gopalan, C. (1998a) Downregulation of specific members of the glutamine synthetase gene family in alfalfa by antisense technology. Plant Mol. Biol. 37, 535-547.
50. Temple, S.J., Vance, C.P. and Gantt, J.S. (1998b) Glutamate synthase and nitrogen assimilation. Trends Plant Sci. 3, 51-56.
51. Tesfaye, M., Temple, S.J., Allan, D.L., Vance, C.P. and Samac, D.A. (2001) Overexpression of malate dehydrogenase in transgenic alfalfa enhanced organic acid synthesis and confers resistance to aluminium. Plant Physiol. 127, 1836-1844.
52. Trepp, G.B., Plank, D.W., Gantt, J.S. and Vance, C.P. (1999a) NADH-glutamate synthase in alfalfa root nodules. Immunocytochemical localization. Plant Physiol. 119, 829-837.
53. Trepp, G.B., Temple, S.J., Bucciarelli, B., Shi, L.F. and Vance, C.P. (1999b) Expression map for genes involved in nitrogen and carbon metabolism in alfalfa root nodules. Mol. Plant Microbe Interact. 12, 526-535.
54. Vance, C.P., Gregerson, R.G., Robinson, D.L., Miller, S.S. and Gantt, J.S. (1994) Primary assimilation of nitrogen in alfalfa nodules: molecular features of the enzymes involved. Plant Sci. 101, 51-64.
55. 2 fixation. Plant J. 8, 345-358.
56. Vasse, J., de Billy, F., Camut, S. and Truchet, G. (1990) Correlation between ultrastructural differentiation of bacteroids and nitrogen fixation in alfalfa nodules. J. Bacteriol. 172, 4295-4306.
57. Wang, R., Guegler, K., LaBrie, S.T. and Crawford, N.M. (2000) Genomic analysis of a nutrient response in Arabidopsis reveals diverse expression patterns and novel metabolic and potential regulatory genes induced by nitrate. Plant Cell. 12, 1491-1509.
58. 2-fixing soybean nodule bacteroids. Proc. Natl. Acad. Sci. USA, 95, 12038-12042.
59. Zhang, X.Q. and Chollet, R. (1997) Phosphoenolpyruvate carboxylase protein kinase from soybean root nodules: partial purification, characterization, and up/down-regulation by photosynthate supply from the shoots. Arch. Biochem. Biophys. 343, 260-268.