Structure and regulation of ferredoxin-dependent glutamase synthase from Arabidopsis thaliana. Cloning of cDNA, expression in different tissues of wild-type and gltS mutant strains, and light induction

European Journal of Biochemistry

Volumn 243, Issue 3, 1997, Pages 708-718

  Suzuki, A ^a   Rothstein, S ^a  

^a CEMAGREF   (France)

Author keywords

Arabidopsis thaliana; cDNA sequence; Glutamate synthase; Light dependence gene expression

Indexed keywords

COMPLEMENTARY DNA; GLUTAMATE SYNTHASE;

AMINO ACID SEQUENCE; ARABIDOPSIS; ARTICLE; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME INDUCTION; GENE EXPRESSION; ILLUMINATION; IMMUNOBLOTTING; IN VITRO STUDY; MOLECULAR CLONING; MUTANT; NUCLEOTIDE SEQUENCE; PLANT LEAF; PRIORITY JOURNAL;

ARABIDOPSIS THALIANA; BACTERIA (MICROORGANISMS); TRIXIS; ZEA MAYS;

EID: 0031033456     PISSN: 00142956     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1432-1033.1997.00708.x     Document Type: Article

References (71)

1. Adman, E. T., Sieker, L. C. & Jensen, L. H. (1973) The structure of a bacterial ferredoxin, J. Biol. Chem. 248, 3987–3996.
2. Anderson, M. P., Vance, C. P., Heichel, G. H. & Miller, S. S. (1989) Purification and characterization of NADH‐glutamate synthase from alfalfa root nodules, Plant Physiol. (Bethesda) 90, 351–358.
3. Atkins, C. A., Pate, J. S., People, M. B. & Joy, K. W. (1983) Amino acid transport and metabolism in relation to the nitrogen economy of a legume leaf, Plant Physiol. (Bethesda) 71, 841–848.
4. Boland, M. J. & Benny, A. G. (1977) Enzymes of nitrogen metabolism in legume nodules. Purification and properties of NADH‐dependent glutamate synthase from lupin nodules, Eur. J. Biochem. 79, 355–362.
5. Botella, J. R., Verbelen, J. P. & Valpuesta, V. (1988) Immunocytolocalization of ferredoxin‐GOGAT in cells of green leaves and cotyledons of Lycopersicon esculentum, Plant Physiol. (Bethesda) 87, 255–257.
6. Bradford, M. M. (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.
7. Carlberg, I. & Nordlund, S. (1991) Purification and partial characterization of glutamate synthase from Rhosospirillum rubrum grown under nitrogen‐fixing conditions, Biochem. J. 279, 151–154.
8. Castaño, I., Bastarrachea, F. & Covarrubias, A. A. (1988) gltBDF operon of Escherichia coli, J. Biol. Chem. 170, 821–827.
9. Chen, F. L. & Cullimore, J. V. (1988) Two isoenzymes of NADH‐dependent glutamate synthase in root nodules of Phaseolus vulgaris, Plant Physiol. (Bethesda) 88, 1411–1417.
10. Chou, P. Y. & Fasman, G. D. (1978) Empirical predictions of protein conformation, Annu. Rev. Biochem. 47, 351–376.
11. Cogoni, C., Valenzuela, L., González‐Halphen, D., Olivera, H., Macino, G., Ballario, P. & González, A. (1995) Saccharomyces cerevisiae has a single glutamate synthase gene coding for a plant‐like high‐molecular‐weight polypeptide, J. Bacteriol. 177, 792–798.
12. Crawford, N. M. & Arst, H. N. (1993) The molecular genetics of nitrate assimilation in fungi and plants, Annu. Rev. Genet. 27, 115–146.
13. Ernes, W. J. & Fowler, M. W. (1979) The intracellular location of the enzymes of nitrate assimilation in the apices of seedling pea roots, Planta (Heidelb.) 144, 249–253.
14. Fentem, P. A., Lea, P. J. & Stewart, G. R. (1983) Ammonia assimilation in the roots of nitrate‐ and ammonia‐grown Hordeum vulgare (cv. Golgen promise), Plant Physiol. (Bethesda) 71, 496–501.
15. Forsman, C. & Pilon, M. (1995) Chloroplast import and sequential maturation of pea carbonic anhydrase: the roles of various parts of the transit peptide, FEBS Lett. 358, 39–42.
16. Galván, F., Márquez, A. J. & Vega, J. M. (1984) Purification and molecular properties of ferredoxin‐glutamate synthase from Chlamydomonas reinhardtii, Planta (Heidelb.) 162, 180–187.
17. Garcíarrubio, A., Lozaya, E., Covarrubias, A. A. & Bolivar, F. (1983) Structural organization of the genes that encode the two glutamate synthase subunits of Escherichia coli K12, Gene (Amst.) 26, 165–170.
18. González, A., Membrillo‐Hernández, J., Olivera, H., Aranda, C., Macino, G. & Ballario, P. (1992) Cloning of yeast gene coding for the glutamate synthase small subunit (GUS2) by complementation of Saccharomyces cerevisiae and Escherichia coli glutamate auxotrophs, Mol. Microbiol. 6, 301–308.
19. Goodall, G. J. & Filipowicz, W. (1991) Different effects of intron nucleotide composition and secondary structure on pre‐mRNA splicing in monocot and dicot plants, EMBO J. 9, 2635–2644.
20. Gregerson, R. G., Miller, S. S., Twary, S. N., Gantt, J. S. & Vance, C. P. (1993) Molecular characterization of NADH‐dependent glutamate synthase from alfalfa nodules, Plant Cell 5, 215–226.
21. Hayakawa, T., Yamaya, T., Kamachi, K. & Ojima, K. (1992) Purification, characterization, and immunological properties of NADH‐dependent glutamate synthase from rice cell cultures, Plant Physiol. (Bethesda) 1317–1322.
22. Hemmilä, I. A. & Mäntsälä, P. I. (1978) Purification and properties of glutamate synthase and glutamate dehydrogenase from Bacillus megaterium, Biochem. J. 173, 45–52.
23. Henikoff, S. (1987) Unidirectional digestion with exonuclease III in DNA sequence analysis, Methods Enzymol. 155, 156–165.
24. Hirasawa, M., Hurley, J. K., Salamon, Z., Tollin, G. & Knaff, D. B. (1996) Oxidation‐reduction and transient kinetic studies of spinach ferredoxin‐dependent glutamate synthase, Arch. Biochem. Biophys. 330, 209–215.
25. Hummlet, G. & Mora, J. (1980) Regulation and function of glutamate synthase, Biochem. Biophys. Res. Commun. 96, 1688–1694.
26. Jones, J. D. G., Dunsmuir, P. & Bedbrook, J. (1985) High level expression of introduced chimaeric genes in regenerated transformed plants, EMBO J. 4, 2411–2418.
27. Karlin‐Neumann, G. A. & Tobin, E. M. (1986) Transit peptides of nuclear‐encoded chloroplast proteins share a common amino acid framework, EMBO J. 5, 9–13.
28. Keegstra, K., Olsen, L. J. & Theg, S. M. (1989) Chloroplastic precursors and their transport across the envelope membranes, Annu. Rev. Plant Physiol. Plant Mol. Biol. 40, 471–501.
29. Laemmli, U. K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4, Nature 227, 680–685.
30. Lam, H.‐M., Coschigano, K. T., Oliveira, I. C., Melo‐Oliveira, R. & 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.
31. Lam, H.‐M., Cashigano, K., Schultz, C., Melo‐Oliveira, R., Tjaden, G., Oliveira, I., Ngai, N., Hsieh, M.‐H. & Coruzzi, G. (1995) Use of Arabidopsis mutants and genes to study amide amino acid biosynthesis, Plant Cell 7, 887–898.
32. Lea, P. J. & Miflin, B. J. (1974) Alternative route for nitrogen assimilation in higher plants, Nature 251, 614–616.
33. Lea, P. J., Robinson, S. A. & Stewart, G. R. (1990) The enzymology and metabolism of glutamine, glutamate and asparagine, in The biochemistry of plants ( Miflin, B. J. & Lea, P. J., eds) pp. 121–159, vol. 16, Academic Press, New York, London.
34. Lederer, F., Cortial, S., Becam, A.‐M., Haumont, P.‐Y. & Perez, L. (1985) Complete amino acid sequence of flavocytochrome b 2 from baker's yeast, Eur. J. Biochem. 152, 419–428.
35. Majeau, N. & Coleman, J. R. (1992) Isolation and characterization of a cDNA coding for pea chloroplastic carbonic anhydrase, Plant Physiol. (Bethesda) 95, 264–268.
36. Marqués, S., Florencio, F. J. & Candau, P. (1992) Purification and characterization of the ferredoxin‐glutamate synthase from the unicellular cyanobacterium Synechococus sp. PCC 6301, Eur. J. Biochem. 206, 69–77.
37. Masters, D. S. & Meister, A. (1982) Inhibition by homocysteine sulfonamide of glutamate synthase purified from Saccharomyces cerevisiae, J. Biol. Chem. 257, 8711–8715.
38. Matoh, T. & Takahashi, E. (1982) Changes in the activities of ferredoxin‐and NADH‐glutamate synthase during seedling development of peas, Planta (Heidelb.) 154, 289–294.
39. Mei, B. & Zalkin, H. (1989) A cystein‐histidine‐aspartate catalytic triad is involved in glutamine amide transfer function in purF ‐type glutamine amidotransferases, J. Biol. Chem. 264, 16613–16619.
40. Miflin, P. J. & Lea, P. J. (1975) Glutamine and asparagine as nitrogen donors for reductant‐dependent glutamate synthesis in pea roots, Biochem. J. 149, 403–409.
41. Miflin, B. J. & Lea, P. J. (1982) Ammonia assimilation and amino acid metabolism, in Encyclopedia of plant physiology ( Boulter, C. & Parthier, B., eds) pp. 3–64, vol. 14A, Springer‐Verlag, Berlin.
42. Miller, R. E. & Standtman, E. R. (1972) Glutamate synthase from Escherichia coli, J. Biol. Chem. 247, 7407–7419.
43. Mishkind, M., Wessler, S. R. & Schmidt, G. W. (1985) Functional determinants in transit sequences: import and partial maturation by vascular plant chloroplasts of the ribulose‐1,5–‐bisphosphate carboxylase small subunit of Chlamydomonas, J. Cell Biol. 100, 226–234.
44. Morris, P. F., Layzell, D. B. & Canvin, D. T. (1988) Ammonia production and assimilation in glutamate synthase mutants of Arabidopsis thaliana, Plant Physiol. (Bethesda) 87, 148–154.
45. Mösinger, E., Batschauer, A., Schäfer, E. & Apel, K. (1985) Phytochrome control of in vivo transcription of specific genes in isolated nuclei from barley (Hordeum vulgare), Eur J. Biochem. 147, 137–142.
46. Murashige, J. & Skoog, F. (1962) A revised medium for rapid growth and bio assay with tobacco tissue culture, Physiol. Plant. 115, 473–497.
47. Murray, M. G. & Thompson, W. F. (1980) Rapid isolation of high molecular weight plant DNA, Nucleic Acids Res. 8, 4321–4325.
48. Navarro, F., Chávez, S., Candau, P. & Florencio, F. J. (1995) Existence of two ferredoxin‐glutamate synthases in the cyanobacterium Synechocystis sp. PCC 6803. Isolation and insertional inactivation of gltB and gltS genes, Plant Mol. Biol. 27, 753–767.
49. Oliver, G., Cosset, G., Sanchez‐Pescador, R., Lozoya, E., Ku, L. M., Flores, N., Becerril, B., Vall, F. & Bolivar, F. (1987) Determination of the nucleotide sequence for the glutamate synthase structural genes of Escherichia coli K‐12, Gene (Amst.) 60, 1–11.
50. Pate, J. S. (1980) Transport and partitioning of nitrogenous solutes, Annu. Rev. Plant Physiol. 31, 313–340.
51. Pelanda, R., Vanoni, M. A., Perego, M., Piubelli, L., Galizzi, A., Curti, B. & Zanetti, G. (1993) Glutamate synthase genes of the diazotroph Azospirillum brasilense, J. Biol. Chem. 268, 3099–3106.
52. Peterman, T. K. & Goodman, H. M. (1991) The glutamine synthetase gene family of Arabidopsis thaliana: light‐regulation and differential expression in leaves, roots, and seeds, Mol. & Gen. Genet. 230, 145–154.
53. Pilon, M., Wienk, H., Sips, W., de Swaaf, M., Talboom, I., van't Hof, R., de Korte‐Kool, G., Demel, R., Weisbeek, P. & de Kruijff, B. (1995) Functional domains of the ferredoxin transit sequence involved in chloroplast import, J. Biol. Chem. 270, 3882–3893.
54. Ratti, S., Curti, B., Zanetti, G. & Galli, E. (1985) Purification and characterization of glutamate synthase from Azospirillum brasilense, J. Bacteriol. 163, 724–729.
55. Reith, M. & Munholland, J. (1993) A high‐resolution gene map of the chloroplast genome of the red alga Porphyra purpurea, Plant Cell 5, 465–475.
56. Sakakibara, H., Watanabe, M., Hase, T. & Sugiyama, T. (1991) Molecular cloning and characterization of complementary DNA encoding for ferredoxin‐dependent glutamate synthase in maize leaf, J. Biol. Chem. 266, 2028–2035.
57. Sambrook, J., Fritsch, E. F. & Maniatis, T. (1989) Molecular cloning: a laboratory manual, 2nd edn, Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
58. Sanger, F., Nicklen, S. & Coulson, A. R. (1977) DNA sequencing with chain‐terminating inhibitors, Proc. Natl Acad. Sci. USA 74, 5463–5467.
59. Somerville, C. R. & Ogren, W. L. (1980) Inhibition of photosynthesis in Arahidopsis mutants lacking in leaf glutamate synthase activity, Nature 286, 257–259.
60. Suzuki, A., Gadal, P. & Oaks, A. (1981) Intracellular distribution of enzymes associated with nitrogen assimilation in roots, Planta (Heidelb.) 15, 457–461.
61. Suzuki, A., Burkhart, W. & Rothstein, S. (1996) Nitrogen effects on the induction of ferredoxin‐dependent glutamate synthase and its mRNA in maize leaves under the light, Plant. Sci. 114, 83–91.
62. Suzuki, A., Vidal, J., Nguyen, J. & Gadal, P. (1984) Occurrence of ferredoxin‐dependent glutamate synthase in plant cell fraction of soybean root nodules (Glycine max), FEBS Lett. 173, 204–208.
63. Suzuki, A., Oaks, A., Jacquot, J. P., Vidal, J. & Gadal, P. (1985) An electron donor system in maize roots for reactions of glutamate synthase and nitrite reductase. Physiological and immunological properties of the electron donor and pyridine nucleotide reductase, Plant Physiol. (Bethesda) 78, 374–378.
64. Suzuki, A., Vergnet, C., Morot‐Gaudry, J. F., Zehnacher, C. & Grosclaude, J. (1994) Immunological characterization of ferredoxin and methyl viologen interacting domains of glutamate synthase using monoclonal antibodies. Plant Physiol. Biochem. (Montrouge) 32, 619–626.
65. Towbin, H., Staehelin, T. & Gordon, J. (1979) Electrophoretic transfer of proteins from plyacrylamide gels to nitrocellulose sheets: procedure and some applications, Proc. Natl Acad. Sci. USA 76, 4350–4354.
66. Trotta, P. P., Platzer, K. E. B., Haschemeyer, R. H. & Meister, A. (1974) Glutamine binding subunits of glutamate synthase and partial reactions catalyzed by this glutamine amidotransferase, Proc. Natl Acad. Sci. USA 71, 4607–4611.
67. Valentin, K., Kostzewa, M. & Zetsche, K. (1993) Glutamate synthase is plastid‐encoded in a red alga: implications for the evolution of glutamate synthases, Plant Mol. Biol. 23, 77–85.
68. Vanoni, M. A., Edmondson, D. E., Zanetti, G. & Curti, B. (1992) Characterization of the flavins and the iron‐sulfur centers of glutamate synthase from Azospirillum brasilense by absorption circular dichroism, and electron paramagnetic resonance spectroscopies, Biochemistry 31, 4613–4623.
69. Vanoni, M. A., Verzotti, E., Zanetti, G. & Curti, B. (1996) Properties of the recombinant β subunit of glutamate synthase, Eur. J. Biochem. 236, 937–946.
70. von Heijne, G., Steppuh, J. & Herrmann, R. G. (1989) Domain structure of mitochondrial and chloroplast targeting peptides, Eur. J. Biochem. 180, 535–545.
71. Wallsgrove, R. M., Lea, P. J. & Miflin, P. J. (1982) The development of NAD(P) H‐dependent and ferredoxin‐dependent glutamate synthases in greening barley and pea leaves, Planta (Heidelb.) 154, 473–476.