Oxidative turnover of soybean root glutamine synthetase. In vitro and in vivo studies

Plant Physiology

Volumn 119, Issue 4, 1999, Pages 1483-1495

  Ortega, Jose Luis ^a   Roche, Dominique ^a,b   Sengupta Gopalan, Champa ^a  

^a NEW MEXICO STATE UNIVERSITY   (United States)

^b AGRICULTURAL RESEARCH SERVICE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; AMMONIUM NITRATE; ASSIMILATION; ENZYME METABOLISM; GENETIC TRANSCRIPTION; GLUTAMINE SYNTHETHASE; GLYCINE MAX; OXIDATION; PLANT PRODUCT;

EID: 0032793014     PISSN: 00320889     EISSN: None     Source Type: Journal    
DOI: 10.1104/pp.119.4.1483     Document Type: Article

References (71)

1. Aguirre J, Hansberg W (1986) Oxidation of Neurospora crassa glutamine synthetase. J Bacteriol 166: 1040-1045
2. Allen RD (1995) Dissection of oxidative stress tolerance using transgenic plants. Plant Physiol 107: 1049-1050
3. Bennett MJ, Lightfoot DA, Cullimore JV (1989) cDNA sequence and differential expression of the gene encoding the glutamine synthetase γ polypeptide of Phaseolus vulgaris L. Plant Mol Biol 12: 553-565
4. Bradford 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
5. Cervera J, Levine RL (1988) Modulation of the hydrophobicity of glutamine synthetase by mixed-function oxidation. FASEB J 2: 2591-2595
6. Climent I, Levine RL (1991) Oxidation of the active site of glutamine synthetase: conversion of arginine-344 to γ-glutamyl semialdehyde. Arch Biochem Biophys 289: 371-375
7. Cock JM, Brock IW, Watson AT, Swarup R, Morby AP, Cullimore JV (1991) Regulation of glutamine synthetase genes in leaves of Phaseolus vulgaris. Plant Mol Biol 17: 761-771
8. Cock JM, Hermon P, Cullimore JV (1992) Characterization of a gene encoding the plastid-located glutamine synthetase of Phaseolus vulgaris: regulation of β-glucuronidase gene fusions in transgenic tobacco. Plant Mol Biol 18: 1141-1149
9. Cullimore JV, Lara M, Lea PJ, Miflin BJ (1983) Purification and properties of two forms of glutamine synthetase from the plant fraction of Phaseolus root nodules. Planta 157: 245-253
10. Dalton DA (1995) Antioxidant defenses of plants and fungi. In S Ahmad, ed, Oxidative Stress and Antioxidant Defenses in Biology. Chapman & Hall, New York, pp 298-355
11. De Vries SC, Springer J, Wessels JGH (1982) Diversity of abundant mRNA sequences and patterns of protein synthesis in etiolated and greened pea seedlings. Planta 156: 120-135
12. del Rio LA, Pastori GM, Palma JM, Sandalio LM, Sevilla F, Corpas FJ, Jiménez A, López-Huertas E, Hernández JA (1998) The activated oxygen: role of peroxisomes in senescence. Plant Physiol 116: 1195-1200
13. Edwards JW, Walker EL, Coruzzi GM (1990) Cell-specific expression in transgenic plants reveals nonoverlapping roles for chloroplast and cytosolic glutamine synthetase. Proc Natl Acad Sci USA 87: 3459-3463
14. Farber JM, Levine RL (1986) Sequence of a peptide susceptible to mixed-function oxidation. Probable cation binding site in glutamine synthetase. J Biol Chem 261: 4574-4578
15. Ferguson AR, Sims AP (1971) Inactivation in vivo of glutamine synthetase and NAD-specific glutamate dehydrogenase. Its role in the regulation of glutamine synthesis in yeast. J Gen Microbiol 69: 423-427
16. Forde BG, Day HM, Turton JF, Shen W-J, Cullimore JV, Oliver JE (1989) Two glutamine synthetase genes from Phaseolus vulgaris L. display contrasting developmental and spatial patterns of expression in transgenic Lotus corniculatus plants. Plant Cell 1: 391-401
17. Foyer CH, Descourvieres P, Kunert KJ (1994) Protection against oxygen radicals: an important defense mechanism studied in transgenic plants. Plant Cell Environ 17: 507-523
18. Fulks RM, Stadtman ER (1985) Regulation of glutamine synthetase, aspartokinase and total protein turnover in Klebsiella arogenes. Biochim Biophys Acta 843: 214-229
19. 2 fixation, carbon metabolism, and oxidative damage in nodules of dark-stressed common bean plants. Plant Physiol 113: 1193-1201
20. Grune T, Reinheckel T, Davies KJ (1997) Degradation of oxidized proteins in mammalian cells. FASEB J 11: 526-534
21. Harding SA, Oh S-H, Roberts DM (1997) Transgenic tobacco expressing a foreign calmodulin gene shows an enhanced production of active oxygen species. EMBO J 16: 1137-1144
22. Hirel B, Bouet C, King B, Layzell D, Jacobs F, Verma DPS (1987) Glutamine synthetase genes are regulated by ammonia provided externally or by symbiotic nitrogen fixation. EMBO J 6: 1167-1171
23. Hoelzle I, Finer JJ, McMullen MD, Streeter JG (1992) Induction of glutamine synthetase activity in nonnodulated roots of Glycine max, Phaseolus vulgaris, and Pisum sativum. Plant Physiol 100: 525-528
24. Hopfner M, Reifferscheid G, Wild A (1988) Molecular composition of glutamine synthetase of Sinapis alba L. Z Naturforsch 43C: 194-198
25. Humanes L, Garcia-Fernandez JM, Lopez-Ruiz A, Diez J (1995) Glutamine synthetase from the green alga Monoraphidium braunii is regulated by oxidative modification. Plant Sci 110: 269-277
26. 2+ and substrate interactions with glutamine synthetase from Escherichia coli. J Biol Chem 255: 590-593
27. Iturbe-Ormaetxe I, Escuredo PR, Arrese-Igor C, Becana M (1998) Oxidative damage in pea plants exposed to water deficit or paraquat. Plant Physiol 116: 173-181
28. Kim KH, Rhee SG (1988) Sequence of peptides from Saccharomyces cerevisiae glutamine synthetase. N-terminal peptide and ATP-binding domain. J Biol Chem 263: 833-838
29. Kimura K, Sugano S (1992) Inactivation of Bacillus subtilis glutamine synthetase by metal-catalyzed oxidation. J Biochem 112: 828-833
30. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 27: 680-685
31. Landgraf P, Ohmann E, Tschiersch H (1997) Light induced oxidative stress in Euglena gracilis. Photosynthetica 33: 433-442
32. Lara M, Porta H, Padilla J, Folch J, Sánchez F (1984) Heterogeneity of glutamine synthetase polypeptides in Phaseolus vulgaris L. Plant Physiol 76: 1019-1023
33. Levine RL (1983a) Oxidative modification of glutamine synthetase. I. Inactivation is due to loss of one histidine residue. J Biol Chem 258: 11823-11827
34. Levine RL (1983b) Oxidative modification of glutamine synthetase. II. Characterization of the ascorbate model system. J Biol Chem 258: 11828-11833
35. Levine RL, Oliver CV, Fulks RM, Stadtman ER (1981) Turnover of bacterial glutamine synthetase: oxidative inactivation precedes proteolysis. Proc Natl Acad Sci USA 78: 2120-2124
36. Liaw S-H, Villafranca JJ, Eisenberg D (1993) A model for oxidative modification of glutamine synthetase, based on crystal structures of mutant H269N and the oxidized enzyme. Biochemistry 32: 7999-8003
37. Low PS, Merida JR (1996) The oxidative burst in plant defense: function and signal transduction. Physiol Plant 96: 533-542
38. Mack G, Tischner R (1990) Glutamine synthetase oligomers and isoforms in sugarbeet (Beta vulgaris). Planta 181: 10-17
39. Martin G, Haehnel W, Böger P (1997) Oxidative inactivation of glutamine synthetase from the cyanobacterium Anabaena variabilis. J Bacteriol 179: 730-734
40. Miao GH, Hirel B, Marsolier MC, Redge RW, Verma DPS (1991) Ammonia-regulated expression of a soybean gene encoding cytosolic glutamine synthetase in transgenic Lotus corniculatus. Plant Cell 3: 11-22
41. Morey KJ (1997) Transcriptional regulation of the glutamine synthetase gene family in soybean: characterization of cis-acting elements involved in the differential expression of individual GS gene family members. PhD dissertation. New Mexico State University, Las Cruces
42. Morrissey JH (1981) Silver stain for proteins in polyacrylamide gels: a modified procedure with enhanced uniform sensitivity. Anal Biochem 117: 307-310
43. Nakamura K, Stadtman ER (1984) Oxidative inactivation of glutamine synthetase subunits. Proc Natl Acad Sci USA 81: 2011-2015
44. Netto LES, Stadtman ER (1996) The iron-catalyzed oxidation of dithiothreitol is a biphasic process: hydrogen peroxide is involved in the initiation of a free radical chain of reactions. Arch Biochem Biophys 333: 233-242
45. O'Farrell PH (1975) High resolution two-dimensional electrophoresis of proteins. J Biol Chem 250: 4007-4021
46. Pell EJ, Schlagnhaufer CD, Arteca RN (1997) Ozone-induced oxidative stress: mechanism of action and reaction. Physiol Plant 100: 264-273
47. Pesole G, Bozzetti MP, Lanave C, Preparata G, Saccone C (1991) Glutamine synthetase gene evolution: a good molecular clock. Proc Natl Acad Sci USA 88: 522-526
48. Rao MV, Paliyath G, Ormod DP, Murr DP, Watkins CB (1997) Influence of salicylic acid on hydrogen peroxide production, oxidative stress and hydrogen peroxide-metabolizing enzymes. Plant Physiol 115: 137-149
49. Rhee SG, Kim K, Kim IH, Stadtman ER (1990) Protein that prevents mercaptan-mediated protein oxidation. Methods Enzymol 186: 478-485
50. Rivett AJ, Levine RL (1990) Metal-catalyzed oxidation of Escherichia coli glutamine synthetase: correlation of structural and functional changes. Arch Biochem Biophys 278: 26-34
51. Roche D (1994) Regulation of glutamine synthetase activity in roots and nodules of soybeans - synthesis, assembly and turnover. PhD dissertation. New Mexico State University, Las Cruces
52. Roche D, Temple SJ, Sengupta-Gopalan C (1993) Two classes of differentially regulated glutamine synthetase genes are expressed in the soybean nodule: a nodule-specific class and a constitutively expressed class. Plant Mol Biol 22: 971-983
53. Roseman JE, Levine RL (1987) Purification of a protease from Escherichia coli with specificity for oxidized glutamine synthetase. J Biol Chem 262: 2101-2110
54. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular Cloning. A Laboratory Manual, Ed 2. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
55. Sanangelantoni AM, Barbarini D, Di Pasquale G, Cammarano P, Tiboni O (1990) Cloning and nucleotide sequence of an archaebacteria glutamine synthetase gene: phylogenetic implications. Mol Gen Genet 221: 187-194
56. Shatters RG, Kahn ML (1989) Glutamine synthetase II in Rhizobium: reexamination of the proposed horizontal transfer of DNA from eukaryotes to prokaryotes. J Mol Evol 29: 422-428
57. Stadtman ER (1990) Discovery of glutamine synthetase cascade. Methods Enzymol 182: 793-809
58. Stadtman ER, Berlett BS (1997) Reactive oxygen-mediated protein oxidation in aging and disease. Chem Res Toxicol 10: 485-494
59. Stadtman ER, Oliver CN (1991) Metal-catalyzed oxidation of proteins. Physiological consequences. J Biol Chem 266: 2005-2008
60. Stewart GR, Mann AF, Fentem PA (1980) Enzymes of glutamate formation: glutamate dehydrogenase, glutamine synthetase and glutamate synthase. In BJ Miflin, ed, The Biochemistry of Plants, Vol 5. Academic Press, New York, pp 271-327
61. Sukanya R, Li M-G, Snustad DP (1994) Root- and shoot-specific responses of individual glutamine synthetase genes of maize to nitrate and ammonium. Plant Mol Biol 26: 1935-1946
62. Tate SS, Meister A (1971) Regulation of rat liver glutamine synthetase: activation by alpha-ketoglutarate and inhibition by glycine, alanine, and carbamyl phosphate. Proc Natl Acad Sci USA 68: 781-785
63. Temple SJ, Heard J, Ganter G, Dunn K, Sengupta-Gopalan C (1995) Characterization of a nodule-enhanced glutamine synthetase from alfalfa: nucleotide sequence, in situ localization and transcript analysis. Mol Plant-Microbe Interact 8: 218-227
64. Temple SJ, Knight TJ, Unkefer PJ, Sengupta-Gopalan C (1993) Modulation of glutamine synthetase gene expression in tobacco by the introduction of an alfalfa glutamine synthetase gene in sense and antisense orientation: molecular and biochemical anaylsis. Mol Gen Genet 236: 315-325
65. Temple SJ, Kunjibettu S, Roche D, Sengupta-Gopalan C (1996) Total glutamine synthetase activity during soybean nodule development is controlled at the level of transcription and holoprotein turnover. Plant Physiol 112: 1723-1733
66. Temple SJ, Sengupta-Gopalan C (1997) Manipulating amino acid biosynthesis. In CH Foyer, WP Quick, eds, A Molecular Approach to Primary Metabolism in Higher Plants. Taylor & Francis, London, pp 155-177
67. Tischer E, Das Sarma S, Goodman HM (1986) Nucleotide sequence of an alfalfa glutamine synthetase gene. Mol Gen Genet 203: 221-229
68. Villafranca JJ, Ranson SC, Gibbs EJ (1985) Biophysical studies of Escherichia coli glutamine synthetase. Curr Top Cell Regul 26: 207-219
69. Walker EL, Coruzzi GM (1989) Developmentally regulated expression of the gene family for cytosolic glutamine synthetase in Pisum sativum. Plant Physiol 91: 702-708
70. Watson AT, Cullimore JV (1996) Characterization of the expression of glutamine synthetase gln-α gene of Phaseolus vulgaris using promoter-reporter gene fusions in transgenic plants. Plant Sci 120: 139-151
71. Yamashita MM, Almassey RJ, Janson CA, Cascio D, Eisenberg D (1989) Refined atomic model of glutamine synthetase at 3.5 Å resolution. J Biol Chem 264: 17681-17690