Photosynthesis Research

, Volume 83, Issue 2, pp 191–217 | Cite as

Glutamate synthase: structural, mechanistic and regulatory properties, and role in the amino acid metabolism

  • Akira Suzuki
  • David B. Knaff


Ammonium ion assimilation constitutes a central metabolic pathway in many organisms, and glutamate synthase, in concert with glutamine synthetase (GS, EC, plays the primary role of ammonium ion incorporation into glutamine and glutamate. Glutamate synthase occurs in three forms that can be distinguished based on whether they use NADPH (NADPH-GOGAT, EC, NADH (NADH-GOGAT, EC or reduced ferredoxin (Fd-GOGAT, EC as the electron donor for the (two-electron) conversion of L-glutamine plus 2-oxoglutarate to L-glutamate. The distribution of these three forms of glutamate synthase in different tissues is quite specific to the organism in question. Gene structures have been determined for Fd-, NADH- and NADPH-dependent glutamate synthases from different organisms, as shown by searches in nucleic acid sequence data banks. Fd-glutamate synthase contains two electron-carrying prosthetic groups, the redox properties of which are discussed. A description of the ferredoxin binding by Fd-glutamate synthase is also presented. In plants, including nitrogen-fixing legumes, Fd-glutamate synthase and NADH-glutamate synthase supply glutamate during the nitrogen assimilation and translocation. The biological functions of Fd-glutamate synthase and NADH-glutamate synthase, which show a highly tissue-specific distribution pattern, are tightly related to the regulation by the light and metabolite sensing systems. Analysis of mutants and transgenic studies have provided insights into the primary individual functions of Fd-glutamate synthase and NADH-glutamate synthase. These studies also provided evidence that glutamate dehydrogenase (NADH-GDH, EC does not represent a significant alternate route for glutamate formation in plants. Taken together, biochemical analysis and genetic and molecular data imply that Fd-glutamate synthase incorporates photorespiratory and non-photorespiratory ammonium and provides nitrogen for transport to maintain nitrogen status in plants. Fd-glutamate synthase also plays a role that is redundant, in several important aspects, to that played by NADH-glutamate synthase in ammonium assimilation and nitrogen transport.


ammonium assimilation glutamate synthase glutamine synthetase higher plants nitrogen metabolism 



asparagine synthetase gene


circular dichroism


electron paramagnetic resonance


free energy change


entropy change


flavin adenine dinucleotide




flavin mononucleodide

Fe/S cluster

iron-sulfur cluster


ferredoxin: NADP+ oxidoreductase


glutamine amidotransferase


glutamate dehydrogenase


glutamate synthase


cytosolic (chloroplastic) glutamine synthetase gene


ferredoxin-glutamate synthase gene


NADH-glutamate synthase gene


NADPH-glutamate synthase α subunit gene


NADPH-glutamate synthase β subunit gene


glutamate synthase


Fd-glutamate synthase gene

GLUI (2)

ferredoxin-glutamate synthase 1(2) gene


cytosolic (chloroplastic/plastidial) glutamine synthetase


nitrate reductase gene


nitrite reductase gene


ribulose-l,5-bisphosphate carboxylase/oxygenase


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  1. Akashi, T, Matsumura, T, Ideguchi, T, Iwakiri, K, Kawakatsu, T, Taniguchi, I, Hase, T 1999Comparison of the electrostatic binding sites on the surface of ferredoxin for two ferredoxin-dependent enzymes, ferredoxin-NADP+ reductase and sulfite reductaseJ Biol Chem412939929405CrossRefGoogle Scholar
  2. Anderson, SL, Teakle, GR, Martino-Catt, SJ, Kay, SA 1994Circadian clock- and phytochrome-regulated transcription is conferred by a 78 bp cis-acting domain of Arabidopsis CAB2 promoterPlant J64457470CrossRefGoogle Scholar
  3. Anderson, MP, Vance, CP, Heichel, GH, Miller, SS 1989Purification and characterization of NADH-glutamate synthase from alfalfa root nodulesPlant Physiol90351358Google Scholar
  4. Andrew, M 1986The partitioning of nitrate assimilation between root and shoot of higher plantsPlant Cell Environ9511519Google Scholar
  5. Aubert, S, Bligny, R, Douce, R, Gout, E, Ratcliffe, RG, Roberts, JKM 2001Contribution of glutamate dehydrogenase to mitochondrial glutamate metabolism studied by 13C and 31P nuclear magnetic resonanceJ Exp Bot523745CrossRefPubMedGoogle Scholar
  6. Avila, C, Mrquez, AJ, Pajuelo, P, Cannell, ME, Wallsgrove, RM, Ford, BG 1993Cloning and sequence analysis of a cDNA for barley ferredoxin-dependent glutamate synthase and molecular analysis of photorespiratory mutants deficient in the enzymePlanta189475483CrossRefPubMedGoogle Scholar
  7. Bast, E 1977Utilization of nitrogen compounds and ammonia assimilation by ChromatiaceaeArch Microbiol1139194CrossRefPubMedGoogle Scholar
  8. Belitsky, BR, Janssen, PJ, Sonenshein, AL 1995Sites required for GltC-dependent regulation of Bacillus subtilis glutamate synthase expressionJ Bacteriol17756865695PubMedGoogle Scholar
  9. Binda, C, Bossi, RT, Wakatsuki, S, Arzt, S, Coda, A, Curti, B, Vanoni, MA, Mattevi, A 2000Cross-talk and ammonia channeling between active centers in the unexpected domain arrangement of glutamate synthaseStruct Fold Des1512991308CrossRefGoogle Scholar
  10. Blackwell, RD, Murray, AJS, Lea, PJ, Joy, KW 1988Photorespiratory amino donors, sucrose synthesis and the induction of CO2 fixation in barley deficient in glutamine synthetase and/or glutamate synthaseJ Exp Bot39845858Google Scholar
  11. Borello, U, Ceccarelli, E, Giuliano, G 1993Constitutive, light-responsive and circadian clock-responsive factors compete for the different Ibox elements in plant light regulated promotersPlant J4611619CrossRefPubMedGoogle Scholar
  12. Botella, JR, Verbelen, JP, Valpuesta, V 1988Immunocytolocalization of ferredoxin-GOGAT in the cells of green leaves and cotyledons of Lycopersicon esculentumPlant Physiol87255257Google Scholar
  13. Bowsher, CG, Boulton, EL, Rose, J, Nayagam, S, Emes, MJ 1992Reductant for glutamate synthase is generated by the oxidative pentose phosphate pathway in non-photosynthetic root plastidsPlant J2893898CrossRefGoogle Scholar
  14. Brenchley, JE, Baker, CA, Patil, LG 1975Regulation of ammonia assimilatory enzymes in Salmonella typhimuriumJ Bacteriol124182189PubMedGoogle Scholar
  15. Bult, CJ, White, O, Olsen, GJ, Zhou, L, Fleishman, RD, Sutton, GG, Blake, JA, Fitzgerald, LM, Clayton, RA, Gocayne, JD, Kerlavage, AR, Doygherty, BA, Tomb, J-F, Adams, MD, Reich, CI, Overbeek, R, Krikness, EF, Weinstoock, KG, Merrick, JM, Glodek, A, Scott, JL, Geoghagen, NSM, Weidman, JF, Fuhrmann, JL, Nguyen, D, Utterback, TR, Kelly, JM, Peterson, JD, Shadow, PW, Hanna, MC, Cotton, MD, Roberts, KM, Hurst, MA, Kaine, BP, Borodovsky, M, Klein, H-P, Fraser, CM, Smith, HO, Woese, CR, Venter, JC 1996Complete genome sequence of the Methanogenic archaean, Methanococcus jannaschiiScience27310581073PubMedGoogle Scholar
  16. Carlberg, I, Nordlund, S 1991Purification and partial characterization of glutamate synthase from Rhodospirillum rubrun grown under nitrogen-fixing conditionsBiochem J279151154PubMedGoogle Scholar
  17. Carvalho, H, Lescure, N, Billy, F, Chabaud, M, Lima, L, Salema, R, Cullimore, J 2000Cellular expression and regulation of the Medicago truncatula cytosolic glutamine synthetase genes in root nodulesPlant Mol Biol42741756CrossRefPubMedGoogle Scholar
  18. Castaño, I, Flores, N, Valle, F, Covarrubias, AA, Bolivar, F 1992gltF, a member of the gltBDF operon of Escherichia coli, is involved in nitrogen-regulated gene expressionMol Microbiol627332741PubMedGoogle Scholar
  19. Castillo, A, Taboada, H, Mendoza, A, Valderrama, B, Encarnacion, S, Mora, J 2000Role of GOGAT in carbon and nitrogen partitioning in Rhizobium etliMicrobiol14616271637Google Scholar
  20. Chen, F-L, Cullimore, JV 1988Two isoenzymes of NADH-dependent glutamate synthase in root nodules of Phaseolus vulgaris L. Purification, properties and activity changes during nodule development.Plant Physiol17914111417Google Scholar
  21. Chevalier, C, Bourgeois, E, Just, D, Raymond, P 1996Metabolic regulation of asparagine synthetase gene expression in maize root tipsPlant J9111CrossRefPubMedGoogle Scholar
  22. Chichkova, S, Arellano, J, Vance, CP, Hernández, G 2001Transgenic tobacco plants that overexpress alfalfa NADH-glutamate synthase have higher carbon and nitrogen contentJ Exp Bot5220792087PubMedGoogle Scholar
  23. Chiu, JY, Shargool, PD 1979Importance of glutamate synthase in glutamate synthesis by soybean cell suspension culturesPlant Physiol63409415Google Scholar
  24. Cogoni, C, Valenzuela, L, González-Halphen, D, Oliveira, H, Macino, G, Ballario, P, González, A 1995Saccharomyces cerevisiare has a single glutamate synthase gene coding for a plant-like high-molecular-weight polypeptideJ Bacteriol177797798Google Scholar
  25. Cooper, HD, Clarkson, DT 1989Cycling of amino-nitrogen and other nutrients between shoots and roots in cereals–a possible mechanism integrating shoot and root in the regulation of nutrient uptakeJ Exp Bot40753762Google Scholar
  26. Cordoba, E, Shishkaava, S, Vance, CP, Hermández, G 2003Antisense inhibition of NADH glutamate synthase impairs carbon/nitrogen assimilation in nodule alfalfa (Medicago sativa L)Plant J3310371049CrossRefPubMedGoogle Scholar
  27. Cordovilla, MP, Prez, J, Ligero, F, Lluch, C, Valpuestra, V 2000Partial purification and characterization of NADH-glutamate synthase from faba bean (Vicia faba) root nodulesPlant Sci150121128CrossRefGoogle Scholar
  28. Coruzzi, GM, Zhou, L 2001Carbon and nitrogen sensing and signaling in plants: emerging ‘matrix effects’Curr Opin Plant Biol4247253CrossRefPubMedGoogle Scholar
  29. Coschigano, K, Melo-Oliveira, R, Lim, J, Coruzzi, GM 1998Arabidopsis gls mutants and distinct Fd-GOGAT genes: implication for photorespiration and primary nitrogen assimilationPlant Cell10741752CrossRefPubMedGoogle Scholar
  30. Deane, SM, Rawling, DE 1996Cloning and sequencing of the gene for the Thiobacillus ferrooxidans ATCC33020 glutamate synthase (GOGAT) small subunit and complementation of an Escherichia coli gltD mutantGene177261263CrossRefPubMedGoogle Scholar
  31. Dincturk, HB, Knaff, DB 2000The evolution of glutamate synthaseMol Biol Rep27141148CrossRefPubMedGoogle Scholar
  32. Dose, MM, Hirasawa, M, Kleis-SanFrancisco, S, Lew, EL, Knaff, DB 1997The ferredoxin-binding site of ferredoxin:nitrite oxidoreductase. Differential chemical modification of the free enzyme and its complex with ferredoxin.Plant Physiol11410471053CrossRefPubMedGoogle Scholar
  33. Doverskog, M, Jacobsson, U, Chapman, BE, Kuchel, PW, Häggström, L 2000Determination of NADH-dependent glutamate synthase (GOGAT) in Spodoptera frugiperda (Sf9) insect cells by a selective 1H/5N NMR in vitro assayJ Bacteriol798797Google Scholar
  34. Edwards, JW, Walker, EL, Coruzzi, GM 1990Cell-specific expression in transgenic plants reveals nonoverlapping roles for chloroplast and cytosolic glutamine synthetaseProc Natl Acad Sci USA8734593463PubMedGoogle Scholar
  35. Elminger, MV, Mohr, H 1991Coaction of blue/ultraviolet-A light and light absorbed by phytochrome in controlling the appearance of ferredoxin-dependent glutamate synthase in Scot pine (Pinus sylvestris L.) seedlingsPlanta183374380Google Scholar
  36. Ely, B, Amarasinghe, ABC, Bender, RA 1978Ammonia assimilation and glutamate formation in Caulibacter crescentusJ Bacteriol133225230PubMedGoogle Scholar
  37. Ferrario-Méry, S, Suzuki, A, Kunz, C, Valadier, MH, Roux, Y, Hirel, B, Foyer, CH 2000Modulation of amino acid metabolism in transformed tobacco plants deficient in Fd-GOGATPlant Soil2216779CrossRefGoogle Scholar
  38. Ferrario-Méry, S, Valadier, MH, Godfroy, N, Miallier, D, Hirel, B, Foyer, CH, Suzuki, A 2002Diurnal changes in ammonia assimilation in transformed tobacco plants expressing ferredoxin-dependent glutamate synthase mRNA in the antisense orientationPlant Sci112524530Google Scholar
  39. Filetici, P, Martegani, MP, Valenzuela, L, González, A, Ballario, P 1996Sequence of the gene from Saccharomyces cerevisiae reveals the domain structure of yeast glutamate synthaseYeast1213591366CrossRefPubMedGoogle Scholar
  40. Fox, GG, Ratcliffe, RG, Robinson, SA, Stewart, GR 1995Evidence for deamination by glutamate-dehydrogenase in higher plantsCan J Bot7311121115Google Scholar
  41. Galván, F, Márquez, J, Vega, JM 1984Purification and molecular properties of ferredoxin-glutamate synthase from Chlamydomonas reinhardiiPlanta162180187CrossRefGoogle Scholar
  42. García-Gutiérrez, A, Cantón, FR, Gallardo, F, Sánchez-Jiménez, F, Cánovas, FM 1995Expression of ferredoxin-dependent glutamate synthase in dark-grown pine seedlingsPlant Mol Biol27115128CrossRefPubMedGoogle Scholar
  43. García-Sánchez, MI, Díaz_Quintana, A, Gotor, C, Jacquot, J-P, Rosa, M, Vega, JM 2000Homology predicted structure and functional interaction of ferredoxin from the eukaryotic alga Chlamydomonas reinhardtii with nitrite reductase and glutamate synthaseJ Biol Inorg Chem5713719CrossRefPubMedGoogle Scholar
  44. Geary, LE, Meister, A 1977On the mechanism of glutamine-dependent reductive amination of α-ketoglutarate catalyzed by glutamate synthaseJ Biol Chem25235013508PubMedGoogle Scholar
  45. Glauser, DA, Bourquin, F, Manieri, W, Schürmann, P 2004Characterization of ferredoxin:thioredoxin reductase modified by site-directed mutagenesisJ Biol Chem2791666216669CrossRefPubMedGoogle Scholar
  46. Goto, S, Akagawa, T, Kojima, S, Hayakawa, T, Yamaya, T 1998Organisation and structure of NADH-dependent glutamate synthase from rice plantsBiochim Biophys Acta1387298308PubMedGoogle Scholar
  47. Gregerson, RG, Miller, SS, Twary, SN, Gantt, JS, Vance, CP 1993Molecular characterization of NADH-dependent glutamate synthase from Alfalfa nodulesPlant Cell5215226CrossRefPubMedGoogle Scholar
  48. Grevarec G, Bouton S, Jaspard E, Riou M-T, Cliquet J-B, Suzuki A, Anis M and Limami AM (2004) Respective roles of GS/GOGAT cycle and GDH in ammonium and amino acids metabolism in germinating Medicago truncatula seeds. Planta (in press).Google Scholar
  49. Grumbles, RM 1989Inability of glutamate synthase-deficient Arabidopsis thalianaPlant Physiol Biochem27185191Google Scholar
  50. Häusler, RE, Blackwell, RD, Lea, PJ, Leegood, RC 1994Control of photosynthesis in barley leaves with reduced activities of glutamine synthetase or glutamate synthase. I. Plant characteristics and changes in nitrate, ammonium and amino acids.Planta194406417Google Scholar
  51. Hayakawa, T, Yamaya, T, Kamachi, K, Ojima, K 1992Purification, characterization, and immunological properties of NADH-dependent glutamate synthase from rice cell culturesPlant Physiol9813171322Google Scholar
  52. Hayakawa, T, Nakamura, T, Hattori, F, Mae, T, Ojima, K, Yamaya, T 1994Cellular localization of NADH-dependent glutamate synthase protein in vascular bundles of unexpanded leaf blades and young grains of rice plantsPlanta193455460CrossRefGoogle Scholar
  53. Hemmilä, IA, Mäntsälä, P 1978Purification and properties of glutamate synthase and glutamate dehydrogenase from Bacillus magateriumBiochem J1734552PubMedGoogle Scholar
  54. Hirasawa, M, Knaff, DB 1993The role of lysine and arginine residues at the ferredoxin-binding site of spinach glutamate synthaseBiochim Biophys Acta11448591Google Scholar
  55. Hirasawa, M, Boyer, JM, Gray, KA, Davis, DJ, Knaff, DB 1986The interaction of ferredoxin with chloroplast ferredoxin-linked enzymesBiochim Biophys Acta8512328Google Scholar
  56. Hirasawa, M, Boyer, MJ, Gray, KA, Davis, DJ, Knaff, DB 1987The interaction of ferredoxin-linked sulfite reductase with ferredoxinFEBS Lett221343348CrossRefGoogle Scholar
  57. Hirasawa, M, Droux, M, Gray, KA, Boyer, JM, Davis, DJ, Buchanan, BB, Knaff, DB 1988Ferredoxin-thioredoxin reductase: Properties of its complex with ferredoxinBiochim Biophys Acta93518Google Scholar
  58. Hirasawa, M, Chang, K-T, Morrow, KJ, Knaff, DB 1989Circular dichroism, binding and immunological studies of the interaction between spinach ferredoxin and glutamate synthaseBiochim Biophys Acta977150156Google Scholar
  59. Hirasawa, M, Chang, K-T, Knaff, DB 1991The interaction of ferredoxin and glutamate synthase: Cross-linking and immunological studiesArch Biochem Biophys286171177CrossRefPubMedGoogle Scholar
  60. Hirasawa, M, Robertson, DE, Ameyibor, E, Johnson, MK, Knaff, DB 1992Oxidation-reduction properties of the ferredoxin-linked glutamate synthase from spinach leafBiochim Biophys Acta1100105108PubMedGoogle Scholar
  61. Hirasawa, M, Hurley, JK, Salamon, Z, Tollin, G, Knaff, DB 1996Oxidation-reduction and transient kinetic studies of spinach ferredoxin-dependent glutamate synthaseArch Biochem Biophys330209215CrossRefPubMedGoogle Scholar
  62. Hirasawa, M, Hurley, JK, Salamon, Z, Tollin, G, Markley, JL, Cheng, H, Xia, B, Knaff, DB 1998The role of aromatic and acidic amino acids in the electron transfer reaction catalyzed by spinach ferredoxin-dependent glutamate synthaseBiochim Biophys Acta1363134136PubMedGoogle Scholar
  63. Hirasawa, M, Rubio, LM, Griffin, JL, Flores, E, Herrero, A, Li, J, Kim, S-K, Hurley, JK, Tollin, G, Knaff, DB 2004Complex formation between ferredoxin and Synechococcus ferredoxin:nitrate oxidoreductaseBiochim Biophys Acta1608155162PubMedGoogle Scholar
  64. Hirayama, C, Saito, H, Konno, K, Shinbo, H 1998Purification and characterization of NADH-dependent glutamate synthase from the silkworm fat body (Bombyx mori)Insect Biochem Mol Biol28473482CrossRefPubMedGoogle Scholar
  65. Hirose, N, Yamaya, T 1999Okadaic acid mimics nitrogen-stimulated transcription of the NADH-glutamate synthase gene in rice cell culturePlant Physiol121805812CrossRefPubMedGoogle Scholar
  66. Holden, HM, Jacobsen, BL, Hurley, JK, Tollin, G, Oh, B-H, Skjeldal, L, Chae, YK, Cheng, H, Xia, B, Markley, JL 1994Structure-function studies of [2Fe-2S] ferredoxinsJ Bioenerg Biomembr266788PubMedGoogle Scholar
  67. Hsieh, MH, Lam, H-M, Loo, FJ, Coruzzi, G 1998A PII-like protein in Arabidopsis: Putative role in nitrogen sensingProc Natl Acad Sci USA951396513970CrossRefPubMedGoogle Scholar
  68. Hummlet, J, Mora, J 1980Regulation and function of glutamate synthaseBiochem Biophys Res Commun9616881694CrossRefPubMedGoogle Scholar
  69. Hurley, JK, Cheng, H, Xia, B, Markley, JL, Medina, M, Gomez-Moreno, C, Tollin, G 1993An aromatic amino acid is required at position 65 in Anabaena ferredoxin for rapid electron transfer to ferredoxin:NADP+ reductaseJ Am Chem Soc1151169811701CrossRefGoogle Scholar
  70. Hurley, JK, Fillat, MF, Gómez-Moreno, C, Tollin, G 1996Electrostatic and hydrophobic interactions during complex formation and electron transfer in the ferredoxin/ferredoxin:NADP+ reductase system from AnabaenaJ Am Chem Soc11855265531CrossRefGoogle Scholar
  71. Hurley, JK, Weber-Main, AM, Stankovich, MT, Benning, MM, Thoden, JB, Vanhooke, JL, Holden, HM, Chae, YK, Xia, B, Cheng, H, Markley, JL, Martinez-Júlvez, M, Gómez-Moreno, C, Schmeits, JL, Tollin, G 1997Structure–function relationships in Anabaena ferredoxin: correlations between X-ray structures, reduction potentials, and rate constants of electron transfer to ferredoxin:NADP+ reductase for site-specific ferredoxin mutantsBiochemistry361110011117CrossRefPubMedGoogle Scholar
  72. Ireland, RJ, Lea, PJ 1999The enzymes of glutamine, glutamate, asparagine, and aspartate metabolismSingh, BK eds. Plant Amino Acids. Biochemistry and BiotechnologyAmerican Cyanamid CompanyPrinceton New Jersey49109Marcel Dekker, New YorkGoogle Scholar
  73. Ishiyama, K, Hayakawa, T, Yamaya, T 1998Expression of NADH-dependent glutamate synthase protein in the epidermis and epidermis of rice roots in response to the supply of nitrogenPlanta204288294CrossRefPubMedGoogle Scholar
  74. Ishiyama, K, Kojima, S, Takahashi, H, Hayakawa, T, Yamaya, T 2003Cell type distinct accumulation of mRNA and protein for NADH-dependent glutamate synthase in rice roots in response to the supply of NH4+Plant Physiol Biochem41643647CrossRefGoogle Scholar
  75. Jelesarov, I, Bosshard, HR 1994Thermodynamics of ferredoxin binding to ferredoxin:NADP+ reductase and the role of water at the complex interfaceBiochemistry331332113328PubMedGoogle Scholar
  76. Jelesarov, I, Pascalis, AR, Koppenol, WH, Hirasawa, M, Knaff, DB, Bosshard, HR 1993Ferredoxin binding site on ferredoxin:NADP+ reductase. Differential chemical modification of free and ferredoxin-bound enzyme.Eur J Biochem2165766CrossRefPubMedGoogle Scholar
  77. Jeschke, WD, Pate, JS 1991Modeling of the partitioning, assimilation and storage of nitrate within root and shoot organs of castor bean (Ricinus communis L.)J Exp Bot4210911103Google Scholar
  78. Jiang, P, Ninfa, AJ 1999Regulation of autophosphorylation of Escherichia coli nitrogen regulator II by the PII signal transduction protein.J Bacteriol18119061911PubMedGoogle Scholar
  79. Jongsareejit, B, Rahman, RNZA, Fujiwara, S, Imanaka, T 1997Gene cloning, sequencing and enzymatic properties of glutamate synthase from the hyperthermophilic archaeon Pyrococcus sp. KOD1.Mol Gen Genet254635642CrossRefPubMedGoogle Scholar
  80. Joy, KW, Blackwell, RD, Lea, PJ 1992Assimilation of nitrogen in mutants lacking enzymes of the glutamate synthase cycleJ Exp Bot43139145Google Scholar
  81. Kaneko, T, Sato, S, Kotani, H, Tanaka, A, Asamizu, E, Nakamura, Y, Miyajima, N, Hirosawa, M, Sugiura, M, Sakamoto, S, Kimura, T, Hosouchi, T, Matsuno, A, Muraki, A, Nakazaki, N, Naruo, K, Okumura, S, Shimpo, S, Takeuchi, C, Wada, T, Watanabe, A, Yamada, M, Yasuda, M, Tabata, S 1996Sequence analysis of the genome of the unicellular cyanobacterium Synechocystis sp. strain PCC6893. II. Sequence determination of the entire genome and assignment of potential protein coding regions.DNA Res3109136PubMedGoogle Scholar
  82. Kawarabayashi, Y, Sawada, M, Horikawa, H, Haikawa, Y, Hino, Y, Yamamoto, S, Sekine, M, Baba, S, Kosugi, H, Hosoyama, A, Nagai, Y, Sakai, M, Ogura, K, Otsuka, R, Nakazawa, H, Takamiya, M, Ohfuku, Y, Funahashi, T, Tanaka, T, Kudo, Y, Yamazaki, J, Kushida, N, Oguchi, A, Aoki, K, Yoshizawa, T, Nakaamura, Y, Robb, FT, Horikoshi, K, Masuchi, Y, Shizuya, H, Kikuchi, H 1998Complete sequence and gene organization of the genome of a hyper-thermophilic archaebacterium, Pyrococcus horikoshii OT3DNA Res55576PubMedGoogle Scholar
  83. Kendall, AC, Wallsgrove, RM, Hall, NP, Turner, JC, Lea, PJ 1986Carbon and nitrogen metabolisms in barley (Hordeum vulgare L.) mutants lacking ferredoxin-dependent glutamate synthasePlanta168316323CrossRefGoogle Scholar
  84. Klenk, H-P, Clayton, R, Tomb, J-F, Whaite, O, Nelson, KE, Ketchum, KA, Dodson, RJ, Gwinn, M, Hickey, EK, Peterson, J, Richardson, DL, Kerlavage, AR, Graham, DE, Krypides, NC, Fleischmann, RD, Quaxkenbush, J, Lee, NH, Sutton, GG, Gill, S, Kirkness, EF, Dougherty, BA, McKenny, K, Adams, MD, Loftus, B, Peterson, S, Reich, CI, McNeil, LK, Badger, JH, Glodek, A, Zhou, L, Overbeek, R, Gocayane, JD, Weidman, JF, McDonald, L, Utterback, T, Cotton, MD, Spriggs, T, Artiach, P, Kaine, BP, Sykes, SM, Sadow, PW, D’Andrea, KP, Bowman, C, Fujii, C, Garland, SA, Mason, TM, Olsen, GJ, Fraser, CM, Smith, HO, Woese, CR, Venter, JC 1997The compete genome sequence of the hyperthermophilic, sulphate-reducing archaeon Archaeoglobus fulgidusNature390364370CrossRefPubMedGoogle Scholar
  85. Knaff, DB 1996Ferredoxin and ferredoxin-dependent enzymesOrt, DRYocum, CF eds. Oxygenic Photosynthesis. The Light ReactionsKluwer Academic PublishersDordrecht, The Netherlands333361Google Scholar
  86. Knaff, DB, Hirasawa, M, Ameyibor, E, Fu, W, Johnson, MK 1991Spectroscopic evidence for a [3Fe-4S] cluster in spinach glutamate synthaseJ Biol Chem2661508015084PubMedGoogle Scholar
  87. Kojima, S, Kimura, M, Nozaki, Y, Yamaya, T 2000Analysis of a promoter for the NADH-glutamate synthase gene in rice (Oryza sativa): cell-type specific expression in developing organs of transgenic rice plantsAust J Plant Physiol27787793Google Scholar
  88. Kurisu, G, Kusunoki, M, Katoh, E, Yamazaki, T, Teshima, K, Onda, Y, Kimata-Ariga, Y, Hase, T 2001Structure of the electron transfer complex between ferredoxin and ferredoxin-NADP+ reductaseNat Struct Biol2117121CrossRefGoogle Scholar
  89. Lam, H-M, Peng, S-SY, Coruzzi, GM 1994Metabolic regulation of the gene encoding glutamine-dependent asparagine synthetase in Arabidopsis thalianaPlant Physiol10613641357CrossRefGoogle Scholar
  90. Lam, H-M, Coschigano, KT, Oliveira, IC, Melo-Oliveira, R, Coruzzi, GM 1996The molecular-genetics of nitrogen assimilation into amino acids in higher plantsAnnu Rev Plant Physiol Plant Mol Biol47569593CrossRefPubMedGoogle Scholar
  91. Lancien, M, Martin, M, Hsieh, M-H, Leustek, T, Goodman, H, Coruzzi, GM 2002Arabidopsis glt-T mutant defines a role for NADH-GOGAT in the non-photorespiratory ammonium assimilatory pathwayPlant J29347358CrossRefPubMedGoogle Scholar
  92. Lea, PJ, Miflin, BJ 2004Glutamate synthase and synthesis of glutamate in plantsPlant Physiol Biochem41555564CrossRefGoogle Scholar
  93. Lea, PJ, Robinson, SA, Stewart, GR 1990The enzymology and metabolism of glutamine, glutamate, and asparagineMiflin, BJLea, PJ eds. The Biochemistry of Plants, Vol 16Academic PressNew York121159Google Scholar
  94. Loulakakis, KA, Roubelakis-Angelakis, KA 1997Molecular cloning and characterization of cDNAs coding for ferredoxin-dependent glutamate synthase from Vitis viniferaPhysiol Plant101220228CrossRefGoogle Scholar
  95. Madonna, MJ, Fuchs, RL, Brenchley, JE 1985Fine structure analysis of Salmonella typhimurium glutamate synthase geneJ Bacteriol161353360PubMedGoogle Scholar
  96. Magalhães, JR, Ju, GC, Rich, PJ, Rhodes, D 1990Kinetics of 15NH4+ assimilation in Zea mays. Preliminary studies with a glutamate dehydrogenase (GDH1) null mutant. Plant Physiol94647656Google Scholar
  97. Marqués, S, Florencio, FJ, Candau, P 1992Purification and characterization of the ferredoxin-glutamate synthase from the unicellular cyanobacterium Synechococcus sp. PCC. 6301.Eur J Biochem2066977CrossRefPubMedGoogle Scholar
  98. Márquez, AJ, Galván, F, Vega, JM 1984Purification and characterization of the NADH-glutamate synthase from Chlamydomonas reinhardiiPlant Sci Lett34305314Google Scholar
  99. Martín-Figueroa, E, Navarro, F, Florencio, FJ 2000The GS-GOGAT pathway is not operative in the heterocists. Cloning and expression of glsF gene from the cyanobacterium Anabaena sp. PCC. 7120.FEBS Lett476282286CrossRefPubMedGoogle Scholar
  100. Matt, P, Geiger, M, Walch-Liu, , Engels, C, Krapp, A, Stitt, M 2001The immediate cause of the diurnal changes of nitrogen metabolism in leaves of nitrate-replete tobacco: a major imbalance between the rate of nitrate reduction and the rates of nitrate uptake and ammonium metabolism during the first part of the light periodPlant Cell Environ24177190Google Scholar
  101. Mattana, M, Coraggio, I, Brambilla, I, Bertani, A, Reggiani, R 1996Nitrate assimilation during the anaerobic germination of rice: Expression of ferredoxin-dependent glutamate synthasePlanta1997478CrossRefGoogle Scholar
  102. McKenzie, GH, Ch’Ng, AL, Gayler, KR 1979Glutamine synthetase/glutamine:α-ketoglutarate aminotransferase in chloroplasts from the marine alga Caulerpa simpliciusculaPlant Physiol63578582Google Scholar
  103. McNeil, DL, Atkins, CA, Pate, JS 1979Uptake and utilization of xylem borne amino compounds by shoot organs of a legumePlant Physiol6310761081Google Scholar
  104. Melo-Olveira, R, Oliveira, IC, Coruzzi, G 1996Arabidopsis mutant analysis and gene regulation define a non-redundant role for glutamate dehydrogenase in nitrogen assimilationProc Natl Acad Sci USA9347184723CrossRefPubMedGoogle Scholar
  105. Meyer C, Roussel H, Thibault C, Gaudon V, Dorbe M-F, Alboresi A, Truong H-N, Brun F, Zobolowska L, Krapp A and Vedele FR (2003) Regulation of the Arabidopsis transcriptome by variations in nitrogen supply. In Prioul J-L, Vidal J, Brulfert J, Miginiac-Maslow M (eds) Proceeding: Plant Biology and the Challenge of Functional Genomics, p 60. 5ème Colloque Général de la Société Française de Physio1ogie Végétale. Université de Paris 11, Orsay, France Google Scholar
  106. Miflin, BJ, Habash, DZ 2002The role of glutamine synthetase and glutamate dehydrogenase in nitrogen assimilation and possibilities for improvement in the nitrogen utilization of cropsJ Exp Bot53979987CrossRefPubMedGoogle Scholar
  107. Migge, A, Becker, TW 1996In tobacco leaves, the genes encoding the nitrate-reducing or the ammonium-assimilating enzymes are regulated differently by external nitrogen sourcesPlant Physiol Biochem34665671Google Scholar
  108. Mikami, B, Ida, S 1989Spinach ferredoxin-nitrite reductase: Characterization of catalytic activity and interaction of the enzyme with substratesJ Biochem1054750PubMedGoogle Scholar
  109. Millar, AJ, Straume, M, Chory, J, Chua, N-H, Kay, SA 1995The regulation of circadian period by phototransduction pathways in ArabidopsisScience26711631166PubMedGoogle Scholar
  110. Morales, R, Charon, M-H, Kachalova, G, Serre, L, Medina, M, Gómez-Moreno, C, Frey, M 2000A redox-dependent interaction between two electron-transfer partners involved in photosynthesisEMBO Rep1271276PubMedGoogle Scholar
  111. Murray, DM, Kennedy, IR 1980Changes in activities of enzymes of nitrogen metabolism in seedcoats and cotyledons during embryo development in pea seedsPlant Physiol66782786Google Scholar
  112. Nagatani, H, Shimizu, M, Valentine, RC 1971The mechanism of ammonia assimilation in nitrogen fixing bacteriaArch Mikrobiol79164175CrossRefPubMedGoogle Scholar
  113. Nalbantoglu, B, Hirasawa, M, Moomaw, C, Nguyen, H, Knaff, DB, Allen, R 1994Cloning and sequencing of the gene encoding spinach ferredoxin-dependent glutamate synthaseBiochim Biophys Acta1183557561PubMedGoogle Scholar
  114. Navarro, F, Chávez, S, Candau, P, Florencio, FJ 1995Existence of two ferredoxin-glutamate synthases in the cyanobacterium Synechocystis sp. PCC. 6803. Isolation and insertional inactivation of gltB and gltS genes.Plant Mol Biol27753767CrossRefPubMedGoogle Scholar
  115. Navarro, F, Martin-Figueroa, E, Candau, P, Florencio, FJ 2000Ferredoxin-dependent iron-sulfur flavoprotein from cyanobacterium Synechocystis sp. PCC 6803: Expression and assembly in Escherichia coli.Arch Biochem Biophys379267276Google Scholar
  116. Neff, MM, Fankhauser, C, Chory, J 2000Light: an indicator of time and placeGenes Dev14553590Google Scholar
  117. Oaks, A, Jones, K, Misra, S 1979A comparison of glutamate synthase obtained from maize endosperms and rootsPlant Physiol63793795Google Scholar
  118. Okon, Y, Albrecht, SL, Burris, RH 1976Carbon and ammonia metabolism of Spirillum lipoferumJ Bacteriol128592597PubMedGoogle Scholar
  119. Okuhara, H, Matsumura, T, Fujita, Y, Hase, T 1999Cloning and inactivation of genes encoding ferredoxin-and NADH-dependent glutamate synthases in the cyanobacterium Plectonema boryanum. Imbalances of nitrogen and carbon assimilations caused by deficiency of the ferredoxin-dependent enzyme.Plant Physiol1203342CrossRefPubMedGoogle Scholar
  120. Oliveira, IC, Coruzzi, GM 1999Carbon and amino acids reciprocally modulate the expression of glutamine synthetase in ArabidopsisPlant Physiol121301309CrossRefPubMedGoogle Scholar
  121. Oliveira, IC, Lam, H-M, Coschigano, K, Melo-Oliveira, R, Coruzzi, GM 1997Molecular-genetic dissection of ammonium assimilation in Arabidopsis thalianaPlant Physiol Biochem35185198Google Scholar
  122. Oliver, G, Gosset, G, Sanchez-Pescador, R, Lzoya, E, Ku, LM, Florez, N, Becerril, B, Valle, F 1987Determination of the nucleotide sequence for the glutamate synthase structural genes of Escherichia coli K-12Gene60111CrossRefPubMedGoogle Scholar
  123. Pajuelo, P, Pajuelo, E, Forde, B, Márquez, AJ 1997Regulation of the expression of ferredoxin-glutamate synthase in barleyPlanta203517525CrossRefPubMedGoogle Scholar
  124. Pate, JS 1980Transport and partitioning of nitrogen solutesAnnu Rev Plant Physiol31313340CrossRefGoogle Scholar
  125. Pate, JS, Layzell, DB 1990Energetics and biological costs of nitrogen assimilationMiflin, BJLea, PJ eds. The Biochemistry of PlantsAcademic PressNew York142Google Scholar
  126. Pelanda, R, Vanoni, MA, Perego, M, Piubelli, L, Galizzi, A, Curti, B, Zanetti, G 1993Glutamate synthase genes of the diazotroph Azospirillum brasilense. Cloning, sequencing, and analysis of functional domains.J Biol Chem26830993106PubMedGoogle Scholar
  127. Peterman, TK, Goodman, HM 1991The glutamine synthetase gene family of Arabidopsis thaliana: light-regulation and differential expression in leaves, roots and seedsMol Gen Genet230145154CrossRefPubMedGoogle Scholar
  128. Petoukhov, MV, Svergun, DI, Kornarev, PV, Ravasio, S, Heuvel, RHH, Curtis, B, Vanoni, M 2003Quaternary structure of Azospirillum brasilense NADPH-dependent glutamate synthase in solution as revealed by synchrotron radiation X-ray scatteringJ Biol Chem2782993329939CrossRefPubMedGoogle Scholar
  129. Petracek, M, Dickey, LF, Nguyen, TT, Gatz, C, Sowinsky, DA, Allen, GC, Thompson, WF 1998Ferredoxin-l mRNA is stabilized by changes in photosynthetic electron transportProc Natl Acad Sci USA9590099013CrossRefPubMedGoogle Scholar
  130. Ravasio, S, Curti, B, Vanoni, MA 2001Determination of the midpoint potential of the FAD and FMN flavin cofactors and of the 3Fe/4S cluster of glutamate synthaseBiochemistry4055335541CrossRefPubMedGoogle Scholar
  131. Ravasio, S, Dossena, L, Martin-Figueroa, E, Florencio, FJ, Mattevi, A, Morandi, P, Curti, B, Vanoni, MA 2002Properties of recombinant ferredoxin-dependent glutamate synthase of Synechocystis PCC6803. Comparison with the Azospirillum brasilense NADPH-dependent enzyme and its isolated α subunit.Biochemistry4181208133CrossRefPubMedGoogle Scholar
  132. Ratcliffe, RG, Shachar-Hill, Y 2001Probing plant metabolism with NMRAnnu Rev Plant Physiol Plant Mol Biol52499526CrossRefPubMedGoogle Scholar
  133. Redinbaugh, MG, Campbell, WH 1993Glutamine synthetase and ferredoxin-dependent glutamate synthase expression in the maize (Zea mays) root primary response to nitratePlant Physiol10112491255PubMedGoogle Scholar
  134. Reith, M, Munholland, J 1993A high-resolution gene map of the chloroplast genome of the red alga Porphyra purpureaPlant Cell5465475CrossRefPubMedGoogle Scholar
  135. Reitzer, LJ 1996Ammonia assimilation and the biosynthesis of glutamine, glutamate, aspartate, asparagine, L-alanine and D-alanineNeidhart, FC eds. Escherichia coli and Salmonella: Cellular and Molecular BiologyASM PressWashington, DC391407Google Scholar
  136. Romero, M, Guzman-León, S, Aranda, C, González-Halphen, D, Valenzuela, L, González, A 2000Pathway for glutamate synthesis in the yeast Kluyveromyces lactisMicrobiol146239245Google Scholar
  137. Rypniewski, WR, Breiter, DR, Benning, MM, Wesenberg, G, Oh, B-H, Markley, JL, Rayment, I, Holden, HM 1991Crystallization and structure determination to 2.5-Å resolution of the oxidized [2Fe-2S] ferredoxin isolated from Anabaena 7120Biochemistry3041264131PubMedGoogle Scholar
  138. Sakakibara, H, Watanabe, M, Hase, T, Sugiyama, T 1991Molecular cloning and characterization of complementary DNA encoding for ferredoxin-dependent glutamate synthase in maize leafJ Biol Chem26620282035PubMedGoogle Scholar
  139. Sakakibara, H, Kawabata, S, Hase, T, Sugiyama, T 1992aMolecular cloning of the family of glutamine synthetase genes from maize. Expression of genes for glutamine synthetase and ferredoxin-dependent glutamate synthase in photosynthetic and non-photosynthetic tissues. Plant Cell Physiol334958Google Scholar
  140. Sakakibara, H, Kawabata, S, Hase, T, Sugiyama, T 1992bDifferential effects of nitrate and light on the expression of glutamine synthetases and ferredoxin-dependent glutamate synthase in maizePlant Cell Physio13311931198Google Scholar
  141. Sakakibara, H, Kobayashi, K, Deji, A, Sugiyama, T 1997Partial characterization of the signaling pathway for the nitrate-dependent expression of genes for nitrogen-assimilatory enzymes using detached maize leavesPlant Cell Physiol38837843Google Scholar
  142. Scheible, W-R, González-Fontes, A, Lauerer, M, Müller-Röber, B, Caboche, M, Stitt, M 1997Nitrate acts as a signal to induce organic acid metabolism and repress starch metabolism in tobaccoPlant Cell9783798CrossRefPubMedGoogle Scholar
  143. Scheible, W-R, Krapp, A, Stitt, M 2000Reciprocal diurnal changes of phosphoenolpyruvate carboxylase expression and cytosolic pyruvate kinase, citrate synthase and NADP-isocitrate dehydrogenase expression regulate organic acid metabolisms during nitrate assimilation in tobacco leavesPlant Cell Environ2311551167CrossRefGoogle Scholar
  144. Schmitz, S, Navarro, F, Kutzki, CK, Florencio, FJ, Böhme, H 1996Glutamate 94 of [2Fe-2S]-ferredoxins is important for efficient electron transfer in the 1: 1 complex with ferredoxin-glutamate synthase (GltS) from Synechocystis sp. PCC 6803.Biochem Biophys Acta1277135140PubMedGoogle Scholar
  145. Schoenbeck, MA, Temple, SJ, Trepp, GB, Blumenthal, JM, Samac, DA, Gantt, JS, Hermandez, G, Vance, CP 2000Decreased NADH-glutamate synthase activity in nodules and flowers of alfalfa (Medicago sativa L.) transformed with an antisense glutamate synthase transgeneJ Exp Bot512939CrossRefPubMedGoogle Scholar
  146. Seshachalam, RV, Subramanyama, MVV, Krishnamoorthy, RV 1992New pathway of utilization of ammonia nitrogen for the synthesis of amino acids through NADH dependent transaminases in Mombyx mori LPhysiol Entomol17281287Google Scholar
  147. Smith, CJ, Hespell, RB, Bryan, MP 1977Ammonia assimilation and glutamate formation in the anaerobe Selenomonas ruminantiumJ Bacteriol141593602Google Scholar
  148. Smith, DR, Doucette-Stamm, LA, Deloughery, C, Lee, H, Dubois, J, Aldredge, T, Bashirzadeh, R, Blakely, D, Cook, R, Gilbert, K, Harrison, D, Hoang, L, Keagle, P, Lumm, W, Pothier, B, Qiu, D, Spadafora, R, Vicaire, R, Wang, Y, Wierzbowski, J, Gibson, R, Jiwani, N, Caruso, A, Bush, D, Safer, H, Patwell, D, Prabhakar, S, McDougall, S, Shimer, G, Goyal, A, Pietrokovski, S, Church, GM, Daniels, CJ, Mao, J-I, Rice, P, Nölling, J, Reeve, JN 1997Complete genome sequence of Methanobacterium thermoautotrophiocum ΔH: functional analysis and comparative genomicsJ Bacteriol17971357155PubMedGoogle Scholar
  149. Somers, DE, Devlin, PF, Kay, SA 1998Phytochromes and cryptochromes in the entrainment of the Arabidopsis circadian clockScience28214881490CrossRefPubMedGoogle Scholar
  150. Somerville, CR, Ogren, WL 1980Inhibition of photosynthesis in Arabidopsis mutants lacking leaf glutamate synthase activityNature286257259CrossRefGoogle Scholar
  151. Staigner, D, Apel, K 1998Circadian clock-regulated expression of an RNA-binding protein in Arabidopsis: characterization of a minimal promoter elementMol Gen Genet261811819Google Scholar
  152. Stitt, M, Müller, C, Matt, P, Gibon, Y, Carillo, P, Morcuende, R, Scheible, W-R, Krapp, A 2002Steps towards an integrated view of nitrogen metabolismJ Exp Bot53959970CrossRefPubMedGoogle Scholar
  153. Suzuki, A, Rothstein, S 1997Structure and regulation of ferredoxin-dependent glutamate synthase from Arabidopsis thaliana. Cloning of cDNA, expression in different tissues of wild-type and gltS mutant strains, and light induction.Eur J Biochem243708718CrossRefPubMedGoogle Scholar
  154. Suzuki, A, Nato, A, Gadal, P 1982Glutamate synthase isoforms in tobacco cultured cellsPlant Sci Lett3393101CrossRefGoogle Scholar
  155. Suzuki, A, Oaks, A, Jacquot, J-P, Vidal, J, Gadal, P 1985An electron donor transport system in maize roots for reactions of glutamate synthase and nitrite reductase. Physiological and immunochemical properties of the electron carrier and pyridine nucleotide reductase.Plant Physiol78374378Google Scholar
  156. Suzuki, A, Burkhart, W, Rothstein, S 1996Nitrogen effects on the induction of ferredoxin-dependent glutamate synthase and its mRNA in maize leaves under the lightPlant Sci1148391CrossRefGoogle Scholar
  157. Suzuki, A, Rioual, S, Godfroy, N, Roux, Y, Boutin, JP, Rothstein, S 2001Regulation by light and metabolites of ferredoxin-dependent glutamate synthase in maizePhysiol Plant112524530CrossRefPubMedGoogle Scholar
  158. Taira, M, Valtersson, U, Burkhardt, B, Ludwig, RA 2004Arabidopsis thaliana GLN2-encoded glutamine synthetase is dual targeted to leaf mitochondria and chloroplastsPlant Cell1620482058CrossRefPubMedGoogle Scholar
  159. Teller, S, Schmidt, KH, Appenroth, KJ 1996Ferredoxin-dependent but not NADH-dependent glutamate synthase is regulated by phytochrome and a blue/UV-A light receptor in turions of Spirodela polyrhizaPlant Physiol Biochem34713719Google Scholar
  160. Thum, KE, Shasha, DE, Lajay, LV, Coruzzi, GM 2003Light- and carbon-signaling pathways. Modeling circuits of interactions.Plant Physiol132440452CrossRefPubMedGoogle Scholar
  161. Tobin, AK, Yamaya, T 2001Cellular compartmentation of ammonium assimilation in rice and barleyJ Exp Bot52591604CrossRefPubMedGoogle Scholar
  162. Trepp, GB, Mortel, M, Yoshioka, H, Miller, SS, Samac, DA, Gantt, JS, Vance, CP 1999aNADH-glutamate synthase in alfalfa root nodules. Genetic regulation and cellular expression.Plant Physiol119817828CrossRefGoogle Scholar
  163. Trepp, GB, Plank, DW, Gantt, JS, Vance, CP l999bNADH-glutamate synthase in alfalfa root nodules. Immunological localization.Plant Physiol 119829837CrossRefGoogle Scholar
  164. Turano, FJ, Muhitch, MJ 1999Differential accumulation of ferredoxin- and NADH- dependent glutamate synthase activities, peptides, and transcripts in developing soybean seedlings in response to light, nitrogen, and nodulationPhysiol Plant107407418CrossRefGoogle Scholar
  165. Valentin, K, Kostrzewa, M, Zetsche, K 1993Glutamate synthase is plastid-encoded in a red alga: implications for the evolution of glutamate synthasesPlant Mol Biol237785CrossRefPubMedGoogle Scholar
  166. Heuvel, RHH, Ferrari, D, Bossi, RT, Ravasio, S, Curti, B, Vanoni, MA, Florencio, FJ, Mattevi, A 2002Structural studies on the synchronization of catalytic centers in glutamate synthaseJ Biol Chem2772457924583CrossRefPubMedGoogle Scholar
  167. Heuvel, RHH, Svergun, DI, Petoukhov, MV, Coda, A, Curti, B, Ravasio, S, Vanoni, MA, Mattevi, A 2003The active conformation of glutamate synthase and its binding to ferredoxinJ Mol Biol330113128CrossRefPubMedGoogle Scholar
  168. Heuvel, RHH, Curti, B, Vanoni, MA, Mattevi, A 2004Glutamate synthase: a fascinating pathway from l-glutamine to l-glutamateCell Mol Life Sci61669681CrossRefPubMedGoogle Scholar
  169. Vance, CP, Gregerson, RG, Robinson, DL, Miller, SS, Gantt, JS 1994Primary assimilation of nitrogen in alfalfa nodules: molecular features of the enzymes involvedPlant Sci1015164CrossRefGoogle Scholar
  170. Vance, CP, Miller, SS, Gregerson, RG, Samac, DA, Robinson, DL, Gantt, S 1995Alfalfa NADH-dependent glutamate synthase: structure of the gene and importance in symbiotic N2 fixationPlant J8345358CrossRefPubMedGoogle Scholar
  171. Vanoni, MA, Curti, B 1999Glutamate synthase: a complex iron-sulfur flavoproteinCell Mol Life Sci55617638CrossRefPubMedGoogle Scholar
  172. Vanoni, MA, Negri, A, Zanetti, G, Ronchi, S, Curti, B 1990Structural studies on the subunits of glutamate synthase from Azospirillum brasilenseBiochim Biophys Acta1039374377PubMedGoogle Scholar
  173. Vanoni, MA, Fischer, F, Ravasio, S, Verzotti, E, Edmondson, DE, Hagen, WR, Zanetti, G, Curti, B 1998The recombinant α subunit of glutamate synthase: spectroscopic and catalytic propertiesBiochemistry3718281838CrossRefPubMedGoogle Scholar
  174. Vanoni, M, Dossena, L, Heuvel, RHH, Curti, B 2005Structure–function studies on the complex iron–sulfur flavoprotein glutamate synthase: the key enzyme of ammonia assimilationPhotosynthe Res83219238(this issue)CrossRefGoogle Scholar
  175. Vigara, AJ, García-Sánchez, MI, Gotor, C, Vega, JM 1996Interaction between glutamate synthase and ferredoxin from Monoraphidium braunii. Chemical modifications and cross-linking studies.Plant Physiol Biochem34707711Google Scholar
  176. Watanabe, S, Sakai, T, Goto, S, Yaginuma, T, Hayakawa, T, Yamaya, T 1996Expression of NADH-dependent glutamate synthase in response to the supply of nitrogen in rice cells in suspension culturePlant Cell Physiol3710341037Google Scholar
  177. Yamaya, T, Hayakawa, T, Tanasawa, K, Kamachi, K, Mae, T, Ojima, K 1992Tissue distribution of glutamate synthase and glutamine synthetase in rice leaves. Occurrence of NADH-dependent glutamate synthase protein and activity in the unexpanded non-green leaf blades.Plant Physiol10014271432Google Scholar
  178. Yamaya, T, Tanno, H, Hirose, N, Watanabe, S, Hayakawa, T 1995A supply of nitrogen causes increase in the level of NADH-dependent glutamate synthase protein and in the activity of the enzyme in roots of rice seedlingsPlant Cell Physiol3611971204Google Scholar
  179. Yonekura-Sakakibara, K, Onda, Y, Ashikari, T, Tanaka, Y, Kusumi, T, Hase, T 2000Analysis of Reductant supply systems for ferredoxin-dependent sulfite reductase in photosynthetic and non-photosynthetic organs of maizePlant Physiol122887894PubMedGoogle Scholar
  180. Zehnacker, C, Becker, TW, Suzuki, A, Carrayol, E, Caboche, M, Hirel, B 1992Purification and properties of tobacco ferredoxin-dependent glutamate synthase, and isolation of corresponding cDNA clones. Light-inducibility and organ-specificity of gene transcription and protein expression.Planta187266274CrossRefGoogle Scholar
  181. Ziegler, C, Feraud, M, Jouglet, T, Viret, L, Spampinato, A, Paganelli, V, Ben Hammouda, M, Suzuki, A 2003Regulation of promoter activity of ferredoxin-dependent glutamate synthasePlant Physiol Biochem41649655CrossRefGoogle Scholar

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© Springer 2005

Authors and Affiliations

  1. 1.Unité de Nutrition Azotée des PlantesInstitut National de la Recherche AgronomiquecedexFrance
  2. 2.Department of Chemistry and BiochemistryTexas Tech UniversityLubbockUSA

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