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

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Abstract

Ammonium ion assimilation constitutes a central metabolic pathway in many organisms, and glutamate synthase, in concert with glutamine synthetase (GS, EC 6.3.1.2), 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 1.4.1.13), NADH (NADH-GOGAT, EC 1.4.1.14) or reduced ferredoxin (Fd-GOGAT, EC 1.4.7.1) 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 1.4.1.2) 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.

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Abbreviations

ASN :

asparagine synthetase gene

CD:

circular dichroism

EPR:

electron paramagnetic resonance

ΔG:

free energy change

ΔS:

entropy change

FAD:

flavin adenine dinucleotide

Fd:

ferredoxin

FMN:

flavin mononucleodide

Fe/S cluster:

iron-sulfur cluster

FNR:

ferredoxin: NADP+ oxidoreductase

GAT:

glutamine amidotransferase

GDH:

glutamate dehydrogenase

GOGAT:

glutamate synthase

GLN1(2) :

cytosolic (chloroplastic) glutamine synthetase gene

glsF :

ferredoxin-glutamate synthase gene

GLT :

NADH-glutamate synthase gene

gltB :

NADPH-glutamate synthase α subunit gene

gltD :

NADPH-glutamate synthase β subunit gene

GltS:

glutamate synthase

gltS :

Fd-glutamate synthase gene

GLUI (2) :

ferredoxin-glutamate synthase 1(2) gene

GS1(2):

cytosolic (chloroplastic/plastidial) glutamine synthetase

NAR :

nitrate reductase gene

NIR :

nitrite reductase gene

Rubisco:

ribulose-l,5-bisphosphate carboxylase/oxygenase

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  1. Unité de Nutrition Azotée des Plantes, Institut National de la Recherche Agronomique, Route de Saint-Cyr, 78026, Versailles, cedex, France

    Akira Suzuki

  2. Department of Chemistry and Biochemistry, Texas Tech University, P.O. Box 41061, Lubbock, TX, 79409-1061, USA

    David B. Knaff

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Suzuki, A., Knaff, D.B. Glutamate synthase: structural, mechanistic and regulatory properties, and role in the amino acid metabolism. Photosynth Res 83, 191–217 (2005). https://doi.org/10.1007/s11120-004-3478-0

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