Cytosolic Glutamine Synthetase Isozymes Play Redundant Roles in Ammonium Assimilation under Low-Ammonium Conditions in Roots of Arabidopsis thaliana

Noriyuki Konishi, Masahide Saito, Fumi Imagawa, Keiich Kanno, Tomoyuki Yamaya, Soichi Kojima

Research output: Contribution to journalArticle

7 Citations (Scopus)

Abstract

Ammonium is a major nitrogen source for plants; it is assimilated into glutamine via a reaction catalyzed by glutamine synthetase (GLN). Arabidopsis expresses four cytosolic GLN genes, GLN1; 1, GLN1; 2, GLN1; 3 and GLN1; 4, in roots. However, the function and organization of these GLN1 isozymes in ammonium assimilation in roots remain unclear. In this study, we aimed to characterize the four GLN1 isozymes. The levels of growth of the wild type and gln1 single and multiple knockout lines were compared in a hydroponic culture at ammonium concentrations of 0.1 and 3 mM. Under the low-ammonium concentration, in single mutants for each GLN1 gene, there was little effect on growth, whereas the triple mutant for GLN1; 1, GLN1; 2 and GLN1; 3 grew slowly and accumulated ammonium. Under the high-ammonium concentration, the single mutant for GLN1; 2 showed 50% decreases in fresh weight and glutamine, whereas the other gln1 single mutants did not show notable changes in the phenotype. The double mutant for GLN1; 1 and GLN1; 2 showed less growth and a lower glutamine concentration than the single mutant for GLN1; 2. Promoter analysis indicated an overlapping expression of GLN1; 1 with GLN1; 2 in the surface layers of the roots. We thus concluded that: (i) at a low concentration, ammonium was assimilated by GLN1; 1, GLN1; 2 and GLN1; 3, and they were redundant; (ii) low-affinity GLN1; 2 could contribute to ammonium assimilation at concentrations ranging from 0.1 to 3 mM; and (iii) GLN1; 1 supported GLN1; 2 within the outer cell layers of the root.

Original languageEnglish
Pages (from-to)601-613
Number of pages13
JournalPlant and Cell Physiology
Volume59
Issue number3
DOIs
Publication statusPublished - Mar 1 2018
Externally publishedYes

Fingerprint

Glutamate-Ammonia Ligase
glutamate-ammonia ligase
Ammonium Compounds
Arabidopsis
Isoenzymes
isozymes
assimilation (physiology)
Arabidopsis thaliana
mutants
glutamine
Glutamine
Growth
Hydroponics
hydroponics
genes
promoter regions
Genes
phenotype
Nitrogen
nitrogen

Keywords

  • Ammonium
  • Arabidopsis
  • Glutamine synthetase
  • Metabolism
  • Root

ASJC Scopus subject areas

  • Physiology
  • Plant Science
  • Cell Biology

Cite this

Cytosolic Glutamine Synthetase Isozymes Play Redundant Roles in Ammonium Assimilation under Low-Ammonium Conditions in Roots of Arabidopsis thaliana. / Konishi, Noriyuki; Saito, Masahide; Imagawa, Fumi; Kanno, Keiich; Yamaya, Tomoyuki; Kojima, Soichi.

In: Plant and Cell Physiology, Vol. 59, No. 3, 01.03.2018, p. 601-613.

Research output: Contribution to journalArticle

Konishi, Noriyuki ; Saito, Masahide ; Imagawa, Fumi ; Kanno, Keiich ; Yamaya, Tomoyuki ; Kojima, Soichi. / Cytosolic Glutamine Synthetase Isozymes Play Redundant Roles in Ammonium Assimilation under Low-Ammonium Conditions in Roots of Arabidopsis thaliana. In: Plant and Cell Physiology. 2018 ; Vol. 59, No. 3. pp. 601-613.
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abstract = "Ammonium is a major nitrogen source for plants; it is assimilated into glutamine via a reaction catalyzed by glutamine synthetase (GLN). Arabidopsis expresses four cytosolic GLN genes, GLN1; 1, GLN1; 2, GLN1; 3 and GLN1; 4, in roots. However, the function and organization of these GLN1 isozymes in ammonium assimilation in roots remain unclear. In this study, we aimed to characterize the four GLN1 isozymes. The levels of growth of the wild type and gln1 single and multiple knockout lines were compared in a hydroponic culture at ammonium concentrations of 0.1 and 3 mM. Under the low-ammonium concentration, in single mutants for each GLN1 gene, there was little effect on growth, whereas the triple mutant for GLN1; 1, GLN1; 2 and GLN1; 3 grew slowly and accumulated ammonium. Under the high-ammonium concentration, the single mutant for GLN1; 2 showed 50{\%} decreases in fresh weight and glutamine, whereas the other gln1 single mutants did not show notable changes in the phenotype. The double mutant for GLN1; 1 and GLN1; 2 showed less growth and a lower glutamine concentration than the single mutant for GLN1; 2. Promoter analysis indicated an overlapping expression of GLN1; 1 with GLN1; 2 in the surface layers of the roots. We thus concluded that: (i) at a low concentration, ammonium was assimilated by GLN1; 1, GLN1; 2 and GLN1; 3, and they were redundant; (ii) low-affinity GLN1; 2 could contribute to ammonium assimilation at concentrations ranging from 0.1 to 3 mM; and (iii) GLN1; 1 supported GLN1; 2 within the outer cell layers of the root.",
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AU - Kojima, Soichi

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AB - Ammonium is a major nitrogen source for plants; it is assimilated into glutamine via a reaction catalyzed by glutamine synthetase (GLN). Arabidopsis expresses four cytosolic GLN genes, GLN1; 1, GLN1; 2, GLN1; 3 and GLN1; 4, in roots. However, the function and organization of these GLN1 isozymes in ammonium assimilation in roots remain unclear. In this study, we aimed to characterize the four GLN1 isozymes. The levels of growth of the wild type and gln1 single and multiple knockout lines were compared in a hydroponic culture at ammonium concentrations of 0.1 and 3 mM. Under the low-ammonium concentration, in single mutants for each GLN1 gene, there was little effect on growth, whereas the triple mutant for GLN1; 1, GLN1; 2 and GLN1; 3 grew slowly and accumulated ammonium. Under the high-ammonium concentration, the single mutant for GLN1; 2 showed 50% decreases in fresh weight and glutamine, whereas the other gln1 single mutants did not show notable changes in the phenotype. The double mutant for GLN1; 1 and GLN1; 2 showed less growth and a lower glutamine concentration than the single mutant for GLN1; 2. Promoter analysis indicated an overlapping expression of GLN1; 1 with GLN1; 2 in the surface layers of the roots. We thus concluded that: (i) at a low concentration, ammonium was assimilated by GLN1; 1, GLN1; 2 and GLN1; 3, and they were redundant; (ii) low-affinity GLN1; 2 could contribute to ammonium assimilation at concentrations ranging from 0.1 to 3 mM; and (iii) GLN1; 1 supported GLN1; 2 within the outer cell layers of the root.

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