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Excessive ammonium assimilation by plastidic glutamine synthetase causes ammonium toxicity in Arabidopsis thaliana.

ABSTRACT: Plants use nitrate, ammonium, and organic nitrogen in the soil as nitrogen sources. Since the elevated CO₂ environment predicted for the near future will reduce nitrate utilization by C₃ species, ammonium is attracting great interest. However, abundant ammonium nutrition impairs growth, i.e., ammonium toxicity, the primary cause of which remains to be determined. Here, we show that ammonium assimilation by GLUTAMINE SYNTHETASE 2 (GLN2) localized in the plastid rather than ammonium accumulation is a primary cause for toxicity, which challenges the textbook knowledge. With exposure to toxic levels of ammonium, the shoot GLN2 reaction produced an abundance of protons within cells, thereby elevating shoot acidity and stimulating expression of acidic stress-responsive genes. Application of an alkaline ammonia solution to the ammonium medium efficiently alleviated the ammonium toxicity with a concomitant reduction in shoot acidity. Consequently, we conclude that a primary cause of ammonium toxicity is acidic stress.

SUBMITTER: Hachiya T

PROVIDER: S-EPMC8367978 | biostudies-literature | 2021 Aug

REPOSITORIES: biostudies-literature

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Excessive ammonium assimilation by plastidic glutamine synthetase causes ammonium toxicity in Arabidopsis thaliana.

Hachiya Takushi T Inaba Jun J Wakazaki Mayumi M Sato Mayuko M Toyooka Kiminori K Miyagi Atsuko A Kawai-Yamada Maki M Sugiura Daisuke D Nakagawa Tsuyoshi T Kiba Takatoshi T Gojon Alain A Sakakibara Hitoshi H

Nature communications 20210816 1

Plants use nitrate, ammonium, and organic nitrogen in the soil as nitrogen sources. Since the elevated CO<sub>2</sub> environment predicted for the near future will reduce nitrate utilization by C<sub>3</sub> species, ammonium is attracting great interest. However, abundant ammonium nutrition impairs growth, i.e., ammonium toxicity, the primary cause of which remains to be determined. Here, we show that ammonium assimilation by GLUTAMINE SYNTHETASE 2 (GLN2) localized in the plastid rather than a ...[more]

PMID: 34400629

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Project description:Drought stress can negatively impact crop yield and quality. Improving wheat yields under drought stress is a major objective of agronomic research. Glutamine synthetase (GS) is a key enzyme of nitrogen metabolism that is critical to plant growth and development in abiotic stress response. However, to date, no systemic characterization of the GS genes has yet been conducted in wheat and its close relatives. We identified a total of 15 GS genes in Triticum aestivum (2n = 6x = 42; AABBDD), as well as 9 GS genes in Triticum dicoccoides (2n = 4x = 28; AABB), 6 in Aegilops tauschii (2n = 2x = 14; DD), and 5 in Triticum urartu (2n = 2x = 14; AA). The 35 GSs were further clustered into five lineages according to the phylogenetic tree. Synteny analysis revealed that the three subgenomes in bread wheat retained extensive synteny between bread wheat and its three relative species. We identified three up-regulated TaGSs (Ta4A.GSe, Ta4B.GSe, and Ta4D.GSe) from transcriptome data after drought and salt stress. Ta4D.GSe was subsequently used for further functional studies, and its subcellular localization were determined in Arabidopsis protoplasts. Its overexpression in Arabidopsis enhanced drought tolerance by increasing the ability of scavenging of reactive oxygen species (ROS) and osmotic adjustment. We identified GS gene family in four wheat species and performed comparative analyses of their relationships, chromosome locations, conserved motif, gene structure, and synteny. The subcellular localization of Ta4D.GSe was detected and its drought tolerance function was demonstrated. Taken together, these findings provide insight into the potential functional roles of the GS genes in abiotic stress tolerance. KEY MESSAGE: This report clearly shows detailed characterization of GS gene family in four wheat species and demonstrates that Ta4D.GSe plays an important role in enhancing drought tolerance by improving the scavenging of ROS and osmotic adjustment ability in Arabidopsis.

Dataset Information

Excessive ammonium assimilation by plastidic glutamine synthetase causes ammonium toxicity in Arabidopsis thaliana.

Publications

Excessive ammonium assimilation by plastidic glutamine synthetase causes ammonium toxicity in Arabidopsis thaliana.

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