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

Hachiya, Takushi; Inaba, Jun; Wakazaki, Mayumi; Sato, Mayuko; Toyooka, Kiminori; Miyagi, Atsuko; Kawai‐Yamada, Maki; Sugiura, Daisuke; Nakagawa, Tsuyoshi; Kiba, Takatoshi; Gojon, Alain; Sakakibara, Hitoshi

doi:10.1038/s41467-021-25238-7

Cited by 128 publications

(118 citation statements)

References 45 publications

Supporting

Mentioning

115

Contrasting

Order By: Relevance

“…We noticed varying degrees of increases in the root GS and NADH-GDH activities when the NH 4 + concentration increased from 0% to 50%. Elevated activities of GS and NADH-GDH were required in the assimilations of the excessive NH 4 + to prevent toxicity, consistent with the results regarding certain studies in vegetables [41,45], crops [15,46], and Arabidopsis [11,47]. As the NH 4 + concentration increased from 50% to 100%, the greatest reinforcements of both the root GS and NADH-GDH activities were monitored in the NH 4 + -tolerant species ageratum, followed by the moderately NH 4 + -sensitive species petunia, but in the extremely NH 4 + -sensitive salvia, root GS and NADH-GDH activities were not significantly affected and in some cases even reduced, in response to high NH 4…”

Section: Explorations Of the Nhsupporting

confidence: 89%

“…These ammonium toxicity symptoms have evoked numerous hypotheses on the cause: depletion of carbon supply [8,9], energy overconsumption for futile ammonium cycling [8,10], and a recently elucidated mechanism of acidic stresses produced by disordered pH regulation [11]. Nonetheless, the information linked with the N assimilation pathways to explain the ammonium tolerances, especially in bedding plants, remains scarce.…”

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

Root GS and NADH-GDH Play Important Roles in Enhancing the Ammonium Tolerance in Three Bedding Plants

Song

Yang

Jeong

2022

IJMS

View full text Add to dashboard Cite

Ammonium is a paradoxical nutrient because it is more metabolically efficient than nitrate, but also causes plant stresses in excess, i.e., ammonium toxicity. Current knowledge indicates that ammonium tolerance is species-specific and related to the ammonium assimilation enzyme activities. However, the mechanisms underlying the ammonium tolerance in bedding plants remain to be elucidated. The study described herein explores the primary traits contributing to the ammonium tolerance in three bedding plants. Three NH4+:NO3− ratios (0:100, 50:50, 100:0) were supplied to salvia, petunia, and ageratum. We determined that they possessed distinct ammonium tolerances: salvia and petunia were, respectively, extremely sensitive and moderately sensitive to high NH4+ concentrations, whereas ageratum was tolerant to NH4+, as characterized by the responses of the shoot and root growth, photosynthetic capacity, and nitrogen (amino acid and soluble protein)-carbohydrate (starch) distributions. An analysis of the major nitrogen assimilation enzymes showed that the root GS (glutamine synthetase) and NADH-GDH (glutamate dehydrogenase) activities in ageratum exhibited a dose-response relationship (reinforced by 25.24% and 6.64%, respectively) as the NH4+ level was raised from 50% to 100%; but both enzyme activities were significantly diminished in salvia. Besides, negligible changes of GS activities monitored in leaves revealed that only the root GS and NADH-GDH underpin the ammonium tolerances of the three bedding plants.

show abstract

Section: Explorations Of the Nhsupporting

confidence: 89%

Section: Introductionmentioning

confidence: 99%

Root GS and NADH-GDH Play Important Roles in Enhancing the Ammonium Tolerance in Three Bedding Plants

Song

Yang

Jeong

2022

IJMS

View full text Add to dashboard Cite

show abstract

“…This aspect should be taken into account in the case of overexpression of NH 4 + transporter genes, when plants do not have enough time to assimilate the absorbed NH 4 + , as has already been noted by some researchers [ 71 , 73 ]. The exact mechanism of plant growth disorders due to NH 4 + toxicity is still unknown, although several hypotheses have been put forward, including futile transmembrane NH 4 + cycling, deficiencies in inorganic cations and organic acids, impaired hormonal homeostasis, disordered pH regulation and the uncoupling of photophosphorylation [ 210 ]. High concentration of NH 4 + is also one of the causes of plant death due to the use of broad-spectrum herbicides based on phosphinotricin (PPT).…”

Section: Ammonium Toxicity and Resistance To Phosphinothricinmentioning

confidence: 99%

“…On the other hand, the multiple hypotheses regarding the NH 4 + toxicity [ 209 , 222 ] were recently joined by another one. According to Hachiya et al [ 210 ], the primary cause of NH 4 + toxicity is not its high concentration, but rather acidic stress resulting from assimilation of these high amounts by the plastid form of GS. Whatever the exact mechanisms of NH 4 + toxicity or of the PPT effect, the increase in plant PPT resistance achieved through overexpression of GS or other N metabolism genes is absolutely insufficient for the commercial use of such plants.…”

Section: Ammonium Toxicity and Resistance To Phosphinothricinmentioning

confidence: 99%

Genetic Engineering and Genome Editing for Improving Nitrogen Use Efficiency in Plants

Lebedev

Popova

Shestibratov

2021

Cells

View full text Add to dashboard Cite

Low nitrogen availability is one of the main limiting factors for plant growth and development, and high doses of N fertilizers are necessary to achieve high yields in agriculture. However, most N is not used by plants and pollutes the environment. This situation can be improved by enhancing the nitrogen use efficiency (NUE) in plants. NUE is a complex trait driven by multiple interactions between genetic and environmental factors, and its improvement requires a fundamental understanding of the key steps in plant N metabolism—uptake, assimilation, and remobilization. This review summarizes two decades of research into bioengineering modification of N metabolism to increase the biomass accumulation and yield in crops. The expression of structural and regulatory genes was most often altered using overexpression strategies, although RNAi and genome editing techniques were also used. Particular attention was paid to woody plants, which have great economic importance, play a crucial role in the ecosystems and have fundamental differences from herbaceous species. The review also considers the issue of unintended effects of transgenic plants with modified N metabolism, e.g., early flowering—a research topic which is currently receiving little attention. The future prospects of improving NUE in crops, essential for the development of sustainable agriculture, using various approaches and in the context of global climate change, are discussed.

show abstract

“…The differences between GS isoforms are increasingly being studied. The main cause of ammonium toxicity in Arabidopsis was found to be ammonium assimilation of GS2 rather than ammonium accumulation [15]. Isotopic-tracing experiments and genetic evidence indicated that three of the five GS1s work together to remobilize nitrogen and fill seeds in Arabidopsis [16].…”

Section: Introductionmentioning

confidence: 99%

Genome-Wide Characterization of Glutamine Synthetase Family Genes in Cucurbitaceae and Their Potential Roles in Cold Response and Rootstock-Scion Signaling Communication

Lü

Liu

et al. 2021

Agriculture

View full text Add to dashboard Cite

Glutamine synthetase (GS; EC 6.3.1.2, L-glutamate: ammonia ligase ADP-forming) is the key enzyme responsible for the primary assimilation and reassimilation of nitrogen (N) in higher plants. There are two main isoforms of GS in higher plants, classified as cytosolic GS (GS1) and chloroplastic GS (GS2) by their size and subcellular localization. In order to improve the stress tolerance, quality, and yield of cucurbit crops such as cucumbers (Csa, Cucumis sativus L.), pumpkins (Cmo, Cucurbita moschata var. Rifu) are often used as rootstocks. Here, the GS family of the two species were comprehensively analyzed using bioinformatics in terms of aspects of the phylogenic tree, gene structure, chromosome location, subcellular localization, and evolutionary and expression patterns. Seven and four GS gene family members were screened in pumpkin and cucumber, respectively. GS family genes were divided into three groups (one for GS2 and two for GS1) according to their homology and phylogenetic relationships with other species. The analysis of gene ontology annotation of GS family genes, promoter regulatory elements, and tissue-specific expression patterns indicates the potential different biological roles of GS isoforms in Cucurbitaceae. In particular, we have identified a potentially available gene (GS1: CmoCh08G004920) from pumpkin that is relatively highly expressed and tissue-specifically expressed. RT-PCR analysis showed that most CmoGSs are induced by low temperature, and long-term (day 2 to day 9) cold stress has a more obvious effect on the RNA abundance of CmoGS. Our work presents the structure and expression patterns of all candidate members of the pumpkin and cucumber GS gene family, and to the best of our knowledge, this is the first time such work has been presented. It is worth focusing on the candidate genes with strong capacity for improving pumpkin rootstock breeding in order to increase nitrogen-use efficiency in cold conditions, as well as rootstock-scion communication.

show abstract

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

Cited by 128 publications

References 45 publications

Root GS and NADH-GDH Play Important Roles in Enhancing the Ammonium Tolerance in Three Bedding Plants

Root GS and NADH-GDH Play Important Roles in Enhancing the Ammonium Tolerance in Three Bedding Plants

Genetic Engineering and Genome Editing for Improving Nitrogen Use Efficiency in Plants

Genome-Wide Characterization of Glutamine Synthetase Family Genes in Cucurbitaceae and Their Potential Roles in Cold Response and Rootstock-Scion Signaling Communication

Contact Info

Product

Resources

About