NRT1.1-Related NH4+ Toxicity Is Associated with a Disturbed Balance between NH4+ Uptake and Assimilation

Jian, Shao-Fen; Liao, Qiong; Song, Haixing; Liu, Qiang; Lepo, Joe Eugene; Guan, Chunyun; Zhang, Jianhua; Am, Ismail; Zhang, Zhenhua

doi:10.1104/pp.18.00410

Cited by 93 publications

(88 citation statements)

References 57 publications

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“…We have already reported that Arabidopsis NITRATE TRANSPORTER 1.1 (NRT1.1), acting as a nitrate transceptor, also aggravates ammonium toxicity (27). This result was recently confirmed by another group (11). Thus, we investigated whether NRT1.1 and GLN2 increase the sensitivity to ammonium through a common mechanism.…”

Section: Resultssupporting

confidence: 76%

Excessive assimilation of ammonium by plastidic glutamine synthetase is a major cause of ammonium toxicity in Arabidopsis thaliana

Hachiya

Inaba

Wakazaki

et al. 2019

Preprint

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23Plants use nitrate and ammonium in the soil as their main nitrogen sources. Recently, 24 ammonium has attracted attention due to evidence suggesting that, in C 3 species, an 25 elevated CO 2 environment inhibits nitrate assimilation. However, high concentrations of 26 ammonium as the sole nitrogen source for plants causes impaired growth, i.e. ammonium 27 toxicity. Although ammonium toxicity has been studied for a long time, the primary cause 28 remains to be elucidated. Here, we show that ammonium assimilation in plastids rather 29 than ammonium accumulation is a primary cause for toxicity. Our genetic screen of 30 ammonium-tolerant Arabidopsis lines with enhanced shoot growth identified plastidic 31 GLUTAMINE SYNTHETASE 2 (GLN2) as the causal gene. Our reciprocal grafting of 32 wild-type and GLN2 or GLN1;2-deficient lines suggested that shoot GLN2 activity results 33 in ammonium toxicity, whilst root GLN1;2 activity prevents it. With exposure to toxic 34 levels of ammonium, the shoot GLN2 reaction produced an abundance of protons within 35 cells, thereby elevating shoot acidity and stimulating expression of acidic stress-36 responsive genes. Application of an alkaline ammonia solution to the toxic ammonium 37 medium efficiently alleviated the ammonium toxicity with a concomitant reduction in 38 shoot acidity. Consequently, we conclude that a primary cause of ammonium toxicity is 39 acidic stress in the shoot. This fundamental insight provides a framework for enhanced 40 understanding of ammonium toxicity in plants. 41 42 43 44Recent studies suggest that elevated CO 2 inhibits nitrate reduction in C 3 species, such as 47 wheat and Arabidopsis, whereas ammonium utilization does not decrease (1). One 48 estimate predicts that only a 1% drop in nitrogen use efficiency could increase worldwide 49 cultivation costs for crops by about $1 billion annually (2). Therefore, increasing 50 ammonium use by crops is an important goal for agriculture as CO 2 levels rise in the 51 world; however, millimolar concentrations of ammonium as the sole N source causes 52 growth suppression and chlorosis in plants, compared with nitrate (3, 4, 5). This 53 phenomenon is widely known as ammonium toxicity, but the primary cause of impaired 54 growth remains to be identified. 55Plants grown in high ammonium conditions show several distinct 56 characteristics from those grown in nitrate (3, 4, 5). These toxic symptoms have evoked 57 several hypotheses about the toxic causes, including futile transmembrane ammonium 58 cycling, deficiencies in inorganic cations and organic acids, impaired hormonal 59 homeostasis, disordered pH regulation, and the uncoupling of photophosphorylation; 60 however, some of the symptoms are not directly associated with growth suppression by 61 ammonium toxicity (6), making it difficult to determine the toxic cause. Several efforts 62 have isolated ammonium-sensitive mutants in Arabidopsis thaliana and determined their 63 causative genes (4, 5). GMP1 is a causal gene whose deficiency causes stunted growth of 6...

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Section: Resultssupporting

confidence: 76%

Excessive assimilation of ammonium by plastidic glutamine synthetase is a major cause of ammonium toxicity in Arabidopsis thaliana

Hachiya

Inaba

Wakazaki

et al. 2019

Preprint

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“…NO 3 may influence the expression of AMTs involved in cytosolic NH 4 + homeostasis or be involved in a more complex feedback response via plant metabolism (Babourina et al, 2007;Hachiya and Sakakibara, 2017). In Arabidopsis, NO 3 mediates NH 4 + uptake and assimilation by NRT1.1 (Jian et al, 2018).…”

Section: Discussionmentioning

confidence: 99%

Ammonium Transporter (BcAMT1.2) Mediates the Interaction of Ammonium and Nitrate in Brassica campestris

et al. 2020

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“…+ concentration in the cultivation environment is 5 mM or higher (6 and 10 mM in most studies) [11,[19][20][21]. Here, 2 mM NH 4 + with 0.1 mM K + was used to generate a high NH 4…”

mentioning

confidence: 99%

NH4+ Toxicity, Which Is Mainly Determined by the High NH4+/K+ Ratio, Is Alleviated by CIPK23 in Arabidopsis

Shi

et al. 2020

Plants

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Ammonium (NH4+) toxicity is always accompanied by ion imbalances, and NH4+ and potassium (K+) exhibit a competitive correlation in their uptake and transport processes. In Arabidopsis thaliana, the typical leaf chlorosis phenotype in the knockout mutant of calcineurin B-like interacting protein kinase 23 (CIPK23) is high-NH4+-dependent under low-K+ condition. However, the correlation of K+ and NH4+ in the occurrence of leaf chlorosis in the cipk23 mutant has not been deeply elucidated. Here, a modified hydroponic experimental system with different gradients of NH4+ and K+ was applied. Comparative treatments showed that NH4+ toxicity, which is triggered mainly by the high ratio of NH4+ to K+ (NH4+/K+ ≥ 10:1 for cipk23) but not by the absolute concentrations of the ions, results in leaf chlorosis. Under high NH4+/K+ ratios, CIPK23 is upregulated abundantly in leaves and roots, which efficiently reduces the leaf chlorosis by regulating the contents of NH4+ and K+ in plant shoots, while promoting the elongation of primary and lateral roots. Physiological data were obtained to further confirm the role CIPK23 in alleviating NH4+ toxicity. Taken all together, CIPK23 might function in different tissues to reduce stress-induced NH4+ toxicity associated with high NH4+/K+ ratios by regulating the NH4+–K+ balance in Arabidopsis.

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NRT1.1-Related NH₄⁺ Toxicity Is Associated with a Disturbed Balance between NH₄⁺ Uptake and Assimilation

Cited by 93 publications

References 57 publications

Excessive assimilation of ammonium by plastidic glutamine synthetase is a major cause of ammonium toxicity in Arabidopsis thaliana

Excessive assimilation of ammonium by plastidic glutamine synthetase is a major cause of ammonium toxicity in Arabidopsis thaliana

Ammonium Transporter (BcAMT1.2) Mediates the Interaction of Ammonium and Nitrate in Brassica campestris

NH4+ Toxicity, Which Is Mainly Determined by the High NH4+/K+ Ratio, Is Alleviated by CIPK23 in Arabidopsis

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