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Glutamate dehydrogenase mediated amino acid metabolism after ammonium uptake enhances rice growth under aeration condition

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Abstract

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Aeration stimulates the rice growth and nitrogen (N) metabolism; in which, the glutamate accumulation limited by the glutamate dehydrogenase pathway after ammonia uptake may control root N metabolism during aeration.

Abstract

Increasing rhizosphere oxygen content greatly improves rice growth and biomass. To study the intrinsic mechanism involved in nitrogen (N) metabolism, a hydroponic experiment was conducted by supplying two different oxygen levels to two different rice genotypes. Compared to the hypoxia-resistant cultivar (Nip; japonica rice ‘Nipponbare’), the hypoxia-sensitive cultivar (U502; upland rice ‘Upland 502’) presented with severe oxidative damage under the lack of aeration. However, aeration significantly reduced root oxidative damage by enhancing root antioxidant capacity and leaf photosynthesis especially in U502, and significantly increased nitrate (NO3−) and ammonia (NH4+) uptake and upregulated the expression of the genes controlling these processes. Additional NO3− was mainly incorporated into amino acids in the leaves whereas NH4+ assimilation occurred mostly in the roots. The 15N gas chromatography–mass spectrometry analysis demonstrated that aeration had no influence on the compositions of the individual amino acids derived from 15NO3− in the roots, but increased labeled glutamic acid (Glu), asparagine, γ-aminobutyric acid, and alanine in 15NH4+-treated roots. Aeration inhibited root glutamate synthetase activity but this did not inhibit 15N-Glu production from 15NH4+. In contrast, aeration upregulated isocitrate dehydrogenase and glutamate dehydrogenase. These mechanisms and soluble carbohydrates may constitute an alternative pathway for Glu production in which amino acid metabolism is enhanced after NH4+ uptake during aeration. Therefore, the rice growth-enhancing effect of aeration is closely correlated with root redox equilibrium, N uptake, and amino acid metabolism. Glutamic acid accumulation is limited by the glutamate dehydrogenase pathway after NH4+ uptake and may control root N metabolism during aeration.

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Abbreviations

2-OG:

2-Oxoglutarate

APX:

Ascorbate peroxidase

AsA:

Reduced ascorbic acid

BSA:

Bovine serum albumen

CAT:

Catalase

DHA:

Dehydroascorbic acid

DO:

Dissolved oxygen

DTT:

Dithiothreitol

GABA:

γ-Aminobutyric acid

GDH:

Glutamate dehydrogenase

GOGAT:

Glutamate synthetase

GOT:

Glutamic oxaloacetic transaminase

GPT:

Glutamic-pyruvic transaminase

GS:

Glutamine synthetase

GSSG:

Glutathione disulfide

ICDH:

Isocitrate dehydrogenase

MDA:

Malondialdehyde

NiR:

Nitrite reductase

NR:

Nitrate reductase

POD:

Peroxidase

ROS:

Reactive oxygen species

SOD:

Superoxide dismutase

tAsA:

Total reduced ascorbic acid

TCA:

Trichloroacetic acid

tGSH:

Total glutathione

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Acknowledgements

This work was supported by the Natural Science Foundation of Zhejiang Province (no. LY18C130005); the National Key R&D Program, Ministry of Science and Technology, China (no. 2017YFD0300100, 2016YFD0101801). We would like to thank Editage for English language editing.

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  1. Cao Xiaochuang and Wu Meiyan contributed equally to this work.

Authors and Affiliations

  1. State Key Laboratory of Rice Biology, China National Rice Research Institute, No. 359 Tiyuchang Road, Hangzhou, 310006, Zhejiang, People’s Republic of China

    Cao Xiaochuang, Zhu Chunquan, Zhong Chu, Zhang Junhua, Zhu Lianfeng & Jin Qianyu

  2. Hubei Collaborative Innovation Center for Grain Industry/Engineering Research Center of Ecology and Agricultural Use of Wetland, Ministry of Education, Yangtze University, Jingzhou, 434025, Hubei, People’s Republic of China

    Wu Meiyan

  3. Ministry of Education Key Laboratory of Environmental Remediation and Ecosystem Health, College of Environmental and Resource Sciences, Zhejiang University, Hangzhou, 310058, People’s Republic of China

    Wu Lianghuan

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  1. Cao Xiaochuang
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Contributions

CXC, WLH and JQY conceived and designed the experiments. CXC, ZC and ZCQ performed the experiments. CXC, ZJH and ZLF analyzed the data. CXC, WMY, and ZCQ wrote the paper. All authors read and approved the manuscript.

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Correspondence to Cao Xiaochuang or Jin Qianyu.

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Xiaochuang, C., Meiyan, W., Chunquan, Z. et al. Glutamate dehydrogenase mediated amino acid metabolism after ammonium uptake enhances rice growth under aeration condition. Plant Cell Rep 39, 363–379 (2020). https://doi.org/10.1007/s00299-019-02496-w

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