Integrative Transcriptomic and Proteomic Analysis Reveals an Alternative Molecular Network of Glutamine Synthetase 2 Corresponding to Nitrogen Deficiency in Rice (<i>Oryza sativa</i> L.)

Nitrogen (N) is an essential nutrient for plant growth and development. The root system architecture is a highly regulated morphological system, which is sensitive to the availability of nutrients, such as N. Phenotypic characterization of roots from LY9348 (a rice variety with high nitrogen use eff...

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Main Authors: Ting Liang, Zhengqing Yuan, Lu Fu, Menghan Zhu, Xiaoyun Luo, Wuwu Xu, Huanran Yuan, Renshan Zhu, Zhongli Hu, Xianting Wu
Format: Article
Language:English
Published: MDPI AG 2021-07-01
Series:International Journal of Molecular Sciences
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Online Access:https://www.mdpi.com/1422-0067/22/14/7674
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spelling doaj-94c300aefaaf4c66a4c807938cf59b022021-07-23T13:46:46ZengMDPI AGInternational Journal of Molecular Sciences1661-65961422-00672021-07-01227674767410.3390/ijms22147674Integrative Transcriptomic and Proteomic Analysis Reveals an Alternative Molecular Network of Glutamine Synthetase 2 Corresponding to Nitrogen Deficiency in Rice (<i>Oryza sativa</i> L.)Ting Liang0Zhengqing Yuan1Lu Fu2Menghan Zhu3Xiaoyun Luo4Wuwu Xu5Huanran Yuan6Renshan Zhu7Zhongli Hu8Xianting Wu9State Key Laboratory of Hybrid Rice, Wuhan University, Wuhan 430072, ChinaState Key Laboratory of Hybrid Rice, Wuhan University, Wuhan 430072, ChinaState Key Laboratory of Hybrid Rice, Wuhan University, Wuhan 430072, ChinaState Key Laboratory of Hybrid Rice, Wuhan University, Wuhan 430072, ChinaState Key Laboratory of Hybrid Rice, Wuhan University, Wuhan 430072, ChinaState Key Laboratory of Hybrid Rice, Wuhan University, Wuhan 430072, ChinaState Key Laboratory of Hybrid Rice, Wuhan University, Wuhan 430072, ChinaState Key Laboratory of Hybrid Rice, Wuhan University, Wuhan 430072, ChinaState Key Laboratory of Hybrid Rice, Wuhan University, Wuhan 430072, ChinaState Key Laboratory of Hybrid Rice, Wuhan University, Wuhan 430072, ChinaNitrogen (N) is an essential nutrient for plant growth and development. The root system architecture is a highly regulated morphological system, which is sensitive to the availability of nutrients, such as N. Phenotypic characterization of roots from LY9348 (a rice variety with high nitrogen use efficiency (NUE)) treated with 0.725 mM NH<sub>4</sub>NO<sub>3</sub> (1/4N) was remarkable, especially primary root (PR) elongation, which was the highest. A comprehensive analysis was performed for transcriptome and proteome profiling of LY9348 roots between 1/4N and 2.9 mM NH<sub>4</sub>NO<sub>3</sub> (1N) treatments. The results indicated 3908 differential expression genes (DEGs; 2569 upregulated and 1339 downregulated) and 411 differential abundance proteins (DAPs; 192 upregulated and 219 downregulated). Among all DAPs in the proteome, glutamine synthetase (GS2), a chloroplastic ammonium assimilation protein, was the most upregulated protein identified. The unexpected concentration of GS2 from the shoot to the root in the 1/4N treatment indicated that the presence of an alternative pathway of N assimilation regulated by GS2 in LY9348 corresponded to the low N signal, which was supported by GS enzyme activity and glutamine/glutamate (Gln/Glu) contents analysis. In addition, N transporters (<i>NRT2.1</i>, <i>NRT2.2</i>, <i>NRT2.3</i>, <i>NRT2.4</i>, <i>NAR2.1</i>, <i>AMT1.3</i>, <i>AMT1.2</i>, and putative <i>AMT3.3</i>) and N assimilators (<i>NR2</i>, <i>GS1;1</i>, <i>GS1;2</i>, <i>GS1;3</i>, <i>NADH-GOGAT2</i>, and <i>AS2</i>) were significantly induced during the long-term N-deficiency response at the transcription level (14 days). Moreover, the Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway analysis demonstrated that phenylpropanoid biosynthesis and glutathione metabolism were significantly modulated by N deficiency. Notably, many transcription factors and plant hormones were found to participate in root morphological adaptation. In conclusion, our study provides valuable information to further understand the response of rice roots to N-deficiency stress.https://www.mdpi.com/1422-0067/22/14/7674riceroot system architecturetranscriptomeproteomeN availability
collection DOAJ
language English
format Article
sources DOAJ
author Ting Liang
Zhengqing Yuan
Lu Fu
Menghan Zhu
Xiaoyun Luo
Wuwu Xu
Huanran Yuan
Renshan Zhu
Zhongli Hu
Xianting Wu
spellingShingle Ting Liang
Zhengqing Yuan
Lu Fu
Menghan Zhu
Xiaoyun Luo
Wuwu Xu
Huanran Yuan
Renshan Zhu
Zhongli Hu
Xianting Wu
Integrative Transcriptomic and Proteomic Analysis Reveals an Alternative Molecular Network of Glutamine Synthetase 2 Corresponding to Nitrogen Deficiency in Rice (<i>Oryza sativa</i> L.)
International Journal of Molecular Sciences
rice
root system architecture
transcriptome
proteome
N availability
author_facet Ting Liang
Zhengqing Yuan
Lu Fu
Menghan Zhu
Xiaoyun Luo
Wuwu Xu
Huanran Yuan
Renshan Zhu
Zhongli Hu
Xianting Wu
author_sort Ting Liang
title Integrative Transcriptomic and Proteomic Analysis Reveals an Alternative Molecular Network of Glutamine Synthetase 2 Corresponding to Nitrogen Deficiency in Rice (<i>Oryza sativa</i> L.)
title_short Integrative Transcriptomic and Proteomic Analysis Reveals an Alternative Molecular Network of Glutamine Synthetase 2 Corresponding to Nitrogen Deficiency in Rice (<i>Oryza sativa</i> L.)
title_full Integrative Transcriptomic and Proteomic Analysis Reveals an Alternative Molecular Network of Glutamine Synthetase 2 Corresponding to Nitrogen Deficiency in Rice (<i>Oryza sativa</i> L.)
title_fullStr Integrative Transcriptomic and Proteomic Analysis Reveals an Alternative Molecular Network of Glutamine Synthetase 2 Corresponding to Nitrogen Deficiency in Rice (<i>Oryza sativa</i> L.)
title_full_unstemmed Integrative Transcriptomic and Proteomic Analysis Reveals an Alternative Molecular Network of Glutamine Synthetase 2 Corresponding to Nitrogen Deficiency in Rice (<i>Oryza sativa</i> L.)
title_sort integrative transcriptomic and proteomic analysis reveals an alternative molecular network of glutamine synthetase 2 corresponding to nitrogen deficiency in rice (<i>oryza sativa</i> l.)
publisher MDPI AG
series International Journal of Molecular Sciences
issn 1661-6596
1422-0067
publishDate 2021-07-01
description Nitrogen (N) is an essential nutrient for plant growth and development. The root system architecture is a highly regulated morphological system, which is sensitive to the availability of nutrients, such as N. Phenotypic characterization of roots from LY9348 (a rice variety with high nitrogen use efficiency (NUE)) treated with 0.725 mM NH<sub>4</sub>NO<sub>3</sub> (1/4N) was remarkable, especially primary root (PR) elongation, which was the highest. A comprehensive analysis was performed for transcriptome and proteome profiling of LY9348 roots between 1/4N and 2.9 mM NH<sub>4</sub>NO<sub>3</sub> (1N) treatments. The results indicated 3908 differential expression genes (DEGs; 2569 upregulated and 1339 downregulated) and 411 differential abundance proteins (DAPs; 192 upregulated and 219 downregulated). Among all DAPs in the proteome, glutamine synthetase (GS2), a chloroplastic ammonium assimilation protein, was the most upregulated protein identified. The unexpected concentration of GS2 from the shoot to the root in the 1/4N treatment indicated that the presence of an alternative pathway of N assimilation regulated by GS2 in LY9348 corresponded to the low N signal, which was supported by GS enzyme activity and glutamine/glutamate (Gln/Glu) contents analysis. In addition, N transporters (<i>NRT2.1</i>, <i>NRT2.2</i>, <i>NRT2.3</i>, <i>NRT2.4</i>, <i>NAR2.1</i>, <i>AMT1.3</i>, <i>AMT1.2</i>, and putative <i>AMT3.3</i>) and N assimilators (<i>NR2</i>, <i>GS1;1</i>, <i>GS1;2</i>, <i>GS1;3</i>, <i>NADH-GOGAT2</i>, and <i>AS2</i>) were significantly induced during the long-term N-deficiency response at the transcription level (14 days). Moreover, the Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway analysis demonstrated that phenylpropanoid biosynthesis and glutathione metabolism were significantly modulated by N deficiency. Notably, many transcription factors and plant hormones were found to participate in root morphological adaptation. In conclusion, our study provides valuable information to further understand the response of rice roots to N-deficiency stress.
topic rice
root system architecture
transcriptome
proteome
N availability
url https://www.mdpi.com/1422-0067/22/14/7674
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