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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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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