Effect of Nickel Ions on the Physiological and Transcriptional Responses to Carbon and Nitrogen Metabolism in Tomato Roots under Low Nitrogen Levels

Nickel (Ni) is an essential trace element for plant growth and a component of the plant body that has many different functions in plants. Although it has been confirmed that nickel ions (Ni<sup>2+</sup>) havea certain regulatory effect on nitrogen (N) metabolism, there are not enough dat...

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Main Authors: Kun Zhang, Shuhao Li, Yang Xu, Yuqi Zhou, Shengxiang Ran, Huanhuan Zhao, Weiqun Huang, Ru Xu, Fenglin Zhong
Format: Article
Language:English
Published: MDPI AG 2022-09-01
Series:International Journal of Molecular Sciences
Subjects:
Online Access:https://www.mdpi.com/1422-0067/23/19/11398
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author Kun Zhang
Shuhao Li
Yang Xu
Yuqi Zhou
Shengxiang Ran
Huanhuan Zhao
Weiqun Huang
Ru Xu
Fenglin Zhong
author_facet Kun Zhang
Shuhao Li
Yang Xu
Yuqi Zhou
Shengxiang Ran
Huanhuan Zhao
Weiqun Huang
Ru Xu
Fenglin Zhong
author_sort Kun Zhang
collection DOAJ
description Nickel (Ni) is an essential trace element for plant growth and a component of the plant body that has many different functions in plants. Although it has been confirmed that nickel ions (Ni<sup>2+</sup>) havea certain regulatory effect on nitrogen (N) metabolism, there are not enough data to prove whether exogenous Ni<sup>2+</sup> can increase the carbon (C) and N metabolism in the roots of tomato seedlingsunder low-nitrogen (LN) conditions. Therefore, through the present experiment, we revealed the key mechanism of Ni<sup>2+</sup>-mediated tomato root tolerance to LN levels. Tomato plants were cultured at two different N levels (7.66 and 0.383 mmol L<sup>−1</sup>) and two different Ni<sup>2+</sup> levels (0 and 0.1 mg L<sup>−1</sup> NiSO<sub>4</sub> 6H<sub>2</sub>O) under hydroponic conditions. After nine days, we collected roots for physiological, biochemical, and transcriptome sequencing analyses and found that the activities of N assimilation-related enzymes decreased at LN levels. In contrast, Ni<sup>2+</sup> significantly increased the activities of N assimilation-related enzymes and increased the contents of nitrate (NO<sub>3</sub><sup>−</sup>), ammonium (NH<sub>4</sub><sup>+</sup>), and total amino acids. Through root transcriptomic analysis, 3738 differentially expressed genes (DEGs) were identified. DEGs related to C and N metabolism were downregulated after LN application. However, after Ni<sup>2+</sup> treatment, <i>PK</i>, <i>PDHB</i>, <i>GAPDH</i>, <i>NR</i>, <i>NiR</i>, <i>GS</i>, <i>GOGAT</i>, and other DEGs related to C and N metabolism were significantly upregulated. In conclusion, our results suggest that Ni<sup>2+</sup> can regulate the C and N metabolism pathways in tomato roots to alleviate the impact of LN levels.
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spelling doaj.art-b1efb49c7b414bc9984c16f066db78602023-11-23T20:32:30ZengMDPI AGInternational Journal of Molecular Sciences1661-65961422-00672022-09-0123191139810.3390/ijms231911398Effect of Nickel Ions on the Physiological and Transcriptional Responses to Carbon and Nitrogen Metabolism in Tomato Roots under Low Nitrogen LevelsKun Zhang0Shuhao Li1Yang Xu2Yuqi Zhou3Shengxiang Ran4Huanhuan Zhao5Weiqun Huang6Ru Xu7Fenglin Zhong8College of Horticulture, Fujian Agriculture and Forestry University, Fuzhou 350002, ChinaCollege of Horticulture, Fujian Agriculture and Forestry University, Fuzhou 350002, ChinaCollege of Horticulture, Fujian Agriculture and Forestry University, Fuzhou 350002, ChinaCollege of Horticulture, Fujian Agriculture and Forestry University, Fuzhou 350002, ChinaCollege of Horticulture, Fujian Agriculture and Forestry University, Fuzhou 350002, ChinaCollege of Horticulture, Fujian Agriculture and Forestry University, Fuzhou 350002, ChinaFujian Seed Station, Fuzhou 350001, ChinaCollege of Horticulture, Fujian Agriculture and Forestry University, Fuzhou 350002, ChinaCollege of Horticulture, Fujian Agriculture and Forestry University, Fuzhou 350002, ChinaNickel (Ni) is an essential trace element for plant growth and a component of the plant body that has many different functions in plants. Although it has been confirmed that nickel ions (Ni<sup>2+</sup>) havea certain regulatory effect on nitrogen (N) metabolism, there are not enough data to prove whether exogenous Ni<sup>2+</sup> can increase the carbon (C) and N metabolism in the roots of tomato seedlingsunder low-nitrogen (LN) conditions. Therefore, through the present experiment, we revealed the key mechanism of Ni<sup>2+</sup>-mediated tomato root tolerance to LN levels. Tomato plants were cultured at two different N levels (7.66 and 0.383 mmol L<sup>−1</sup>) and two different Ni<sup>2+</sup> levels (0 and 0.1 mg L<sup>−1</sup> NiSO<sub>4</sub> 6H<sub>2</sub>O) under hydroponic conditions. After nine days, we collected roots for physiological, biochemical, and transcriptome sequencing analyses and found that the activities of N assimilation-related enzymes decreased at LN levels. In contrast, Ni<sup>2+</sup> significantly increased the activities of N assimilation-related enzymes and increased the contents of nitrate (NO<sub>3</sub><sup>−</sup>), ammonium (NH<sub>4</sub><sup>+</sup>), and total amino acids. Through root transcriptomic analysis, 3738 differentially expressed genes (DEGs) were identified. DEGs related to C and N metabolism were downregulated after LN application. However, after Ni<sup>2+</sup> treatment, <i>PK</i>, <i>PDHB</i>, <i>GAPDH</i>, <i>NR</i>, <i>NiR</i>, <i>GS</i>, <i>GOGAT</i>, and other DEGs related to C and N metabolism were significantly upregulated. In conclusion, our results suggest that Ni<sup>2+</sup> can regulate the C and N metabolism pathways in tomato roots to alleviate the impact of LN levels.https://www.mdpi.com/1422-0067/23/19/11398nickeltomato rootRNA-seqcarbon and nitrogen metabolismglycolytic pathway-tricarboxylic acid cyclelow nitrogen
spellingShingle Kun Zhang
Shuhao Li
Yang Xu
Yuqi Zhou
Shengxiang Ran
Huanhuan Zhao
Weiqun Huang
Ru Xu
Fenglin Zhong
Effect of Nickel Ions on the Physiological and Transcriptional Responses to Carbon and Nitrogen Metabolism in Tomato Roots under Low Nitrogen Levels
International Journal of Molecular Sciences
nickel
tomato root
RNA-seq
carbon and nitrogen metabolism
glycolytic pathway-tricarboxylic acid cycle
low nitrogen
title Effect of Nickel Ions on the Physiological and Transcriptional Responses to Carbon and Nitrogen Metabolism in Tomato Roots under Low Nitrogen Levels
title_full Effect of Nickel Ions on the Physiological and Transcriptional Responses to Carbon and Nitrogen Metabolism in Tomato Roots under Low Nitrogen Levels
title_fullStr Effect of Nickel Ions on the Physiological and Transcriptional Responses to Carbon and Nitrogen Metabolism in Tomato Roots under Low Nitrogen Levels
title_full_unstemmed Effect of Nickel Ions on the Physiological and Transcriptional Responses to Carbon and Nitrogen Metabolism in Tomato Roots under Low Nitrogen Levels
title_short Effect of Nickel Ions on the Physiological and Transcriptional Responses to Carbon and Nitrogen Metabolism in Tomato Roots under Low Nitrogen Levels
title_sort effect of nickel ions on the physiological and transcriptional responses to carbon and nitrogen metabolism in tomato roots under low nitrogen levels
topic nickel
tomato root
RNA-seq
carbon and nitrogen metabolism
glycolytic pathway-tricarboxylic acid cycle
low nitrogen
url https://www.mdpi.com/1422-0067/23/19/11398
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