Nitrogen application regulates antioxidant capacity and flavonoid metabolism, especially quercetin, in grape seedlings under salt stress

doi:10.1016/j.jia.2024.07.013

Journal of Integrative Agriculture

2024, Vol. 23

Issue (12): 4074-4092 DOI: 10.1016/j.jia.2024.07.013

Special Issue: 园艺作物品质提升与逆境适应性Horticulture——Quality Improvement & Stress adaptation

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Nitrogen application regulates antioxidant capacity and flavonoid metabolism, especially quercetin, in grape seedlings under salt stress

Congcong Zhang¹, Han Wang¹, Guojie Nai¹, Lei Ma³, Xu Lu¹, Haokai Yan¹, Meishuang Gong², Yuanyuan Li², Ying Lai², Zhihui Pu², Li Wei², Guiping Chen³, Ping Sun², Baihong Chen¹, Shaoying Ma⁴, Sheng Li^{1, 2, 5#}

¹College of Horticulture, Gansu Agricultural University, Lanzhou 730070, China
² College of Life Science and Technology, Gansu Agricultural University, Lanzhou 730070, China
³ College of Agronomy, Gansu Agricultural University, Lanzhou 730070, China
⁴ Laboratory and Practice Base Management Center, Gansu Agricultural University, Lanzhou 730070, China
⁵ State Key Laboratory of Aridland Crop Science, Gansu Agricultural University, Lanzhou 730070, China

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摘要

盐胁迫是一种典型的非生物胁迫，导致植物生长缓慢、发育迟缓、产量和果实品质下降。施肥是保证作物正常生长的必要措施，其中，氮素更是关键元素。研究报道氮肥施加可提高作物耐盐性，但是，氮肥对葡萄耐盐性的影响尚不清楚。因此，本研究以酿酒葡萄幼苗‘黑比诺’为植物材料，研究200 mmol L^-1NaCl处理下施用0.01和0.1 mol L^-1 硝酸铵（N）对葡萄耐盐性的影响。通过对葡萄幼苗叶片的生理指标、转录组和代谢组分析，发现0.01 mol L^-1的N施加显著降低了盐胁迫下葡萄叶片中超氧阴离子（O₂^.-）的积累，提高了超氧化物歧化酶（SOD）和过氧化物酶（POD）的活性，促进了抗坏血酸（AsA）和谷胱甘肽（GSH）的积累。转录组和代谢组的联合分析表明，黄酮生物合成途径（ko00941）和黄酮和黄酮醇生物合成途径（ko00944）是关键的响应通路。进一步发现，槲皮素（C00389）的积累受到盐和氮的显著调节。同时，筛选到10个关键差异基因与槲皮素含量变化高度相关（R²>0.9）并构成互作网络。此外，我们也发现，盐胁迫下叶面喷施槲皮素可提高葡萄的SOD和POD活性，增加AsA和GSH的含量，降低H₂O₂和O₂^.-的含量。因此，本研究应用氮肥和槲皮素改善了葡萄的耐盐性，并鉴定到关键的响应基因，此结果为葡萄耐盐性的提高和分子机制研究提供了新的思路。

Abstract

Salt stress is a typical abiotic stress in plants that causes slow growth, stunting, and reduced yield and fruit quality. Fertilization is necessary to ensure proper crop growth. However, the effect of fertilization on salt tolerance in grapevine is unclear. In this study, we investigated the effect of nitrogen fertilizer (0.01 and 0.1 mol L^–1 NH₄NO₃) application on the salt (200 mmol L^–1 NaCl) tolerance of grapevine based on physiological indices, and transcriptomic and metabolomic analyses. The results revealed that 0.01 mol L^–1 NH₄NO₃ supplementation significantly reduced the accumulation of superoxide anion (O₂^–·), enhanced the activities of superoxide dismutase (SOD) and peroxidase (POD), and improved the levels of ascorbic acid (AsA) and glutathione (GSH) in grape leaves compared to salt treatment alone. Specifically, joint transcriptome and metabolome analyses showed that the differentially expressed genes (DEGs) and differentially accumulated metabolites (DAMs) were significantly enriched in the flavonoid biosynthesis pathway (ko00941) and the flavone and flavonol biosynthesis pathway (ko00944). In particular, the relative content of quercetin (C00389) was markedly regulated by salt and nitrogen. Further analysis revealed that exogenous foliar application of quercetin improved the SOD and POD activities, increased the AsA and GSH contents, and reduced the H₂O₂and O₂^–· contents. Meanwhile, 10 hub DEGs, which had high Pearson correlations (R²>0.9) with quercetin, were repressed by nitrogen. In conclusion, all the results indicated that moderate nitrogen and quercetin application under salt stress enhanced the antioxidant system defense response, thus providing a new perspective for improving salt tolerance in grapes.

Keywords: grapevine salt stress nitrogen multi-omics quercetin antioxidant

Received: 07 September 2023 Accepted: 25 April 2024

Fund:

This work was supported by the Key Talent Project of Gansu Provincial Party Committee Organization Department Funding, China (2023RCXM23), the Industrial Support of Gansu Provincial Department of Education Funding, China (2021CYZC-55) and the Key Research and Development Projects of Gansu Provincial Funding, China (21YF5NA090).

About author: Congcong Zhang, E-mail: 919634096@qq.com; #Correspondence Sheng Li, E-mail: lish@gsau.edu.cn

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Congcong Zhang, Han Wang, Guojie Nai, Lei Ma, Xu Lu, Haokai Yan, Meishuang Gong, Yuanyuan Li, Ying Lai, Zhihui Pu, Li Wei, Guiping Chen, Ping Sun, Baihong Chen, Shaoying Ma, Sheng Li. 2024. Nitrogen application regulates antioxidant capacity and flavonoid metabolism, especially quercetin, in grape seedlings under salt stress. Journal of Integrative Agriculture, 23(12): 4074-4092.

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