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Multi-omics analysis reveals WRKY31 and MATE as key regulators of flavonoid-based waterlogging tolerance in Welsh Onion (Allium fistulosum L.)

Yueting Li, Pengtao Yang1, Yu Yuan1, Chao Yan1, Yue Jia1, Yongqin Wang2, Yue Liu1,#, Zhonghua Zhang1,#, Bingsheng Lv1,#

1 Engineering Laboratory of Genetic Improvement of Horticultural Crops of Shandong Province, College of Horticulture, Qingdao Agricultural University, Qingdao 266109, China;

2 State Key Laboratory of Vegetable Biobreeding, National Engineering Research Center for Vegetables, Beijing Key Laboratory of Vegetable Germplasms Improvement, Key Laboratory of Biology and Genetics Improvement of Horticultural Crops (North China), Beijing Vegetable Research Center, Beijing Academy of Agricultural and Forestry Sciences, Beijing 100097, China

 Highlights 

1.Integrated transcriptomic and GWAS analyses identified WRKY31 and MATE as key regulators of flavonoid biosynthesis driving waterlogging tolerance in Welsh onion.

2.The waterlogging-tolerant Welsh onion cultivar BJQC enhances flavonoid accumulation by transcriptionally activating genes in the flavonoid biosynthetic pathway, providing new genetic targets for breeding waterlogging-resistant crops.

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摘要  

淹水胁迫对大葱(Allium fistulosum L.)的生产构成了重大挑战,且气候变化引发的极端天气使这一问题更加严重。揭示耐性分子机制对于培育抗涝品种至关重要。本研究对比了两种大葱品种:BJQC(耐涝品种)和YZDC(涝敏感品种)。淹水处理结果表明,YZDC在淹水胁迫下表现出较高的活性氧(ROS)积累,包括过氧化氢(H2O2)、超氧阴离子(O2⁻)和丙二醛(MDA),死亡率较高。相比之下,BJQC表现出较强的耐涝性,这归因于其能够上调类黄酮生物合成基因,导致淹水胁迫下类黄酮积累增加。转录组学分析发现,BJQC中类黄酮代谢途径相关基因的激活是其耐涝反应的核心。此外,茉莉酸和赤霉素信号通路相关基因也被激活。加权基因共表达网络分析(WGCNA)揭示,WRKY31MATE可能在淹水条件下调控类黄酮生物合成过程中发挥关键作用。使用自然群体的全基因组关联分析(GWAS)结果进一步支持了这些基因在耐涝性中的重要性。我们综合多组学分析,包括表型学、生理学、转录组学和基因组学方法,为揭示大葱水涝反应的分子机制提供了新视角。这些发现突出了WRKY31MATE作为提高作物耐涝性的关键候选基因,在作物育种项目中具有潜在应用价值。

 



Abstract  

Waterlogging poses a major challenge to Welsh onion (Allium fistulosum L.) production, exacerbated by climate change-induced extreme weather. Unraveling the molecular mechanisms of waterlogging tolerance is essential for breeding resilient cultivars. Here, we compared two Welsh onion varieties: BJQC (tolerant) and YZDC (sensitive). Waterlogging treatment revealed that YZDC exhibited higher accumulation of reactive oxygen species (ROS), including hydrogen peroxide (H2O2), superoxide ions (O2⁻), and malondialdehyde (MDA), leading to increased mortality. In contrast, BJQC demonstrated enhanced waterlogging tolerance, attributed to its ability to upregulate flavonoid biosynthesis genes, resulting in higher flavonoid accumulation under waterlogging stress. Transcriptomic analysis identified that the activation of flavonoid pathway-related genes in BJQC was central to this response. In addition, genes associated with jasmonic acid and gibberellin signaling were also activated. Weighted gene co-expression network analysis (WGCNA) revealed that WRKY31 and MATE likely play critical roles in regulating flavonoid biosynthesis under waterlogging conditions. Genome-wide association study (GWAS) results from natural populations further supported the significance of these genes in waterlogging tolerance. Our comprehensive multi-omics analysis, including phenotypic, physiological, transcriptomic, and genomic approaches, provides new insights into the molecular mechanisms underlying Welsh onion responses to waterlogging. These findings highlight WRKY31 and MATE as key candidates for improving waterlogging tolerance in crop breeding programs. 

Keywords:  Welsh onion       waterlogging tolerance       GWAS       RNA-seq  
Online: 31 December 2025  
Fund: 

This work was supported by grants from the Shandong Province Natural Science Foundation (ZR2024YQ022), the Key Research and Development Program of Shandong Province (Agricultural Seed Improvement Project, 2024LZGC014), Breeding Plan of Shandong Provincial Qingchuang Research Team (2021), the National Natural Science Foundation of China (32170313), the Taishan Scholar Foundation of the People’s Government of Shandong Province in China (tsqn202211193).

About author:  Yueting Li, E-mail: liyueting033@163.com; #Correspondence Bingsheng Lv, Tel: +158 6671 9328, E-mail: lvbingsheng@qau.edu.cn

Cite this article: 

Yueting Li, Pengtao Yang, Yu Yuan, Chao Yan, Yue Jia, Yongqin Wang, Yue Liu, Zhonghua Zhang, Bingsheng Lv. 2025. Multi-omics analysis reveals WRKY31 and MATE as key regulators of flavonoid-based waterlogging tolerance in Welsh Onion (Allium fistulosum L.). Journal of Integrative Agriculture, Doi:10.1016/j.jia.2025.12.068

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