A short-chain dehydrogenase/reductase gene confers resistance to Verticillium wilt in cotton and reveals adaptive selection during domestication

IF 6.8 Q1 PLANT SCIENCES

Plant Stress Pub Date : 2025-07-26 DOI:10.1016/j.stress.2025.100971

Mubashir Abbas , Muhammad Jawad Umer , Aamir Ali Abro , Zhang Menghan , Chao Lu , Qiankun Liu , Heng Wang , Mengying Yang , Yiman Liu , Huang Wenjuan , Muhammad Aamir Khan , Muhammad Ali Abid , Muhammad Askari , Muhammad Aneeq Ur Rahman , Yuqing Hou , Jie Zhang , Yanchao Xu , Xiaoyan Cai , Zhongli Zhou , Rui Zhang , Fang Liu

{"title":"A short-chain dehydrogenase/reductase gene confers resistance to Verticillium wilt in cotton and reveals adaptive selection during domestication","authors":"Mubashir Abbas , Muhammad Jawad Umer , Aamir Ali Abro , Zhang Menghan , Chao Lu , Qiankun Liu , Heng Wang , Mengying Yang , Yiman Liu , Huang Wenjuan , Muhammad Aamir Khan , Muhammad Ali Abid , Muhammad Askari , Muhammad Aneeq Ur Rahman , Yuqing Hou , Jie Zhang , Yanchao Xu , Xiaoyan Cai , Zhongli Zhou , Rui Zhang , Fang Liu","doi":"10.1016/j.stress.2025.100971","DOIUrl":null,"url":null,"abstract":"<div><div>Cotton is a globally important fiber crop that faces significant yield losses due to Verticillium wilt caused by Verticillium dahliae. Short-chain dehydrogenase/reductases (SDRs) are NAD(P)(H)-dependent enzymes involved in metabolic pathways and stress responses, but their role in disease resistance is not well understood in cotton. The objective of this study was to investigate the function of GhSDR500 in cotton defense against V. dahliae. A combination of population genetics, pangenome analysis, gene expression profiling, transcription factor binding analysis, and functional validation through Virus-Induced Gene Silencing (VIGS) was employed. Population genetic analysis revealed a favorable GhSDR500 allele selected during cotton domestication. A G > C mutation causing a glycine-to-alanine substitution in the NAD domain was identified, with the G allele strongly favored in modern cultivars due to its association with enhanced resistance. Pangenome analysis further highlighted presence–absence variations and transposable elements around GhSDR500. Expression studies showed strong upregulation of GhSDR500 in resistant cotton varieties during early infection stages. VIGS confirmed its role in disease resistance, as silencing GhSDR500 increased susceptibility to V. dahliae and reduced expression of pathogenesis-related genes. Transcription factor binding analysis identified WRKY genes as key regulators. These results demonstrate that GhSDR500 plays a key role in resistance to V. dahliae and represents a potential target for breeding Verticillium wilt-resistant cotton varieties.</div></div>","PeriodicalId":34736,"journal":{"name":"Plant Stress","volume":"17 ","pages":"Article 100971"},"PeriodicalIF":6.8000,"publicationDate":"2025-07-26","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Plant Stress","FirstCategoryId":"1085","ListUrlMain":"https://www.sciencedirect.com/science/article/pii/S2667064X25002398","RegionNum":0,"RegionCategory":null,"ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"PLANT SCIENCES","Score":null,"Total":0}

引用次数: 0

Abstract

Cotton is a globally important fiber crop that faces significant yield losses due to Verticillium wilt caused by Verticillium dahliae. Short-chain dehydrogenase/reductases (SDRs) are NAD(P)(H)-dependent enzymes involved in metabolic pathways and stress responses, but their role in disease resistance is not well understood in cotton. The objective of this study was to investigate the function of GhSDR500 in cotton defense against V. dahliae. A combination of population genetics, pangenome analysis, gene expression profiling, transcription factor binding analysis, and functional validation through Virus-Induced Gene Silencing (VIGS) was employed. Population genetic analysis revealed a favorable GhSDR500 allele selected during cotton domestication. A G > C mutation causing a glycine-to-alanine substitution in the NAD domain was identified, with the G allele strongly favored in modern cultivars due to its association with enhanced resistance. Pangenome analysis further highlighted presence–absence variations and transposable elements around GhSDR500. Expression studies showed strong upregulation of GhSDR500 in resistant cotton varieties during early infection stages. VIGS confirmed its role in disease resistance, as silencing GhSDR500 increased susceptibility to V. dahliae and reduced expression of pathogenesis-related genes. Transcription factor binding analysis identified WRKY genes as key regulators. These results demonstrate that GhSDR500 plays a key role in resistance to V. dahliae and represents a potential target for breeding Verticillium wilt-resistant cotton varieties.

查看原文本刊更多论文

短链脱氢酶/还原酶基因赋予棉花对黄萎病的抗性，揭示了驯化过程中的适应性选择

棉花是全球重要的纤维作物，由于大丽花黄萎病引起的黄萎病，棉花面临着重大的产量损失。短链脱氢酶/还原酶（SDRs）是NAD(P)(H)依赖性酶，参与代谢途径和胁迫反应，但其在棉花抗病中的作用尚不清楚。本研究旨在探讨GhSDR500在棉花抗大丽花病菌中的作用。采用群体遗传学、泛基因组分析、基因表达谱、转录因子结合分析和病毒诱导基因沉默（VIGS）功能验证相结合的方法。群体遗传分析表明，GhSDR500等位基因在棉花驯化过程中被筛选出。A >；C突变导致NAD结构域甘氨酸到丙氨酸的替换，其中G等位基因在现代品种中受到强烈青睐，因为它与增强的抗性有关。泛基因组分析进一步突出了GhSDR500周围的存在-缺失差异和转座因子。表达研究表明，GhSDR500在抗性棉花品种的早期侵染阶段有明显上调。VIGS证实了其在抗病中的作用，因为沉默GhSDR500增加了对大丽花弧菌的易感性，并降低了致病相关基因的表达。转录因子结合分析确定WRKY基因为关键调控因子。这些结果表明，GhSDR500在抗性大丽花中起关键作用，是培育抗黄萎病棉花品种的潜在靶点。

本文章由计算机程序翻译，如有差异，请以英文原文为准。

求助全文

约1分钟内获得全文求助全文

来源期刊

Plant Stress PLANT SCIENCES-

CiteScore

5.20

自引率

8.00%

发文量

审稿时长

63 days

期刊介绍： The journal Plant Stress deals with plant (or other photoautotrophs, such as algae, cyanobacteria and lichens) responses to abiotic and biotic stress factors that can result in limited growth and productivity. Such responses can be analyzed and described at a physiological, biochemical and molecular level. Experimental approaches/technologies aiming to improve growth and productivity with a potential for downstream validation under stress conditions will also be considered. Both fundamental and applied research manuscripts are welcome, provided that clear mechanistic hypotheses are made and descriptive approaches are avoided. In addition, high-quality review articles will also be considered, provided they follow a critical approach and stimulate thought for future research avenues. Plant Stress welcomes high-quality manuscripts related (but not limited) to interactions between plants and: Lack of water (drought) and excess (flooding), Salinity stress, Elevated temperature and/or low temperature (chilling and freezing), Hypoxia and/or anoxia, Mineral nutrient excess and/or deficiency, Heavy metals and/or metalloids, Plant priming (chemical, biological, physiological, nanomaterial, biostimulant) approaches for improved stress protection, Viral, phytoplasma, bacterial and fungal plant-pathogen interactions. The journal welcomes basic and applied research articles, as well as review articles and short communications. All submitted manuscripts will be subject to a thorough peer-reviewing process.