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A panoramic view of cotton resistance to <i>Verticillium dahliae</i>: From genetic architectures to precision genomic selection

Xiaojun ZhangHubei Hongshan Laboratory Wuhan ChinaShiming LiuHubei Hongshan Laboratory Wuhan ChinaPeng WuNational Key Laboratory of Crop Genetic Improvement Huazhong Agricultural University Wuhan ChinaWanying XuHubei Hongshan Laboratory Wuhan ChinaDingyi YangHubei Hongshan Laboratory Wuhan ChinaYuqing MingHubei Hongshan Laboratory Wuhan ChinaShenghua XiaoNational Key Laboratory of Crop Genetic Improvement Huazhong Agricultural University Wuhan ChinaWeiran WangInstitute of Economic Crops Xinjiang Academy of Agricultural Sciences Urumqi ChinaJun MaInstitute of Economic Crops Xinjiang Academy of Agricultural Sciences Urumqi ChinaXinhui NieCollege of Agriculture Shihezi University Shihezi ChinaZhan GaoNational Key Laboratory of Crop Genetic Improvement Huazhong Agricultural University Wuhan ChinaJunyuan LvHubei Hongshan Laboratory Wuhan ChinaFei WuHubei Hongshan Laboratory Wuhan ChinaZhaoguang YangNational Key Laboratory of Crop Genetic Improvement Huazhong Agricultural University Wuhan ChinaBaoxin ZhengHubei Hongshan Laboratory Wuhan ChinaPing DuHubei Hongshan Laboratory Wuhan ChinaJiangmei WangHubei Hongshan Laboratory Wuhan ChinaHao DingNational Key Laboratory of Crop Genetic Improvement Huazhong Agricultural University Wuhan ChinaJie KongInstitute of Economic Crops Xinjiang Academy of Agricultural Sciences Urumqi ChinaAlifu AierxiInstitute of Economic Crops Xinjiang Academy of Agricultural Sciences Urumqi ChinaYu YuCotton Research Institute Xinjiang Academy of Agriculture and Reclamation Science Shihezi ChinaWei GaoState Key Laboratory of Cotton Biology Henan University Kaifeng ChinaZhongxu LinNational Key Laboratory of Crop Genetic Improvement Huazhong Agricultural University Wuhan ChinaChunyuan YouHubei Hongshan Laboratory Wuhan ChinaKeith LindseyDepartment of Biosciences Durham University Durham UKNataša ŠtajnerBiotechnical Faculty University of Ljubljana Ljubljana SloveniaMaojun WangHubei Hongshan Laboratory Wuhan ChinaJiahe WuState Key Laboratory of Plant Genomics, Institute of Microbiology Chinese Academy of Sciences Beijing ChinaShuangxia JinHubei Hongshan Laboratory Wuhan ChinaXianlong ZhangHubei Hongshan Laboratory Wuhan ChinaLongfu ZhuHubei Hongshan Laboratory Wuhan China
2025en
ABI

Аннотация

Abstract Investigating the genetic regulatory mechanisms underlying complex traits forms the foundation for crop improvement. Verticillium wilt (VW), caused by Verticillium dahlia e ( V. dahliae ), is one of the most devastating diseases affecting crop production worldwide. However, the genetic basis underlying crop resistance to V. dahliae remains largely obscure, hindering progress in the genomic selection for VW resistance breeding. Here, we unraveled the genetic architectures and regulatory landscape of VW resistance in cotton by combining genome‐wide association studies (GWAS) and transcriptome‐wide association studies (TWAS) using 1152 transcriptomes derived from 290 cotton accessions. We identified 10 reliable quantitative trait loci (QTLs) associated with VW resistance across multiple environments. These QTLs showed a pyramiding resistance effect and exhibited promising efficacy in the genomic prediction of cotton's VW resistance supported by an F 2:3 population. Moreover, trace analysis of these elite alleles revealed a notably increased utilization of Lsnp1, Lsnp4, Lsnp5, Lsnp8, and Lsnp9, which potentially contribute to the improvement of VW resistance in Chinese cotton breeding since the 1990s. We also identified remarkable gene modules and expression QTL (eQTL) hotspots related to the regulation of reactive oxygen species (ROS) homeostasis and immune response. Furthermore, 15 candidate causal genes were prioritized by TWAS. Knocking down eight genes with a negative effect significantly enhanced cotton resistance to V. dahliae . Among them, GhARM , encoding an armadillo (ARM)‐repeat protein, was verified to modulate cotton resistance to V. dahliae by regulating ROS homeostasis. Overall, this study updates the understanding of the genetic basis and regulatory mechanisms of cotton's VW resistance, providing valuable strategies for VW management through genomic selection in cotton breeding.

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