A panoramic view of cotton resistance to Verticillium dahliae: From genetic architectures to precision genomic selection
Abstract Investigating the genetic regulatory mechanisms underlying complex traits forms the foundation for crop improvement. Verticillium wilt (VW), caused by Verticillium dahliae (V. dahliae), is one of the most devastating diseases affecting crop production worldwide. However, the genetic basis u...
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2025-06-01
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| Online Access: | https://doi.org/10.1002/imt2.70029 |
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| author | Xiaojun Zhang Shiming Liu Peng Wu Wanying Xu Dingyi Yang Yuqing Ming Shenghua Xiao Weiran Wang Jun Ma Xinhui Nie Zhan Gao Junyuan Lv Fei Wu Zhaoguang Yang Baoxin Zheng Ping Du Jiangmei Wang Hao Ding Jie Kong Alifu Aierxi Yu Yu Wei Gao Zhongxu Lin Chunyuan You Keith Lindsey Nataša Štajner Maojun Wang Jiahe Wu Shuangxia Jin Xianlong Zhang Longfu Zhu |
| author_facet | Xiaojun Zhang Shiming Liu Peng Wu Wanying Xu Dingyi Yang Yuqing Ming Shenghua Xiao Weiran Wang Jun Ma Xinhui Nie Zhan Gao Junyuan Lv Fei Wu Zhaoguang Yang Baoxin Zheng Ping Du Jiangmei Wang Hao Ding Jie Kong Alifu Aierxi Yu Yu Wei Gao Zhongxu Lin Chunyuan You Keith Lindsey Nataša Štajner Maojun Wang Jiahe Wu Shuangxia Jin Xianlong Zhang Longfu Zhu |
| author_sort | Xiaojun Zhang |
| collection | DOAJ |
| description | Abstract Investigating the genetic regulatory mechanisms underlying complex traits forms the foundation for crop improvement. Verticillium wilt (VW), caused by Verticillium dahliae (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 F2:3 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. |
| format | Article |
| id | doaj-art-833c2ac127b14d4f9abbd89f0ab29886 |
| institution | OA Journals |
| issn | 2770-596X |
| language | English |
| publishDate | 2025-06-01 |
| publisher | Wiley |
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| spelling | doaj-art-833c2ac127b14d4f9abbd89f0ab298862025-08-20T02:24:23ZengWileyiMeta2770-596X2025-06-0143n/an/a10.1002/imt2.70029A panoramic view of cotton resistance to Verticillium dahliae: From genetic architectures to precision genomic selectionXiaojun Zhang0Shiming Liu1Peng Wu2Wanying Xu3Dingyi Yang4Yuqing Ming5Shenghua Xiao6Weiran Wang7Jun Ma8Xinhui Nie9Zhan Gao10Junyuan Lv11Fei Wu12Zhaoguang Yang13Baoxin Zheng14Ping Du15Jiangmei Wang16Hao Ding17Jie Kong18Alifu Aierxi19Yu Yu20Wei Gao21Zhongxu Lin22Chunyuan You23Keith Lindsey24Nataša Štajner25Maojun Wang26Jiahe Wu27Shuangxia Jin28Xianlong Zhang29Longfu Zhu30National Key Laboratory of Crop Genetic Improvement Huazhong Agricultural University Wuhan ChinaNational Key Laboratory of Crop Genetic Improvement Huazhong Agricultural University Wuhan ChinaNational Key Laboratory of Crop Genetic Improvement Huazhong Agricultural University Wuhan ChinaNational Key Laboratory of Crop Genetic Improvement Huazhong Agricultural University Wuhan ChinaNational Key Laboratory of Crop Genetic Improvement Huazhong Agricultural University Wuhan ChinaNational Key Laboratory of Crop Genetic Improvement Huazhong Agricultural University Wuhan ChinaNational Key Laboratory of Crop Genetic Improvement Huazhong Agricultural University Wuhan ChinaNational Key Laboratory of Crop Genetic Improvement Huazhong Agricultural University Wuhan ChinaInstitute of Economic Crops Xinjiang Academy of Agricultural Sciences Urumqi ChinaCollege of Agriculture Shihezi University Shihezi ChinaNational Key Laboratory of Crop Genetic Improvement Huazhong Agricultural University Wuhan ChinaNational Key Laboratory of Crop Genetic Improvement Huazhong Agricultural University Wuhan ChinaNational Key Laboratory of Crop Genetic Improvement Huazhong Agricultural University Wuhan ChinaNational Key Laboratory of Crop Genetic Improvement Huazhong Agricultural University Wuhan ChinaNational Key Laboratory of Crop Genetic Improvement Huazhong Agricultural University Wuhan ChinaNational Key Laboratory of Crop Genetic Improvement Huazhong Agricultural University Wuhan ChinaNational Key Laboratory of Crop Genetic Improvement Huazhong Agricultural University Wuhan ChinaNational Key Laboratory of Crop Genetic Improvement Huazhong Agricultural University Wuhan ChinaInstitute of Economic Crops Xinjiang Academy of Agricultural Sciences Urumqi ChinaInstitute of Economic Crops Xinjiang Academy of Agricultural Sciences Urumqi ChinaCotton Research Institute Xinjiang Academy of Agriculture and Reclamation Science Shihezi ChinaState Key Laboratory of Cotton Biology Henan University Kaifeng ChinaNational Key Laboratory of Crop Genetic Improvement Huazhong Agricultural University Wuhan ChinaNational Key Laboratory of Crop Genetic Improvement Huazhong Agricultural University Wuhan ChinaDepartment of Biosciences Durham University Durham UKBiotechnical Faculty University of Ljubljana Ljubljana SloveniaNational Key Laboratory of Crop Genetic Improvement Huazhong Agricultural University Wuhan ChinaState Key Laboratory of Plant Genomics, Institute of Microbiology Chinese Academy of Sciences Beijing ChinaNational Key Laboratory of Crop Genetic Improvement Huazhong Agricultural University Wuhan ChinaNational Key Laboratory of Crop Genetic Improvement Huazhong Agricultural University Wuhan ChinaNational Key Laboratory of Crop Genetic Improvement Huazhong Agricultural University Wuhan ChinaAbstract Investigating the genetic regulatory mechanisms underlying complex traits forms the foundation for crop improvement. Verticillium wilt (VW), caused by Verticillium dahliae (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 F2:3 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.https://doi.org/10.1002/imt2.70029armadillo‐repeat proteincottongenomic selectiongenome‐wide association studiesROS homeostasistranscriptome‐wide association studies |
| spellingShingle | Xiaojun Zhang Shiming Liu Peng Wu Wanying Xu Dingyi Yang Yuqing Ming Shenghua Xiao Weiran Wang Jun Ma Xinhui Nie Zhan Gao Junyuan Lv Fei Wu Zhaoguang Yang Baoxin Zheng Ping Du Jiangmei Wang Hao Ding Jie Kong Alifu Aierxi Yu Yu Wei Gao Zhongxu Lin Chunyuan You Keith Lindsey Nataša Štajner Maojun Wang Jiahe Wu Shuangxia Jin Xianlong Zhang Longfu Zhu A panoramic view of cotton resistance to Verticillium dahliae: From genetic architectures to precision genomic selection iMeta armadillo‐repeat protein cotton genomic selection genome‐wide association studies ROS homeostasis transcriptome‐wide association studies |
| title | A panoramic view of cotton resistance to Verticillium dahliae: From genetic architectures to precision genomic selection |
| title_full | A panoramic view of cotton resistance to Verticillium dahliae: From genetic architectures to precision genomic selection |
| title_fullStr | A panoramic view of cotton resistance to Verticillium dahliae: From genetic architectures to precision genomic selection |
| title_full_unstemmed | A panoramic view of cotton resistance to Verticillium dahliae: From genetic architectures to precision genomic selection |
| title_short | A panoramic view of cotton resistance to Verticillium dahliae: From genetic architectures to precision genomic selection |
| title_sort | panoramic view of cotton resistance to verticillium dahliae from genetic architectures to precision genomic selection |
| topic | armadillo‐repeat protein cotton genomic selection genome‐wide association studies ROS homeostasis transcriptome‐wide association studies |
| url | https://doi.org/10.1002/imt2.70029 |
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