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

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 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.