Promotion of apoplastic oxidative burst by artificially selected GhCBSX3A enhances Verticillium dahliae resistance in upland cotton.

SUMMARY: Verticillium wilt (VW) is a devasting disease affecting various plants, including upland cotton, a crucial fiber crop. Despite its impact, the genetic basis underlying cotton's susceptibility or defense against VW remains unclear. Here, we conducted a genome‐wide association study on VW phenotyping in upland cotton and identified a locus on A13 that is significantly associated with VW resistance. We then identified a cystathionine β‐synthase domain gene at A13 locus, GhCBSX3A, which was induced by Verticillium dahliae. Functional analysis, including expression silencing in cotton and overexpression in Arabidopsis thaliana, confirmed that GhCBSX3A is a causal gene at the A13 locus, enhancing SAR‐RBOHs‐mediated apoplastic oxidative burst. We found allelic variation on the TATA‐box of GhCBSX3A promoter attenuated its expression in upland cotton, thereby weakening VW resistance. Interestingly, we discovered that altered artificial selection of GhCBSX3A_R (an elite allele for VW) under different VW pressures during domestication and other improved processes allows specific human needs to be met. Our findings underscore the importance of GhCBSX3A in response to VW, and we propose a model for defense‐associated genes being selected depending on the pathogen's pressure. The identified locus and gene serve as promising targets for VW resistance enhancement in cotton through genetic engineering. Significance Statement: Upland cotton cultivars demonstrate limited resistance to Verticillium wilt (VW), with most studies indicating that upland cotton (AD1) possesses an inherent disadvantage concerning VW resistance. We found that the artificial selection of GhCBSX3A_R, an elite allele for VW resistance, achieved through enhanced reactive oxygen species accumulation, resulted in reduced VW resistance in improved accessions. This evidence supports the idea that the susceptibility against VW may be attributed to a significant decline in VW resistance during upland cotton domestication. [ABSTRACT FROM AUTHOR]