Comparative transcriptome analysis of interspecific CSSLs reveals candidate genes and pathways involved in verticillium wilt resistance in cotton (Gossypium hirsutum L.)

Verticillium wilt (VW), known as the ‘cancer’ of cotton, is a vascular disease of cotton caused by Verticillium dahliae, which seriously affects the yield and quality of cotton. Upland cotton (Gossypium hirsutum, Gh) has good yield but low resistance to VW, while Sea-island cotton (G. barbadense, Gb) has excellent resistance to VW and good fiber quality but low yield. Creating chromosome segment substitution lines (CSSLs) from progeny of interspecific cross between Gh and Gb is a way to combine the superior traits of Gh and Gb to breed cotton varieties with high yield and fiber quality as well as good disease resistance. In this study, a CSSL population derived from Emian22 (Gh) × 3–79 (Gb) was subject to disease assay in multiple environments to identify VW-resistant CSSLs. The two CSSLs (M20 and M34) showing stable VW-resistance in different assay conditions together with the VW susceptible parent Emian22 were selected for comparative transcriptome analysis to identify genes associated with cotton response to V. dahliae infection. Significant transcriptome changes were found to occur at each time point (24, 48, and 72 h) after V. dahliae infection in all three lines. Gene ontology (GO) analysis of the DEGs identified in each line revealed enriched terms shared by the three lines or unique to each line. Based on gene expression trend analysis, the DEGs identified in M20, M34, and Emian22 were clustered into 8, 8, and 7 cluster, respectively, with one unique to Emian22 and one unique to both M20 and M34. Weighted gene co-expression network analysis (WGCNA) identified 8 modules significantly related to cotton response to V. dahliae infection, especially the cyan module with 22 hub genes, including two genes (Ghi_D02G10111 and Ghi_A03G10581) encoding probable protein phosphatase 2. Suppressing the expression level of Ghi_D02G10111 (GhPP2C52) by virus-induced gene silencing led to the reduction of VW-resistance, implying GhPP2C52 being a positive regulator of VW-resistance. In addition, genes of the ABA and Ca2+ signaling pathways were found to be associated with the response of cotton plants to V. dahliae infection. The findings of the study revealed the molecular difference between the VW-resistant and VW-susceptible cotton lines. Combining the genetic mapping results of the same population, the results of this study will facilitate cloning and molecular characterization of the genes responsible for VW-resistance observed in M20 and M34 and finally accelerate breeding VW-resistant cotton varieties through marker assisted selection and gene editing.