GhSTZ-Mediated Suppression of Metabolic–Immune Coordination Compromises Cotton Defense Against Verticillium Wilt

Verticillium wilt (VW), caused by <i>Verticillium dahliae</i>, poses a significant threat to global cotton production. Through analysis of public transcriptome databases, this study identified <i>GhSTZ</i>, a C2H2 zinc finger protein transcription factor gene, which was significantly induced by <i>V. dahliae</i>. Suppressing <i>GhSTZ</i> expression via virus-induced gene silencing significantly enhanced cotton resistance to VW. This resistance manifested as a 1.2-fold increase in lignin deposition, optimized ROS (reactive oxygen species) homeostasis, and a 1.3-fold elevation in glucose levels. Transcriptome analysis revealed 338 differentially expressed genes in <i>GhSTZ</i>-silenced plants, with 97 upregulated and 241 downregulated. Key downregulated genes included <i>PME</i> (pectin methylesterase) and <i>PG1-pec</i> (polygalacturonase) in the pentose phosphate pathway, while the key upregulated genes comprised <i>C4H</i> (cinnamate 4-hydroxylase) and <i>C3H</i> (p-coumarate 3-hydroxylase) in the phenylpropanoid biosynthesis pathway. Notably, in the plant-pathogen interaction signaling pathway, approximately half of the genes exhibited upregulated expression while the other half showed downregulation. Protein-protein interaction network analysis further revealed cooperative interaction between <i>PME</i> and the secoisolariciresinol dehydrogenase <i>SIRD</i>. This study is the first to elucidate <i>GhSTZ</i> as a negative regulator that compromises cotton disease resistance through a tripartite mechanism. These findings offer a novel approach to enhancing crop disease resistance by targeting the negative regulatory genes.