In the plant response to pathogen infection, many genes’ expression is temporally induced, while few spatially induced expression genes have been reported. Here, we show that GhBOP1 can autonomously expand expression from restrained tissue when Gossypium hirsutum plants are attacked by Verticillium dahliae, which is considered to be spatially induced expression. Loss- and gain-of-function analyses show that GhBOP1 is a positive regulator in the modulation of plant resistance to V. dahliae. Yeast two-hybrid assays, luciferase complementation imaging and GUS reporting show that GhBOP1 interaction with GhTGA3 promotes its activation activity, regulating the expression of down-stream defence-related genes. Moreover, the induced spatial expression of GhBOP1 is accompanied by GhBP1 repression. Both antagonistically regulate the lignin biosynthesis, conferring cotton plants enhanced resistance to V. dahliae. Taken together, these results demonstrate that GhBOP1 is an economic positive regulator participating in plant defence through both the GhBOP1-GhTGA3 module and lignin accumulation.