Mirids Secrete a TOPLESS-Targeted Protein to Outcompete Cotton Bollworms on Cotton Plant

Insects that coexist on plants often exhibit stunted growth compared to those that live individually. This phenomenon reflects an interspecific competition that draws extensive attention while the underlying mechanisms remain unknown. Mirids (Apolygus lucorum) and cotton bollworms (Helicoverpa armigera) are two common pests in cotton fields. We identified a rapidly evolving protein, ASP1, from the oral secretion of mirids, which can localize in the nucleus of cotton plants. ASP1 specifically targets the transcriptional corepressor TOPLESS (TPL), inhibiting TPL recruitment mediated by NINJA leading to the promoted plant defense response and gossypol accumulation in cotton glands. ASP1-enhanced defense contributes to the resistance to cotton bollworms, while having little impact on mirids. The mesophyll-feeding characteristics allow mirids to avoid most cotton glands thus invalidating the cotton defense. Our investigation reveals the molecular mechanism that mirids employ cotton defense to selectively inhibit cotton bollworm feedings.