Mirids secrete a TOPLESS targeting protein to enhance JA-mediated defense and gossypol accumulation for antagonizing cotton bollworms on cotton plants.

Most coexisting insect species exhibit stunted growth compared to individual species on plants. This phenomenon reflects an interspecific antagonism drawing extensive attention, while the underlying mechanisms remain largely uncharacterized. Mirids (Apolygus lucorum) and cotton bollworms (Helicoverpa armigera) are two common cotton pests. We identified a secretory protein, ASP1, from the oral secretion of mirids, found in the nucleus of mirid-infested cotton leaves. ASP1 specifically targets the transcriptional co-repressor TOPLESS (TPL) and inhibits NINJA-mediated recruitment of TPL, promoting plant defense response and gossypol accumulation in cotton glands. ASP1-enhanced defense inhibits the growth of cotton bollworms on cotton plants, while having limited impact on mirids. The mesophyll-feeding characteristic allows mirids to avoid most cotton glands, invalidating cotton defense. Our investigation reveals the molecular mechanism by which mirids employ cotton defense to selectively inhibit the feeding of cotton bollworms.