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

Yu-Pei Mu; Dian-Yang Chen; Yu-Jie Liu; Ming-Yu Zhu; Xian Zhang; Yin Tang; Jia-Ling Lin; Mu-Yang Wang; Xiao-Xia Shangguan; Xiao-Ya Chen; Chengshu Wang; Ying-Bo Mao

doi:10.1016/j.molp.2024.09.008

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

Mol Plant. 2024 Sep 23:S1674-2052(24)00297-1. doi: 10.1016/j.molp.2024.09.008. Online ahead of print.

Authors

Affiliations

¹ CAS Key Laboratory of Insect Developmental and Evolutionary Biology, CAS Center for Excellence in Molecular Plant Sciences, Shanghai Institute of Plant Physiology and Ecology, University of CAS, Chinese Academy of Sciences, Shanghai 200032, China.
² National Key Laboratory of Plant Molecular Genetics, CAS Center for Excellence in Molecular Plant Sciences, Shanghai Institute of Plant Physiology and Ecology, University of CAS, Chinese Academy of Sciences, Shanghai 200032, China.
³ Institute of Cotton Research, Shanxi Agricultural University, Yuncheng 044000, China.
⁴ CAS Key Laboratory of Insect Developmental and Evolutionary Biology, CAS Center for Excellence in Molecular Plant Sciences, Shanghai Institute of Plant Physiology and Ecology, University of CAS, Chinese Academy of Sciences, Shanghai 200032, China. Electronic address: ybmao@cemps.ac.cn.

PMID: 39318096
DOI: 10.1016/j.molp.2024.09.008

Abstract

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

Keywords: corepressor TOPLESS; cotton bollworms (Helicoverpa armigera); mirids (Apolygus lucorum); oral secretion; plant defense.