A small peptide APP3-14 disrupts pathogen-insect mutualism by modulating plant MYC2-mediated olfactory defense.
Pingzhi Zhao, Yanwei Sun, Xiaoyue Chen, Jingyin Zhang, Huan Yang, Xiaojiang Hao, Rongxiang Fang, Jian Ye
Abstract
Open AccessThe dissemination of insect-borne plant pathogens relies on their ability to influence vector behavior. Certain bacteria-infected plants exhibit increased attractiveness to vectors; however, the underlying mechanisms remain poorly characterized. Huanglongbing (HLB), a devastating citrus disease, is primarily caused by the bacterium "Candidatus Liberibacter asiaticus" (CLas) and transmitted by psyllid vectors. In this study, we demonstrate that the effector protein SDE5, secreted by CLas, suppresses the biosynthesis of volatile terpenoids in host citrus plants, thereby enhancing psyllid attraction. Biochemically, SDE5 functions as an inhibitor of bacterial C-type lysozyme, facilitating both CLas infection and psyllid vector attraction. Two plant U-box (PUB) E3 ligases, PUB10 and PUB21, are recruited by SDE5 to promote ubiquitination and proteasomal degradation of MYC2, a key transcription factor in jasmonate signaling and terpene-based anti-herbivore defenses. Furthermore, SDE5 interferes with MYC2 dimerization, diminishing its ability to activate terpene biosynthesis genes. This dual suppression markedly reduces volatile terpenoid emissions in SDE5-transgenic citrus lines, resulting in increased psyllid attraction and enhanced psyllid fitness. Conversely, the anti-proteolysis peptide 3-14 (APP 3-14), which stabilizes the MYC2 protein and inhibits the HLB pathogen, enhances volatile terpenoid emission and repels psyllids. These findings provide a novel strategy for disrupting mutualistic interactions between plant bacterial pathogens and insect vectors by modulation of olfactory defense.