Jie Cheng , Jing-Kai Liu , Tian-Li Wang , Wei Wei , Hui-Ming Xiang , Xian-Wei Li , Rui-Yan Ma , Zhi-Guo Zhao
{"title":"Myosuppressin signaling deficiency affects ovarian development via repression of 20-hydroxyecdysone biosynthesis in Grapholita molesta","authors":"Jie Cheng , Jing-Kai Liu , Tian-Li Wang , Wei Wei , Hui-Ming Xiang , Xian-Wei Li , Rui-Yan Ma , Zhi-Guo Zhao","doi":"10.1016/j.pestbp.2024.106116","DOIUrl":null,"url":null,"abstract":"<div><p>The steroid 20-hydroxyecdysone (20E) is crucial in regulating ovarian development. However, the neuropeptidergic mechanisms underlying ovarian development via 20E are underexplored. In this study, we investigated myosuppressin (MS) signaling in the dominant fruit pest <em>Grapholita molesta</em> and revealed that MS signaling is necessary for 20E biosynthesis during ovarian maturation. Pharmacological and molecular docking analyses confirmed that the GmMS mature peptide could activate its receptor GmMSR. Additionally, transcript expression analyses of <em>GmMS</em> and <em>GmMSR</em> showed different distribution patterns in adults. Notably, <em>GmMSR</em> was also detected in the ovaries of sexually mature females. RNAi-mediated dysfunction of <em>GmMS</em> or <em>GmMSR</em> specifically decreased fertility in females. Furthermore, <em>GmMS</em> or <em>GmMSR</em> knockdown decreased vitellogenin synthesis and uptake, thereby delaying ovarian development. RNA-seq, gene expression validation, and hormone quantification further revealed that GmMS signaling depletion blocked 20E biosynthesis in the ovary. Finally, exogenous MS rescued most dsGmMS<em>-</em> or dsGmMSR-induced ovarian defects and 20E titers. These results suggest that MS/MSR-to-20E signaling regulates ovarian development through vitellogenesis, providing a new perspective on the development of neuroendocrine targets that suppress pest field populations.</p></div>","PeriodicalId":19828,"journal":{"name":"Pesticide Biochemistry and Physiology","volume":"205 ","pages":"Article 106116"},"PeriodicalIF":4.2000,"publicationDate":"2024-09-02","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Pesticide Biochemistry and Physiology","FirstCategoryId":"97","ListUrlMain":"https://www.sciencedirect.com/science/article/pii/S0048357524003493","RegionNum":1,"RegionCategory":"农林科学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q2","JCRName":"BIOCHEMISTRY & MOLECULAR BIOLOGY","Score":null,"Total":0}
引用次数: 0
Abstract
The steroid 20-hydroxyecdysone (20E) is crucial in regulating ovarian development. However, the neuropeptidergic mechanisms underlying ovarian development via 20E are underexplored. In this study, we investigated myosuppressin (MS) signaling in the dominant fruit pest Grapholita molesta and revealed that MS signaling is necessary for 20E biosynthesis during ovarian maturation. Pharmacological and molecular docking analyses confirmed that the GmMS mature peptide could activate its receptor GmMSR. Additionally, transcript expression analyses of GmMS and GmMSR showed different distribution patterns in adults. Notably, GmMSR was also detected in the ovaries of sexually mature females. RNAi-mediated dysfunction of GmMS or GmMSR specifically decreased fertility in females. Furthermore, GmMS or GmMSR knockdown decreased vitellogenin synthesis and uptake, thereby delaying ovarian development. RNA-seq, gene expression validation, and hormone quantification further revealed that GmMS signaling depletion blocked 20E biosynthesis in the ovary. Finally, exogenous MS rescued most dsGmMS- or dsGmMSR-induced ovarian defects and 20E titers. These results suggest that MS/MSR-to-20E signaling regulates ovarian development through vitellogenesis, providing a new perspective on the development of neuroendocrine targets that suppress pest field populations.
期刊介绍:
Pesticide Biochemistry and Physiology publishes original scientific articles pertaining to the mode of action of plant protection agents such as insecticides, fungicides, herbicides, and similar compounds, including nonlethal pest control agents, biosynthesis of pheromones, hormones, and plant resistance agents. Manuscripts may include a biochemical, physiological, or molecular study for an understanding of comparative toxicology or selective toxicity of both target and nontarget organisms. Particular interest will be given to studies on the molecular biology of pest control, toxicology, and pesticide resistance.
Research Areas Emphasized Include the Biochemistry and Physiology of:
• Comparative toxicity
• Mode of action
• Pathophysiology
• Plant growth regulators
• Resistance
• Other effects of pesticides on both parasites and hosts.