Jie Cheng , Jing-Kai Liu , Tian-Li Wang , Wei Wei , Hui-Ming Xiang , Xian-Wei Li , Rui-Yan Ma , Zhi-Guo Zhao
{"title":"肌抑素信号缺乏通过抑制 20-hydroxyecdysone 生物合成影响 Grapholita molesta 的卵巢发育","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":"{\"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}","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
摘要
类固醇 20-羟基蜕皮激素(20E)对调节卵巢发育至关重要。然而,通过 20E 实现卵巢发育的神经肽能机制尚未得到充分探索。在这项研究中,我们研究了优势果实害虫 Grapholita molesta 的肌抑素(MS)信号传导,发现 MS 信号传导是卵巢成熟过程中 20E 生物合成所必需的。药理和分子对接分析证实,GmMS成熟肽可激活其受体GmMSR。此外,GmMS和GmMSR的转录本表达分析显示了它们在成体中的不同分布模式。值得注意的是,在性成熟雌性动物的卵巢中也检测到了GmMSR。RNAi- 介导的 GmMS 或 GmMSR 功能障碍特异性地降低了雌性的生育能力。此外,GmMS或GmMSR敲除会减少卵黄素的合成和吸收,从而延迟卵巢发育。RNA-seq、基因表达验证和激素定量分析进一步表明,GmMS信号消耗阻碍了卵巢中20E的生物合成。最后,外源MS能挽救大多数dsGmMS或dsGmMSR诱导的卵巢缺陷和20E滴度。这些结果表明,MS/MSR-20E 信号通过卵黄发生调节卵巢发育,为抑制害虫田间种群的神经内分泌靶标的发展提供了一个新的视角。
Myosuppressin signaling deficiency affects ovarian development via repression of 20-hydroxyecdysone biosynthesis in Grapholita molesta
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.