Myosuppressin signaling deficiency affects ovarian development via repression of 20-hydroxyecdysone biosynthesis in Grapholita molesta

Pestic Biochem Physiol. 2024 Nov:205:106116. doi: 10.1016/j.pestbp.2024.106116. Epub 2024 Sep 2.

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.

Keywords: 20-hydroxyecdysone; Female fertility; Myosuppressin; Oriental fruit moth; Ovarian development.

MeSH terms

  • Animals
  • Ecdysterone* / metabolism
  • Female
  • Hemiptera / genetics
  • Hemiptera / growth & development
  • Hemiptera / metabolism
  • Insect Proteins / genetics
  • Insect Proteins / metabolism
  • Neuropeptides / genetics
  • Neuropeptides / metabolism
  • Ovary* / growth & development
  • Ovary* / metabolism
  • Signal Transduction*
  • Vitellogenesis
  • Vitellogenins / genetics
  • Vitellogenins / metabolism

Substances

  • Ecdysterone
  • Insect Proteins
  • Neuropeptides
  • Vitellogenins