Knockdown of the salivary protein gene NlG14 caused displacement of the lateral oviduct secreted components and inhibited ovulation in Nilaparvata lugens

PLoS Genet. 2023 Apr 3;19(4):e1010704. doi: 10.1371/journal.pgen.1010704. eCollection 2023 Apr.

Abstract

Saliva plays important roles in insect feeding, but its roles in insect reproduction were rarely reported. Here we reported that the knockdown of a salivary gland-specific gene NlG14 disrupted the reproduction through inhibiting the ovulation of the brown planthopper (BPH), Nilaparvata lugens (Stål), one of the most devastating rice pests in Asia. NlG14 knockdown caused the displacement of the lateral oviduct secreted components (LOSC), leading to the ovulation disorder and the accumulation of mature eggs in the ovary. The RNAi-treated females laid much less eggs than their control counterparts, though they had the similar oviposition behavior on rice stems as controls. NlG14 protein was not secreted into the hemolymph, indicating an indirect effect of NlG14 knockdown on BPH reproduction. NlG14 knockdown caused the malformation of A-follicle of the principal gland and affected the underlying endocrine mechanism of salivary glands. NlG14 reduction might promote the secretion of insulin-like peptides NlILP1 and NlILP3 from the brain, which up-regulated the expression of Nllaminin gene and then caused the abnormal contraction of lateral oviduct muscle. Another explanation was NlG14 reduction disrupted the ecdysone biosynthesis and action through the insulin-PI3K-Akt signaling in ovary. Altogether, this study indicated that the salivary gland specific protein NlG14 indirectly mediated BPH ovulation process, which established a connexon in function between insect salivary gland and ovary.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Female
  • Hemiptera* / genetics
  • Hemiptera* / metabolism
  • Insulin / metabolism
  • Oryza*
  • Oviducts
  • Ovulation / genetics
  • Phosphatidylinositol 3-Kinases / metabolism
  • Salivary Proteins and Peptides / metabolism

Substances

  • Insulin
  • Phosphatidylinositol 3-Kinases
  • Salivary Proteins and Peptides

Grants and funding

The work is supported by National Natural Science Foundation of China (grant number 31830075), to ZWL. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.