Chuvirus-Derived Endogenous Viral Elements Contribute to Nymphal Development Through Modulating the IIS/TOR - 20E Pathway in Rice Planthoppers.

Abstract

Non-retroviral endogenous viral elements (nrEVEs) are viral-derived sequences integrated into host genomes, but the biological functions of Chuvirus-derived nrEVEs (ChuEVEs) in insects remain poorly understood. Here, we identified homologous ChuEVEs in the genomes of rice insect vectors Sogatella furcifera and Laodelphax striatellus, designated SfChuEVE and LsChuEVE. SfChuEVE and LsChuEVE showed similarity to the glycoprotein of Sanya chuvirus 2 and were detectable in most examined individuals. Transcript analysis revealed that ChuEVEs were transcriptionally active and contained predicted ORFs with distinct coding organisations. Both ChuEVEs were transcriptionally active across developmental stages and were highly expressed in salivary glands. RNAi-mediated knockdown of SfChuEVE or LsChuEVE significantly prolonged nymphal development and altered genes involved in the 20-hydroxyecdysone (20E) and insulin/insulin-like signalling/target of rapamycin (IIS/TOR) pathways in both planthopper species. Further silencing of IIS/TOR components, including S6K and FOXO, affected selected 20E pathway-related genes, particularly USP and EcR, whereas silencing IIS/TOR components did not alter ChuEVE transcription. Moreover, exogenous 20E restored the expression of representative 20E signalling genes but failed to rescue the reduced expression of IIS/TOR-related genes following ChuEVE knockdown. Together, these findings support a role for ChuEVEs in nymphal development through an IIS/TOR-20E regulatory axis. Our study provides evidence that virus-derived genomic elements may acquire developmental functions after endogenisation, expanding our understanding of the functional domestication of endogenous viral elements and their potential contribution to the developmental and ecological adaptation of rice planthoppers.