Insect ribosome-rescuer Pelo-Hbs1 complex on sperm surface mediates paternal arbovirus transmission

作者：Xinyan Sun, Yu Du, Yu Cheng, Guan Wang, You Li, Hongyan Chen, Dongsheng Jia, Tàiyún Wèi · 发表于：Nature Communications · 年份：2024 · DOI：10.1038/s41467-024-51020-6 · 被引用次数：9 · 研究领域：Mosquito-borne diseases and control、Viral Infections and Vectors、Plant Virus Research Studies

Arboviruses can be paternally transmitted by male insects to offspring for long-term persistence, but the mechanism remains largely unknown. Here, we use a model system of a destructive rice reovirus and its leafhopper vector to find that insect ribosome-rescuer Pelo-Hbs1 complex expressed on the sperm surface mediates paternal arbovirus transmission. This occurs through targeting virus-containing tubules constituted by viral nonstructural protein Pns11 to sperm surface via Pns11-Pelo interaction. Tubule assembly is dependent on Hsp70 activity, while Pelo-Hbs1 complex inhibits tubule assembly via suppressing Hsp70 activity. However, virus-activated ubiquitin ligase E3 mediates Pelo ubiquitinated degradation, synergistically causing Hbs1 degradation. Importantly, Pns11 effectively competes with Pelo for binding to E3, thus antagonizing E3-mediated Pelo-Hbs1 degradation. These processes cause a slight reduction of Pelo-Hbs1 complex in infected testes, promoting effective tubule assembly. Our findings provide insight into how insect sperm-specific Pelo-Hbs1 complex is modulated to promote paternal virus transmission without disrupting sperm function. In this study, Sun et al identify the leafhopper Pelo-Hbs1 complex in protein translational quality control as a sperm factor that mediates paternal arbovirus transmission to offspring without impairing sperm function, which contributes to long-term virus persistence in its natural vector.