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

• Published in: Nature communications 2024-08, Vol.15 (1), p.6817-16, Article 6817
• Main Authors: Sun, Xinyan, Du, Yu, Cheng, Yu, Guan, Wang, Li, You, Chen, Hongyan, Jia, Dongsheng, Wei, Taiyun
• Format: Article
• Language: English
• Subjects: 631/326/596/2557; 631/326/596/2561; 631/326/596/2563; 82/1; 82/111; 82/80; 82/83; Animals; Arbovirus Infections - metabolism; Arbovirus Infections - transmission; Arbovirus Infections - virology; Arboviruses; Assembly; Degradation; Hemiptera - metabolism; Hemiptera - virology; HSP70 Heat-Shock Proteins - metabolism; Hsp70 protein; Humanities and Social Sciences; Insect Proteins - genetics; Insect Proteins - metabolism; Insect Vectors - metabolism; Insect Vectors - virology; Insects; Male; multidisciplinary; Offspring; Plant viruses; Proteins; Quality control; Reoviridae - physiology; Ribonucleic acid; Ribosomes - metabolism; RNA; Science; Science (multidisciplinary); Sperm; Spermatozoa - metabolism; Spermatozoa - virology; Tubules; Ubiquitin-protein ligase; Ubiquitin-Protein Ligases - genetics; Ubiquitin-Protein Ligases - metabolism; Viruses
• ISSN: 2041-1723; 2041-1723
• DOI: 10.1038/s41467-024-51020-6

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.