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

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 sp...

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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
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Language:English
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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
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container_title Nature communications
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creator Sun, Xinyan
Du, Yu
Cheng, Yu
Guan, Wang
Li, You
Chen, Hongyan
Jia, Dongsheng
Wei, Taiyun
description 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.
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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
title Insect ribosome-rescuer Pelo-Hbs1 complex on sperm surface mediates paternal arbovirus transmission
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