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

Xinyan Sun, Yu Du, Yu Cheng, Wang Guan, You Li, Hongyan Chen, Dongsheng Jia and Taiyun Wei ()
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Xinyan Sun: Fujian Agriculture and Forestry University
Yu Du: Fujian Agriculture and Forestry University
Yu Cheng: Fujian Agriculture and Forestry University
Wang Guan: Fujian Agriculture and Forestry University
You Li: Fujian Agriculture and Forestry University
Hongyan Chen: Fujian Agriculture and Forestry University
Dongsheng Jia: Fujian Agriculture and Forestry University
Taiyun Wei: Fujian Agriculture and Forestry University

Nature Communications, 2024, vol. 15, issue 1, 1-16

Abstract: Abstract 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.

Date: 2024
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DOI: 10.1038/s41467-024-51020-6

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