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

Author

Listed:
  • 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)

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.

Suggested Citation

  • Xinyan Sun & Yu Du & Yu Cheng & Wang Guan & You Li & Hongyan Chen & Dongsheng Jia & Taiyun Wei, 2024. "Insect ribosome-rescuer Pelo-Hbs1 complex on sperm surface mediates paternal arbovirus transmission," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-51020-6
    DOI: 10.1038/s41467-024-51020-6
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    1. Kifayathullah Liakath-Ali & Eric W. Mills & Inês Sequeira & Beate M. Lichtenberger & Angela Oliveira Pisco & Kalle H. Sipilä & Ajay Mishra & Harunori Yoshikawa & Colin Chih-Chien Wu & Tony Ly & Angus , 2018. "An evolutionarily conserved ribosome-rescue pathway maintains epidermal homeostasis," Nature, Nature, vol. 556(7701), pages 376-380, April.
    2. Yang Li & Ping Xie & Liang Lu & Jian Wang & Lihong Diao & Zhongyang Liu & Feifei Guo & Yangzhige He & Yuan Liu & Qin Huang & Han Liang & Dong Li & Fuchu He, 2017. "An integrated bioinformatics platform for investigating the human E3 ubiquitin ligase-substrate interaction network," Nature Communications, Nature, vol. 8(1), pages 1-9, December.
    3. Jiajia Wan & Qifu Liang & Ruonan Zhang & Yu Cheng & Xin Wang & Hui Wang & Jieting Zhang & Dongsheng Jia & Yu Du & Wenhui Zheng & Dingzhong Tang & Taiyun Wei & Qian Chen, 2023. "Arboviruses and symbiotic viruses cooperatively hijack insect sperm-specific proteins for paternal transmission," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    4. Qianzhuo Mao & Wei Wu & Zhenfeng Liao & Jiajia Li & Dongsheng Jia & Xiaofeng Zhang & Qian Chen & Hongyan Chen & Jing Wei & Taiyun Wei, 2019. "Viral pathogens hitchhike with insect sperm for paternal transmission," Nature Communications, Nature, vol. 10(1), pages 1-10, December.
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