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Arboviruses and symbiotic viruses cooperatively hijack insect sperm-specific proteins for paternal transmission

Author

Listed:
  • Jiajia Wan

    (Fujian Agriculture and Forestry University)

  • Qifu Liang

    (Fujian Agriculture and Forestry University)

  • Ruonan Zhang

    (Fujian Agriculture and Forestry University)

  • Yu Cheng

    (Fujian Agriculture and Forestry University)

  • Xin Wang

    (Fujian Agriculture and Forestry University)

  • Hui Wang

    (Fujian Agriculture and Forestry University)

  • Jieting Zhang

    (Fujian Agriculture and Forestry University)

  • Dongsheng Jia

    (Fujian Agriculture and Forestry University)

  • Yu Du

    (Fujian Agriculture and Forestry University)

  • Wenhui Zheng

    (Fujian Agriculture and Forestry University)

  • Dingzhong Tang

    (Fujian Agriculture and Forestry University)

  • Taiyun Wei

    (Fujian Agriculture and Forestry University)

  • Qian Chen

    (Fujian Agriculture and Forestry University)

Abstract

Arboviruses and symbiotic viruses can be paternally transmitted by male insects to their offspring for long-term viral persistence in nature, but the mechanism remains largely unknown. Here, we identify the sperm-specific serpin protein HongrES1 of leafhopper Recilia dorsalis as a mediator of paternal transmission of the reovirus Rice gall dwarf virus (RGDV) and a previously undescribed symbiotic virus of the Virgaviridae family, Recilia dorsalis filamentous virus (RdFV). We show that HongrES1 mediates the direct binding of virions to leafhopper sperm surfaces and subsequent paternal transmission via interaction with both viral capsid proteins. Direct interaction of viral capsid proteins mediates simultaneously invasion of two viruses into male reproductive organs. Moreover, arbovirus activates HongrES1 expression to suppress the conversion of prophenoloxidase to active phenoloxidase, potentially producing a mild antiviral melanization defense. Paternal virus transmission scarcely affects offspring fitness. These findings provide insights into how different viruses cooperatively hijack insect sperm-specific proteins for paternal transmission without disturbing sperm functions.

Suggested Citation

  • 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.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-36993-0
    DOI: 10.1038/s41467-023-36993-0
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    References listed on IDEAS

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    1. Jennifer Govero & Prabagaran Esakky & Suzanne M. Scheaffer & Estefania Fernandez & Andrea Drury & Derek J. Platt & Matthew J. Gorman & Justin M. Richner & Elizabeth A. Caine & Vanessa Salazar & Kelle , 2016. "Zika virus infection damages the testes in mice," Nature, Nature, vol. 540(7633), pages 438-442, December.
    2. 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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    Cited by:

    1. 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.

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