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Viral pathogens hitchhike with insect sperm for paternal transmission

Author

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  • Qianzhuo Mao

    (Fujian Agriculture and Forestry University, Fuzhou
    Fujian Agriculture and Forestry University)

  • Wei Wu

    (Fujian Agriculture and Forestry University, Fuzhou)

  • Zhenfeng Liao

    (Fujian Agriculture and Forestry University, Fuzhou)

  • Jiajia Li

    (Fujian Agriculture and Forestry University, Fuzhou)

  • Dongsheng Jia

    (Fujian Agriculture and Forestry University, Fuzhou
    Fujian Agriculture and Forestry University)

  • Xiaofeng Zhang

    (Fujian Agriculture and Forestry University, Fuzhou)

  • Qian Chen

    (Fujian Agriculture and Forestry University, Fuzhou)

  • Hongyan Chen

    (Fujian Agriculture and Forestry University, Fuzhou)

  • Jing Wei

    (Fujian Agriculture and Forestry University, Fuzhou)

  • Taiyun Wei

    (Fujian Agriculture and Forestry University, Fuzhou
    Fujian Agriculture and Forestry University)

Abstract

Arthropod-borne viruses (arboviruses) can be maternally transmitted by female insects to their offspring, however, it is unknown whether male sperm can directly interact with the arbovirus and mediate its paternal transmission. Here we report that an important rice arbovirus is paternally transmitted by the male leafhoppers by hitchhiking with the sperm. The virus-sperm binding is mediated by the interaction of viral capsid protein and heparan sulfate proteoglycan on the sperm head surfaces. Mating experiments reveal that paternal virus transmission is more efficient than maternal transmission. Such paternal virus transmission scarcely affects the fitness of adult males or their offspring, and plays a pivotal role in maintenance of viral population during seasons unfavorable for rice hosts in the field. Our findings reveal that a preferred mode of vertical arbovirus transmission has been evolved by hitchhiking with insect sperm without disturbing sperm functioning, facilitating the long-term viral epidemic and persistence in nature.

Suggested Citation

  • 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.
    • Handle: RePEc:nat:natcom:v:10:y:2019:i:1:d:10.1038_s41467-019-08860-4
    DOI: 10.1038/s41467-019-08860-4
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    Cited by:

    1. Xin Wang & Haibo Wu & Zhongkai Yu & Jing Wu & Chengcong Lu & Taiyun Wei & Qian Chen, 2024. "Plant viruses exploit insect salivary GAPDH to modulate plant defenses," Nature Communications, Nature, vol. 15(1), pages 1-21, December.
    2. 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.
    3. 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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