Viral pathogens hitchhike with insect sperm for paternal transmission

Qianzhuo Mao, Wei Wu, Zhenfeng Liao, Jiajia Li, Dongsheng Jia, Xiaofeng Zhang, Qian Chen, Hongyan Chen, Jing Wei () and Taiyun Wei ()
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Qianzhuo Mao: Fujian Agriculture and Forestry University, Fuzhou
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
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

Nature Communications, 2019, vol. 10, issue 1, 1-10

Abstract: 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.

Date: 2019
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DOI: 10.1038/s41467-019-08860-4

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