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

Jiajia Wan, Qifu Liang, Ruonan Zhang, Yu Cheng, Xin Wang, Hui Wang, Jieting Zhang, Dongsheng Jia, Yu Du, Wenhui Zheng, Dingzhong Tang, Taiyun Wei () and Qian Chen ()
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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

Nature Communications, 2023, vol. 14, issue 1, 1-16

Abstract: 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.

Date: 2023
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DOI: 10.1038/s41467-023-36993-0

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