Vector-Borne Virus Research Center, Fujian Agriculture and Forestry University, Fuzhou, Fujian, 350002, China.
State Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, Fujian Agriculture and Forestry University, Fuzhou, Fujian, 350002, China.
Nat Commun. 2023 Mar 9;14(1):1289. doi: 10.1038/s41467-023-36993-0.
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.
节肢动物病毒和共生病毒可以通过雄性昆虫向其后代进行垂直传递，从而在自然界中长期维持病毒的存在，但其中的机制仍知之甚少。在这里，我们鉴定出了斜纹叶蝉 Recilia dorsalis 的精子特异性丝氨酸蛋白酶抑制剂 HongrES1 是呼肠孤病毒科水稻矮缩病毒（RGDV）和一种以前未被描述的 Virgaviridae 科共生病毒——斜纹叶蝉丝状病毒（RdFV）的垂直传递的介体。我们表明，HongrES1 介导病毒粒子与叶蝉精子表面的直接结合，并通过与两种病毒衣壳蛋白的相互作用，随后进行垂直传递。病毒衣壳蛋白的直接相互作用介导了两种病毒同时侵入雄性生殖器官。此外，节肢动物病毒激活 HongrES1 的表达以抑制酚氧化酶原向活性酚氧化酶的转化，从而可能产生一种温和的抗病毒黑化防御。父代病毒的传递几乎不会影响后代的适应性。这些发现为我们提供了深入了解不同病毒如何协同劫持昆虫精子特异性蛋白进行垂直传递而不干扰精子功能的机制。
