叶蝉精子介导病毒垂直传播导致水稻瘤矮病在我国常态流行的机制

The reported vector-transmitted viral pathogens are generally transovarially transmitted by female insects into their offspring. We found that the vertical transmission of Rice gall dwarf virus (RGDV) by leafhopper vectors Recilia dorsalis adults into their offspring is dominantly mediated by male mating, with a low frequency of transovarial transmission by female adults. Such unique vertical transmission pathway is possibly mediated by the interaction of outer capsid protein of RGDV with the surface receptor of the sperm, heparin sulfate proteoglycan (HSPG). It is supposed that the preference of RGDV for maintaining in male insect, as well as the high efficiency of sperm-mediated vertical transmission, cause normal epidemic pattern of RGDV throughout Southern Provinces of China for more than 30 years. This proposal will further analyze the mechanisms how RGDV is encountered by various membrane or tissue barriers during the process of viral invasion into the ovary oocyte in female insects, and reveal the mechanisms how the specific interaction of coat protein of RGDV with HSPG of sperm mediates the vertical transmission of viruses into offspring by male mating with high efficiency. We will also compare the differences of mating competitiveness, development and passage ability to offspring between viruliferous male and female adults, discussing the intrinsic mechanism for RGDV to evolve the male mating-mediated vertical transmission. We hope to uncover the association of this unique vertical transmission of viruses with normal epidemic of viral diseases in the field. The results will promote the development of the study field of vector-transmitted viral pathogens, and provide the theoretical base for green control exploration of the viruses by inhibiting the recognition of virus and the sperm of male insect.

已报道的虫媒病毒病原通常通过雌虫经卵垂直传播至子代昆虫，前期发现水稻瘤矮病毒(RGDV)经介体电光叶蝉以雄虫交配为主雌虫经卵为辅的方式传至子代，这种奇特的垂直传播方式可能是由RGDV外壳蛋白与精子表面受体硫酸乙酰肝素糖蛋白(HSPG)互作介导的。推测由于RGDV更适合在雄虫中存在且经精子垂直传播的效率较高，导致RGDV在我国南方省份长达30余年的常态流行。本项目将深入解析RGDV经雌虫经卵传播过程中受到各种屏障限制的机制，揭示RGDV外壳蛋白与精子HSPG识别介导病毒以雄虫交配高效传至子代的机制；通过比较带毒雌雄虫交配竞争力、生长发育及其持续传至后代等能力差异，探讨RGDV进化为以雄虫交配为主的垂直传播方式的内在机制；阐明自然条件下这种奇特病毒垂直传播方式与田间病毒病害常态流行之间的关系。研究结果将推动虫媒病毒相关领域发展，为探索通过抑制病毒与精子识别来对虫媒病毒进行绿色防控提供理论基础。

本项目针对叶蝉精子介导水稻瘤矮病毒（RGDV）通过父系垂直传播导致水稻瘤矮病在我国南方稻区常态流行的机制展开深入研究。发现RGDV外壳蛋白P8与叶蝉精子质膜受体HSPG互作介导病毒附着在精子上，使病毒被精子携带，并通过交配和授精，像“搭便车”一样进入卵中实现从父本传播至子代。发现精子介导的经父本高效垂直传播对子代卵的影响较小，是越冬期病毒持续在田间存在的关键，这可能导致我国南方稻区RGDV常态流行的原因。电光叶蝉自然种群约80%存在Virgaviridae科丝状共生病毒RdFV，可通过父本垂直传播促进虫卵的发育。RGDV和RdFV的外壳蛋白通过互作，在叶蝉精巢中形成复合体，并通过与精子质膜受体HongrES1互作协同附着于精子表面共同跨代传播至昆虫子代，表明昆虫共生病毒与植物病毒间存在直接互作的协生关系。发现RGDV非结构蛋白Pns11与线粒体外膜孔蛋白VDAC1的互作在雌虫生殖系统等触发了有利于病毒的凋亡反应，而VDAC1与起始自噬的ATG8互作，将衰退的线粒体隔离在自噬体内激发线粒体自噬反应，从而抑制过度凋亡，解析了病毒-昆虫"和平共存"的机制。发现与RGDV同属的水稻矮缩病毒（RDV）外壳蛋白和卵黄原蛋白（Vg）与叶蝉初级共生菌Nasuia外膜孔蛋白特异性互作，使RDV和Vg借助Nasuia入卵途径入卵，表明Vg、病毒和共生菌在共进化过中形成互惠关系。本项目系统解析了病毒突破介体昆虫免疫和垂直传播屏障的机制，为通过阻断介体传毒的防控策略奠定理论基础。研究成果在Nature Communications、Autophagy、PLoS Pathogens、mBio等期刊发表 11 篇SCI 学术论文，多次应邀在国际会议上做报告，在Current Opinion in Virology等撰写综述，入选首批全国高校黄大年式教师团队、福建省首批特级后备人才和最美科技工作者等。