Huo Yan, Liu Wenwen, Zhang Fujie, Chen Xiaoying, Li Li, Liu Qifei, Zhou Yijun, Wei Taiyun, Fang Rongxiang, Wang Xifeng
State Key Laboratory of Plant Genomics, Institute of Microbiology, Chinese Academy of Sciences, Beijing, China; National Plant Gene Research Center, Beijing, China; Graduate School of the Chinese Academy of Sciences, Beijing, China.
State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, China.
PLoS Pathog. 2014 Mar 6;10(3):e1003949. doi: 10.1371/journal.ppat.1003949. eCollection 2014 Mar.
Most plant viruses are transmitted by hemipteroid insects. Some viruses can be transmitted from female parent to offspring usually through eggs, but the mechanism of this transovarial transmission remains unclear. Rice stripe virus (RSV), a Tenuivirus, transmitted mainly by the small brown planthopper (Laodelphax striatellus), is also spread to the offspring through the eggs. Here, we used the RSV-planthopper system as a model to investigate the mechanism of transovarial transmission and demonstrated the central role of vitellogenin (Vg) of L. striatellus in the process of virus transmission into the eggs. Our data showed Vg can bind to pc3 in vivo and in vitro and colocalize in the germarium. RSV filamentous ribonucleoprotein particles (RNPs) only accumulated in the terminal filaments and pedicel areas prior to Vg expression and was not present in the germarium until Vg was expressed, where RSV RNPs and Vg had colocalized. Observations by immunoelectron microscopy (IEM) also indicated that these two proteins colocalized in nurse cells. Knockdown of Vg expression due to RNA interference resulted in inhibition of the invasion of ovarioles by RSV. Together, the data obtained indicated that RSV RNPs may enter the nurse cell of the germarium via endocytosis through binding with Vg. Finally, the virus enters the oocytes through nutritive cords, using the same route as for Vg transport. Our results show that the Vg of L. striatellus played a critical role in transovarial transmission of RSV and shows how viruses can use existing transovarial transportation systems in insect vectors for their own purposes.
大多数植物病毒是由半翅目昆虫传播的。一些病毒可以通常通过卵从母本传播给后代,但其经卵传播的机制仍不清楚。水稻条纹病毒(RSV),一种纤细病毒属病毒,主要由灰飞虱(Laodelphax striatellus)传播,也通过卵传播给后代。在这里,我们以RSV-飞虱系统为模型来研究经卵传播的机制,并证明了灰飞虱卵黄原蛋白(Vg)在病毒传播到卵中的过程中起着核心作用。我们的数据表明,Vg在体内和体外都能与pc3结合,并在卵巢管中共同定位。在Vg表达之前,RSV丝状核糖核蛋白颗粒(RNPs)仅在终丝和柄部区域积累,直到Vg表达后才出现在卵巢管中,RSV RNPs和Vg在那里共同定位。免疫电子显微镜(IEM)观察也表明这两种蛋白在滋养细胞中共定位。由于RNA干扰导致Vg表达下调,从而抑制了RSV对卵巢小管的入侵。总之,所获得的数据表明,RSV RNPs可能通过与Vg结合经内吞作用进入卵巢管的滋养细胞。最后病毒通过营养索进入卵母细胞,与Vg运输途径相同。我们的结果表明,灰飞虱的Vg在RSV的经卵传播中起关键作用,并揭示了病毒如何利用昆虫载体中现有的经卵运输系统来实现自身目的。