Research Article: Transovarial Transmission of a Plant Virus Is Mediated by Vitellogenin of Its Insect Vector

Date Published: March 6, 2014

Publisher: Public Library of Science

Author(s): Yan Huo, Wenwen Liu, Fujie Zhang, Xiaoying Chen, Li Li, Qifei Liu, Yijun Zhou, Taiyun Wei, Rongxiang Fang, Xifeng Wang, Peter D. Nagy.

http://doi.org/10.1371/journal.ppat.1003949

Abstract

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.

Partial Text

Many viruses, especially plant viruses, are transmitted by insects. Viruses can be transmitted horizontally from individual to individual and vertically from parents to offspring [1]. More than 200 plant viruses are transmitted by specific arthropod vectors; some are retained for a few hours or days after acquisition and others for up to the life of the insect, i.e., in a persistent circulative or persistent-propagative manner [2]. Plant viruses such as tospoviruses, rhabdoviruses, marafiviruses, tenuiviruses, and reoviruses are transmitted by their respective insect vectors in a persistent-propagative manner [1]. The persistent-propagative viruses can replicate in different organs of insect vectors, and some of these viruses can be transmitted vertically from female parent to offspring in a transovarial manner. The transmission process is a critical step for every virus because it controls dispersal in space and time, thus directly influencing virus ecology and disease epidemiology.

Vg, present in the female individuals of most oviparous species and invertebrates, is a member of the large lipid transfer protein superfamily [26], [27]. As the egg yolk precursor protein, Vg is usually synthesized extra-ovarially under hormonal control [28]–[32]. After its synthesis primarily by the fat body of insects, Vg is secreted into the hemolymph, then transported by the circulatory system to the ovary, from where it is absorbed into the growing oocytes via receptor-mediated endocytosis. Once in the growing oocytes, Vg is proteolytically cleaved to generate yolk proteins, lipovitellin and phosvitin, finally serving as nutrients for developing embryos [33]–[36]. Clearly, there is a transovarial transportation system for absorbing nutrients in the oviparous species, including insects.

 

Source:

http://doi.org/10.1371/journal.ppat.1003949

 

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