Abstract
Many arthropod-borne viruses are persistently propagated and transovarially transmitted by female insect vectors through eggs, but the mechanism remains poorly understood. Insect oocytes are surrounded by a layer of follicular cells, which are connected to the oocyte through actin-based microvilli. Here, we demonstrate that a plant reovirus, rice gall dwarf virus (RGDV), exploits virus-containing tubules composed of viral non-structural protein Pns11 to pass through actin-based junctions between follicular cells or through actin-based microvilli from follicular cells into oocyte of its leafhopper vector Recilia dorsalis, thus overcoming transovarial transmission barriers. We further determine that the association of Pns11 tubules with actin-based cellular junctions or microvilli of the ovary is mediated by a specific interaction between Pns11 and actin. Interestingly, RGDV can replicate and assemble progeny virions in the oocyte cytoplasm. The destruction of the tubule assembly by RNA interference with synthesized double-stranded RNA targeting the Pns11 gene strongly inhibits transovarial transmission of RGDV by its vectors. For the first time, we show that a virus can exploit virus-induced tubule as a vehicle to overcome the transovarial transmission barrier by insect vectors.
Highlights
Many arthropod-borne animal viruses or plant viruses that cause significant global health as well as agricultural problems are vertically transmitted by female insects through eggs in a process known as transovarial transmission (Hogenhout et al, 2008; Huo et al, 2014)
We first dissected the ovaries of R. dorsalis at different days after eclosion and immunolabeled them with actin dye phalloidinFITC and virus-rhodamine to follow rice gall dwarf virus (RGDV) infection
At 9 days after eclosion, about 21% leafhopper ovaries were infected by RGDV, but viruses had entered the mature oocyte near the pedicel in only about one-third of virus-infected ovaries (Figure 1D and Table 1)
Summary
Many arthropod-borne animal viruses (arboviruses) or plant viruses that cause significant global health as well as agricultural problems are vertically transmitted by female insects through eggs in a process known as transovarial transmission (Hogenhout et al, 2008; Huo et al, 2014). Rice dwarf virus (RDV), a plant reovirus, is the first plant virus recorded to be transmitted transovarially by insect vectors (Fukushi, 1933). The insect ovary is composed of ovarioles, and each ovariole contains a germarium, vitellarium, and pedicel from apex to base (Szklarzewicz et al, 2007). The oocytes produced by the germarium are arranged linearly in the vitellarium and surrounded by a layer of follicular cells (Szklarzewicz et al, 2007). The plasma membrane of the follicular cell facing the oocyte has abundant actin-based
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