Filamentous Structures Induced by a Phytoreovirus Mediate Viral Release from Salivary Glands in Its Insect Vector

Abstract

Numerous viral pathogens are persistently transmitted by insect vectors and cause agricultural or health problems. These viruses circulate in the vector body, enter the salivary gland, and then are released into the apical plasmalemma-lined cavities, where saliva is stored. The cavity plasmalemma of vector salivary glands thus represents the last membrane barrier for viral transmission. Here, we report a novel mechanism used by a persistent virus to overcome this essential barrier. We observed that the infection by rice gall dwarf virus (RGDV), a species of the genus in the family, induced the formation of virus-associated filaments constructed by viral nonstructural protein Pns11 within the salivary glands of its leafhopper vector, Such filaments attached to actin-based apical plasmalemma and induced an exocytosis-like process for viral release into vector salivary gland cavities, through a direct interaction of Pns11 of RGDV and actin of Failure of virus-induced filaments assembly by RNA interference with synthesized double-stranded RNA targeting the Pns11 gene inhibited the dissemination of RGDV into salivary cavities, preventing viral transmission by For the first time, we show that a virus can exploit virus-induced inclusion as a vehicle to pass through the apical plasmalemma into vector salivary gland cavities, thus overcoming the last membrane barrier for viral transmission by insect vectors. Understanding how persistent viruses overcome multiple tissue and membrane barriers within the insect vectors until final transmission is the key for viral disease control. The apical plasmalemma of the cavities where saliva is stored in the salivary glands is the last barrier for viral transmission by insect vectors; however, the mechanism is still poorly understood. Here we show that a virus has evolved to exploit virus-induced filaments to perform an exocytosis-like process that enables viral passage through the apical plasmalemma into salivary cavities. This mechanism could be extensively exploited by other persistent viruses to overcome salivary gland release barriers in insect vectors, opening new perspectives for viral control.

Fibrillar structures induced by a plant reovirus target mitochondria to activate typical apoptotic response and promote viral infection in insect vectors

“…The outer capsid shell is composed of the major outer capsid protein P8 and the minor outer capsid protein P2 [24]. Nonstructural protein Pns11 assembles into fibrillar or tubular structures to facilitate viral spread in insect vectors [17, 30–31]. The leafhopper R .…”

RNA interference‐mediated knockdown and virus‐induced suppression of Troponin C gene adversely affect the behavior or fitness of the green rice leafhopper, Nephotettix cincticeps

“…Many intracellular pathogens, including viruses, parasites, and bacteria, invade, traffic within, and exit their target cells in a cytoskeleton‐dependent manner (Greber & Way, ; Gruenheid & Finlay, ). Recently, a model of actin‐based tubule motility for the spread of rice virus including RDV in insect vector has been proposed (Chen et al., ; Jia et al., ; Liao et al., ; Mao et al., ; Wei & Li, ). In this model, a direct interaction of tubule composed of RDV Pns10 , RGDV Pns11 , or SRBSDV P7‐1 protein with cellular skeleton components (actin, myosin, profilin, gelsolin, cofilin, and tropomodulin) was observed; these components formed a “lighted rocket” to propel the tubule to break through the membrane or tissue barriers for spread and transmission in insect vectors.…”

Spatiotemporal dynamics and quantitative analysis of phytoplasmas in insect vectors

“…In type III cells, actin filaments are distributed on the inner sides of both basal plasmalemma (Fig. 4C-F) and apical plasmalemma 33 . OY Amp-specific fluorescence was observed on the surfaces of type III cells at 14 daas ( Table 1, Fig.…”

“…Salivary gland cells are composed of a single layer of secretory cells, with apical plasmalemma-lined cavities (intracellular canaliculi) for saliva secretion and a basal plasmalemma covered by the basal lamina on the surface 6,31,33 . In type III cells, actin filaments are distributed on the inner sides of both basal plasmalemma (Fig.…”