title: 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 genusPhytoreovirusin the familyReoviridae, induced the formation of virus-associated filaments constructed by viral nonstructural protein Pns11 within the salivary glands of its leafhopper vector,Recilia dorsalisSuch 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 ofR. dorsalisFailure 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 byR. dorsalisFor 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.IMPORTANCEUnderstanding 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.
authors.affiliation: Fujian Province Key Laboratory of Plant Virology, Institute of Plant Virology, Fujian Agriculture and Forestry University, Fuzhou, Fujian, People's Republic of China.
authors.forename: Qianzhuo
authors.initials: Q
authors.lastname: Mao
authors.affiliation: Fujian Province Key Laboratory of Plant Virology, Institute of Plant Virology, Fujian Agriculture and Forestry University, Fuzhou, Fujian, People's Republic of China.
authors.forename: Zhenfeng
authors.initials: Z
authors.lastname: Liao
authors.affiliation: Fujian Province Key Laboratory of Plant Virology, Institute of Plant Virology, Fujian Agriculture and Forestry University, Fuzhou, Fujian, People's Republic of China.
authors.forename: Jiajia
authors.initials: J
authors.lastname: Li
authors.affiliation: Fujian Province Key Laboratory of Plant Virology, Institute of Plant Virology, Fujian Agriculture and Forestry University, Fuzhou, Fujian, People's Republic of China.
authors.forename: Yuyan
authors.initials: Y
authors.lastname: Liu
authors.affiliation: Fujian Province Key Laboratory of Plant Virology, Institute of Plant Virology, Fujian Agriculture and Forestry University, Fuzhou, Fujian, People's Republic of China.
authors.forename: Wei
authors.initials: W
authors.lastname: Wu
authors.affiliation: Fujian Province Key Laboratory of Plant Virology, Institute of Plant Virology, Fujian Agriculture and Forestry University, Fuzhou, Fujian, People's Republic of China.
authors.forename: Hongyan
authors.initials: H
authors.lastname: Chen
authors.affiliation: Fujian Province Key Laboratory of Plant Virology, Institute of Plant Virology, Fujian Agriculture and Forestry University, Fuzhou, Fujian, People's Republic of China.
authors.forename: Qian
authors.initials: Q
authors.lastname: Chen
authors.affiliation: Fujian Province Key Laboratory of Plant Virology, Institute of Plant Virology, Fujian Agriculture and Forestry University, Fuzhou, Fujian, People's Republic of China.
authors.forename: Dongsheng
authors.initials: D
authors.lastname: Jia
authors.affiliation: Fujian Province Key Laboratory of Plant Virology, Institute of Plant Virology, Fujian Agriculture and Forestry University, Fuzhou, Fujian, People's Republic of China weitaiyun@fafu.edu.cn.
authors.forename: Taiyun
authors.initials: T
authors.lastname: Wei
mesh_terms: D000199:Actins / Q000378:metabolism; D000818:Animals; D005089:Exocytosis; D006430:Hemiptera / Q000821:virology*; D007303:Insect Vectors / Q000821:virology; D008856:Microscopy, Fluorescence; D034622:RNA Interference; D012330:RNA, Double-Stranded / Q000378:metabolism; D012087:Reoviridae / Q000502:physiology* / Q000648:ultrastructure; D012469:Salivary Glands / Q000648:ultrastructure / Q000821:virology; D061987:Sf9 Cells; D017361:Viral Nonstructural Proteins / Q000378:metabolism*; D019065:Virus Assembly; D057074:Virus Release; D014779:Virus Replication
chemical_list: D000199:Actins; D012330:RNA, Double-Stranded; D017361:Viral Nonstructural Proteins
keywords: Pns11 filament; RGDV; insect vector; plant reovirus; salivary gland barrier; viral transmission