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Tubular structure induced by a plant virus facilitates viral spread in its vector insect.

ABSTRACT: Rice dwarf virus (RDV) replicates in and is transmitted by a leafhopper vector in a persistent-propagative manner. Previous cytopathologic and genetic data revealed that tubular structures, constructed by the nonstructural viral protein Pns10, contain viral particles and are directly involved in the intercellular spread of RDV among cultured leafhopper cells. Here, we demonstrated that RDV exploited these virus-containing tubules to move along actin-based microvilli of the epithelial cells and muscle fibers of visceral muscle tissues in the alimentary canal, facilitating the spread of virus in the body of its insect vector leafhoppers. In cultured leafhopper cells, the knockdown of Pns10 expression due to RNA interference (RNAi) induced by synthesized dsRNA from Pns10 gene strongly inhibited tubule formation and prevented the spread of virus among insect vector cells. RNAi induced after ingestion of dsRNA from Pns10 gene strongly inhibited formation of tubules, preventing intercellular spread and transmission of the virus by the leafhopper. All these results, for the first time, show that a persistent-propagative virus exploits virus-containing tubules composed of a nonstructural viral protein to traffic along actin-based cellular protrusions, facilitating the intercellular spread of the virus in the vector insect. The RNAi strategy and the insect vector cell culture provide useful tools to investigate the molecular mechanisms enabling efficient transmission of persistent-propagative plant viruses by vector insects.

SUBMITTER: Chen Q

PROVIDER: S-EPMC3499585 | biostudies-other | 2012

REPOSITORIES: biostudies-other

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Tubular structure induced by a plant virus facilitates viral spread in its vector insect.

Chen Qian Q Chen Hongyan H Mao Qianzhuo Q Liu Qifei Q Shimizu Takumi T Uehara-Ichiki Tamaki T Wu Zujian Z Xie Lianhui L Omura Toshihiro T Wei Taiyun T

PLoS pathogens 20121115 11

Rice dwarf virus (RDV) replicates in and is transmitted by a leafhopper vector in a persistent-propagative manner. Previous cytopathologic and genetic data revealed that tubular structures, constructed by the nonstructural viral protein Pns10, contain viral particles and are directly involved in the intercellular spread of RDV among cultured leafhopper cells. Here, we demonstrated that RDV exploited these virus-containing tubules to move along actin-based microvilli of the epithelial cells and m ...[more]

PMID: 23166500

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Project description:Many viral pathogens of global importance to plant and animal health are persistently transmitted by insect vectors. Midgut of insects forms the first major barrier that these viruses encounter during their entry into the vectors. However, the vector ligand(s) involved in the movement of plant viruses across the midgut barrier remains largely uncharacterized. Begomoviruses, many of which are disease agents of some major crops worldwide, are persistently transmitted by whiteflies (Bemisia tabaci). Here, in order to identify whitefly midgut proteins that interact with a devastating begomovirus, tomato yellow leaf curl virus (TYLCV), we performed midgut-specific TYLCV coat protein (CP) immunoprecipitation followed by high-throughput mass spectrometry proteomic analysis. We find that vitellogenin (Vg), a critical insect reproductive protein that has been considered to be synthesized by the fat body, is also synthesized by and interacts with TYLCV CP in the whitefly midgut. TYLCV appears to be internalized into midgut epithelial cells as a complex with Vg through endocytosis. Virus-containing vesicles then deliver the virus-Vg complexes to early endosomes for intracellular transport. Systematic silencing of Vg or midgut-specific immune blocking of Vg inhibited virus movement across the midgut wall and decreased viral acquisition and transmission by whitefly. Our findings show that a functional Vg protein is synthesized in the midgut of an insect and suggest a novel Vg mechanism that facilitates virus movement across the midgut barrier of its insect vector. IMPORTANCE An essential step in the life cycle of many viruses is transmission to a new host by insect vectors, and one critical step in the transmission of persistently transmitted viruses is overcoming the midgut barrier to enter vectors and complete their cycle. Most viruses enter vector midgut epithelial cells via specific interaction between viral structural proteins and vector cell surface receptor complexes. Tomato yellow leaf curl virus (TYLCV) is persistently transmitted by the whitefly Bemisia tabaci between host plants. Here, we find that TYLCV coat protein interacts with vitellogenin (Vg) in the whitefly midgut. This interaction is required for the movement of the virus crossing the midgut wall and thus facilitates viral acquisition and transmission by whitefly. This study reveals a novel mechanism of virus overcoming the insect midgut barrier and provides new insights into the function of Vg beyond serving as nutrition for developing embryos in insects.

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Tubular structure induced by a plant virus facilitates viral spread in its vector insect.

Publications

Tubular structure induced by a plant virus facilitates viral spread in its vector insect.

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