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Tenuivirus utilizes its glycoprotein as a helper component to overcome insect midgut barriers for its circulative and propagative transmission

Gang Lu, Shuo Li, Changwei Zhou, Xin Qian, Qing Xiang, Tongqing Yang, Jianxiang Wu, Xueping Zhou, Yijun Zhou, Xin S. Ding, Xiaorong Tao, Bryce W. Falk
2019 PLoS Pathogens  
Many persistent transmitted plant viruses, including rice stripe virus (RSV), cause serious damage to crop production worldwide. Although many reports have indicated that a successful insect-mediated virus transmission depends on a proper interaction between the virus and its insect vector, the mechanism(s) controlling this interaction remained poorly understood. In this study, we used RSV and its small brown planthopper (SBPH) vector as a working model to elucidate the molecular mechanisms
more » ... ular mechanisms underlying the entrance of RSV virions into SBPH midgut cells for virus circulative and propagative transmission. We have determined that this non-enveloped tenuivirus uses its non-structural glycoprotein NSvc2 as a helper component to overcome the midgut barrier(s) for RSV replication and transmission. In the absence of this glycoprotein, purified RSV virions were unable to enter SBPH midgut cells. In the RSV-infected cells, this glycoprotein was processed into two mature proteins: an amino-terminal protein (NSvc2-N) and a carboxyl-terminal protein (NSvc2-C). Both NSvc2-N and NSvc2-C interact with RSV virions. Our results showed that the NSvc2-N could bind directly to the surface of midgut lumen via its N-glycosylation sites. Upon recognition, the midgut cells underwent endocytosis followed by compartmentalization of RSV virions and NSvc2 into early and then late endosomes. The NSvc2-C triggered cell membrane fusion via its highly conserved fusion loop motifs under the acidic condition inside the late endosomes, leading to the release of RSV virions from endosomes into cytosol. In summary, our results showed for the first time that a rice tenuivirus utilized its glycoprotein NSvc2 as a helper component to ensure a proper interaction between its virions and SBPH midgut cells for its circulative and propagative transmission. Author summary Over 75% of the known plant viruses are insect transmitted. Understanding how plant viruses interact with their insect vectors during virus transmission is a key step towards the successful management of plant viruses worldwide. Several models for the direct or indirect virus-insect vector interactions have been proposed for the non-persistent or semi-persistent virus transmissions. However, the mechanisms controlling the interactions between viruses and their insect vector midgut barriers are poorly understood. In this study, we demonstrated that the circulative and propagative transmitted rice stripe virus (RSV) utilized its glycoprotein NSvc2 as a helper component to ensure a specific interaction between its virions and SBPH midgut cells to overcome the midgut barriers inside this vector. This is the first report of a viral helper component mediated mechanism for persistent-propagative virus transmission. Our new findings and working model should expand our knowledge on the molecular mechanism(s) controlling the interaction between virus and its insect vector during virus circulative and propagative transmission in nature. A helper component model for Tenuivirus persistent transmission PLOS Pathogens |
doi:10.1371/journal.ppat.1007655 fatcat:vhxnnwcjgzcnzfq73rxsofg3uq