Structural Insights into Viral Determinants of Nematode Mediated Grapevine fanleaf virus Transmission
Open Access
- 19 May 2011
- journal article
- research article
- Published by Public Library of Science (PLoS) in PLoS Pathogens
- Vol. 7 (5), e1002034
- https://doi.org/10.1371/journal.ppat.1002034
Abstract
Many animal and plant viruses rely on vectors for their transmission from host to host. Grapevine fanleaf virus (GFLV), a picorna-like virus from plants, is transmitted specifically by the ectoparasitic nematode Xiphinema index. The icosahedral capsid of GFLV, which consists of 60 identical coat protein subunits (CP), carries the determinants of this specificity. Here, we provide novel insight into GFLV transmission by nematodes through a comparative structural and functional analysis of two GFLV variants. We isolated a mutant GFLV strain (GFLV-TD) poorly transmissible by nematodes, and showed that the transmission defect is due to a glycine to aspartate mutation at position 297 (Gly297Asp) in the CP. We next determined the crystal structures of the wild-type GFLV strain F13 at 3.0 Å and of GFLV-TD at 2.7 Å resolution. The Gly297Asp mutation mapped to an exposed loop at the outer surface of the capsid and did not affect the conformation of the assembled capsid, nor of individual CP molecules. The loop is part of a positively charged pocket that includes a previously identified determinant of transmission. We propose that this pocket is a ligand-binding site with essential function in GFLV transmission by X. index. Our data suggest that perturbation of the electrostatic landscape of this pocket affects the interaction of the virion with specific receptors of the nematode's feeding apparatus, and thereby severely diminishes its transmission efficiency. These data provide a first structural insight into the interactions between a plant virus and a nematode vector. Numerous pathogenic viruses from animals and plants rely on vectors such as insects, worms or other organisms for their transmission from host to host. The reasons why certain vectors transmit some viruses but not others remain poorly understood. In plants, Grapevine fanleaf virus (GFLV), a major pathogen of grapes worldwide and its specific vector, the dagger nematode Xiphinema index, provides a well-established model illustrating this specificity. Here, we determined the high-resolution structures of two GFLV isolates that differ in their transmissibility. We show that this difference is due to a single mutation in a region exposed at the outer surface of the viral particles. This mutation does not alter the conformation of the particles but modifies the distribution of charges within a positively-charged pocket at the outer surface of virions which likely affects particle retention by X. index and, thereby also transmission efficiency. Therefore, we propose that this pocket is involved in the specific recognition of GFLV by its nematode vector. This work paves the way towards the characterization of the specific compound(s) within the nematodes that trigger vector specificity and provides novel perspectives to interfere with virus transmission.Keywords
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