Résumé
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.