A Single Amino Acid Position in the Helper Component of Cauliflower Mosaic Virus Can Change the Spectrum of Transmitting Vector Species

UMR Biologie et Génétique des Interactions Plantes-Parasites, CIRAD-INRA-ENSAM, TA 41/K, Campus International de Baillarguet, 34398 Montpellier cedex 05, France.
Journal of Virology (Impact Factor: 4.44). 12/2005; 79(21):13587-93. DOI: 10.1128/JVI.79.21.13587-13593.2005
Source: PubMed

ABSTRACT Viruses frequently use insect vectors to effect rapid spread through host populations. In plant viruses, vector transmission is the major mode of transmission, used by nearly 80% of species described to date. Despite the importance of this phenomenon in epidemiology, the specificity of the virus-vector relationship is poorly understood at both the molecular and the evolutionary level, and very limited data are available on the precise viral protein motifs that control specificity. Here, using the aphid-transmitted Cauliflower mosaic virus (CaMV) as a biological model, we confirm that the "noncirculative" mode of transmission dominant in plant viruses (designated "mechanical vector transmission" in animal viruses) involves extremely specific virus-vector recognition, and we identify an amino acid position in the "helper component" (HC) protein of CaMV involved in such recognition. Site-directed mutagenesis revealed that changing the residue at this position can differentially affect transmission rates obtained with various aphid species, thus modifying the spectrum of vector species for CaMV. Most interestingly, in a virus line transmitted by a single vector species, we observed the rapid appearance of a spontaneous mutant specifically losing its transmissibility by another aphid species. Hence, in addition to the first identification of an HC motif directly involved in specific vector recognition, we demonstrate that change of a virus to a different vector species requires only a single mutation and can occur rapidly and spontaneously.

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Available from: Alberto Fereres, Sep 27, 2015
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    • "Third, a mutant P2:GFP with a Q to Y substitution at amino acid 6 in P2 (P2Rev5:GFP) did not bind to vector aphid stylets. This mutation had previously been shown to disable the biological activity of P2, rendering it unable to support CaMV aphid transmission (Moreno et al., 2005). Most important, the fluorescence for P2:GFP was not randomly distributed, or scattered along the stylets, but was localized to a unique and tiny region at the aphid stylet tip (Uzest et al., 2007). "
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    ABSTRACT: The majority of plant-infecting viruses are transmitted to their host plants by vectors. The interactions between viruses and vector vary in duration and specificity but some common themes in vector transmission have emerged: 1) plant viruses encode structural proteins on the surface of the virion that are essential for transmission, and in some cases additional non-structural helper proteins that act to bridge the virion to the vector binding site; 2) viruses bind to specific sites in or on vectors and are retained there until they are transmitted to their plant hosts; and 3) viral determinants of vector transmission are promising candidates for translational research aimed at disrupting transmission or decreasing vector populations. In this review, we focus on well-characterized insect vector-transmitted viruses in the following genera: Caulimovirus, Crinivirus, Luteovirus, Geminiviridae, Reovirus, Tospovirus, and Tenuivirus. New discoveries regarding these genera have increased our understanding of the basic mechanisms of virus transmission by arthropods, which in turn have enabled the development of innovative strategies for breaking the transmission cycle. Copyright © 2015 Elsevier Inc. All rights reserved.
    Virology 03/2015; 479-480. DOI:10.1016/j.virol.2015.03.026 · 3.32 Impact Factor
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    • "A limiting factor in this approach has been the limited availability of atomic structures for the virions and proteins of interest. For example, elegant studies have identified essential regions of helper components of potyviruses and Cauliflower mosaic virus (Moreno et al., 2005; Syller, 2005), but structural information on these viruses is only available in low resolution models. Modeling studies of the structure of geminiviruses have resulted in predictions of the capsid protein structure based on cryoelectron microscopic reconstructions (Bottcher et al., 2004; Zhang et al., 2001). "
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    ABSTRACT: In the atomic model of Cucumber mosaic virus (CMV), six amino acid residues form stabilizing salt bridges between subunits of the asymmetric unit at the quasi-threefold axis of symmetry. To evaluate the effects of these positions on virion stability and aphid vector transmissibility, six charged amino acid residues were individually mutated to alanine. All of the six engineered viruses were viable and exhibited near wild type levels of virion stability in the presence of urea. Aphid vector transmissibility was nearly or completely eliminated in the case of four of the mutants; two mutants demonstrated intermediate aphid transmissibility. For the majority of the engineered mutants, second-site mutations were observed following aphid transmission and/or mechanical passaging, and one restored transmission rates to that of the wild type. CMV capsids tolerate disruption of acid-base pairing interactions at the quasi-threefold axis of symmetry, but these interactions are essential for maintaining aphid vector transmissibility.
    Virology 03/2013; 440(2). DOI:10.1016/j.virol.2013.02.020 · 3.32 Impact Factor
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    • "In this study, we used the aphid M. persicae to quantify CaMV transmission . This aphid is one of the two main vectors of CaMV in the field (Broadbent 1957; Kennedy et al. 1962; Moreno et al. 2005). Moreover, M. persicae has a worldwide distribution (Blackman and Eastop 2000) such that all viral isolates used in our study have potentially encountered this aphid vector. "
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    ABSTRACT: The transmission-virulence trade-off hypothesis is one of the few adaptive explanations of virulence evolution, and assumes that there is an overall positive correlation between parasite transmission and virulence. The shape of the transmission-virulence relationship predicts whether virulence should evolve toward either a maximum or to an intermediate optimum. A positive correlation between each of these traits and within-host growth is often suggested to underlie the relationship between virulence and transmission. There are few experimental tests of this hypothesis; this study reports on the first empirical test on a plant pathogen. We infected Brassica rapa plants with nine natural isolates of Cauliflower mosaic virus and then estimated three traits: transmission, virulence, and within-host viral accumulation. As predicted by the trade-off hypothesis, we observed a positive correlation between transmission and virulence, suggestive of the existence of an intermediate optimum. We discovered the unexpected existence of two groups of within-host accumulation, differing by at least an order of magnitude. When accumulation groups were not accounted for, within-host accumulation was correlated neither to virulence nor transmission, although our results suggest that within each group these correlations exist.
    Evolution 02/2013; 67(2):477-486. DOI:10.1111/j.1558-5646.2012.01780.x · 4.61 Impact Factor
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