Most noncirculative plant viruses transmitted by insect vectors bind to their mouthparts. They are acquired and inoculated within seconds when insects hop from plant to plant. The receptors involved remain totally elusive due to a long-standing technical bottleneck in working with insect cuticle. Here we characterize the role of the two first cuticular proteins ever identified in arthropod mouthparts. A domain of these proteins is directly accessible at the surface of the cuticle of the acrostyle, an organ at the tip of aphid stylets. The acrostyle has been shown to bind a plant virus, and we consistently demonstrated that one of the identified proteins is involved in viral transmission. Our findings provide an approach to identify proteins in insect mouthparts and point at an unprecedented gene candidate for a plant virus receptor.
gThe family Geminiviridae comprises seven genera differentiated by genome organization, sequence similarity, and insect vector. Capulavirus, an eighth genus, has been proposed to accommodate two newly discovered highly divergent geminiviruses that presently have no known vector. Alfalfa leaf curl virus, identified here as a third capulavirus, is shown to be transmitted by Aphis craccivora. This is the first report of an aphid-transmitted geminivirus. P lant-infecting viruses in the family Geminiviridae have one or two genome components of less than 3.0 kb composed of circular single-stranded DNA (ssDNA) that are encapsidated in typical geminate particles. The seven approved geminivirus genera are Begomovirus, Curtovirus, Topocuvirus, Mastrevirus, Becurtovirus, Turncurtovirus, and Eragrovirus (1). Recently, two highly divergent geminiviruses, euphorbia caput-medusae latent virus (EcmLV) and French bean severe leaf curl virus (FbSLCV), were discovered in South Africa and India, respectively (2). Based on genomic sequence divergence and genome organization, EcmLV and FbSLCV have been proposed to belong to a new genus named Capulavirus. The primary reason that the Capulavirus genus has not been formally accepted within the family Geminiviridae is the absence of any evidence that either EcmLV or FbSLCV forms geminate particles. Here, however, we confirm that EcmLV produces twinned quasi-icosahedral particles ( Fig. 1) and that the capulaviruses are therefore bona fide geminiviruses.Besides genome relatedness and genome organization, the insect vector is an important criterion for defining new virus genera within the family Geminiviridae. Viruses of the genus Begomovirus are transmitted by whiteflies, those of the genera Mastrevirus, Curtovirus, Becurtovirus, Turncurtovirus, and probably Eragrovirus are transmitted by leafhoppers, and those of the genus Topocuvirus are transmitted by treehoppers.Since the discovery of EcmLV and FbSLCV (2), a third capulavirus has been discovered in leaf curl-exhibiting alfalfa (Medicago sativa, Fabaceae) plants collected from 2010 to 2014 during large-scale sampling surveys in the south of France (Rhône delta, Tour du Valat).Capulavirus-related sequences were identified in one of these plants (44-1E) using a virion-associated nucleic acids (VANA)-based metagenomics approach (3). Total DNA extracted from 44-1E was subjected to Phi29 DNA polymerase treatment (TempliPhi; GE Healthcare, USA), and a linear DNA fragment of about 2.8 kbp was generated with DraI, NcoI, or NdeI digestion. No fragment falling within the size ranges of reported geminivirus satellite sequences was produced with any of these restriction enzymes. A viral genomic DNA fragment of about 2.8 kbp was amplified from the Phi29 polymerase product with the partially overlapping PCR primers Dar-1981F and Dar-1966R, previously designed to amplify full-length EcmLV genomes (2). The amplification product was cloned (clone 44-1E) and sequenced as previously reported (2). Although the 2,745-nucleotide (nt) viral insert displaye...
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