Identification of Plant Virus Receptor Candidates in the Stylets of Their Aphid Vectors

• Published in: Journal of virology Vol. 92; no. 14; pp. e00432 - 18
• Main Authors: Webster, Craig G, Pichon, Elodie, van Munster, Manuella, Monsion, Baptiste, Deshoux, Maëlle, Gargani, Daniel, Calevro, Federica, Jimenez, Jaime, Moreno, Aranzazu, Krenz, Björn, Thompson, Jeremy R, Perry, Keith L, Fereres, Alberto, Blanc, Stéphane, Uzest, Marilyne
• Format: Journal Article
• Language: English
• Published: United States American Society for Microbiology 15-07-2018
• Subjects: Animals; Aphids - metabolism; Aphids - virology; Brassica - virology; Conserved Sequence; Evolution, Molecular; Insect Proteins - chemistry; Insect Proteins - metabolism; Insect Vectors - virology; Life Sciences; Microbiology and Parasitology; Multigene Family; Phytopathology and phytopharmacy; Pisum sativum - virology; Plant Viruses - metabolism; Prunus persica - virology; Receptors, Virus - chemistry; Receptors, Virus - metabolism; Spotlight; Vegetal Biology; Virology; Virus-Cell Interactions; cuticular protein; stylets; receptor; transmission; aphid; plant virus
• ISSN: 0022-538X; 1098-5514
• DOI: 10.1128/JVI.00432-18

Plant viruses transmitted by insects cause tremendous losses in most important crops around the world. The identification of receptors of plant viruses within their insect vectors is a key challenge to understanding the mechanisms of transmission and offers an avenue for future alternative control strategies to limit viral spread. We here report the identification of two cuticular proteins within aphid mouthparts, and we provide experimental support for the role of one of them in the transmission of a noncirculative virus. These two proteins, named Stylin-01 and Stylin-02, belong to the RR-1 cuticular protein subfamily and are highly conserved among aphid species. Using an immunolabeling approach, they were localized in the maxillary stylets of the pea aphid
and the green peach aphid
, in the acrostyle, an organ earlier shown to harbor receptors of a noncirculative virus. A peptide motif present at the C termini of both Stylin-01 and Stylin-02 is readily accessible all over the surface of the acrostyle. Competition for
binding to the acrostyle was observed between an antibody targeting this peptide and the helper component protein P2 of
Furthermore, silencing the
but not
gene through RNA interference decreased the efficiency of
transmission by
These results identify the first cuticular proteins ever reported within arthropod mouthparts and distinguish Stylin-01 as the best candidate receptor for the aphid transmission of noncirculative plant viruses.
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.