Abstract
Aphids are phloem-feeding insects known as major pests in agriculture that are able to transmit hundreds of plant viruses. The majority of these viruses, classified as noncirculative, are retained and transported on the inner surface of the cuticle of the needle-like mouthparts while the aphids move from plant to plant. Identification of receptors of viruses within insect vectors is a key challenge because they are promising targets for alternative control strategies. The acrostyle, an organ discovered earlier within the common food/salivary canal at the tip of aphid maxillary stylets, displays proteins at the cuticle–fluid interface, some of which are receptors of noncirculative viruses. To assess the presence of stylet- and acrostyle-specific proteins and identify putative receptors, we have developed a comprehensive comparative analysis of the proteomes of four cuticular anatomical structures of the pea aphid, stylets, antennae, legs, and wings. In addition, we performed systematic immunolabeling detection of the cuticular proteins identified by mass spectrometry in dissected stylets. We thereby establish the first proteome of stylets of an insect and determine the minimal repertoire of the cuticular proteins composing the acrostyle. Most importantly, we propose a short list of plant virus receptor candidates, among which RR-1 proteins are remarkably predominant. The data are available via ProteomeXchange (PXD016517).
Highlights
Aphids are phloem-feeding insects, well-known as major pests in agriculture
We provide through this study the first comparative proteomics analysis of four aphid cuticular anatomical structures, namely antennae, legs, wings, and stylets
The stylet, which was of main interest to better understand the vector/virus interaction was found to be distinct in composition compared to the other three studied appendages
Summary
Aphids are phloem-feeding insects, well-known as major pests in agriculture. More than 5,000 aphid species have been described. They colonize countless plant species and have been reported on 300 plant families ranging from gymnosperms to angiosperms.[1,2] Aphids have a complex life cycle alternating between sexual and asexual reproduction and seasonal host changes They are and have long been extensively studied, because of interesting life traits such as reproductive and wing polyphenisms and because they transmit numerous plant diseases.[3] With more than 300 species transmitted, aphids are one of the most efficient and important vectors of plant viruses and are the best studied-model to characterize the mechanisms of vectormediated virus transmission (recently reviewed by Whitfield and colleagues).[4−7] Most aphid-transmitted viruses bind reversibly to retention sites on the inner cuticle of insect mouthparts to which they remain attached during transport to a new host plant.[4] This so-called noncirculative virus transmission is difficult to limit and control in field conditions, as the viruses can be acquired and inoculated by nonresident aphids mostly within a single puncture lasting only a few seconds.[8] During this process, an intimate association occurs between viruses and their vectors. This interaction is highly specific and involves the capsid proteins or viral-encoded proteins called helper components, together with poorly characterized molecular compounds in the insect cuticle acting as receptors.[9−12] These vector molecules are promising targets for alternative viral control strategies, and their identification would help characterizing further the molecular mechanisms of virus−vector interaction
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