Insect Mouthpart Transcriptome Unveils Extension of Cuticular Protein Repertoire and Complex Organization

Insects have developed intriguing cuticles with very specific structures and functions, including microstructures governing their interactions with transmitted microbes, such as in aphid mouthparts harboring virus receptors within such microstructures. Here, we provide the first transcriptome analysis of an insect mouthpart cuticle (“retort organs” [ROs], the stylets' precursors). This analysis defined stylets as a complex composite material. The retort transcriptome also allowed us to propose an algorithmic definition of a new cuticular protein (CP) family with low complexity and biased amino acid composition. Finally, we identified a differentially expressed gene encoding a pyrokinin (PK) neuropeptide precursor and characterizing the mandibular glands. Injection of three predicted synthetic peptides PK1/2/3 into aphids prior to ecdysis caused a molt-specific phenotype with altered head formation. Our study provides the most complete description to date of the potential protein composition of aphid stylets, which should improve the understanding of the transmission of stylet-borne viruses.