Revealing the molecular mechanisms underlying neural transmission of female pheromone signals in the male antennae of Antheraea pernyi by integrative proteomics and metabolomics analysis

Abstract

Detection of sex pheromones of insects relies on the antennae. The female pheromone signal transmission in the male antennae ultimately initiates the courtship and mating behaviors of males. To investigate the proteins and metabolites involved in this neural transduction, the study adopted integrative proteomics and metabolomics analysis including tandem mass tag (TMT) proteomic quantification and liquid chromatography tandem mass spectrometry (LC/MS)-based metabolomics for comparing proteomic and metabolic changes between the antennae of male moths following stimulation by females and the non-stimulated males of A. pernyi. A total of 92 differentially expressed proteins (DEPs) containing 52 up-regulated and 40 down-regulated proteins and 545 differentially expressed metabolites (DEMs) including 218 up- and 327 down-regulated metabolites were identified from the antennae of female-stimulated male moths based on the proteome and metabolome data, respectively. GO enrichment analysis showed that 45 DEPs could be enriched into different GO terms on different levels. COG analysis indicated that 61 DEPs were assigned to 20 functional categories. The 160 DEMs respectively fell into 11 and 44 classes at SuperClass and Class levels based on HMDB annotation. KEGG pathway enrichment analysis indicated that totally 43 DEMs were enriched into 6, 27, and 87 pathways on level 1, 2, and 3, respectively. A number of DEPs and DEMs related to neural transmission of female pheromone signals in the male antennae of A. pernyi were screened, including tyrosine hydroxylase, cryptochrome-1, tachykinin, arylalkylamine N-acetyltransferase, cadherin-23, glutathione S-transferase delta 3, tyramine, tryptamine, n-oleoyl dopamine, n-stearoyl dopamine, and n-stearoyl tyrosine. We concluded that the altered expression levels of those proteins or metabolites were involved in regulating the neuron activity for enhanced transmission of neural impulses and continuous perception, reception, and transduction of female pheromone signals. Our findings yielded novel insights into the potential molecular mechanisms in the antennae of male A. pernyi responding to female attraction.