Transcriptional identification of differentially expressed genes associated with division of labor in Apis cerana cerana. Transcriptional identification of differentially expressed genes associated with division of labor in Apis cerana cerana

While Apis cerana cerana, like Apis mellifera, undergoes a behavioral transition from in-hive nursing to outdoor foraging duties, nothing is known about the genes underlying this social signal-triggered aged-related transition in this species. Here, we simultaneously sequenced the head transcriptomes of the 7-day-old normal nurses (N7BY), 18- and 22-day-old normal foragers (N18CJ and N22CJ), 7-day-old precocious foragers (Tq7CJ) and 22-day-old overaged or reverted nurses (Tq22BY) of A. cerana cerana by RNA-seq and made a 3-tier comparison (from pairwise to group-wise and between-group) to unravel the genes associated with this transition. Six pairwise comparisons revealed 165-492 differentially expressed genes between nurses vs. foragers. Subsequent 3 group-wise and 1 between-group comparisons narrowed the transition-associated genes down to 18 nurse- and 41 forager-unique genes and 29 (14 and 15 genes upregulated in nurses and foragers, respectively) differentially expressed genes between the 3 types of foragers and 2 types of nurses. The uniquely expressed genes are usually low-abundance long noncoding RNAs, transcription factors, transcription coactivators, RNA-binding proteins, kinases or phosphatases involved in signaling transduction and/or gene expression regulation, whereas the differentially expressed genes are often high-abundance downstream genes that directly perform the tasks of nurses or foragers, such as major royal jelly proteins for nurses and the genes involved in sugar/protein digestion, lipids/fatty acids metabolism, plant allelochemicals detoxification and defense against pathogens and predators for foragers. Mapping of the clean reads to the published A. mellifera genome uncovered that the 3 types of foragers had a greater percentage of reads from annotated exons and intergenic regions, whereas the 2 types of nurses had a greater percentage of reads from introns. Taken together, these results suggest that the reciprocal nurse-forager behavioral transition of the A. cerana cerana is regulated by a social signal-triggered intron-exon/intergenic epigenetic shift and the resulted transcriptional shift of the nurse- and forager-associated genes. Overall design: The head transcriptomes of the 7-day-old normal nurses (N7BY), 18- and 22-day-old normal foragers (N18CJ and N22CJ), 7-day-old precocious foragers (Tq7CJ) and 22-day-old overaged or reverted nurses (Tq22BY) of A. cerana cerana