Epigenetic Modification of Gene Expression in Honey Bees by Heterospecific Gland Secretions

BACKGROUND: In the honey bee (Apis mellifera), queen and workers have different behavior and reproductive capacity despite possessing the same genome. The primary substance that leads to this differentiation is royal jelly (RJ), which contains a range of proteins, amino acids, vitamins and nucleic acids. MicroRNA (miRNA) has been found to play an important role in regulating the expression of protein-coding genes and cell biology. In this study, we characterized the miRNAs in RJ from two honey bee sister species and determined their possible effect on transcriptome in one species. METHODOLOGY/PRINCIPAL FINDINGS: We sequenced the miRNAs in RJ either from A. mellifera (RJM) or A. cerana (RJC). We then determined the global transcriptomes of adult A. mellifera developed from larvae fed either with RJM (mRJM) or RJC (mRJC). Finally we analyzed the target genes of those miRNA that are species specific or differentially expressed in the two honey bee species. We show that there were differences in miRNA between RJM and RJC, and that transcriptomes of adult A. mellifera were affected by the two types of RJ. A high proportion (23.3%) of the affected genes were target genes of differential miRNAs. CONCLUSION: We show for the first time that there are differences in miRNAs in RJ between A. mellifera and A. cerana. Further, the differences in transcriptomes of bees reared from these two RJs might be related to miRNA differences of the two species. This study provides the first evidence that heterospecific royal jelly can modify gene expression in honey bees through an epigenetic mechanism.