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Background  The honey bee ( Apis mellifera ) is a highly diverse species commonly used for honey production and pollination services. The oviposition of the honey bee queen affects the development and overall performance of the colony. To investigate the ovary activation and oviposition processes on a molecular level, a genome-wide analysis of lncRNAs, miRNAs and mRNA expression in the ovaries of the queens was performed to screen for differentially expressed coding and noncoding RNAs. Further analysis identified relevant candidate genes or RNAs.    Results  The analysis of the RNA profiles in different oviposition phase of the queens revealed that 740 lncRNAs, 81 miRNAs and 5,481 mRNAs were differently expressed during the ovary activation; 88 lncRNAs, 13 miRNAs and 338 mRNAs were differently expressed during the oviposition inhibition process; and finally, 100 lncRNAs, four miRNAs and 497 mRNAs were differently expressed during the oviposition recovery process. In addition, functional annotation of differentially expressed RNAs revealed several pathways that are closely related to oviposition, including hippo, MAPK, notch, Wnt, mTOR, TGF-beta and FoxO signaling pathways. Furthermore, in the QTL region for ovary size, 73 differentially expressed genes and 14 differentially expressed lncRNAs were located, which are considered as candidate genes affecting ovary size and oviposition. Moreover, a core set of genes served as bridges among different miRNAs were identified through the integrated analysis of lncRNA-miRNA-mRNA network.    Conclusion  The observed dramatic expression changes of coding and noncoding RNAs suggest that they may play a critical role in honey bee queens’ oviposition. The identified candidate genes for oviposition activation and regulation could serve as a resource for further studies of genetic markers of oviposition in honey bees.

Integration of lncRNA–miRNA–mRNA reveals novel insights into oviposition regulation in honey bees