Comparative Transcriptomic and ceRNA Network Analyses of Non-Coding and Coding RNAs in Heads of Apis mellifera Workers from Queenright and Queenless Colonies

Emerging evidence indicates that non-coding RNAs (ncRNAs) play important regulatory roles in honeybee social behavior and development. However, the regulatory roles of ncRNAs in honeybees remain largely elusive. To systematically identify ncRNAs associated with queen-regulated ovary activation, we conducted whole-transcriptome sequencing on the heads of Apis mellifera workers from queenright and queenless colonies. Subsequent bioinformatics analyses were conducted to profile differentially expressed (DE) RNAs and construct potential regulatory networks. High-quality sequencing data provided a foundation for subsequent analyses. This transcriptome data yielded 3968 lncRNA transcripts, comprising 3146 known and 822 novel candidates, all of which exhibited typical structural features of lncRNAs. Comparative expression analyses revealed that 246 lncRNAs, 1439 mRNAs, and 10 miRNAs were differentially expressed. Comprehensive functional analyses indicated that the identified DElncRNAs potentially regulate sensory perception-related target mRNAs via cis-regulation, and coordinate metabolic and proteostatic reprogramming via trans-regulation to support the transition to reproductive activation in workers. Furthermore, a competing endogenous RNA network was constructed which integrated 74 DElncRNAs, 5 DEmiRNAs, and 36 DEmRNAs to predict their potential post-transcriptional interactions. Our findings highlight a comprehensive analysis of ncRNAs and mRNAs in worker heads, providing a foundation for functional validation of their roles in honeybee ovary development.