Identification of miRNAs, lncRNAs, circRNAs, and their ceRNA networks in the establishment of sexual size dimorphism in the olive flounder (Paralichthys olivaceus)

Abstract

Olive flounder (Paralichthys olivaceus), a valuable mariculture species, exhibits a significant female-biased sexual size dimorphism (SSD). Despite its economic and biological importance, the molecular mechanisms underlying this phenomenon, in particular the contribution of non-coding RNAs (ncRNAs) and their associated competitive endogenous RNA (ceRNA) regulatory mechanisms, remain unclear. In this study, we conducted whole transcriptome sequencing of the brains/pituitaries and muscles of olive flounder during the critical period for SSD establishment, identifying 23/282/85 and 25/193/82 differentially expressed (DE) miRNAs/circRNAs/lncRNAs, respectively. Based on the regulatory interactions among these DE RNAs, we constructed the lncRNA-miRNA-mRNA and circRNA-miRNA-mRNA ceRNA networks. Our analyses revealed crucial SSD-related pathways regulated by these ncRNAs/ceRNA networks, including “ovarian steroidogenesis”, “prolactin signaling pathway”, “cell adhesion molecules”, “GABAergic synapse”, and “dopaminergic synapse” pathways in brains/pituitaries, “ECM-receptor interaction”, “PI3K-Akt signaling pathway”, “focal adhesion”, “regulation of actin cytoskeleton”, and several metabolism-related pathways in muscles. Moreover, numerous genes regulated by these ncRNAs/ceRNA networks emerged as potential candidates for SSD establishment, such as frizzled3 (fzd3), cholecystokinin A receptor (cckar), carbonic anhydrase 4 (ca4), and calcium voltage-gated channel subunit alpha1 B (cacna1b) in brains/pituitaries, and DNA (cytosine-5) methyltransferase 3A (dnmt3a), Krüppel-like factor 11 (klf11), myocyte enhancer factor 2c (mef2c), insulin receptor (insr), serum- and glucocorticoid-inducible kinase 1 (sgk1), nuclear receptor 4A1 (nr4a1), and apelin in muscles. This study provides the first preliminary insights into the ncRNAs and their ceRNA networks implicated in SSD-related growth traits in flounder, providing potential targets for selective breeding programs aimed at enhancing growth in aquaculture.