Deciphering gonadal transcriptome reveals circRNA-miRNA-mRNA regulatory network involved in sex differentiation and gametogenesis of Apostichopus japonicus.

Abstract

As stable and conserved non-coding RNAs, circular RNAs (circRNAs) play vital roles in gene regulation, particularly in reproductive development. However, their functions in marine invertebrate gonadal differentiation remain largely unexplored. Understanding the molecular mechanisms of sexual differentiation and gonadal development is essential for advancing reproductive biology in marine invertebrates. The sea cucumber Apostichopus japonicus is a vital species in economic aquaculture. Before the breeding season, A. japonicus exhibits minimal sexual dimorphism, significantly impeding breeding efficiency and posing challenges for the development of superior germplasm resources. Investigating the role of circRNAs in mature A. japonicus will enhance our understanding of its specific molecular mechanism during sexual differentiation and gonadal reproduction. In this study, we constructed differential expression profiles of circRNAs. A total of 18,121 circRNAs were identified, distributed across the 23 chromosomes of A. japonicus. 584 circRNAs exhibited significant expression differences, with 296 up-regulated and 288 down-regulated. Through GO enrichment and KEGG pathway analysis of these circRNAs, two pathways related to sexual differentiation were identified: the AMPK signaling pathway and the TGF-β signaling pathway, which may regulate sexual differentiation by influencing sex hormone synthesis. Additionally, several genes, such as smad3, smoc2, and ppp2r1a may play critical regulatory roles in the development and activity of germ cells. Our study elucidates the molecular regulatory roles of circRNAs in the sexual differentiation and gonadal development of A. japonicus. Given its evolutionary position as the closest phylum to chordates, the present study on A. japonicus provides valuable insights into the non-coding RNA resource for marine invertebrates.