Analysis of gonadal transcriptome reveals core long non-coding RNA-mRNA regulatory network in sea cucumber Apostichopus japonicus

Abstract

Apostichopus japonicus is a representative temperate sea cucumber species, that mainly inhabits in coastal zone of the continental shelf. With high nutritional value and important medical value, A. japonicus become an important commercial aquaculture species and produce significant economic value in recent years. A. japonicus has no sexual dimorphism that can be used to distinguish female and male individuals by external appearance and morphology. The phenotype sex can be only detected by dissecting and observing gonad tissue, thus the breeding efficiency could be greatly reduced. This limitation has hindered the advancement of selective breeding programs and sea cucumber industry. To investigate the genetic basis of reproductive biology in A. japonicus, advanced sequencing techniques, such as next- and third-generation sequencing, have been employed to explore the roles of non-coding RNAs and other genetic factors, offering new insights into sex determination mechanisms. To further gain a deeper understanding of the knowledge underlying lncRNAs in gonadal differentiation, we conducted a comparative transcriptome sequencing analysis of gonadal tissues from both sexes. In our research, a total of 3990 novel lncRNAs and 1441 differentially expressed lncRNAs were identified between female and male gonads. Additionally, a molecular regulatory network indicating lncRNA-mRNA interactions was constructed based on transcriptional profiles, which provide insights into the potential cis- and trans- target genes of lncRNAs. The gonadal transcriptome analysis identified a number of novel long non-coding RNAs involved in female and male reproduction process. Both cis- and trans-acting regulatory networks indicating lncRNA-mRNA interaction were constructed based on transcriptional profiles. These findings provide new insights into the lncRNA-mediated regulation of reproductive biology in marine invertebrates, indicating the crucial roles of long non-coding sequences in regulating expression profiles. Further, the GO and KEGG enrichment analyses of cis- and trans- targeted mRNA for differentially expressed lncRNA indicated that sexual reproduction (GO:0019953), germ cell development (GO:0007281), and negative regulation of hormone secretion (GO:0046888) are potentially involved in gonadal differentiation through the regulation of long non-coding sequences. Notably, besides the classical reproduction related signaling pathway like Gonadotropin-releasing hormone (GnRH) secretion (ko04929), several regulatory pathways, such as Epidermal growth factor receptor (ErbB) signaling pathway (ko04012), TGF-beta signaling pathway (ko04350), and neurotrophin signaling pathway (ko04722) were also enriched and potentially involved in sex differentiation and gonadal development.