Identification of growth-associated miRNAs, circRNAs, and their corresponding regulatory networks in fast- and slow- growing families of Takifugu rubripes

Abstract

Tiger puffer (Takifugu rubripes) is one of the most expensive farmed marine fish species in East Asia. Growth traits are important economic factors in cultured fish, miRNAs and circRNAs play important roles in growth and development. However, little is known of how miRNAs and circRNAs contribute to regulating fish growth through neuroendocrine regulation. To explore the role of miRNAs and circRNAs in regulating T. rubripes growth, RNA sequencing technology was used to sequence whole brain tissue transcriptomes from fast and slow-growing T. rubripes families. A total of 14 and 261 differentially expressed (DE) circRNAs and miRNAs were identified, respectively, in brain tissues. Among these, the expression levels of circCacna1c may maintain stable neuroendocrine environments by precisely regulating intracellular calcium (Ca2+) concentrations, thereby accelerating T. rubripes growth. Notably, genes including tgfb3, bmp2b, and bmp16 appeared to modulate T. rubripes development by coordinating neural activities during development via the Smad pathway. A miRNA-mRNA regulatory network was also identified that comprised 98 and 113 DE miRNAs and mRNAs, respectively. miR-124-4-3p and miR-124-4-5p of the miR-124 family were implicated in the regulation of neural development in T. rubripes by suppressing target genes like runx3, hoxb3a, mdfic, flt3, smo and syt10. In addition, 8 circRNA-miRNA-mRNA pathways were constructed including 2 circRNAs, 5 miRNAs, and 2 mRNAs. DE miRNAs and circRNAs identified here are primarily involved in nerve development and the maintenance of Ca2+ homeostasis in fast- and slow-growing T. rubripes. Overall, these results inform a better understanding of growth-related transcriptional dyanmics in T. rubripes brains, but also aid in the systematic selection and breeding of new varieties with higher qualities and yields.