Integrated lncRNA and mRNA Transcriptome Analyses of IGF1 and IGF2 Stimulated Ovaries Reveal Genes and Pathways Potentially Associated with Ovarian Development and Oocyte Maturation in Golden Pompano (Trachinotus ovatus)

Insulin-like growth factors (IGFs) play crucial roles in the regulation of animal growth and reproduction. However, the functional and regulatory mechanisms underlying ovarian growth and oocyte maturation in teleosts remain unclear. In this study, the expression profiles of lncRNAs and mRNAs were analyzed in the ovaries of golden pompano (<i>Trachinotus ovatus</i>) treated with IGF1 and IGF2 proteins to gain insights into the role of these two IGF ligands in the regulation of ovarian development and maturation. A total of 1494 lncRNAs and 8728 mRNAs were differentially expressed following IGF1 treatment compared with the control group. A total of 101 lncRNAs and 377 mRNAs were differentially expressed after IGF2 treatment compared to those in the control group. The results revealed that KEGG pathways enriched by target genes of the DE lncRNAs overlapped significantly with those enriched by the DE mRNAs in both the IGF1 and IGF2 groups. The key overlapping enriched pathways included ECM receptor interaction, gap junction, Hedgehog signaling pathway, Ras signaling pathway, Rap1 signaling pathway, TGF beta signaling pathway, Wnt signaling pathway, GnRH signaling pathway, progesterone-mediated oocyte maturation, oocyte meiosis, cell cycle, and MAPK signaling pathway. The differentially expressed genes (DEGs) involved in ovarian development and oocyte maturation were <i>cyp17a1</i>, <i>cyp19a1</i>, <i>star</i>, <i>hsd17b3</i>, <i>hsd17b7</i>, <i>adam23</i>, <i>slc26a6</i>, <i>htr2b</i>, <i>h2ax</i>, <i>nanos3</i>, <i>krt18</i>, <i>pgr</i>, and <i>inhbb</i>, following IGF1 and IGF2 treatment. Furthermore, four lncRNAs (MSTRG.66521.1, MSTRG.49969.1, MSTRG.59923.1, and MSTRG.13767.1) for IGF1 and two (MSTRG.20896.2 and MSTRG.58123.2) for IGF2 within the lncRNA-mRNA network were found to target DEGs related to ovarian development and maturation. This suggests that IGFs may affect reproductive processes by regulating the expression of lncRNAs and mRNAs. RT-qPCR analysis revealed that these six lncRNAs showed high expression levels in the brain, pituitary, liver, and gonad tissues, indicating their potential involvement in regulating ovarian growth and development. This study elucidates the lncRNA-mRNA regulatory mechanism in response to IGF1 and IGF2 treatment during stage III of ovarian development in golden pompano, thereby deepening our understanding of its functional role.