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Sci Rep
2025 Dec 20;161:2715. doi: 10.1038/s41598-025-32582-x.
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Integrated application of transcriptomics and metabolomics provides insights into gonadal differentiation in Mesocentrotus nudus.
Abulizi A, Su W, Huang X, Xiang H, Sun Z, Chang Y.
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Mesocentrotus nudus is an important aquaculture species in East Asia, valued for its gonads as the only edible part. However, the molecular basis of gonadal differentiation in this species remains poorly understood. In this study, we determined that morphological gonadal differentiation occurs when individuals reach a test diameter of approximately 40 mm. Amino acid profiling revealed sex-specific differences between ovaries and testes, with higher levels of lysine, proline, alanine, and glutamic acid in testes, suggesting sexual dimorphism in metabolic demand. To investigate the regulatory mechanisms involved, we conducted integrated transcriptomic and metabolomic analyses between differentiated and undifferentiated gonads. Differentially expressed genes (DEGs) and differentially expressed metabolites (DEMs) including retinoic acid, linoleic acid, and arachidonic acid, were significantly enriched in retinol metabolism, steroid biosynthesis, and amino acid metabolic pathways. Several key genes, such as GATA4, CYP17A1, and HSD17B, were identified as potential markers for gonadal differentiation. Furthermore, components of the TGF-β signaling pathway (Smads, Rbx1, SKP) and retinol metabolism genes (CYP26, CYP1A, CYP3A) exhibited sex-biased expression patterns. This study provides novel insights into the molecular mechanisms underlying sex differentiation in sea urchins and lays a molecular foundation for the development of sex-control breeding strategies.
Fig. 1. Morphological and histological observations of juvenile gonads in sea urchins. Morphological observations based on anatomical dissection (top panels) and paraffin sections of gonads (bottom panels). Red triangles indicate the gonads. (A–D) represent M. nudus individuals with test diameters (TD) of 2, 5, 8, and 13 mm, respectively. (E, F) represent female and male sea urchins with a TD of 24 mm, and (G, H) represent female and male sea urchins with a TD of 40 mm. TD, test diameter; NP, nutritive phagocytes; Oo, oogonia; SPC, spermatocyte. Bar = 50 µm.
Fig. 2. GO term enrichment analysis was performed for the DEGs between the compared gonadal groups. (A) GO term enrichment analysis of DEGs between differentiated ovaries and testes. (B) GO term enrichment analysis of DEGs between undifferentiated ovaries and testes.
Fig. 3. GO term enrichment analysis was performed for the DEGs between the compared gonadal groups. (A) GO term enrichment analysis of DEGs between differentiated testes and undifferentiated testes. (B) GO term enrichment analysis of DEGs between differentiated ovaries and undifferentiated ovaries.
Fig. 4. KEGG pathway analysis of DEGs between the compared gonadal groups. (A) KEGG pathway analysis of DEGs between differentiated testes and undifferentiated testes. (B) KEGG pathway analysis of DEGs between undifferentiated ovaries and undifferentiated testes. The vertical axis shows KEGG pathways that are significantly enriched by DEGs, and the horizontal axis indicates the corresponding enrichment factors. Pathway maps are based on the KEGG database 42–44.
Fig. 5. Validation of six key differentially expressed genes in M. nudus by qRT-PCR. Data are expressed as the mean ± standard deviation (SD) of three replicates. DO, differentiated ovaries; DT, differentiated testes; UDO, undifferentiated ovaries; UDT, undifferentiated testes. Identical letters indicate no significant differences among individuals, whereas different letters denote significant differences (p < 0.05).
Fig. 6. KEGG pathway analysis of DEMs between the compared gonadal groups. The vertical axis represents the number of DEMs associated with each pathway, while the horizontal axis indicates the KEGG significantly pathways enriched by DEMs. Pathway maps are based on the KEGG database 42–44.
Fig. 7. An integrative metabolic network map constructed from differentially expressed genes and metabolites between the compared gonadal groups. (A) DO vs DT group. (B) DO vs UDO group. (C) DT vs UDT group. (D) UDO vs UDT group. DO, differentiated ovaries; DT, differentiated testes; UDO, undifferentiated ovaries; UDT, undifferentiated testes. Differentially expressed genes (DEGs) are represented by boxes, and differentially expressed metabolites (DEMs) are represented by circles. Red indicates upregulation, while green indicates downregulation.
