Sex specific gene expression is present prior to metamorphosis in the sea urchin

• Published in: Developmental biology 2025-01, Vol.517, p.217-233
• Main Authors: Pieplow, Cosmo, Furze, Aidan, Gregory, Pauline, Oulhen, Nathalie, Wessel, Gary M.
• Format: Article
• Language: English
• Subjects: Animals; Echinoderm; Female; Gametogenesis - genetics; Gene Expression Regulation, Developmental; Germ line; Gonads; Gonads - growth & development; Gonads - metabolism; Larva - genetics; Larva - growth & development; Larva - metabolism; Lytechinus - embryology; Lytechinus - genetics; Lytechinus variegatus; Male; Meiosis - genetics; Metamorphosis, Biological - genetics; Ovary; Ovary - growth & development; Ovary - metabolism; Sea urchin; Sea Urchins - embryology; Sea Urchins - genetics; Sea Urchins - growth & development; Sex determination; Sex Determination Processes - genetics; Testis; Testis - growth & development; Testis - metabolism
• ISSN: 0012-1606; 1095-564X; 1095-564X
• DOI: 10.1016/j.ydbio.2024.10.003

A profound collaboration between the germline and somatic cells of an organism is the creation of a functional gonad. Here we establish a foundation for studying molecular gonadogenesis in the sea urchin by use of RNA-seq, quantitative mRNA measurements, and in-situ hybridizations throughout the life cycle of the variegated sea urchin, Lytechinus variegatus (Lv). We found through three distinct analyses that the ovary and testis of this echinoderm expresses unique transcripts involved in gametogenesis, and also discovered uncharacterized gene products unique to each gonad. We further developed a pipeline integrating timepoint RNA-seq data throughout development to identify hallmark gene expression in gonads. We found that meiotic and candidate genes involved in sex determination are first expressed surprisingly early during larval growth, and well before metamorphosis. We further discovered that individual larvae express varying amounts of male- or female-hallmarks before metamorphosis, including germline, oocyte, sperm, and meiotic related genes. These distinct male- or female-gonad gene profiles may indicate the onset of, and commitment to, development of a bipotential gonad primordium, and may include metabolic differences, supported by the observation that transcripts involved in glycolysis are highly enriched in the ovary compared to the testis. Together these data support a hypothesis that sex determination is initiated prior to metamorphosis in the sea urchin and that the many uncharacterized genes unique to each gonad type characterized herein may reveal unique pathways and mechanisms in echinoderm reproduction. [Display omitted] •Gonads of the sea urchin, Lytechinus variegatus, have distinct transcriptome profiles based on sex.•Expression of sex-specific genes begins well prior to metamorphosis.•Sex specific gene expression includes, but is not limited to, genes involved in gametogenesis.•Male sex-specific profiles emerge earlier in development than the female profile.•Female sex-specific transcripts, including glycolytic enzymes, fluctuate with the reproductive stage of the ovary.