Differential regulation of ribogenesis genes throughout oogenesis in thicklip grey mullets, Chelon labrosus, preparing the maternal contribution to embryo development

Oocytes in teleosts undergo complex changes during oogenesis, including the accumulation of ribosomal RNAs and tRNAs needed to support protein synthesis during early embryogenesis. Previous studies show that high levels of 5S rRNA and tRNAs in perinucleolar previtellogenic (PV) oocytes, and the easily calculated 5S rRNA/18S rRNA index, reliably distinguish testes from ovaries, especially when ovaries are in PV. Building on this, we examined whether the tRNA/5.8S rRNA index follows a similar pattern during oogenesis in thicklip grey mullet Chelon labrosus, a species with synchronous ovarian development. The index values revealed very high tRNA levels during previtellogenesis, when only perinucleolar oocytes are present, tRNA levels being gradually met by 5.8S rRNA ones during secondary growth towards vitellogenesis. Transcription of 5S rRNA and tRNAs by RNAP-III is regulated by general transcription factors (Gtf3a, b, and c) and the inhibitor Maf1. We analyzed ovarian transcription patterns of Gtf3b-related genes (brf1a, brf1b, brf2, bdp1, and tbpl2), comparing them with previously described gtf3aa and gtf3ab, which act specifically in 5S rRNA transcription. We also quantified transcript levels of maf1 and dap1b, the latter involved in keeping ribosomes dormant until fertilization. Most Gtf3b-related genes, as well as maf1 and dap1b, showed higher transcription in ovaries than in testes and intersex testes. Transcript levels peaked in PV ovaries and declined in cortical alveoli and late-vitellogenic stages. brf1a and tbpl2 also differentiated intersex testes from normal testes. These observations reinforce the hypothesis that primary oocyte differentiation is marked by a strong activation of RNAP-III activity for ribogenesis.