Conserved Sex-Specific Timing of Meiotic Initiation During Sex Differentiation in the Protandrous Black Porgy Acanthopagrus schlegelii

Meiosis is an essential mechanism of gametogenesis for all sexually reproducing species. In vertebrates, one conserved aspect of sex differentiation is that female embryonic germ cells enter meiosis earlier than male germ cells. In some lower vertebrates, female germ cells proliferate prior to entering meiosis, whereas male cells remain in mitotic arrest. Protandrous black porgy fish, Acanthopagrus schlegelii, have a dramatic life cycle involving a characteristic sex change. Black porgy are functional males for their first and second spawning seasons, but approximately half of the fish transform into females during their third year. We cloned the black porgy homologs of dosage suppressor of mck1 homolog (dmc1) and synaptonemal complex protein 3 (sycp3), and examined their expression profiles as well as those of cytochrome P450 family 26 genes (cyp26: cyp26a and cyp26b), retinaldehyde dehydrogenases (raldh: raldh2 and raldh3), retinoic acid receptors (rars: raralpha, rarbeta, rargamma, and rargammab), retinoid X receptors (rxrs: rxralpha, rxrbeta, and rxrgamma) and deleted azoospermia-like (dazl) during gonadal sex differentiation by RT-PCR, quantitative RT-PCR, and immunohistochemistry. Our results show that during gonadal development, germ cells located in ovarian tissue proceed into meiosis earlier than germ cells in testicular tissue. Furthermore, treatment with estradiol-17beta, which induced cyp26 expression, blocked dazl and raldh expression and reduced the expression of rars, rxrs, dmc1, and sycp3. This unique model therefore suggests that the temporal differences in meiosis initiation between females and males are conserved during gonadal sex differentiation in hermaphroditic vertebrates.