Foxl2 Regulates Ovarian Development Through Cyp19a1a-Mediated Estrogen Biosynthesis in the Silver Pomfret (Pampus argenteus)

The silver pomfret (Pampus argenteus) is a marine species with considerable economic value. The processes involved in gonadal maturation in P. argenteus are still mostly unclear, presenting obstacles to artificial breeding. The foxl2 gene is fundamental to the development of ovarian tissues, and its absence causes early ovarian failure and sex reversal. cyp19a1a encodes ovarian aromatase, a key enzyme responsible for estrogen biosynthesis by converting androgens into estrogens, and is essential for ovarian differentiation and maintenance in teleosts. This study aimed to elucidate the function of foxl2 in P. argenteus. Our results show that foxl2 expression was primarily observed in undifferentiated gonads and ovaries, with a notable increase during stages I and V of ovarian development, where it was predominantly localized in granulosa cells. Foxl2 seems to play a role in the initial stages of testicular development, with expression observed in stage I testes, where Foxl2 were primarily localized to the cytoplasm of spermatogonia. Immunofluorescence analysis of Foxl2 and Cyp19a1a protein distribution during gonadal development in P. argenteus revealed that Foxl2 was primarily localized to the cytoplasm of primary and previtellogenic oocytes, as well as in granulosa cells, while Cyp19a1a was detected predominantly in granulosa cells. The expression of foxl2 was markedly upregulated following treatment with estradiol (E2) and recombinant Cyp19a1a (rCyp19a1a). In summary, the evidence implies that foxl2, a gene with a female-specific expression pattern, may play an essential role in granulosa cell formation and estrogen production. Additionally, Foxl2 could have a complementary function with Cyp19a1a in P. argenteus.