Dual Roles of cyp19a1a in Gonadal Sex Differentiation and Development in the Protandrous Black Porgy, Acanthopagrus schlegeli

Protandrous black porgy fish, Acanthopagrus schlegeli, have a striking life cycle, with male sex differentiation at the juvenile stage, a bisexual gonad during first 2 yr of life, and a male-to-female sex change (with vitellogenic oocytes) at 3 yr of age. The present study investigated the role of aromatase (cyp19a1a/ Cyp19a1a) in gonadal development in this species, especially in relation to sexual differentiation and sex change. Fish of various ages were treated with estradiol (E-2) or aromatase inhibitor (AI) to determine whether manipulation of the hormonal environment has an impact on these processes. We report an integrative immunohistochemical, cellular, and molecular data set describing these interesting phenomena. During male sex differentiation, high levels of cyp19a1a/Cyp19a1a expression were observed in the undifferentiated gonad (4 mo of age), in marked contrast to the low cyp19a1a/Cyp19a1a levels detected in the differentiated testis at the age of 5 -6 mo. A low dose of E-2 (0.25 mg/kg feed) stimulated testicular growth and function in sexually differentiated fish, whereas a high dose of E-2 (6 mg/kg feed) induced female development. Furthermore, administration of AI suppressed male development and promoted female sexual differentiation. An increased number of figla transcripts (an oocyte-specific gene) were observed prior to cyp19a1a expression, concomitant with the development of oogonia and early primary oocytes in the ovaries of both E-2- and AI-treated groups. Immunohistochemical Pcna staining showed that the regression of testicular tissue occurred prior to the development of ovarian tissue in both E-2- and AI-induced females. The importance of cyp19a1a in female development was further demonstrated by the increase in cyp19a1a transcripts during the naturally occurring sex change. Transcripts of foxl2 increased in the gonads of 2- to 3-yr-old black porgy during the early stages of the natural sex change, followed by a gradual elevation of cyp19a1a levels. The levels of both genes peaked in the resulting ovarian tissue. Thus, cyp19a1a/Cyp19a1a plays dual roles in the gonadal development, namely, in testicular development during the initial period of sexual differentiation and later in ovarian development during the natural sex change.