Oogenesis in Atlantic salmon (Salmo salar L.) occurs by zonagenesis preceding vitellogenesis in vivo and in vitro

Abstract

Fish oogenesis represents pleiotropic cytodifferentiative programs including hepatic synthesis of the molecular components for both the eggshell and the oocytic energy deposits. Both hepatic processes are directly controlled by plasma levels of estradiol (E2), and injected E2 induces both biogenetic processes in prepubertal fish of both sexes. This work compares the temporal pattern of E2-induced biosynthesis of zona radiata proteins (zr-proteins) and vitellogenin in Atlantic salmon (Salmo salar L.) in vivo and in vitro. We monitored the presence of plasma zr-proteins and vitellogenin, using homologous polyclonal antiserum to zr-proteins and a monoclonal antibody to vitellogenin. Zr-proteins were induced by all E2 concentrations (0.001-1.1 mg/kg body weight (bw)) within one week of exposure while vitellogenin was not induced until two weeks post-injection and then only in plasma from fish injected with high E2 concentrations (0.4 mg or 1.1 mg/kg bw). After E2 treatment, hepatocytes isolated from male fish synthesized zr-proteins and vitellogenin in vitro. However, zr-proteins were secreted into the medium two days before vitellogenin, as measured by ELISA. The data indicate a preferential induction of zr-proteins compared with vitellogenin, both with regard to E2 sensitivity and response time to E2 treatment. These findings suggest an obligate sequence in salmon oogenesis. During sexual maturation low E2 levels at first induce only zonagenesis, while increasing levels of E2 subsequently induce both zonagenesis and vitellogenesis. In nature, the interval between zonagenesis and vitellogenesis may, therefore, be considerable. The data suggest new control mechanisms in fish oogenesis.