Developmental and Sexual Plasticity of Spermatogonia in Fish.

Primordial germ cells (PGCs) differentiate into oogonia or spermatogonia in the ovary or testis, respectively. Morphologically, spermatogonia and oogonia are smaller than PGCs and possess distinctive microstructures. However, the functional differences among PGCs, spermatogonia, and oogonia are poorly understood in fish. In this study, we characterized developmental and sexual plasticity of these pre-meiotic germ cells by transplanting them into sexually undifferentiated embryonic gonads in rainbow trout (Oncorhynchus mykiss). Spermatogonia or oogonia isolated from meiotic gonads of vasa-Gfp transgenic trout were transplanted into the peritoneal cavity of newly hatched embryos of both sexes and the behaviour of GFP-labelled donor cells was observed. The transplanted spermatogonia and oogonia migrated towards the recipient genital ridges with extending pseudopodia and were subsequently incorporated into them. We further confirmed that the donor-derived gonial germ cells resumed gametogenesis in the recipient somatic microenvironment synchronously with endogenous germ cells. Surprisingly, donor-derived spermatogonia started to proliferate and differentiate into oocytes in female recipients. At 2 years post transplantation, the eggs from mature female recipients were artificially inseminated with sperm from intact male trout. The results demonstrated that normal live offspring with the donor-derived haplotype were obtained. In addition, oogonium-derived sperm were produced in the male recipients as well. The donor-derived sperm were shown to be fully functional, as live offspring carrying GFP-labelled germ cells with the donor haplotype were obtained in the F1. These findings indicate that fish pre-meiotic germ cells, probably spermatogonial stem cells or oogonial stem cells, possess a high level of developmental and sexual plasticity and sexual differentiation of germ cells is controlled solely by the somatic microenvironment, rather than being cell autonomous.