Abstract
BackgroundThe genes boule and dazl are members of the DAZ (Deleted in Azoospermia) family encoding RNA binding proteins essential for germ cell development. Although dazl exhibits bisexual expression in mitotic and meiotic germ cells in diverse animals, boule shows unisexual meiotic expression in invertebrates and mammals but a bisexual mitotic and meiotic expression in medaka. How boule and dazl have evolved different expression patterns in diverse organisms has remained unknown.Methodology and Principal FindingsHere we chose the fish rainbow trout (Oncorhynchus mykiss) as a second lower vertebrate model to investigate the expression of boule and dazl. By molecular cloning and sequence comparison, we identified cDNAs encoding the trout Boule and Dazl proteins, which have a conserved RNA-recognition motif and a maximal similarity to their homologs. By RT-PCR analysis, adult RNA expression of trout boule and dazl is restricted to the gonads of both sexes. By chromogenic and two-color fluorescence in situ hybridization, we revealed bisexual and germline-specific expression of boule and dazl. We found that dazl displays conserved expression throughout gametogenesis and concentrates in the Balbinani's body of early oocytes and the chromatoid body of sperm. Surprisingly, boule exhibits mitotic and meiotic expression in the male but meiosis-specific expression in the female.ConclusionsOur data underscores differential conservation and divergence of DAZ family genes during vertebrate evolution. We propose a model in which the diversity of boule expression in sex and stage specificity might have resulted from selective loss or gain of its expression in one sex and mitotic germ cells.
Highlights
Gametogenesis, oogenesis in the ovary and spermatogenesis in the testis, proceeds in multiple processes including mitotic proliferation of germ stem cells and meiosis, as well as postmeiotic spermiogenesis in male
We propose a model in which the diversity of boule expression in sex and stage specificity might have resulted from selective loss or gain of its expression in one sex and mitotic germ cells
The functional conservation between dazl and boule was demonstrated by the fact that transgenic expression of the Xenopus dazl was capable of rescuing the boule meiotic entry phenotype in Drosophila [8]
Summary
Gametogenesis, oogenesis in the ovary and spermatogenesis in the testis, proceeds in multiple processes including mitotic proliferation of germ stem cells and meiosis, as well as postmeiotic spermiogenesis in male. The DAZ (Deleted in Azoospermia) gene family represents one of the few lines of evidence for evolutionary conservation of these processes at the molecular level [1]. This family comprises daz, dazl and boule, which encode RNAbinding proteins characteristic of a conserved RNA recognition motif (RRM) and one or multiple repeats of the DAZ motif. The founder member of the DAZ family is the human Daz gene that forms a cluster on the Y chromosome [2,3]. The genes boule and dazl are members of the DAZ (Deleted in Azoospermia) family encoding RNA binding proteins essential for germ cell development. How boule and dazl have evolved different expression patterns in diverse organisms has remained unknown
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