Autosomal gsdf acts as a male sex initiator in the fish medaka.

Xi Zhang,Yunhan Hong,Qizhi Liu,Mingyou Li,Yoshitaka Nagahama,Jiale Li,Guijun Guan,Feng Zhu,Kiyoshi Naruse,Amaury Herpin

doi:10.1038/srep19738

Abstract

Sex is pivotal for reproduction, healthcare and evolution. In the fish medaka, the Y-chromosomal dmy (also dmrt1bY) serves the sex determiner, which activates dmrt1 for male sex maintenance. However, how dmy makes the male decision via initiating testicular differentiation has remained unknown. Here we report that autosomal gsdf serves a male sex initiator. Gene addition and deletion revealed that gsdf was necessary and sufficient for maleness via initiating testicular differentiation. We show that gsdf transcription is activated directly by dmy. These results establish the autosomal gsdf as the first male sex initiator. We propose that dmy determines maleness through activating gsdf and dmrt1 without its own participation in developmental processes of sex initiation and maintenance. gsdf may easily become a sex determiner or other autosomal genes can be recruited as new sex determiners to initiate gsdf expression. Our findings offer new insights into molecular mechanisms underlying sex development and evolution of sex-controlling genes in vertebrates.

Highlights

The gene gsdf is emerging as a novel sex related factor in several distantly related fish species
It has been reported that two genes are sufficient to induce medaka masculinization upon transgenic addition, one is dmy[24] and the other is gsdf Y, a Y-chromosomal copy of gsdf acting as the sex determiners (SDs) in O. luzonesis[25]
We examined the histology of adult gonads and spatial gene expression patterns by fluorescence in situ hybridization (FISH) and immunofluorescence (IF)

Summary

Introduction

The gene gsdf is emerging as a novel sex related factor in several distantly related fish species. This teleost-specific gene[21] encodes the gonadal soma derived factor, which belongs to the transforming growth factor-β superfamily[22]. Gsdf is located on chromosome 12 and is predominantly expressed in the Sertoli cells and granulosa cells in mature gonads[23]. We show this autosomal gene gsdf acts as a male sex initiator downstream of dmy and renders itself a prime candidate for the searched autosomal gene essential for maleness

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Results

Conclusion