Abstract

During embryonic gonadal development, the supporting cell lineage is the first cell type to differentiate, giving rise to Sertoli cells in the testis and pre-granulosa cells in the ovary. These cells are thought to direct other gonadal cell lineages down the testis or ovarian pathways, including the germline. Recent research has shown that, in contrast to mouse, chicken gonadal supporting cells derive from a PAX2/OSR1/DMRT1/WNT4 positive mesenchymal cell population. These cells colonize the undifferentiated genital ridge during early gonadogenesis, around the time that germ cells migrate into the gonad. During the process of somatic gonadal sex differentiation, PAX2 expression is down-regulated in embryonic chicken gonads just prior to up-regulation of testis- and ovary-specific markers and prior to germ cell differentiation. Most research on avian gonadal development has focused on the chicken model, and related species from the Galloanserae clade. There is a lack of knowledge on gonadal sex differentiation in other avian lineages. Comparative analysis in birds is required to fully understand the mechanisms of avian sex determination and gonadal differentiation. Here we report the first comparative molecular characterization of gonadal supporting cell differentiation in birds from each of the three main clades, Galloanserae (chicken and quail), Neoaves (zebra finch) and Palaeognathe (emu). Our analysis reveals conservation of PAX2+ expression and a mesenchymal origin of supporting cells in each clade. Moreover, down-regulation of PAX2 expression precisely defines the onset of gonadal sex differentiation in each species. Altogether, these results indicate that gonadal morphogenesis is conserved among the major bird clades.

Highlights

  • Gonadal sex differentiation during embryogenesis provides an excellent model for studying the genetic regulation of development

  • The supporting cell lineage derives from the coelomic epithelium (Stevant et al, 2018, 2019)

  • The gonadal supporting cells in birds do not derive from the coelomic epithelium but rather from a DMRT1 and PAX2 positive mesenchymal population

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Summary

Introduction

Gonadal sex differentiation during embryogenesis provides an excellent model for studying the genetic regulation of development. For which most data are available, proliferation of cells in the coelomic epithelium gives rise to so-called supporting cell progenitors, which enter the medulla This key cell lineage generates Sertoli cells in the testis and pre-granulosa cells in the ovary. They lose pluripotency and enter mitotic arrest (Spiller et al, 2017) These sexually dimorphic germ cell fates are intimately linked to the development of the gonadal somatic cells. In males, this lineage gives rise to pre-Sertoli cells and, in females, pre-granulosa cells (Stevant and Nef, 2019). The sexual fate of the gonadal soma and the germ cells hinges upon the key supporting cell lineage

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