The transcriptional repressor Blimp-1 acts downstream of BMP signaling to generate primordial germ cells in the cricket Gryllus bimaculatus.

Taro Nakamura,Cassandra G Extavour

doi:10.1242/dev.127563

Abstract

Segregation of the germ line from the soma is an essential event for transmission of genetic information across generations in all sexually reproducing animals. Although some well-studied systems such as Drosophila and Xenopus use maternally inherited germ determinants to specify germ cells, most animals, including mice, appear to utilize zygotic inductive cell signals to specify germ cells during later embryogenesis. Such inductive germ cell specification is thought to be an ancestral trait of Bilateria, but major questions remain as to the nature of an ancestral mechanism to induce germ cells, and how that mechanism evolved. We previously reported that BMP signaling-based germ cell induction is conserved in both the mouse Mus musculus and the cricket Gryllus bimaculatus, which is an emerging model organism for functional studies of induction-based germ cell formation. In order to gain further insight into the functional evolution of germ cell specification, here we examined the Gryllus ortholog of the transcription factor Blimp-1 (also known as Prdm1), which is a widely conserved bilaterian gene known to play a crucial role in the specification of germ cells in mice. Our functional analyses of the Gryllus Blimp-1 ortholog revealed that it is essential for Gryllus primordial germ cell development, and is regulated by upstream input from the BMP signaling pathway. This functional conservation of the epistatic relationship between BMP signaling and Blimp-1 in inductive germ cell specification between mouse and cricket supports the hypothesis that this molecular mechanism regulated primordial germ cell specification in a last common bilaterian ancestor.

Highlights

The cells that make up multicellular organisms can be divided into two major categories based on the contribution of their genome to the evolutionary process: somatic cells and germ cells
We recently reported that G. bimaculatus primordial germ cell (PGC) formation requires bone morphogenetic protein (BMP) signaling, demonstrating conservation of this mechanism between mice and cricket (Donoughe et al, 2014)
Cloning of the cricket G. bimaculatus homolog of Blimp-1 In order to investigate whether Blimp-1-mediated germ cell induction operates in G. bimaculatus, we first searched for Prdm family genes using G. bimaculatus embryonic transcriptome data

Summary

Introduction

The cells that make up multicellular organisms can be divided into two major categories based on the contribution of their genome to the evolutionary process: somatic cells and germ cells. Germ cells are specified through one of two well-characterized modes, either maternally inherited germ plasm or zygotic inductive signals during. In the inheritance mode, which is used by a majority of traditional laboratory model organisms including Drosophila melanogaster, Caenorhabditis elegans, Xenopus laevis and Danio rerio, maternally provided cytoplasmic determinants called germ plasm confer germ cell fate on a specific cell population in early embryos. In contrast to this inheritance mode, Mus musculus specifies germ cells through zygotic cell-cell signaling mechanisms during later embryogenesis. Experimental evidence for the inductive mode was until recently available only for two vertebrates, namely salamander and mice (reviewed by Extavour and Akam, 2003)

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