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Proc Natl Acad Sci U S A. 2016 Jun 21;113(25):E3509-18. doi: 10.1073/pnas.1521341113. Epub 2016 Jun 2.

A premeiotic function for boule in the planarian Schmidtea mediterranea.

Author information

1
Department of Cell and Developmental Biology, University of Illinois at Urbana-Champaign, Urbana, IL 61801; Howard Hughes Medical Institute, University of Illinois at Urbana-Champaign, Urbana, IL 61801;
2
Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA 02138.
3
Department of Cell and Developmental Biology, University of Illinois at Urbana-Champaign, Urbana, IL 61801; Howard Hughes Medical Institute, University of Illinois at Urbana-Champaign, Urbana, IL 61801; pnewmark@life.illinois.edu.

Abstract

Mutations in Deleted in Azoospermia (DAZ), a Y chromosome gene, are an important cause of human male infertility. DAZ is found exclusively in primates, limiting functional studies of this gene to its homologs: boule, required for meiotic progression of germ cells in invertebrate model systems, and Daz-like (Dazl), required for early germ cell maintenance in vertebrates. Dazl is believed to have acquired its premeiotic role in a vertebrate ancestor following the duplication and functional divergence of the single-copy gene boule. However, multiple homologs of boule have been identified in some invertebrates, raising the possibility that some of these genes may play other roles, including a premeiotic function. Here we identify two boule paralogs in the freshwater planarian Schmidtea mediterranea Smed-boule1 is necessary for meiotic progression of male germ cells, similar to the known function of boule in invertebrates. By contrast, Smed-boule2 is required for the maintenance of early male germ cells, similar to vertebrate Dazl To examine if Boule2 may be functionally similar to vertebrate Dazl, we identify and functionally characterize planarian homologs of human DAZL/DAZ-interacting partners and DAZ family mRNA targets. Finally, our phylogenetic analyses indicate that premeiotic functions of planarian boule2 and vertebrate Dazl evolved independently. Our study uncovers a premeiotic role for an invertebrate boule homolog and offers a tractable invertebrate model system for studying the premeiotic functions of the DAZ protein family.

KEYWORDS:

DAZ; DAZL; Deleted in Azoospermia; germ cells; spermatogenesis

PMID:
27330085
PMCID:
PMC4922153
DOI:
10.1073/pnas.1521341113
[Indexed for MEDLINE]
Free PMC Article

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