A premeiotic function for boule in the planarian Schmidtea mediterranea

Harini Iyer, Melanie Issigonis, Prashant P. Sharma, Cassandra G. Extavour, Phillip A. Newmark

Research output: Contribution to journalArticlepeer-review

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.

Original languageEnglish (US)
Pages (from-to)E3509-E3518
JournalProceedings of the National Academy of Sciences of the United States of America
Volume113
Issue number25
DOIs
StatePublished - Jun 21 2016

Keywords

  • DAZ
  • DAZL
  • Deleted in Azoospermia
  • Germ cells
  • Spermatogenesis

ASJC Scopus subject areas

  • General

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