A Network of HMG-box Transcription Factors Regulates Sexual Cycle in the Fungus Podospora Anserina

PLoS Genet. 2013;9(7):e1003642. doi: 10.1371/journal.pgen.1003642. Epub 2013 Jul 18.

Abstract

High-mobility group (HMG) B proteins are eukaryotic DNA-binding proteins characterized by the HMG-box functional motif. These transcription factors play a pivotal role in global genomic functions and in the control of genes involved in specific developmental or metabolic pathways. The filamentous ascomycete Podospora anserina contains 12 HMG-box genes. Of these, four have been previously characterized; three are mating-type genes that control fertilization and development of the fruit-body, whereas the last one encodes a factor involved in mitochondrial DNA stability. Systematic deletion analysis of the eight remaining uncharacterized HMG-box genes indicated that none were essential for viability, but that seven were involved in the sexual cycle. Two HMG-box genes display striking features. PaHMG5, an ortholog of SpSte11 from Schizosaccharomyces pombe, is a pivotal activator of mating-type genes in P. anserina, whereas PaHMG9 is a repressor of several phenomena specific to the stationary phase, most notably hyphal anastomoses. Transcriptional analyses of HMG-box genes in HMG-box deletion strains indicated that PaHMG5 is at the hub of a network of several HMG-box factors that regulate mating-type genes and mating-type target genes. Genetic analyses revealed that this network also controls fertility genes that are not regulated by mating-type transcription factors. This study points to the critical role of HMG-box members in sexual reproduction in fungi, as 11 out of 12 members were involved in the sexual cycle in P. anserina. PaHMG5 and SpSte11 are conserved transcriptional regulators of mating-type genes, although P. anserina and S. pombe diverged 550 million years ago. Two HMG-box genes, SOX9 and its upstream regulator SRY, also play an important role in sex determination in mammals. The P. anserina and S. pombe mating-type genes and their upstream regulatory factor form a module of HMG-box genes analogous to the SRY/SOX9 module, revealing a commonality of sex regulation in animals and fungi.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • DNA-Binding Proteins / genetics*
  • DNA-Binding Proteins / metabolism
  • Fertilization / genetics
  • Gene Expression Regulation, Fungal
  • Genes, Mating Type, Fungal*
  • HMG-Box Domains / genetics
  • High Mobility Group Proteins / genetics*
  • High Mobility Group Proteins / metabolism
  • Multigene Family
  • Podospora / genetics*
  • Podospora / physiology
  • SOX9 Transcription Factor / genetics
  • SOX9 Transcription Factor / metabolism
  • Schizosaccharomyces / genetics
  • Sequence Deletion
  • Transcription Factors / genetics
  • Transcription Factors / metabolism

Substances

  • DNA-Binding Proteins
  • High Mobility Group Proteins
  • SOX9 Transcription Factor
  • Transcription Factors

Grant support

JAB was funded by the doctoral school GGC 426. TM and CD were funded by the Sida SWE-2005-453 and the Swedish University of Agricultural Sciences. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.