Promoter architecture and transcriptional regulation of Abf1-dependent ribosomal protein genes in Saccharomyces cerevisiae

Nucleic Acids Res. 2016 Jul 27;44(13):6113-26. doi: 10.1093/nar/gkw194. Epub 2016 Mar 25.

Abstract

In Saccharomyces cerevisiae, ribosomal protein gene (RPG) promoters display binding sites for either Rap1 or Abf1 transcription factors. Unlike Rap1-associated promoters, the small cohort of Abf1-dependent RPGs (Abf1-RPGs) has not been extensively investigated. We show that RPL3, RPL4B, RPP1A, RPS22B and RPS28A/B share a common promoter architecture, with an Abf1 site upstream of a conserved element matching the sequence recognized by Fhl1, a transcription factor which together with Ifh1 orchestrates Rap1-associated RPG regulation. Abf1 and Fhl1 promoter association was confirmed by ChIP and/or gel retardation assays. Mutational analysis revealed a more severe requirement of Abf1 than Fhl1 binding sites for RPG transcription. In the case of RPS22B an unusual Tbf1 binding site promoted both RPS22B and intron-hosted SNR44 expression. Abf1-RPG down-regulation upon TOR pathway inhibition was much attenuated at defective mutant promoters unable to bind Abf1. TORC1 inactivation caused the expected reduction of Ifh1 occupancy at RPS22B and RPL3 promoters, but unexpectedly it entailed largely increased Abf1 association with Abf1-RPG promoters. We present evidence that Abf1 recruitment upon nutritional stress, also observed for representative ribosome biogenesis genes, favours RPG transcriptional rescue upon nutrient replenishment, thus pointing to nutrient-regulated Abf1 dynamics at promoters as a novel mechanism in ribosome biogenesis control.

MeSH terms

  • Binding Sites
  • DNA-Binding Proteins / genetics*
  • DNA-Binding Proteins / metabolism
  • Forkhead Transcription Factors / genetics
  • Gene Expression Regulation, Fungal
  • Mechanistic Target of Rapamycin Complex 1
  • Multiprotein Complexes / genetics
  • Promoter Regions, Genetic*
  • Ribosomal Proteins / genetics*
  • Ribosomal Proteins / metabolism
  • Saccharomyces cerevisiae / genetics
  • Saccharomyces cerevisiae Proteins / genetics*
  • Saccharomyces cerevisiae Proteins / metabolism
  • TOR Serine-Threonine Kinases / genetics
  • Telomere-Binding Proteins / genetics
  • Trans-Activators / genetics
  • Transcription Factors / genetics*
  • Transcription Factors / metabolism
  • Transcription, Genetic*

Substances

  • ABF1 protein, S cerevisiae
  • DNA-Binding Proteins
  • FHL1 protein, S cerevisiae
  • Forkhead Transcription Factors
  • IFH1 protein, S cerevisiae
  • Multiprotein Complexes
  • Ribosomal Proteins
  • Saccharomyces cerevisiae Proteins
  • Telomere-Binding Proteins
  • Trans-Activators
  • Transcription Factors
  • Mechanistic Target of Rapamycin Complex 1
  • TOR Serine-Threonine Kinases