title: Two distinct promoter architectures centered on dynamic nucleosomes control ribosomal protein gene transcription.
abstract: In yeast, ribosome production is controlled transcriptionally by tight coregulation of the 138 ribosomal protein genes (RPGs). RPG promoters display limited sequence homology, and the molecular basis for their coregulation remains largely unknown. Here we identify two prevalent RPG promoter types, both characterized by upstream binding of the general transcription factor (TF) Rap1 followed by the RPG-specific Fhl1/Ifh1 pair, with one type also binding the HMG-B protein Hmo1. We show that the regulatory properties of the two promoter types are remarkably similar, suggesting that they are determined to a large extent by Rap1 and the Fhl1/Ifh1 pair. Rapid depletion experiments allowed us to define a hierarchy of TF binding in which Rap1 acts as a pioneer factor required for binding of all other TFs. We also uncovered unexpected features underlying recruitment of Fhl1, whose forkhead DNA-binding domain is not required for binding at most promoters, and Hmo1, whose binding is supported by repeated motifs. Finally, we describe unusually micrococcal nuclease (MNase)-sensitive nucleosomes at all RPG promoters, located between the canonical +1 and -1 nucleosomes, which coincide with sites of Fhl1/Ifh1 and Hmo1 binding. We speculate that these "fragile" nucleosomes play an important role in regulating RPG transcriptional output.
authors.affiliation: Department of Molecular Biology, National Centres of Competence in Research Program "Frontiers in Genetics," Institute of Genetics and Genomics of Geneva (iGE3), University of Geneva, 1211 Geneva, Switzerland;
authors.forename: Britta
authors.initials: B
authors.lastname: Knight
authors.affiliation: Department of Molecular Biology, National Centres of Competence in Research Program "Frontiers in Genetics," Institute of Genetics and Genomics of Geneva (iGE3), University of Geneva, 1211 Geneva, Switzerland;
authors.forename: Slawomir
authors.initials: S
authors.lastname: Kubik
authors.affiliation: The Institute of Bioengineering, Ecole Polytechnique Fédérale de Lausanne, 1015 Lausanne, Switzerland;
authors.forename: Bhaswar
authors.initials: B
authors.lastname: Ghosh
authors.affiliation: Department of Molecular Biology, National Centres of Competence in Research Program "Frontiers in Genetics," Institute of Genetics and Genomics of Geneva (iGE3), University of Geneva, 1211 Geneva, Switzerland;
authors.forename: Maria Jessica
authors.initials: MJ
authors.lastname: Bruzzone
authors.affiliation: Department of Molecular Biology, National Centres of Competence in Research Program "Frontiers in Genetics," Institute of Genetics and Genomics of Geneva (iGE3), University of Geneva, 1211 Geneva, Switzerland; The Institute of Bioengineering, Ecole Polytechnique Fédérale de Lausanne, 1015 Lausanne, Switzerland;
authors.forename: Marcel
authors.initials: M
authors.lastname: Geertz
authors.affiliation: Department of Molecular Biology, National Centres of Competence in Research Program "Frontiers in Genetics," Institute of Genetics and Genomics of Geneva (iGE3), University of Geneva, 1211 Geneva, Switzerland;
authors.forename: Victoria
authors.initials: V
authors.lastname: Martin
authors.affiliation: The Institute of Bioengineering, Ecole Polytechnique Fédérale de Lausanne, 1015 Lausanne, Switzerland;
authors.forename: Nicolas
authors.initials: N
authors.lastname: Dénervaud
authors.affiliation: Bioinformatics and Biostatistics Core Facility, School of Life Sciences, Ecole Polytechnique Fédérale de Lausanne, 1015 Lausanne, Switzerland.
authors.forename: Philippe
authors.initials: P
authors.lastname: Jacquet
authors.affiliation: Department of Molecular Biology, National Centres of Competence in Research Program "Frontiers in Genetics," Institute of Genetics and Genomics of Geneva (iGE3), University of Geneva, 1211 Geneva, Switzerland;
authors.forename: Burak
authors.initials: B
authors.lastname: Ozkan
authors.affiliation: Bioinformatics and Biostatistics Core Facility, School of Life Sciences, Ecole Polytechnique Fédérale de Lausanne, 1015 Lausanne, Switzerland.
authors.forename: Jacques
authors.initials: J
authors.lastname: Rougemont
authors.affiliation: The Institute of Bioengineering, Ecole Polytechnique Fédérale de Lausanne, 1015 Lausanne, Switzerland;
authors.forename: Sebastian J
authors.initials: SJ
authors.lastname: Maerkl
authors.affiliation: The Institute of Bioengineering, Ecole Polytechnique Fédérale de Lausanne, 1015 Lausanne, Switzerland;
authors.forename: Félix
authors.initials: F
authors.lastname: Naef
authors.affiliation: Department of Molecular Biology, National Centres of Competence in Research Program "Frontiers in Genetics," Institute of Genetics and Genomics of Geneva (iGE3), University of Geneva, 1211 Geneva, Switzerland; david.shore@unige.ch.
authors.forename: David
authors.initials: D
authors.lastname: Shore
mesh_terms: D020816:Amino Acid Motifs; D015966:Gene Expression Regulation, Fungal; D009707:Nucleosomes / Q000378:metabolism*; D011401:Promoter Regions, Genetic / Q000235:genetics*; D011485:Protein Binding; D012269:Ribosomal Proteins / Q000235:genetics*; D012441:Saccharomyces cerevisiae / Q000235:genetics*; D029701:Saccharomyces cerevisiae Proteins / Q000235:genetics / Q000378:metabolism; D000089804:Shelterin Complex; D034501:Telomere-Binding Proteins / Q000235:genetics / Q000378:metabolism; D014157:Transcription Factors / Q000235:genetics / Q000378:metabolism
chemical_list: D009707:Nucleosomes; C440829:RAP1 protein, S cerevisiae; D012269:Ribosomal Proteins; D029701:Saccharomyces cerevisiae Proteins; D000089804:Shelterin Complex; D034501:Telomere-Binding Proteins; D014157:Transcription Factors
keywords: Rap1; fragile nucleosome; ribosomal protein gene; transcription; yeast
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