Universal promoter scanning by Pol II during transcription initiation in Saccharomyces cerevisiae.

DNA Polymerase II / metabolism Models, Genetic Promoter Regions, Genetic Saccharomyces cerevisiae / enzymology Transcription Factors, General / metabolism Transcription Initiation Site Transcription Initiation, Genetic

Journal

Genome biology
ISSN: 1474-760X
Titre abrégé: Genome Biol
Pays: England
ID NLM: 100960660

Informations de publication

Date de publication:
02 06 2020
Historique:
received: 24 10 2019
accepted: 08 05 2020
entrez: 4 6 2020
pubmed: 4 6 2020
medline: 2 4 2021
Statut: epublish

Résumé

The majority of eukaryotic promoters utilize multiple transcription start sites (TSSs). How multiple TSSs are specified at individual promoters across eukaryotes is not understood for most species. In Saccharomyces cerevisiae, a pre-initiation complex (PIC) comprised of Pol II and conserved general transcription factors (GTFs) assembles and opens DNA upstream of TSSs. Evidence from model promoters indicates that the PIC scans from upstream to downstream to identify TSSs. Prior results suggest that TSS distributions at promoters where scanning occurs shift in a polar fashion upon alteration in Pol II catalytic activity or GTF function. To determine the extent of promoter scanning across promoter classes in S. cerevisiae, we perturb Pol II catalytic activity and GTF function and analyze their effects on TSS usage genome-wide. We find that alterations to Pol II, TFIIB, or TFIIF function widely alter the initiation landscape consistent with promoter scanning operating at all yeast promoters, regardless of promoter class. Promoter architecture, however, can determine the extent of promoter sensitivity to altered Pol II activity in ways that are predicted by a scanning model. Our observations coupled with previous data validate key predictions of the scanning model for Pol II initiation in yeast, which we term the shooting gallery. In this model, Pol II catalytic activity and the rate and processivity of Pol II scanning together with promoter sequence determine the distribution of TSSs and their usage.

Sections du résumé

BACKGROUND
The majority of eukaryotic promoters utilize multiple transcription start sites (TSSs). How multiple TSSs are specified at individual promoters across eukaryotes is not understood for most species. In Saccharomyces cerevisiae, a pre-initiation complex (PIC) comprised of Pol II and conserved general transcription factors (GTFs) assembles and opens DNA upstream of TSSs. Evidence from model promoters indicates that the PIC scans from upstream to downstream to identify TSSs. Prior results suggest that TSS distributions at promoters where scanning occurs shift in a polar fashion upon alteration in Pol II catalytic activity or GTF function.
RESULTS
To determine the extent of promoter scanning across promoter classes in S. cerevisiae, we perturb Pol II catalytic activity and GTF function and analyze their effects on TSS usage genome-wide. We find that alterations to Pol II, TFIIB, or TFIIF function widely alter the initiation landscape consistent with promoter scanning operating at all yeast promoters, regardless of promoter class. Promoter architecture, however, can determine the extent of promoter sensitivity to altered Pol II activity in ways that are predicted by a scanning model.
CONCLUSIONS
Our observations coupled with previous data validate key predictions of the scanning model for Pol II initiation in yeast, which we term the shooting gallery. In this model, Pol II catalytic activity and the rate and processivity of Pol II scanning together with promoter sequence determine the distribution of TSSs and their usage.

Identifiants

DOI: 10.1186/s13059-020-02040-0 PMID: 32487207 PMC: PMC7265651
pubmed: 32487207
doi: 10.1186/s13059-020-02040-0
pii: 10.1186/s13059-020-02040-0
pmc: PMC7265651
doi:

Substances chimiques

Transcription Factors, General 0
DNA Polymerase II EC 2.7.7.7

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

132

Subventions

Organisme : NIGMS NIH HHS
ID : R01 GM088343
Pays : United States
Organisme : NIGMS NIH HHS
ID : R35 GM118059
Pays : United States
Organisme : NIGMS NIH HHS
ID : R01 GM120450
Pays : United States
Organisme : NIGMS NIH HHS
ID : R01 GM097260
Pays : United States

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Auteurs

Chenxi Qiu (C)

Department of Biochemistry and Biophysics, Texas A&M University, College Station, TX, 77843-2128, USA.
Present Address: Department of Medicine, Division of Translational Therapeutics, Beth Israel Deaconess Medical Center, Harvard Medical School, Boston, MA, 02215, USA.

Huiyan Jin (H)

Department of Biochemistry and Biophysics, Texas A&M University, College Station, TX, 77843-2128, USA.

Irina Vvedenskaya (I)

Waksman Institute of Microbiology, Rutgers University, Piscataway, NJ, 08854, USA.
Department of Genetics, Rutgers University, Piscataway, NJ, 08854, USA.

Jordi Abante Llenas (JA)

Department of Electrical and Computer Engineering, Texas A&M University, College Station, TX, 77843-3128, USA.
Present Address: Whitaker Biomedical Engineering Institute, Johns Hopkins University, Baltimore, MD, 21218, USA.

Tingting Zhao (T)

Department of Biological Sciences, University of Pittsburgh, Pittsburgh, PA, 15260, USA.

Indranil Malik (I)

Department of Biochemistry and Biophysics, Texas A&M University, College Station, TX, 77843-2128, USA.
Present Address: Department of Neurology, University of Michigan, Ann Arbor, MI, 48109, USA.

Alex M Visbisky (AM)

Department of Biological Sciences, University of Pittsburgh, Pittsburgh, PA, 15260, USA.

Scott L Schwartz (SL)

Genomics and Bioinformatics Service, Texas A&M AgriLife, College Station, TX, 77845, USA.

Ping Cui (P)

Department of Biochemistry and Biophysics, Texas A&M University, College Station, TX, 77843-2128, USA.

Pavel Čabart (P)

Department of Biochemistry and Biophysics, Texas A&M University, College Station, TX, 77843-2128, USA.
Present Address: First Faculty of Medicine, Charles University, BIOCEV, 252 42, Vestec, Czech Republic.

Kang Hoo Han (KH)

Department of Biochemistry and Molecular Biology, Penn State University, University Park, PA, 16802, USA.

William K M Lai (WKM)

Department of Biochemistry and Molecular Biology, Penn State University, University Park, PA, 16802, USA.
Present Address: Department of Molecular Biology and Genetics, 458 Biotechnology, Cornell University, New York, 14853, USA.

Richard P Metz (RP)

Genomics and Bioinformatics Service, Texas A&M AgriLife, College Station, TX, 77845, USA.

Charles D Johnson (CD)

Genomics and Bioinformatics Service, Texas A&M AgriLife, College Station, TX, 77845, USA.

Sing-Hoi Sze (SH)

Department of Biochemistry and Biophysics, Texas A&M University, College Station, TX, 77843-2128, USA.
Department of Computer Science and Engineering, Texas A&M University, College Station, TX, 77843-3127, USA.

B Franklin Pugh (BF)

Department of Biochemistry and Molecular Biology, Penn State University, University Park, PA, 16802, USA.
Present Address: Department of Molecular Biology and Genetics, 458 Biotechnology, Cornell University, New York, 14853, USA.

Bryce E Nickels (BE)

Waksman Institute of Microbiology, Rutgers University, Piscataway, NJ, 08854, USA.
Department of Genetics, Rutgers University, Piscataway, NJ, 08854, USA.

Craig D Kaplan (CD)

Department of Biological Sciences, University of Pittsburgh, Pittsburgh, PA, 15260, USA. craig.kaplan@pitt.edu.
ORCID: 0000-0002-7518-695X

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Classifications MeSH

questionsmedicales.fr › Enzymes et coenzymes › Enzymes › Transferases › Phosphotransferases › Nucleotidyltransferases › DNA nucleotidyltransferases › DNA-directed DNA polymerase › DNA polymerase II › Universal promoter scanning by Pol II during...
questionsmedicales.fr › Techniques d'investigation › Modèles théoriques › Modèles biologiques › Modèles génétiques › Universal promoter scanning by Pol II during...
questionsmedicales.fr › Phénomènes génétiques › Structures génétiques › Génome › Composants de génome › Gènes › Composants de gène › Éléments de régulation transcriptionnelle › Régions promotrices (génétique) › Universal promoter scanning by Pol II during...
questionsmedicales.fr › Eucaryotes › Champignons › Levures › Saccharomyces › Saccharomyces cerevisiae › Universal promoter scanning by Pol II during...
questionsmedicales.fr › Acides aminés, peptides et protéines › Protéines › Facteurs de transcription › Facteurs généraux de transcription › Universal promoter scanning by Pol II during...
questionsmedicales.fr › Phénomènes génétiques › Structures génétiques › Génome › Composants de génome › Gènes › Composants de gène › Éléments de régulation transcriptionnelle › Site d'initiation de la transcription › Universal promoter scanning by Pol II during...
questionsmedicales.fr › Phénomènes génétiques › Expression des gènes › Transcription génétique › Initiation de la transcription › Universal promoter scanning by Pol II during...