Effective dynamics of nucleosome configurations at the yeast PHO5 promoter

Abstract
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Abstract

Chromatin dynamics are mediated by remodeling enzymes and play crucial roles in gene regulation, as established in a paradigmatic model, the S. cerevisiae PHO5 promoter. However, effective nucleosome dynamics, i.e. trajectories of promoter nucleosome configurations, remain elusive. Here, we infer such dynamics from the integration of published single-molecule data capturing multi-nucleosome configurations for repressed to fully active PHO5 promoter states with other existing histone turnover and new chromatin accessibility data. We devised and systematically investigated a new class of 'regulated on-off-slide' models simulating global and local nucleosome (dis)assembly and sliding. Only seven of 68145 models agreed well with all data. All seven models involve sliding and the known central role of the N-2 nucleosome, but regulate promoter state transitions by modulating just one assembly rather than disassembly process. This is consistent with but challenges common interpretations of previous observations at the PHO5 promoter and suggests chromatin opening by binding competition.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting files. Source data files have been provided for Figure 1,Table 1 and Figure 4. Program code has been uploaded to github (link in Methods).

The following previously published data sets were used

1. Dion MF
2. Kaplan T
3. Kim M
4. Buratowski S
5. Friedman N
6. Rando OJ
(2007) Dynamics of Replication-Independent Histone Turnover in Budding Yeast
NCBI Gene Expression Omnibus, GSE6666.

https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE6666
1. Rufiange A
2. Jacques PÉ
3. Bhat W
4. Robert F
5. Nourani A
(2007) Genome-Wide Replication-Independent Histone H3 Exchange Occurs Predominantly at Promoters and Implicates H3 K56 Acetylation and Asf1
NCBI Gene Expression Omnibus, GSE8299.

https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE8299

Article and author information

Author details

Michael Roland Wolff

Department of Physics, Technical University of Munich, Garching, Germany

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0002-4677-4023
Andrea Schmid

Molecular Biology Division, Biomedical Center, Faculty of Medicine, Ludwig-Maximilians-Universität München, Planegg-Martinsried, Germany

Competing interests
The authors declare that no competing interests exist.
Philipp Korber

Molecular Biology Division, Biomedical Center, Faculty of Medicine, Ludwig-Maximilians-Universität München, Planegg-Martinsried, Germany

For correspondence
pkorber@lmu.de

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0001-7526-6549
Ulrich Gerland

Department of Physics, Technical University of Munich, Garching, Germany

For correspondence
gerland@tum.de

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0002-0859-6422

Funding

Deutsche Forschungsgemeinschaft (SFB863)

Ulrich Gerland

Deutsche Forschungsgemeinschaft (SFB1064)

Philipp Korber

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Copyright

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.