SWI/SNF and RSC cooperate to reposition and evict promoter nucleosomes at highly expressed genes in yeast

Yashpal Rawal; Răzvan V. Chereji; Hongfang Qiu; Sudha Ananthakrishnan; Chhabi K. Govind; David J. Clark; Alan G. Hinnebusch

doi:10.1101/gad.312850.118

SWI/SNF and RSC cooperate to reposition and evict promoter nucleosomes at highly expressed genes in yeast

¹Eunice Kennedy Shriver National Institute of Child Health and Human Development, National Institutes of Health, Bethesda, Maryland 20892, USA;
²Division of Developmental Biology, Eunice Kennedy Shriver National Institute of Child Health and Human Development, National Institutes of Health, Bethesda, Maryland 20892, USA;
³Department of Biological Science, Oakland University, Rochester, Michigan 48309, USA

Corresponding author: ahinnebusch{at}nih.gov, govind{at}oakland.edu, clarkda{at}mail.nih.gov

↵4 These authors contributed equally to this work.

Abstract

The nucleosome remodeling complex RSC functions throughout the yeast genome to set the positions of −1 and +1 nucleosomes and thereby determines the widths of nucleosome-depleted regions (NDRs). The related complex SWI/SNF participates in nucleosome remodeling/eviction and promoter activation at certain yeast genes, including those activated by transcription factor Gcn4, but did not appear to function broadly in establishing NDRs. By analyzing the large cohort of Gcn4-induced genes in mutants lacking the catalytic subunits of SWI/SNF or RSC, we uncovered cooperation between these remodelers in evicting nucleosomes from different locations in the promoter and repositioning the +1 nucleosome downstream to produce wider NDRs—highly depleted of nucleosomes—during transcriptional activation. SWI/SNF also functions on a par with RSC at the most highly transcribed constitutively expressed genes, suggesting general cooperation by these remodelers for maximal transcription. SWI/SNF and RSC occupancies are greatest at the most highly expressed genes, consistent with their cooperative functions in nucleosome remodeling and transcriptional activation. Thus, SWI/SNF acts comparably with RSC in forming wide nucleosome-free NDRs to achieve high-level transcription but only at the most highly expressed genes exhibiting the greatest SWI/SNF occupancies.

Keywords

Footnotes

Supplemental material is available for this article.
Article published online ahead of print. Article and publication date are online at http://www.genesdev.org/cgi/doi/10.1101/gad.312850.118.

Received February 7, 2018.
Accepted April 12, 2018.

This article is distributed exclusively by Cold Spring Harbor Laboratory Press for the first six months after the full-issue publication date (see http://genesdev.cshlp.org/site/misc/terms.xhtml). After six months, it is available under a Creative Commons License (Attribution-NonCommercial 4.0 International), as described at http://creativecommons.org/licenses/by-nc/4.0/.