The ACF chromatin remodeling complex is essential for Polycomb repression

  1. Elizabeth T Wiles  Is a corresponding author
  2. Colleen C Mumford
  3. Kevin J McNaught
  4. Hideki Tanizawa
  5. Eric U Selker  Is a corresponding author
  1. University of Oregon, United States

Abstract

Establishing and maintaining appropriate gene repression is critical for the health and development of multicellular organisms. Histone H3 lysine 27 (H3K27) methylation is a chromatin modification associated with repressed facultative heterochromatin, but the mechanism of this repression remains unclear. We used a forward genetic approach to identify genes involved in transcriptional silencing of H3K27-methylated chromatin in the filamentous fungus Neurospora crassa. We found that the N. crassa homologs of ISWI (NCU03875) and ACF1 (NCU00164) are required for repression of a subset of H3K27- methylated genes and that they form an ACF chromatin remodeling complex. This ACF complex interacts with chromatin throughout the genome, yet association with facultative heterochromatin is specifically promoted by the H3K27 methyltransferase, SET-7. H3K27-methylated genes that are upregulated when iswi or acf1 are deleted show a downstream shift of the +1 nucleosome, suggesting that proper nucleosome positioning is critical for repression of facultative heterochromatin. Our findings support a direct role for the ACF complex in Polycomb repression.

Data availability

All RNA-seq, ChIP-seq, DamID-seq and MNase-seq data generated in this study have been submitted to the NCBI Gene Expression Omnibus (GEO; https://www.ncbi.nlm.nih.gov/geo/) under accession number GSE168277. All whole genome sequencing data haven been submitted to the NCBI Sequence Read Archive(SRA, https://www.ncbi.nlm.nih.gov/sra) under accession number PRJNA714693.

The following data sets were generated

Article and author information

Author details

  1. Elizabeth T Wiles

    Institute of Molecular Biology, University of Oregon, Eugene, United States
    For correspondence
    tish.wiles@gmail.com
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7269-7466
  2. Colleen C Mumford

    Institute of Molecular Biology, University of Oregon, Eugene, United States
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0213-0901
  3. Kevin J McNaught

    Institute of Molecular Biology, University of Oregon, Eugene, United States
    Competing interests
    Kevin J McNaught, is affiliated with Genapsys, Inc. The author has no financial interests to declare.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6887-3161
  4. Hideki Tanizawa

    Institute of Molecular Biology, University of Oregon, Eugene, United States
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2573-2473
  5. Eric U Selker

    Institute of Molecular Biology, University of Oregon, Eugene, United States
    For correspondence
    selker@uoregon.edu
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6465-0094

Funding

National Institutes of Health (GM127142)

  • Eric U Selker

National Institutes of Health (GM093061)

  • Eric U Selker

American Heart Association (14POST20450071)

  • Eric U Selker

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

Reviewing Editor

  1. Jerry L Workman, Stowers Institute for Medical Research, United States

Publication history

  1. Preprint posted: June 30, 2021 (view preprint)
  2. Received: February 4, 2022
  3. Accepted: March 3, 2022
  4. Accepted Manuscript published: March 8, 2022 (version 1)
  5. Accepted Manuscript updated: March 9, 2022 (version 2)
  6. Version of Record published: April 25, 2022 (version 3)
  7. Version of Record updated: April 28, 2022 (version 4)

Copyright

© 2022, Wiles et al.

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.

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  1. Elizabeth T Wiles
  2. Colleen C Mumford
  3. Kevin J McNaught
  4. Hideki Tanizawa
  5. Eric U Selker
(2022)
The ACF chromatin remodeling complex is essential for Polycomb repression
eLife 11:e77595.
https://doi.org/10.7554/eLife.77595

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