The dynamic three-dimensional organization of the diploid yeast genome

  1. Seungsoo Kim
  2. Ivan Liachko
  3. Donna G Brickner
  4. Kate Cook
  5. William S Noble
  6. Jason H Brickner
  7. Jay Shendure
  8. Maitreya J Dunham  Is a corresponding author
  1. University of Washington, United States
  2. Northwestern University, United States

Abstract

The budding yeast Saccharomyces cerevisiae is a long-standing model for the three-dimensional organization of eukaryotic genomes. However, even in this well-studied model, it is unclear how homolog pairing in diploids or environmental conditions influence overall genome organization. Here, we performed high-throughput chromosome conformation capture on diverged Saccharomyces hybrid diploids to obtain the first global view of chromosome conformation in diploid yeasts. After controlling for the Rabl-like orientation using a polymer model, we observe significant homolog proximity that increases in saturated culture conditions. Surprisingly, we observe a localized increase in homologous interactions between the HAS1-TDA1 alleles specifically under galactose induction and saturated growth. This pairing is accompanied by relocalization to the nuclear periphery and requires Nup2, suggesting a role for nuclear pore complexes. Together, these results reveal that the diploid yeast genome has a dynamic and complex 3D organization.

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The following data sets were generated

Article and author information

Author details

  1. Seungsoo Kim

    Department of Genome Sciences, University of Washington, Seattle, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Ivan Liachko

    Department of Genome Sciences, University of Washington, Seattle, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Donna G Brickner

    Department of Molecular Biosciences, Northwestern University, Evanston, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Kate Cook

    Department of Genome Sciences, University of Washington, Seattle, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. William S Noble

    Department of Genome Sciences, University of Washington, Seattle, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Jason H Brickner

    Department of Molecular Biosciences, Northwestern University, Evanston, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8019-3743
  7. Jay Shendure

    Department of Genome Sciences, University of Washington, Seattle, United States
    Competing interests
    The authors declare that no competing interests exist.
  8. Maitreya J Dunham

    Department of Genome Sciences, University of Washington, Seattle, United States
    For correspondence
    maitreya@uw.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9944-2666

Funding

National Institutes of Health (GM080484 to JHB P41GM103533 to MJD U54 DK107979 to JS and WSN)

  • William S Noble
  • Jason H Brickner
  • Jay Shendure
  • Maitreya J Dunham

National Science Foundation (graduate research fellowship DGE-1256082 to SK 1516330 to MJD)

  • Seungsoo Kim

Howard Hughes Medical Institute (JS is an investigator of HHMI MJD was supported in part by a Faculty Scholar grant from HHMI)

  • Jay Shendure
  • Maitreya J Dunham

Canadian Institute for Advanced Research (MJD is a senior fellow in the Genetic Networks Program)

  • Maitreya J Dunham

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

Reviewing Editor

  1. Bing Ren, University of California, San Diego School of Medicine, United States

Version history

  1. Received: November 24, 2016
  2. Accepted: May 22, 2017
  3. Accepted Manuscript published: May 24, 2017 (version 1)
  4. Version of Record published: June 19, 2017 (version 2)

Copyright

© 2017, Kim 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. Seungsoo Kim
  2. Ivan Liachko
  3. Donna G Brickner
  4. Kate Cook
  5. William S Noble
  6. Jason H Brickner
  7. Jay Shendure
  8. Maitreya J Dunham
(2017)
The dynamic three-dimensional organization of the diploid yeast genome
eLife 6:e23623.
https://doi.org/10.7554/eLife.23623

Share this article

https://doi.org/10.7554/eLife.23623

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