Intrinsic cooperativity potentiates parallel cis-regulatory evolution

  1. Trevor R Sorrells  Is a corresponding author
  2. Amanda N Johnson
  3. Conor J Howard
  4. Candace S Britton
  5. Kyle R Fowler
  6. Jordan T Feigerle
  7. P Anthony Weil
  8. Alexander D Johnson  Is a corresponding author
  1. University of California, San Francisco, United States
  2. Vanderbilt University School of Medicine, United States

Abstract

Convergent evolutionary events in independent lineages provide an opportunity to understand why evolution favors certain outcomes over others. We studied such a case where a large set of genes-those coding for the ribosomal proteins-gained cis-regulatory sequences for a particular transcription regulator (Mcm1) in independent fungal lineages. We present evidence that these gains occurred because Mcm1 shares a mechanism of transcriptional activation with an ancestral regulator of the ribosomal protein genes, Rap1. Specifically, we show that Mcm1 and Rap1 have the inherent ability to cooperatively activate transcription through contacts with the general transcription factor TFIID. Because the two regulatory proteins share a common interaction partner, the presence of one ancestral cis-regulatory sequence can 'channel' random mutations into functional sites for the second regulator. At a genomic scale, this type of intrinsic cooperativity can account for a pattern of parallel evolution involving the fixation of hundreds of substitutions.

Data availability

Interspecies hybrid expression data is available at the Gene Expression Omnibus (GEO) repository under accession number GSE108389. Flow cytometry data is available at Flow Repository under accession numbers FR-FCM-ZYWS, FR-FCM-ZYWT, FR-FCM-ZYWU, FR-FCM-ZYWV, FR-FCM-ZYJZ, FR-FCM-ZYJY, and FR-FCM-ZYJ2. Code used in computational analyses is available at doi.org/10.5281/zenodo.1341284.

The following data sets were generated
    1. Sorrells TR
    (2018) Interspecies hybrid expression data
    Publicly available at the NCBI Gene Expression Omnibus (accession no: GSE108389).

Article and author information

Author details

  1. Trevor R Sorrells

    Department of Biochemistry and Biophysics, University of California, San Francisco, San Francisco, United States
    For correspondence
    trevorsorrells@gmail.com
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3527-8622
  2. Amanda N Johnson

    Department of Molecular Physiology and Biophysics, Vanderbilt University School of Medicine, Nashville, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Conor J Howard

    Department of Biochemistry and Biophysics, University of California, San Francisco, San Francisco, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5375-6248
  4. Candace S Britton

    Department of Biochemistry and Biophysics, University of California, San Francisco, San Francisco, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Kyle R Fowler

    Department of Biochemistry and Biophysics, University of California, San Francisco, San Francisco, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Jordan T Feigerle

    Department of Molecular Physiology and Biophysics, Vanderbilt University School of Medicine, Nashville, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. P Anthony Weil

    Department of Molecular Physiology and Biophysics, Vanderbilt University School of Medicine, Nashville, United States
    Competing interests
    The authors declare that no competing interests exist.
  8. Alexander D Johnson

    Department of Biochemistry and Biophysics, University of California, San Francisco, San Francisco, United States
    For correspondence
    ajohnson@cgl.ucsf.edu
    Competing interests
    The authors declare that no competing interests exist.

Funding

National Institutes of Health (GM115892)

  • Amanda N Johnson
  • Jordan T Feigerle
  • P Anthony Weil

National Institutes of Health (GM037049)

  • Trevor R Sorrells
  • Conor J Howard
  • Candace S Britton
  • Kyle R Fowler
  • Alexander D Johnson

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

Copyright

© 2018, Sorrells 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. Trevor R Sorrells
  2. Amanda N Johnson
  3. Conor J Howard
  4. Candace S Britton
  5. Kyle R Fowler
  6. Jordan T Feigerle
  7. P Anthony Weil
  8. Alexander D Johnson
(2018)
Intrinsic cooperativity potentiates parallel cis-regulatory evolution
eLife 7:e37563.
https://doi.org/10.7554/eLife.37563

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https://doi.org/10.7554/eLife.37563