1. Evolutionary Biology
  2. Microbiology and Infectious Disease

Transcriptional rewiring over evolutionary timescales changes quantitative and qualitative properties of gene expression

  1. Chiraj K Dalal  Is a corresponding author
  2. Ignacio A Zuleta
  3. Kaitlin F Mitchell
  4. David R Andes
  5. Hana El-Samad
  6. Alexander D Johnson  Is a corresponding author
  1. University of California, San Francisco, United States
  2. University of Wisconsin, United States
https://doi.org/10.7554/eLife.18981
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  1. Chiraj K Dalal
  2. Ignacio A Zuleta
  3. Kaitlin F Mitchell
  4. David R Andes
  5. Hana El-Samad
  6. Alexander D Johnson
(2016)
Transcriptional rewiring over evolutionary timescales changes quantitative and qualitative properties of gene expression
eLife 5:e18981.
https://doi.org/10.7554/eLife.18981
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Abstract

Evolutionary changes in transcription networks are an important source of diversity across species, yet the quantitative consequences of network evolution have rarely been studied. Here we consider the transcriptional 'rewiring' of the three GAL genes that encode the enzymes needed for cells to convert galactose to glucose. In Saccharomyces cerevisiae, the transcriptional regulator Gal4 binds and activates these genes. In the human pathogen Candida albicans (which last shared a common ancestor with S. cerevisiae some 300 million years ago), we show that different regulators, Rtg1 and Rtg3, activate the three GAL genes. Using single-cell dynamics and RNA-sequencing, we demonstrate that although the overall logic of regulation is the same in both species-the GAL genes are induced by galactose-there are major differences in both the quantitative response of these genes to galactose and in the position of these genes in the overall transcription network structure of the two species.

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Article and author information

Author details

  1. Chiraj K Dalal

    Department of Microbiology and Immunology, University of California, San Francisco, San Francisco, United States
    For correspondence
    chirajdalal.ucsf@gmail.com
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3624-8409

  2. Ignacio A Zuleta

    Department of Biochemistry and Biophysics, California Institute for Quantitative Biosciences, University of California, San Francisco, San Francisco, United States
    Competing interests
    The authors declare that no competing interests exist.

  3. Kaitlin F Mitchell

    Departments of Medicine and Medical Microbiology and Immunology, University of Wisconsin, Madison, United States
    Competing interests
    The authors declare that no competing interests exist.

  4. David R Andes

    Departments of Medicine and Medical Microbiology and Immunology, University of Wisconsin, Madison, United States
    Competing interests
    The authors declare that no competing interests exist.

  5. Hana El-Samad

    Department of Biochemistry and Biophysics, California Institute for Quantitative Biosciences, University of California, San Francisco, San Francisco, United States
    Competing interests
    The authors declare that no competing interests exist.

  6. Alexander D Johnson

    Department of Microbiology and Immunology, 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

Paul G. Allen Family Foundation

  • Ignacio A Zuleta
  • Hana El-Samad

National Institute of General Medical Sciences (P50 GM081879)

  • Ignacio A Zuleta
  • Hana El-Samad

National Institutes of Health (R01AI073289)

  • Kaitlin F Mitchell
  • David R Andes

National Institutes of Health (R01AI049187)

  • Chiraj K Dalal
  • Alexander D Johnson

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

Reviewing Editor

  1. Naama Barkai, Weizmann Institute of Science, Israel

Ethics

Animal experimentation: All procedures in this study were approved by the Institutional Animal Care and Use Committee (IACUC) at the University of Wisconsin (protocol number MV1947) according to the guidelines of the Animal Welfare Act, and The Institute of Laboratory Animal Resources Guide for the Care and Use of Laboratory Animals and Public Health Service Policy.

Version history

  1. Received: June 21, 2016
  2. Accepted: September 5, 2016
  3. Accepted Manuscript published: September 10, 2016 (version 1)
  4. Accepted Manuscript updated: September 15, 2016 (version 2)
  5. Version of Record published: October 17, 2016 (version 3)
  6. Version of Record updated: November 10, 2016 (version 4)

Copyright

© 2016, Dalal 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. Chiraj K Dalal
  2. Ignacio A Zuleta
  3. Kaitlin F Mitchell
  4. David R Andes
  5. Hana El-Samad
  6. Alexander D Johnson
(2016)
Transcriptional rewiring over evolutionary timescales changes quantitative and qualitative properties of gene expression
eLife 5:e18981.
https://doi.org/10.7554/eLife.18981

Share this article

https://doi.org/10.7554/eLife.18981

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