1. Evolutionary Biology
Download icon

Ongoing resolution of duplicate gene functions shapes the diversification of a metabolic network

  1. Meihua Christina Kuang
  2. Paul D Hutchins
  3. Jason D Russell
  4. Joshua J Coon
  5. Chris Todd Hittinger  Is a corresponding author
  1. University of Wisconsin-Madison, United States
Research Article
  • Cited 11
  • Views 1,866
  • Annotations
Cite this article as: eLife 2016;5:e19027 doi: 10.7554/eLife.19027

Abstract

The evolutionary mechanisms leading to duplicate gene retention are well understood, but the long-term impacts of paralog differentiation on the regulation of metabolism remain underappreciated. Here we experimentally dissect the functions of two pairs of ancient paralogs of the GALactose sugar utilization network in two yeast species. We show that the Saccharomyces uvarum network is more active, even as over-induction is prevented by a second co-repressor that the model yeast Saccharomyces cerevisiae lacks. Surprisingly, removal of this repression system leads to a strong growth arrest, likely due to overly rapid galactose catabolism and metabolic overload. Alternative sugars, such as fructose, circumvent metabolic control systems and exacerbate this phenotype. We further show that S. cerevisiae experiences homologous metabolic constraints that are subtler due to how the paralogs have diversified. These results show how the functional differentiation of paralogs continues to shape regulatory network architectures and metabolic strategies long after initial preservation.

Article and author information

Author details

  1. Meihua Christina Kuang

    Laboratory of Genetics, University of Wisconsin-Madison, Madison, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3206-6525
  2. Paul D Hutchins

    Genome Center of Wisconsin, University of Wisconsin-Madison, Madison, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Jason D Russell

    Genome Center of Wisconsin, University of Wisconsin-Madison, Madison, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Joshua J Coon

    Genome Center of Wisconsin, University of Wisconsin-Madison, Madison, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Chris Todd Hittinger

    Laboratory of Genetics, University of Wisconsin-Madison, Madison, United States
    For correspondence
    cthittinger@wisc.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5088-7461

Funding

National Science Foundation (DEB-1253634 , DEB-1442148)

  • Chris Todd Hittinger

National Institute of Food and Agriculture (Hatch Project 1003258)

  • Chris Todd Hittinger

DOE Great Lakes Bioenergy Research Center (DOE Office of Science BER DE-FC02-07ER64494)

  • Joshua J Coon
  • Chris Todd Hittinger

Pew Charitable Trusts (Pew Scholar in the Biomedical Sciences)

  • Chris Todd Hittinger

Alexander von Humboldt-Stiftung (Alfred Toepfer Faculty Fellow)

  • Chris Todd Hittinger

National Institutes of Health (R35 GM118110)

  • Joshua J Coon

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

Reviewing Editor

  1. Leonid Kruglyak, Howard Hughes Medical Institute, Uuniversity of California, Los Angeles, United States

Publication history

  1. Received: June 21, 2016
  2. Accepted: September 28, 2016
  3. Accepted Manuscript published: September 30, 2016 (version 1)
  4. Accepted Manuscript updated: October 5, 2016 (version 2)
  5. Version of Record published: November 1, 2016 (version 3)

Copyright

© 2016, Kuang 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.

Metrics

  • 1,866
    Page views
  • 473
    Downloads
  • 11
    Citations

Article citation count generated by polling the highest count across the following sources: Crossref, Scopus, PubMed Central.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Download citations (links to download the citations from this article in formats compatible with various reference manager tools)

Open citations (links to open the citations from this article in various online reference manager services)

Further reading

    1. Ecology
    2. Evolutionary Biology
    Anthony B Lapsansky et al.
    Research Article Updated
    1. Developmental Biology
    2. Evolutionary Biology
    Neal Anthwal et al.
    Research Article