1. Evolutionary Biology
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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 15
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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.

Data availability

The following data sets were generated
    1. Kuang MC
    2. Hittinger T
    (2016) RNA-Seq of Saccharomyces uvarum
    Publicly available at the NCBI Short Read Archive (accession no: SRP077015).

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.

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Further reading

    1. Developmental Biology
    2. Evolutionary Biology
    Tetsuya Hisanaga et al.
    Research Article

    KNOX and BELL transcription factors regulate distinct steps of diploid development in plants. In the green alga Chlamydomonas reinhardtii, KNOX and BELL proteins are inherited by gametes of the opposite mating types and heterodimerize in zygotes to activate diploid development. By contrast, in land plants such as Physcomitrium patens and Arabidopsis thaliana, KNOX and BELL proteins function in meristem maintenance and organogenesis during the later stages of diploid development. However, whether the contrasting functions of KNOX and BELL were acquired independently in algae and land plants is currently unknown. Here, we show that in the basal land plant species Marchantia polymorpha, gamete-expressed KNOX and BELL are required to initiate zygotic development by promoting nuclear fusion in a manner strikingly similar to that in C. reinhardtii. Our results indicate that zygote activation is the ancestral role of KNOX/BELL transcription factors, which shifted toward meristem maintenance as land plants evolved.

    1. Developmental Biology
    2. Evolutionary Biology
    Tom Dierschke et al.
    Research Article Updated

    Eukaryotic life cycles alternate between haploid and diploid phases and in phylogenetically diverse unicellular eukaryotes, expression of paralogous homeodomain genes in gametes primes the haploid-to-diploid transition. In the unicellular chlorophyte alga Chlamydomonas, KNOX and BELL TALE-homeodomain genes mediate this transition. We demonstrate that in the liverwort Marchantia polymorpha, paternal (sperm) expression of three of five phylogenetically diverse BELL genes, MpBELL234, and maternal (egg) expression of both MpKNOX1 and MpBELL34 mediate the haploid-to-diploid transition. Loss-of-function alleles of MpKNOX1 result in zygotic arrest, whereas a loss of either maternal or paternal MpBELL234 results in variable zygotic and early embryonic arrest. Expression of MpKNOX1 and MpBELL34 during diploid sporophyte development is consistent with a later role for these genes in patterning the sporophyte. These results indicate that the ancestral mechanism to activate diploid gene expression was retained in early diverging land plants and subsequently co-opted during evolution of the diploid sporophyte body.