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Elife. 2016 Sep 30;5. pii: e19027. doi: 10.7554/eLife.19027.

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

Kuang MC1,2,3,4,5, Hutchins PD5,6,7, Russell JD5,7,8, Coon JJ5,6,7,8,9, Hittinger CT1,2,3,4,5,7.

Author information

1
Laboratory of Genetics, University of Wisconsin-Madison, Madison, United States.
2
Graduate Program in Cellular and Molecular Biology, University of Wisconsin-Madison, Madison, United States.
3
Wisconsin Energy Institute, University of Wisconsin-Madison, Madison, United States.
4
JF Crow Institute for the Study of Evolution, University of Wisconsin-Madison, Madison, Madison, United States.
5
Genome Center of Wisconsin, University of Wisconsin-Madison, Madison, United States.
6
Department of Chemistry, University of Wisconsin-Madison, Madison, United States.
7
DOE Great Lakes Bioenergy Research Center, University of Wisconsin-Madison, Madison, United States.
8
Metabolism Research Group, Morgridge Institute for Research, Madison, United States.
9
Department of Biomolecular Chemistry, University of Wisconsin-Madison, Madison, United States.

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.

KEYWORDS:

S. cerevisiae; Saccharomyces bayanus; Saccharomyces uvarum; evolutionary biology; galactose; gene duplication; gene network; genomics; sugar metabolism

PMID:
27690225
PMCID:
PMC5089864
DOI:
10.7554/eLife.19027
[Indexed for MEDLINE]
Free PMC Article

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