Fitness effects of altering gene expression noise in Saccharomyces cerevisiae

Abstract

Gene expression noise is an evolvable property of biological systems that describes differences in expression among genetically identical cells in the same environment. Prior work has shown that expression noise is heritable and can be shaped by selection, but the impact of variation in expression noise on organismal fitness has proven difficult to measure. Here, we quantify the fitness effects of altering expression noise for the TDH3 gene in Saccharomyces cerevisiae. We show that increases in expression noise can be deleterious or beneficial depending on the difference between the average expression level of a genotype and the expression level maximizing fitness. We also show that a simple model relating single-cell expression levels to population growth produces patterns consistent with our empirical data. We use this model to explore a broad range of average expression levels and expression noise, providing additional insight into the fitness effects of variation in expression noise.

Data availability

Flow data (FCS files) used to quantify fluorescence levels produced by the 43 TDH3 promoter alleles are available in the FlowRepository (flowrepository.org) under experiment ID FR-FCM-ZY8Y.Raw bright field and fluorescence images, as well as bright field images where cell division events were annotated, are available on Zenodo (https://zenodo.org) with DOI 10.5281/zenodo.1327545All other data are provided as source data and/or supplementary files with the manuscript.

Article and author information

Author details

  1. Fabien Duveau

    Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, United States
    Competing interests
    No competing interests declared.
  2. Andrea Hodgins-Davis

    Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, United States
    Competing interests
    No competing interests declared.
  3. Brian PH Metzger

    Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, United States
    Competing interests
    No competing interests declared.
  4. Bing Yang

    Department of Molecular, Cellular and Developmental Biology, University of Michigan, Ann Arbor, United States
    Competing interests
    No competing interests declared.
  5. Stephen Tryban

    Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, United States
    Competing interests
    No competing interests declared.
  6. Elizabeth A Walker

    Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, United States
    Competing interests
    No competing interests declared.
  7. Tricia Lybrook

    Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, United States
    Competing interests
    No competing interests declared.
  8. Patricia J Wittkopp

    Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, United States
    For correspondence
    wittkopp@umich.edu
    Competing interests
    Patricia J Wittkopp, Senior editor, eLife.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7619-0048

Funding

National Institutes of Health (R01GM108826)

  • Patricia J Wittkopp

European Molecular Biology Organization (EMBO ALTF 1114-2012)

  • Brian PH Metzger

National Science Foundation (CB-1021398)

  • Patricia J Wittkopp

National Institutes of Health (1F32GM115198)

  • Andrea Hodgins-Davis

National Institutes of Health (R35GM118073)

  • Patricia J Wittkopp

National Institutes of Health (T32 HG000040)

  • Brian PH Metzger

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

Publication history

  1. Received: April 5, 2018
  2. Accepted: August 17, 2018
  3. Accepted Manuscript published: August 20, 2018 (version 1)
  4. Version of Record published: September 11, 2018 (version 2)

Copyright

© 2018, Duveau 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. Fabien Duveau
  2. Andrea Hodgins-Davis
  3. Brian PH Metzger
  4. Bing Yang
  5. Stephen Tryban
  6. Elizabeth A Walker
  7. Tricia Lybrook
  8. Patricia J Wittkopp
(2018)
Fitness effects of altering gene expression noise in Saccharomyces cerevisiae
eLife 7:e37272.
https://doi.org/10.7554/eLife.37272
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