Fitness effects of altering gene expression noise in Saccharomyces cerevisiae

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Cite this article as: eLife 2018;7:e37272 doi: 10.7554/eLife.37272

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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.

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Author details

Fabien Duveau

Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, United States

Competing interests
No competing interests declared.
Andrea Hodgins-Davis

Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, United States

Competing interests
No competing interests declared.
Brian PH Metzger

Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, United States

Competing interests
No competing interests declared.
Bing Yang

Department of Molecular, Cellular and Developmental Biology, University of Michigan, Ann Arbor, United States

Competing interests
No competing interests declared.
Stephen Tryban

Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, United States

Competing interests
No competing interests declared.
Elizabeth A Walker

Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, United States

Competing interests
No competing interests declared.
Tricia Lybrook

Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, United States

Competing interests
No competing interests declared.
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.

"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

Naama Barkai, Weizmann Institute of Science, Israel

Publication history

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

Copyright

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.