Literature DB >> 30124429

Fitness effects of altering gene expression noise in Saccharomyces cerevisiae.

Fabien Duveau1,2, Andrea Hodgins-Davis1, Brian Ph Metzger1,3, Bing Yang4, Stephen Tryban1, Elizabeth A Walker1, Tricia Lybrook1, Patricia J Wittkopp1,4.   

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.
© 2018, Duveau et al.

Entities:  

Keywords:  S. cerevisiae; TDH3; competitive growth; evolution; evolutionary biology; gene expression; promoter; selection

Mesh:

Substances:

Year:  2018        PMID: 30124429      PMCID: PMC6133559          DOI: 10.7554/eLife.37272

Source DB:  PubMed          Journal:  Elife        ISSN: 2050-084X            Impact factor:   8.140


  62 in total

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Authors:  Patricia J Wittkopp
Journal:  Methods Mol Biol       Date:  2011

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Authors:  C E Paquin; J Adams
Journal:  Nature       Date:  1983 Nov 24-30       Impact factor: 49.962

3.  Quantitative trait loci mapped to single-nucleotide resolution in yeast.

Authors:  Adam M Deutschbauer; Ronald W Davis
Journal:  Nat Genet       Date:  2005-11-06       Impact factor: 38.330

4.  Stochasticity of metabolism and growth at the single-cell level.

Authors:  Daniel J Kiviet; Philippe Nghe; Noreen Walker; Sarah Boulineau; Vanda Sunderlikova; Sander J Tans
Journal:  Nature       Date:  2014-09-03       Impact factor: 49.962

5.  Differential expression of the three yeast glyceraldehyde-3-phosphate dehydrogenase genes.

Authors:  L McAlister; M J Holland
Journal:  J Biol Chem       Date:  1985-12-05       Impact factor: 5.157

6.  Evolution of chromosome organization driven by selection for reduced gene expression noise.

Authors:  Nizar N Batada; Laurence D Hurst
Journal:  Nat Genet       Date:  2007-08       Impact factor: 38.330

Review 7.  Adaptive noise.

Authors:  Mark Viney; Sarah E Reece
Journal:  Proc Biol Sci       Date:  2013-07-31       Impact factor: 5.349

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Authors:  Lili Wang; Adolfas K Gaigalas
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Journal:  Cell Rep       Date:  2015-12-24       Impact factor: 9.423

10.  Long-term experimental evolution in Escherichia coli. XI. Rejection of non-transitive interactions as cause of declining rate of adaptation.

Authors:  J Arjan G M de Visser; Richard E Lenski
Journal:  BMC Evol Biol       Date:  2002-10-30       Impact factor: 3.260

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  17 in total

1.  Polymerization in the actin ATPase clan regulates hexokinase activity in yeast.

Authors:  Patrick R Stoddard; Eric M Lynch; Daniel P Farrell; Annie M Dosey; Frank DiMaio; Tom A Williams; Justin M Kollman; Andrew W Murray; Ethan C Garner
Journal:  Science       Date:  2020-02-28       Impact factor: 47.728

2.  Empirical measures of mutational effects define neutral models of regulatory evolution in Saccharomyces cerevisiae.

Authors:  Andrea Hodgins-Davis; Fabien Duveau; Elizabeth A Walker; Patricia J Wittkopp
Journal:  Proc Natl Acad Sci U S A       Date:  2019-09-30       Impact factor: 11.205

3.  The interplay of phenotypic variability and fitness in finite microbial populations.

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4.  The strength and pattern of natural selection on gene expression in rice.

Authors:  Simon C Groen; Irina Ćalić; Zoé Joly-Lopez; Adrian E Platts; Jae Young Choi; Mignon Natividad; Katherine Dorph; William M Mauck; Bernadette Bracken; Carlo Leo U Cabral; Arvind Kumar; Rolando O Torres; Rahul Satija; Georgina Vergara; Amelia Henry; Steven J Franks; Michael D Purugganan
Journal:  Nature       Date:  2020-02-12       Impact factor: 49.962

5.  Pleiotropic effects of trans-regulatory mutations on fitness and gene expression.

Authors:  Pétra Vande Zande; Mark S Hill; Patricia J Wittkopp
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6.  Species-specific chromatin landscape determines how transposable elements shape genome evolution.

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7.  Gene regulation in Escherichia coli is commonly selected for both high plasticity and low noise.

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Journal:  Nat Ecol Evol       Date:  2022-06-20       Impact factor: 19.100

8.  Compensatory trans-regulatory alleles minimizing variation in TDH3 expression are common within Saccharomyces cerevisiae.

Authors:  Brian P H Metzger; Patricia J Wittkopp
Journal:  Evol Lett       Date:  2019-08-29

9.  Empirical mean-noise fitness landscapes reveal the fitness impact of gene expression noise.

Authors:  Jörn M Schmiedel; Lucas B Carey; Ben Lehner
Journal:  Nat Commun       Date:  2019-07-18       Impact factor: 14.919

10.  Quantitative genetic analysis deciphers the impact of cis and trans regulation on cell-to-cell variability in protein expression levels.

Authors:  Michael D Morgan; Etienne Patin; Bernd Jagla; Milena Hasan; Lluís Quintana-Murci; John C Marioni
Journal:  PLoS Genet       Date:  2020-03-13       Impact factor: 5.917

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