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No Evidence That Protein Noise-Induced Epigenetic Epistasis Constrains Gene Expression Evolution.

ABSTRACT: Changes in gene expression can affect phenotypes and therefore both its level and stochastic variability are frequently under selection. It has recently been proposed that epistatic interactions influence gene expression evolution: gene pairs where simultaneous knockout is more deleterious than expected should evolve reduced expression noise to avoid concurrent low expression of both proteins. In apparent support, yeast genes with many epistatic partners have low expression variation both among isogenic individuals and between species. However, the specific predictions and basic assumptions of this verbal model remain untested. Using bioinformatics analysis, we first demonstrate that the model's predictions are unsupported by available large-scale data. Based on quantitative biochemical modeling, we then show that epistasis between expression reductions (epigenetic epistasis) is not expected to aggravate the fitness cost of stochastic expression, which is in sharp contrast to the verbal argument. This nonintuitive result can be readily explained by the typical diminishing return of fitness on gene activity and by the fact that expression noise not only decreases but also increases the abundance of proteins. Overall, we conclude that stochastic variation in epistatic partners is unlikely to drive noise minimization or constrain gene expression divergence on a genomic scale.

SUBMITTER: Boross G

PROVIDER: S-EPMC6544514 | biostudies-literature | 2017 Feb

REPOSITORIES: biostudies-literature

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No Evidence That Protein Noise-Induced Epigenetic Epistasis Constrains Gene Expression Evolution.

Boross Gábor G Papp Balázs B

Molecular biology and evolution 20170201 2

Changes in gene expression can affect phenotypes and therefore both its level and stochastic variability are frequently under selection. It has recently been proposed that epistatic interactions influence gene expression evolution: gene pairs where simultaneous knockout is more deleterious than expected should evolve reduced expression noise to avoid concurrent low expression of both proteins. In apparent support, yeast genes with many epistatic partners have low expression variation both among ...[more]

PMID: 28025271

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Project description:Many biological processes depend on very few copies of intervening elements, which makes such processes particularly susceptible to the stochastic fluctuations of these elements. The intrinsic stochasticity of certain processes is propagated across biological levels, causing genotype- and environment-independent biological variation which might permit populations to better cope with variable environments. Biological variations of stochastic nature might also allow the accumulation of variations at the genetic level that are hidden from natural selection, which might have a great potential for population diversification. The study of any mechanism that resulted in the modulation of stochastic variation is, therefore, of potentially wide interest. I propose that sex might be an important modulator of the stochastic variation in gene expression, i.e., gene expression noise. Based on known associations between different patterns of gene expression variation, I hypothesize that in metazoans the gene expression noise might be generally larger in heterogametic than in homogametic individuals. I directly tested this hypothesis by comparing putative genotype- and environment-independent variations in gene expression between females and males of Drosophila melanogaster strains. Also, considering the potential effect of the propagation of gene expression noise across biological levels, I indirectly tested the existence of a metazoan sexual dimorphism in gene expression noise by analyzing putative genotype- and environment-independent variation in phenotypes related to interaction with the environment in D. melanogaster strains and metazoan species. The results of these analyses are consistent with the hypothesis that gene expression is generally noisier in heterogametic than in homogametic individuals. Further analyses and discussion of existing literature permits the speculation that the sexual dimorphism in gene expression noise is ultimately based on the nuclear dynamics in gametogenesis and very early embryogenesis of sex-specific chromosomes, i.e., Y and W chromosomes.

Dataset Information

No Evidence That Protein Noise-Induced Epigenetic Epistasis Constrains Gene Expression Evolution.

Publications

No Evidence That Protein Noise-Induced Epigenetic Epistasis Constrains Gene Expression Evolution.

Similar Datasets

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