Dataset Information

Positive selection for elevated gene expression noise in yeast.

ABSTRACT: It is well known that the expression noise is lessened by natural selection for genes that are important for cell growth or are sensitive to dosage. In theory, expression noise can also be elevated by natural selection when noisy gene expression is advantageous. Here we analyze yeast genome-wide gene expression noise data and show that plasma-membrane transporters show significantly elevated expression noise after controlling all confounding factors. We propose a model that explains why and under what conditions elevated expression noise may be beneficial and subject to positive selection. Our model predicts and the simulation confirms that, under certain conditions, expression noise also increases the evolvability of gene expression by promoting the fixation of favorable expression level-altering mutations. Indeed, yeast genes with higher noise show greater between-strain and between-species divergences in expression, even when all confounding factors are excluded. Together, our theoretical model and empirical results suggest that, for yeast genes such as plasma-membrane transporters, elevated expression noise is advantageous, is subject to positive selection, and is a facilitator of adaptive gene expression evolution.

SUBMITTER: Zhang Z

PROVIDER: S-EPMC2736655 | biostudies-literature | 2009

REPOSITORIES: biostudies-literature

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Positive selection for elevated gene expression noise in yeast.

Zhang Zhihua Z Qian Wenfeng W Zhang Jianzhi J

Molecular systems biology 20090818

It is well known that the expression noise is lessened by natural selection for genes that are important for cell growth or are sensitive to dosage. In theory, expression noise can also be elevated by natural selection when noisy gene expression is advantageous. Here we analyze yeast genome-wide gene expression noise data and show that plasma-membrane transporters show significantly elevated expression noise after controlling all confounding factors. We propose a model that explains why and unde ...[more]

PMID: 19690568

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Project description:BACKGROUND: Synonymous DNA substitution rates in the plant chloroplast genome are generally relatively slow and lineage dependent. Non-synonymous rates are usually even slower due to purifying selection acting on the genes. Positive selection is expected to speed up non-synonymous substitution rates, whereas synonymous rates are expected to be unaffected. Until recently, positive selection has seldom been observed in chloroplast genes, and large-scale structural rearrangements leading to gene duplications are hitherto supposed to be rare. METHODOLOGY/PRINCIPLE FINDINGS: We found high substitution rates in the exons of the plastid clpP1 gene in Oenothera (the Evening Primrose family) and three separate lineages in the tribe Sileneae (Caryophyllaceae, the Carnation family). Introns have been lost in some of the lineages, but where present, the intron sequences have substitution rates similar to those found in other introns of their genomes. The elevated substitution rates of clpP1 are associated with statistically significant whole-gene positive selection in three branches of the phylogeny. In two of the lineages we found multiple copies of the gene. Neighboring genes present in the duplicated fragments do not show signs of elevated substitution rates or positive selection. Although non-synonymous substitutions account for most of the increase in substitution rates, synonymous rates are also markedly elevated in some lineages. Whereas plant clpP1 genes experiencing negative (purifying) selection are characterized by having very conserved lengths, genes under positive selection often have large insertions of more or less repetitive amino acid sequence motifs. CONCLUSIONS/SIGNIFICANCE: We found positive selection of the clpP1 gene in various plant lineages to correlated with repeated duplication of the clpP1 gene and surrounding regions, repetitive amino acid sequences, and increase in synonymous substitution rates. The present study sheds light on the controversial issue of whether negative or positive selection is to be expected after gene duplications by providing evidence for the latter alternative. The observed increase in synonymous substitution rates in some of the lineages indicates that the detection of positive selection may be obscured under such circumstances. Future studies are required to explore the functional significance of the large inserted repeated amino acid motifs, as well as the possibility that synonymous substitution rates may be affected by positive selection.

Dataset Information

Positive selection for elevated gene expression noise in yeast.

Publications

Positive selection for elevated gene expression noise in yeast.

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