The Evolution of Gene Expression QTL in Saccharomyces cerevisiae

Ronald, James; Akey, Joshua M.

doi:10.1371/journal.pone.0000678

Cited by 53 publications

(54 citation statements)

References 49 publications

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“…Despite these caveats, we did observe a nominally significant association between genes with AI in both species (P = 0.003). Purifying selection has recently been described for cis-eQTL in yeast (Ronald and Akey 2007), which lends support to our findings that certain genes may be more tolerant of regulatory variation.…”

Section: Discussionsupporting

confidence: 90%

A survey of allelic imbalance in F1 mice

Campbell¹,

Kirby²,

Nemesh³

et al. 2008

Genome Res.

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There are widespread, genetically determined differences in gene expression. However, methods that compare transcript levels between individuals are subject to trans-acting effects and environmental differences. By looking at allele-specific expression in the F1 progeny of inbred mice, we can directly test for allelic imbalance (AI), which must be due to cis-acting variants in the parental strains. We tested over one hundred genes for AI between C57Bl/6J and A/J alleles in F1 mice, including a validation set of 23 genes enriched for cis-acting variants and a second set of 92 genes whose orthologs were previously examined for AI in humans. We assayed an average of two transcribed SNPs per gene in liver, spleen, and brain from three male and three female F1 mice. In the set of 92 genes, we observed 33 genes (36%) with significant AI including genes with AI that was specific to certain tissues or transcripts. We also observed extensive tissue-specific AI, with 11 out of 92 genes (12%) having differences in AI between tissues. Interestingly, several genes with alternate transcripts have transcript-specific AI. Finally, we observed that the presence of AI in human genes was correlated to the presence of AI in the mouse orthologs (one-tailed P = 0.003), suggesting that certain genes may be more tolerant of cis-acting variation across species.

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Section: Discussionsupporting

confidence: 90%

A survey of allelic imbalance in F1 mice

Campbell¹,

Kirby²,

Nemesh³

et al. 2008

Genome Res.

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“…Because these therefore represent largely distinct lineages, adaptive differences may have accumulated in each. Previous studies have used these expression data to map thousands of eQTL (14) and also to show that negative selection acts on many cis eQTL (16).…”

Section: Resultsmentioning

confidence: 99%

Evidence for widespread adaptive evolution of gene expression in budding yeast

Fraser

Moses

Schadt

2010

Proc. Natl. Acad. Sci. U.S.A.

158

183

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Changes in gene expression have been proposed to underlie many, or even most, adaptive differences between species. Despite the increasing acceptance of this view, only a handful of cases of adaptive gene expression evolution have been demonstrated. To address this discrepancy, we introduce a simple test for lineage-specific selection on gene expression. Applying the test to genome-wide gene expression data from the budding yeast Saccharomyces cerevisiae , we find that hundreds of gene expression levels have been subject to lineage-specific selection. Comparing these findings with independent population genetic evidence of selective sweeps suggests that this lineage-specific selection has resulted in recent sweeps at over a hundred genes, most of which led to increased transcript levels. Examination of the implicated genes revealed a specific biochemical pathway—ergosterol biosynthesis—where the expression of multiple genes has been subject to selection for reduced levels. In sum, these results suggest that adaptive evolution of gene expression is common in yeast, that regulatory adaptation can occur at the level of entire pathways, and that similar genome-wide scans may be possible in other species, including humans.

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“…Another S288C allele that confers easy dispersal is AMN1-368V (Yvert et al 2003;Ronald et al 2005). However, the EM93 strain, which contributed 88% of its genome to S288C, contains a functional FLO8 gene (Liu et al 1996) and the more common AMN1-368D allele (Ronald and Akey 2007). Given the desire for cellular dispersal, it is easy to appreciate why the common EM93 alleles of FLO8 and AMN1 were not fixed in S288C.…”

Section: Discussionmentioning

confidence: 99%

Polymorphisms in Multiple Genes Contribute to the Spontaneous Mitochondrial Genome Instability ofSaccharomyces cerevisiaeS288C Strains

et al. 2009

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The mitochondrial genome (mtDNA) is required for normal cellular function; inherited and somatic mutations in mtDNA lead to a variety of diseases. Saccharomyces cerevisiae has served as a model to study mtDNA integrity, in part because it can survive without mtDNA. A measure of defective mtDNA in S. cerevisiae is the formation of petite colonies. The frequency at which spontaneous petite colonies arise varies by $100-fold between laboratory and natural isolate strains. To determine the genetic basis of this difference, we applied quantitative trait locus (QTL) mapping to two strains at the opposite extremes of the phenotypic spectrum: the widely studied laboratory strain S288C and the vineyard isolate RM11-1a. Four main genetic determinants explained the phenotypic difference. Alleles of SAL1, CAT5, and MIP1 contributed to the high petite frequency of S288C and its derivatives by increasing the formation of petite colonies. By contrast, the S288C allele of MKT1 reduced the formation of petite colonies and compromised the growth of petite cells. The former three alleles were found in the EM93 strain, the founder that contributed $88% of the S288C genome. Nearly all of the phenotypic difference between S288C and RM11-1a was reconstituted by introducing the common alleles of these four genes into the S288C background. In addition to the nuclear gene contribution, the source of the mtDNA influenced its stability. These results demonstrate that a few rare genetic variants with individually small effects can have a profound phenotypic effect in combination. Moreover, the polymorphisms identified in this study open new lines of investigation into mtDNA maintenance.

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The Evolution of Gene Expression QTL in Saccharomyces cerevisiae

Cited by 53 publications

References 49 publications

A survey of allelic imbalance in F1 mice

A survey of allelic imbalance in F1 mice

Evidence for widespread adaptive evolution of gene expression in budding yeast

Polymorphisms in Multiple Genes Contribute to the Spontaneous Mitochondrial Genome Instability ofSaccharomyces cerevisiaeS288C Strains

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