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Divergence of the yeast transcription factor FZF1 affects sulfite resistance.

Engle EK, Fay JC - PLoS Genet. (2012)

Bottom Line: Yet, some changes in transcriptional regulators may be constrained by their pleiotropic effects on gene expression.Both coding and noncoding changes also affect the expression of many other genes.Our results show how divergence in the coding and promoter region of a transcription factor alters the response to an environmental stress.

View Article: PubMed Central - PubMed

Affiliation: Molecular Genetics and Genomics Program, Washington University, St. Louis, Missouri, United States of America.

ABSTRACT
Changes in gene expression are commonly observed during evolution. However, the phenotypic consequences of expression divergence are frequently unknown and difficult to measure. Transcriptional regulators provide a mechanism by which phenotypic divergence can occur through multiple, coordinated changes in gene expression during development or in response to environmental changes. Yet, some changes in transcriptional regulators may be constrained by their pleiotropic effects on gene expression. Here, we use a genome-wide screen for promoters that are likely to have diverged in function and identify a yeast transcription factor, FZF1, that has evolved substantial differences in its ability to confer resistance to sulfites. Chimeric alleles from four Saccharomyces species show that divergence in FZF1 activity is due to changes in both its coding and upstream noncoding sequence. Between the two closest species, noncoding changes affect the expression of FZF1, whereas coding changes affect the expression of SSU1, a sulfite efflux pump activated by FZF1. Both coding and noncoding changes also affect the expression of many other genes. Our results show how divergence in the coding and promoter region of a transcription factor alters the response to an environmental stress.

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Multiple noncoding and coding changes contribute to sulfite resistance.Sulfite resistance is shown for chimeric alleles of FZF1 from S. cerevisiae and S. paradoxus. Chimera breakpoints are shown in Figure 3 and are labeled 5′ to 3′ based on the origin of each region: S. cerevisiae (red, “C”) and S. paradoxus (yellow, “P”). Error bars show the 95% confidence interval of the mean.
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pgen-1002763-g004: Multiple noncoding and coding changes contribute to sulfite resistance.Sulfite resistance is shown for chimeric alleles of FZF1 from S. cerevisiae and S. paradoxus. Chimera breakpoints are shown in Figure 3 and are labeled 5′ to 3′ based on the origin of each region: S. cerevisiae (red, “C”) and S. paradoxus (yellow, “P”). Error bars show the 95% confidence interval of the mean.

Mentions: Including the full length S. cerevisiae and S. paradoxus alleles of FZF1, the 22 constructs show a nearly continuous distribution of sulfite resistance (Figure 4). Using an additive model, the estimated effects of the first three FZF1 regions individually account for 8.2%, 39.0%, and 49.5%, respectively, of the difference in sulfite resistance between the S. cerevisiae and S. paradoxus alleles (Table 1). The latter two regions are not statistically significant. Some of the variation in sulfite resistance can be attributed to non-additive interactions among regions. The additive model explains a total of 66% of the variance among alleles, significantly less than a model that allows for pairwise epistatic interactions, which explains 70% of the variance (Likelihood ratio test, 2Δln(L) = 56.48, 10 d.f., P = 1.7×10−8). However, out of all the pairwise interactions, only the interaction between the two coding regions is individually significant after correcting for multiple tests (Table 1). The interaction indicates that the two coding regions have a smaller effect in combination compared to that expected from each region individually.


Divergence of the yeast transcription factor FZF1 affects sulfite resistance.

Engle EK, Fay JC - PLoS Genet. (2012)

Multiple noncoding and coding changes contribute to sulfite resistance.Sulfite resistance is shown for chimeric alleles of FZF1 from S. cerevisiae and S. paradoxus. Chimera breakpoints are shown in Figure 3 and are labeled 5′ to 3′ based on the origin of each region: S. cerevisiae (red, “C”) and S. paradoxus (yellow, “P”). Error bars show the 95% confidence interval of the mean.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3375221&req=5

pgen-1002763-g004: Multiple noncoding and coding changes contribute to sulfite resistance.Sulfite resistance is shown for chimeric alleles of FZF1 from S. cerevisiae and S. paradoxus. Chimera breakpoints are shown in Figure 3 and are labeled 5′ to 3′ based on the origin of each region: S. cerevisiae (red, “C”) and S. paradoxus (yellow, “P”). Error bars show the 95% confidence interval of the mean.
Mentions: Including the full length S. cerevisiae and S. paradoxus alleles of FZF1, the 22 constructs show a nearly continuous distribution of sulfite resistance (Figure 4). Using an additive model, the estimated effects of the first three FZF1 regions individually account for 8.2%, 39.0%, and 49.5%, respectively, of the difference in sulfite resistance between the S. cerevisiae and S. paradoxus alleles (Table 1). The latter two regions are not statistically significant. Some of the variation in sulfite resistance can be attributed to non-additive interactions among regions. The additive model explains a total of 66% of the variance among alleles, significantly less than a model that allows for pairwise epistatic interactions, which explains 70% of the variance (Likelihood ratio test, 2Δln(L) = 56.48, 10 d.f., P = 1.7×10−8). However, out of all the pairwise interactions, only the interaction between the two coding regions is individually significant after correcting for multiple tests (Table 1). The interaction indicates that the two coding regions have a smaller effect in combination compared to that expected from each region individually.

Bottom Line: Yet, some changes in transcriptional regulators may be constrained by their pleiotropic effects on gene expression.Both coding and noncoding changes also affect the expression of many other genes.Our results show how divergence in the coding and promoter region of a transcription factor alters the response to an environmental stress.

View Article: PubMed Central - PubMed

Affiliation: Molecular Genetics and Genomics Program, Washington University, St. Louis, Missouri, United States of America.

ABSTRACT
Changes in gene expression are commonly observed during evolution. However, the phenotypic consequences of expression divergence are frequently unknown and difficult to measure. Transcriptional regulators provide a mechanism by which phenotypic divergence can occur through multiple, coordinated changes in gene expression during development or in response to environmental changes. Yet, some changes in transcriptional regulators may be constrained by their pleiotropic effects on gene expression. Here, we use a genome-wide screen for promoters that are likely to have diverged in function and identify a yeast transcription factor, FZF1, that has evolved substantial differences in its ability to confer resistance to sulfites. Chimeric alleles from four Saccharomyces species show that divergence in FZF1 activity is due to changes in both its coding and upstream noncoding sequence. Between the two closest species, noncoding changes affect the expression of FZF1, whereas coding changes affect the expression of SSU1, a sulfite efflux pump activated by FZF1. Both coding and noncoding changes also affect the expression of many other genes. Our results show how divergence in the coding and promoter region of a transcription factor alters the response to an environmental stress.

Show MeSH
Related in: MedlinePlus