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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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FZF1 alleles from different species have diverged in function.The left side of the figure shows sulfite resistance of FZF1 alleles from four different species: S. cerevisiae (red), S. paradoxus (yellow), S. mikatae (blue), and S. bayanus (green) in an S. cerevisiae strain background. The right side of the figure shows sulfite resistance of chimeric alleles of FZF1 composed of the 5′ noncoding region from S. paradoxus, S. mikatae and S. bayanus combined with the S. cerevisiae coding region. Error bars show the 95% confidence interval of the mean.
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pgen-1002763-g002: FZF1 alleles from different species have diverged in function.The left side of the figure shows sulfite resistance of FZF1 alleles from four different species: S. cerevisiae (red), S. paradoxus (yellow), S. mikatae (blue), and S. bayanus (green) in an S. cerevisiae strain background. The right side of the figure shows sulfite resistance of chimeric alleles of FZF1 composed of the 5′ noncoding region from S. paradoxus, S. mikatae and S. bayanus combined with the S. cerevisiae coding region. Error bars show the 95% confidence interval of the mean.

Mentions: FZF1 encodes a five zinc finger transcription factor that activates the plasma membrane sulfite pump, SSU1[37]. Gain of function mutations in FZF1 result in hyperactivation of SSU1 and increased sulfite resistance [36], [38]. To determine whether FZF1 has diverged in its ability to confer sulfite resistance, we tested FZF1 alleles from four Saccharomyces species: S. cerevisiae, S. paradoxus, S. mikitae, and S. bayanus, for their ability to complement a deletion of FZF1 in S. cerevisiae. The S. cerevisiae allele of FZF1 showed nearly complete complementation of the FZF1 deletion, as measured by the delay in exponential growth following sulfite treatment (Figure S1). In comparison, FZF1 alleles from the other three species all showed a shorter delay in growth relative to that of S. cerevisiae, indicating that these FZF1 alleles confer greater resistance to sulfites (Figure 2, Kruskal-Wallis test, P = 5.3×10−13).


Divergence of the yeast transcription factor FZF1 affects sulfite resistance.

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

FZF1 alleles from different species have diverged in function.The left side of the figure shows sulfite resistance of FZF1 alleles from four different species: S. cerevisiae (red), S. paradoxus (yellow), S. mikatae (blue), and S. bayanus (green) in an S. cerevisiae strain background. The right side of the figure shows sulfite resistance of chimeric alleles of FZF1 composed of the 5′ noncoding region from S. paradoxus, S. mikatae and S. bayanus combined with the S. cerevisiae coding region. 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-g002: FZF1 alleles from different species have diverged in function.The left side of the figure shows sulfite resistance of FZF1 alleles from four different species: S. cerevisiae (red), S. paradoxus (yellow), S. mikatae (blue), and S. bayanus (green) in an S. cerevisiae strain background. The right side of the figure shows sulfite resistance of chimeric alleles of FZF1 composed of the 5′ noncoding region from S. paradoxus, S. mikatae and S. bayanus combined with the S. cerevisiae coding region. Error bars show the 95% confidence interval of the mean.
Mentions: FZF1 encodes a five zinc finger transcription factor that activates the plasma membrane sulfite pump, SSU1[37]. Gain of function mutations in FZF1 result in hyperactivation of SSU1 and increased sulfite resistance [36], [38]. To determine whether FZF1 has diverged in its ability to confer sulfite resistance, we tested FZF1 alleles from four Saccharomyces species: S. cerevisiae, S. paradoxus, S. mikitae, and S. bayanus, for their ability to complement a deletion of FZF1 in S. cerevisiae. The S. cerevisiae allele of FZF1 showed nearly complete complementation of the FZF1 deletion, as measured by the delay in exponential growth following sulfite treatment (Figure S1). In comparison, FZF1 alleles from the other three species all showed a shorter delay in growth relative to that of S. cerevisiae, indicating that these FZF1 alleles confer greater resistance to sulfites (Figure 2, Kruskal-Wallis test, P = 5.3×10−13).

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