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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 gene region and chimeric alleles.The FZF1 gene region is shown along with the breakpoints used to generate reciprocal chimeric alleles. Regions with non-neutral evolution are indicated by gray boxes and the predicted zinc fingers are indicated by black boxes [73]. Region lengths between chimera junctions are given for S. cerevisiae. One set of chimeric alleles between S. cerevisiae and S. paradoxus are shown below. The reciprocal set is not shown.
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pgen-1002763-g003: FZF1 gene region and chimeric alleles.The FZF1 gene region is shown along with the breakpoints used to generate reciprocal chimeric alleles. Regions with non-neutral evolution are indicated by gray boxes and the predicted zinc fingers are indicated by black boxes [73]. Region lengths between chimera junctions are given for S. cerevisiae. One set of chimeric alleles between S. cerevisiae and S. paradoxus are shown below. The reciprocal set is not shown.

Mentions: The S. cerevisiae FZF1 protein is 900 amino acids long and has 195 bases in the 5′ noncoding region. Between the S. cerevisiae and S. paradoxus FZF1 alleles there are 67 amino acid differences and 82 differences in the 5′ noncoding region, 31 of which are insertion/deletion differences. To delineate which subset of these differences are responsible for divergence in sulfite resistance, we generated ten sets of reciprocal chimeric constructs between the two species (Figure 3). The FZF1 chimeric breakpoints were located (1) in the middle of the 5′ noncoding region, (2) at the junction between the 5′ noncoding and the coding region, (3) in the coding region between the first zinc finger domain, known to bind DNA [37], and the region under positive selection [35], and (4) at the junction between the coding and 3′ noncoding region. Five sets of chimeric constructs contain a single region in the opposite background and the remaining sets of constructs contain five of the ten possible pairwise combinations of each region.


Divergence of the yeast transcription factor FZF1 affects sulfite resistance.

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

FZF1 gene region and chimeric alleles.The FZF1 gene region is shown along with the breakpoints used to generate reciprocal chimeric alleles. Regions with non-neutral evolution are indicated by gray boxes and the predicted zinc fingers are indicated by black boxes [73]. Region lengths between chimera junctions are given for S. cerevisiae. One set of chimeric alleles between S. cerevisiae and S. paradoxus are shown below. The reciprocal set is not shown.
© Copyright Policy
Related In: Results  -  Collection

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

pgen-1002763-g003: FZF1 gene region and chimeric alleles.The FZF1 gene region is shown along with the breakpoints used to generate reciprocal chimeric alleles. Regions with non-neutral evolution are indicated by gray boxes and the predicted zinc fingers are indicated by black boxes [73]. Region lengths between chimera junctions are given for S. cerevisiae. One set of chimeric alleles between S. cerevisiae and S. paradoxus are shown below. The reciprocal set is not shown.
Mentions: The S. cerevisiae FZF1 protein is 900 amino acids long and has 195 bases in the 5′ noncoding region. Between the S. cerevisiae and S. paradoxus FZF1 alleles there are 67 amino acid differences and 82 differences in the 5′ noncoding region, 31 of which are insertion/deletion differences. To delineate which subset of these differences are responsible for divergence in sulfite resistance, we generated ten sets of reciprocal chimeric constructs between the two species (Figure 3). The FZF1 chimeric breakpoints were located (1) in the middle of the 5′ noncoding region, (2) at the junction between the 5′ noncoding and the coding region, (3) in the coding region between the first zinc finger domain, known to bind DNA [37], and the region under positive selection [35], and (4) at the junction between the coding and 3′ noncoding region. Five sets of chimeric constructs contain a single region in the opposite background and the remaining sets of constructs contain five of the ten possible pairwise combinations of each region.

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