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Variations in stress sensitivity and genomic expression in diverse S. cerevisiae isolates.

Kvitek DJ, Will JL, Gasch AP - PLoS Genet. (2008)

Bottom Line: Our results demonstrate a large degree of phenotypic variation in stress sensitivity and gene expression.Using a simple metric to suggest cases of selection, we found that strains collected from oak exudates are phenotypically more similar than expected based on their genetic diversity, while sake and vineyard isolates display more diverse phenotypes than expected under a neutral model.These results highlight the value of understanding the genetic basis of phenotypic variation and raise caution about using laboratory strains for comparative genomics.

View Article: PubMed Central - PubMed

Affiliation: Laboratory of Genetics, University of Wisconsin-Madison, Madison, Wisconsin, United States of America.

ABSTRACT
Interactions between an organism and its environment can significantly influence phenotypic evolution. A first step toward understanding this process is to characterize phenotypic diversity within and between populations. We explored the phenotypic variation in stress sensitivity and genomic expression in a large panel of Saccharomyces strains collected from diverse environments. We measured the sensitivity of 52 strains to 14 environmental conditions, compared genomic expression in 18 strains, and identified gene copy-number variations in six of these isolates. Our results demonstrate a large degree of phenotypic variation in stress sensitivity and gene expression. Analysis of these datasets reveals relationships between strains from similar niches, suggests common and unique features of yeast habitats, and implicates genes whose variable expression is linked to stress resistance. Using a simple metric to suggest cases of selection, we found that strains collected from oak exudates are phenotypically more similar than expected based on their genetic diversity, while sake and vineyard isolates display more diverse phenotypes than expected under a neutral model. We also show that the laboratory strain S288c is phenotypically distinct from all of the other strains studied here, in terms of stress sensitivity, gene expression, Ty copy number, mitochondrial content, and gene-dosage control. These results highlight the value of understanding the genetic basis of phenotypic variation and raise caution about using laboratory strains for comparative genomics.

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Variation in gene expression in S. cerevisiae                            isolates.The diagrams show the average log2 expression differences measured in the                            denoted strains. Each row represents a given gene and each column                            represents a different strain, color-coded as described in Figure 1. (A)                            Expression patterns of 2,680 genes that varied significantly                            (FDR = 0.01, paired t-test) in at least                            one strain compared to S288c. (B) Expression patterns of 953 genes that                            varied significantly in at least one strain compared to strain YPS163                            (FDR = 0.01, unpaired t-test). For (A)                            and (B), a red color indicates higher expression and a green color                            represents lower expression in the denoted strain compared to S288c,                            according to the key. (C) Expression patterns of 1,330 genes that varied                            significantly (FDR = 0.01, paired                            t-test) in at least one strain compared to the mean expression of all 17                            strains. Here, red and green correspond to higher and lower expression,                            respectively, compared to the mean expression of that gene in all                            strains. Genes were organized independently in each plot by hierarchical                            clustering.
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pgen-1000223-g003: Variation in gene expression in S. cerevisiae isolates.The diagrams show the average log2 expression differences measured in the denoted strains. Each row represents a given gene and each column represents a different strain, color-coded as described in Figure 1. (A) Expression patterns of 2,680 genes that varied significantly (FDR = 0.01, paired t-test) in at least one strain compared to S288c. (B) Expression patterns of 953 genes that varied significantly in at least one strain compared to strain YPS163 (FDR = 0.01, unpaired t-test). For (A) and (B), a red color indicates higher expression and a green color represents lower expression in the denoted strain compared to S288c, according to the key. (C) Expression patterns of 1,330 genes that varied significantly (FDR = 0.01, paired t-test) in at least one strain compared to the mean expression of all 17 strains. Here, red and green correspond to higher and lower expression, respectively, compared to the mean expression of that gene in all strains. Genes were organized independently in each plot by hierarchical clustering.

Mentions: A striking number of yeast genes showed differential expression from the laboratory strain in at least one other strain (Figure 3A). Of the ∼5,700 predicted S. cerevisiae open reading frames, 2680 (∼47%) were statistically significantly altered in expression (false discovery rate, FDR = 0.01) in at least one non-laboratory strain compared to S288c, with an average of 480 genes per strain. At an FDR of 0.05, over 70% of genes were significantly altered in expression in at least one non-lab strain (Table 1). The number of expression differences is comparable to that observed by Brem et al., who reported over half of yeast genes differentially expressed between the vineyard strain RM11-1a and S288c [27].


Variations in stress sensitivity and genomic expression in diverse S. cerevisiae isolates.

Kvitek DJ, Will JL, Gasch AP - PLoS Genet. (2008)

Variation in gene expression in S. cerevisiae                            isolates.The diagrams show the average log2 expression differences measured in the                            denoted strains. Each row represents a given gene and each column                            represents a different strain, color-coded as described in Figure 1. (A)                            Expression patterns of 2,680 genes that varied significantly                            (FDR = 0.01, paired t-test) in at least                            one strain compared to S288c. (B) Expression patterns of 953 genes that                            varied significantly in at least one strain compared to strain YPS163                            (FDR = 0.01, unpaired t-test). For (A)                            and (B), a red color indicates higher expression and a green color                            represents lower expression in the denoted strain compared to S288c,                            according to the key. (C) Expression patterns of 1,330 genes that varied                            significantly (FDR = 0.01, paired                            t-test) in at least one strain compared to the mean expression of all 17                            strains. Here, red and green correspond to higher and lower expression,                            respectively, compared to the mean expression of that gene in all                            strains. Genes were organized independently in each plot by hierarchical                            clustering.
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getmorefigures.php?uid=PMC2562515&req=5

pgen-1000223-g003: Variation in gene expression in S. cerevisiae isolates.The diagrams show the average log2 expression differences measured in the denoted strains. Each row represents a given gene and each column represents a different strain, color-coded as described in Figure 1. (A) Expression patterns of 2,680 genes that varied significantly (FDR = 0.01, paired t-test) in at least one strain compared to S288c. (B) Expression patterns of 953 genes that varied significantly in at least one strain compared to strain YPS163 (FDR = 0.01, unpaired t-test). For (A) and (B), a red color indicates higher expression and a green color represents lower expression in the denoted strain compared to S288c, according to the key. (C) Expression patterns of 1,330 genes that varied significantly (FDR = 0.01, paired t-test) in at least one strain compared to the mean expression of all 17 strains. Here, red and green correspond to higher and lower expression, respectively, compared to the mean expression of that gene in all strains. Genes were organized independently in each plot by hierarchical clustering.
Mentions: A striking number of yeast genes showed differential expression from the laboratory strain in at least one other strain (Figure 3A). Of the ∼5,700 predicted S. cerevisiae open reading frames, 2680 (∼47%) were statistically significantly altered in expression (false discovery rate, FDR = 0.01) in at least one non-laboratory strain compared to S288c, with an average of 480 genes per strain. At an FDR of 0.05, over 70% of genes were significantly altered in expression in at least one non-lab strain (Table 1). The number of expression differences is comparable to that observed by Brem et al., who reported over half of yeast genes differentially expressed between the vineyard strain RM11-1a and S288c [27].

Bottom Line: Our results demonstrate a large degree of phenotypic variation in stress sensitivity and gene expression.Using a simple metric to suggest cases of selection, we found that strains collected from oak exudates are phenotypically more similar than expected based on their genetic diversity, while sake and vineyard isolates display more diverse phenotypes than expected under a neutral model.These results highlight the value of understanding the genetic basis of phenotypic variation and raise caution about using laboratory strains for comparative genomics.

View Article: PubMed Central - PubMed

Affiliation: Laboratory of Genetics, University of Wisconsin-Madison, Madison, Wisconsin, United States of America.

ABSTRACT
Interactions between an organism and its environment can significantly influence phenotypic evolution. A first step toward understanding this process is to characterize phenotypic diversity within and between populations. We explored the phenotypic variation in stress sensitivity and genomic expression in a large panel of Saccharomyces strains collected from diverse environments. We measured the sensitivity of 52 strains to 14 environmental conditions, compared genomic expression in 18 strains, and identified gene copy-number variations in six of these isolates. Our results demonstrate a large degree of phenotypic variation in stress sensitivity and gene expression. Analysis of these datasets reveals relationships between strains from similar niches, suggests common and unique features of yeast habitats, and implicates genes whose variable expression is linked to stress resistance. Using a simple metric to suggest cases of selection, we found that strains collected from oak exudates are phenotypically more similar than expected based on their genetic diversity, while sake and vineyard isolates display more diverse phenotypes than expected under a neutral model. We also show that the laboratory strain S288c is phenotypically distinct from all of the other strains studied here, in terms of stress sensitivity, gene expression, Ty copy number, mitochondrial content, and gene-dosage control. These results highlight the value of understanding the genetic basis of phenotypic variation and raise caution about using laboratory strains for comparative genomics.

Show MeSH
Related in: MedlinePlus