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Four linked genes participate in controlling sporulation efficiency in budding yeast.

Ben-Ari G, Zenvirth D, Sherman A, David L, Klutstein M, Lavi U, Hillel J, Simchen G - PLoS Genet. (2006)

Bottom Line: Through reciprocal hemizygosity analysis, four genes, RAS2, PMS1, SWS2, and FKH2, located in a region of 60 kilobases on Chromosome 14, were found to be associated with sporulation efficiency.Our results provide a detailed view of genetic complexity in one "QTL region" that controls a quantitative trait and reports a single nucleotide polymorphism-trait association in wild strains.Moreover, these findings have implications on QTL identification in higher eukaryotes.

View Article: PubMed Central - PubMed

Affiliation: Institute of Plant Sciences and Genetics, Faculty of Agriculture, Hebrew University of Jerusalem, Rehovot, Israel.

ABSTRACT
Quantitative traits are conditioned by several genetic determinants. Since such genes influence many important complex traits in various organisms, the identification of quantitative trait loci (QTLs) is of major interest, but still encounters serious difficulties. We detected four linked genes within one QTL, which participate in controlling sporulation efficiency in Saccharomyces cerevisiae. Following the identification of single nucleotide polymorphisms by comparing the sequences of 145 genes between the parental strains SK1 and S288c, we analyzed the segregating progeny of the cross between them. Through reciprocal hemizygosity analysis, four genes, RAS2, PMS1, SWS2, and FKH2, located in a region of 60 kilobases on Chromosome 14, were found to be associated with sporulation efficiency. Three of the four "high" sporulation alleles are derived from the "low" sporulating strain. Two of these sporulation-related genes were verified through allele replacements. For RAS2, the causative variation was suggested to be a single nucleotide difference in the upstream region of the gene. This quantitative trait nucleotide accounts for sporulation variability among a set of ten closely related winery yeast strains. Our results provide a detailed view of genetic complexity in one "QTL region" that controls a quantitative trait and reports a single nucleotide polymorphism-trait association in wild strains. Moreover, these findings have implications on QTL identification in higher eukaryotes.

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Effects of Reciprocal Hemizygosity and of Allele Replacements on Sporulation(A) Sporulation efficiency of pairs of hybrid strains (S288c × SK1) with single-gene heterozygous deletions. Strains deleted for the S288c allele (only the SK1 allele is present) are presented by black bars and the isogenic strains deleted for the corresponding SK1 allele (only the S288c allele is present) are presented as diagonally hatched bars. The non-deleted hybrid is presented for reference (gray bar).(B) Sporulation efficiency of double-gene and four-gene deletion mutants. Every pair consisted of two isogenic hybrid strains (S288c × SK1), each with two (or four) hemizygosities: One strain had deletions of the two (or four) sporulation-promoting alleles (empty bars) and the other had deletions of the corresponding sporulation-inhibiting alleles (bars with horizontal lines).(C) Sporulation of the four-gene deletion mutants. In the hybrid strain containing the four sporulation-promoting alleles (left microscopic image), almost all cells formed asci, whereas in the strain with the sporulation-inhibiting alleles (right image), most of the cells did not form asci. The genotypes of the two “reciprocal” strains are given below each image.(D) Sporulation efficiencies of a diploid S288c strain and two isogenic allele-replacement strains, one containing the two SWS2 alleles from strain SK1 and the other containing the two RAS2 alleles from SK1. A fourth isogenic strain contains, homozygotically, only a single additional A in the promoter poly-A stretch of RAS2, as found in strain SK1. For each strain, sporulation was assessed four times. The average sporulation efficiencies and their confidence intervals (p = 0.95) are shown.
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pgen-0020195-g004: Effects of Reciprocal Hemizygosity and of Allele Replacements on Sporulation(A) Sporulation efficiency of pairs of hybrid strains (S288c × SK1) with single-gene heterozygous deletions. Strains deleted for the S288c allele (only the SK1 allele is present) are presented by black bars and the isogenic strains deleted for the corresponding SK1 allele (only the S288c allele is present) are presented as diagonally hatched bars. The non-deleted hybrid is presented for reference (gray bar).(B) Sporulation efficiency of double-gene and four-gene deletion mutants. Every pair consisted of two isogenic hybrid strains (S288c × SK1), each with two (or four) hemizygosities: One strain had deletions of the two (or four) sporulation-promoting alleles (empty bars) and the other had deletions of the corresponding sporulation-inhibiting alleles (bars with horizontal lines).(C) Sporulation of the four-gene deletion mutants. In the hybrid strain containing the four sporulation-promoting alleles (left microscopic image), almost all cells formed asci, whereas in the strain with the sporulation-inhibiting alleles (right image), most of the cells did not form asci. The genotypes of the two “reciprocal” strains are given below each image.(D) Sporulation efficiencies of a diploid S288c strain and two isogenic allele-replacement strains, one containing the two SWS2 alleles from strain SK1 and the other containing the two RAS2 alleles from SK1. A fourth isogenic strain contains, homozygotically, only a single additional A in the promoter poly-A stretch of RAS2, as found in strain SK1. For each strain, sporulation was assessed four times. The average sporulation efficiencies and their confidence intervals (p = 0.95) are shown.

Mentions: Unlike the assessment of sporulation phenotypes of the original segregants, for all reciprocal-hemizygosity and allele-replacement tests we determined sporulation efficiency after 48 h in liquid sporulation medium. Significant differences in sporulation efficiencies (10%–20%) were detected between reciprocal hemizygosity strains of four genes: FKH2, PMS1, RAS2, and SWS2 (Figure 4A). Counterintuitive to the phenotype of strain S288c (low sporulation efficiency), the presence of the sole S288c allele for each of the genes FKH2, PMS1, or RAS2 resulted in higher sporulation efficiency compared to the presence of the single SK1 allele (in the same hybrid background). Only for the gene SWS2, the SK1 allele resulted in higher sporulation. These four genes were further analyzed as follows.


Four linked genes participate in controlling sporulation efficiency in budding yeast.

Ben-Ari G, Zenvirth D, Sherman A, David L, Klutstein M, Lavi U, Hillel J, Simchen G - PLoS Genet. (2006)

Effects of Reciprocal Hemizygosity and of Allele Replacements on Sporulation(A) Sporulation efficiency of pairs of hybrid strains (S288c × SK1) with single-gene heterozygous deletions. Strains deleted for the S288c allele (only the SK1 allele is present) are presented by black bars and the isogenic strains deleted for the corresponding SK1 allele (only the S288c allele is present) are presented as diagonally hatched bars. The non-deleted hybrid is presented for reference (gray bar).(B) Sporulation efficiency of double-gene and four-gene deletion mutants. Every pair consisted of two isogenic hybrid strains (S288c × SK1), each with two (or four) hemizygosities: One strain had deletions of the two (or four) sporulation-promoting alleles (empty bars) and the other had deletions of the corresponding sporulation-inhibiting alleles (bars with horizontal lines).(C) Sporulation of the four-gene deletion mutants. In the hybrid strain containing the four sporulation-promoting alleles (left microscopic image), almost all cells formed asci, whereas in the strain with the sporulation-inhibiting alleles (right image), most of the cells did not form asci. The genotypes of the two “reciprocal” strains are given below each image.(D) Sporulation efficiencies of a diploid S288c strain and two isogenic allele-replacement strains, one containing the two SWS2 alleles from strain SK1 and the other containing the two RAS2 alleles from SK1. A fourth isogenic strain contains, homozygotically, only a single additional A in the promoter poly-A stretch of RAS2, as found in strain SK1. For each strain, sporulation was assessed four times. The average sporulation efficiencies and their confidence intervals (p = 0.95) are shown.
© Copyright Policy
Related In: Results  -  Collection

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Show All Figures
getmorefigures.php?uid=PMC1636695&req=5

pgen-0020195-g004: Effects of Reciprocal Hemizygosity and of Allele Replacements on Sporulation(A) Sporulation efficiency of pairs of hybrid strains (S288c × SK1) with single-gene heterozygous deletions. Strains deleted for the S288c allele (only the SK1 allele is present) are presented by black bars and the isogenic strains deleted for the corresponding SK1 allele (only the S288c allele is present) are presented as diagonally hatched bars. The non-deleted hybrid is presented for reference (gray bar).(B) Sporulation efficiency of double-gene and four-gene deletion mutants. Every pair consisted of two isogenic hybrid strains (S288c × SK1), each with two (or four) hemizygosities: One strain had deletions of the two (or four) sporulation-promoting alleles (empty bars) and the other had deletions of the corresponding sporulation-inhibiting alleles (bars with horizontal lines).(C) Sporulation of the four-gene deletion mutants. In the hybrid strain containing the four sporulation-promoting alleles (left microscopic image), almost all cells formed asci, whereas in the strain with the sporulation-inhibiting alleles (right image), most of the cells did not form asci. The genotypes of the two “reciprocal” strains are given below each image.(D) Sporulation efficiencies of a diploid S288c strain and two isogenic allele-replacement strains, one containing the two SWS2 alleles from strain SK1 and the other containing the two RAS2 alleles from SK1. A fourth isogenic strain contains, homozygotically, only a single additional A in the promoter poly-A stretch of RAS2, as found in strain SK1. For each strain, sporulation was assessed four times. The average sporulation efficiencies and their confidence intervals (p = 0.95) are shown.
Mentions: Unlike the assessment of sporulation phenotypes of the original segregants, for all reciprocal-hemizygosity and allele-replacement tests we determined sporulation efficiency after 48 h in liquid sporulation medium. Significant differences in sporulation efficiencies (10%–20%) were detected between reciprocal hemizygosity strains of four genes: FKH2, PMS1, RAS2, and SWS2 (Figure 4A). Counterintuitive to the phenotype of strain S288c (low sporulation efficiency), the presence of the sole S288c allele for each of the genes FKH2, PMS1, or RAS2 resulted in higher sporulation efficiency compared to the presence of the single SK1 allele (in the same hybrid background). Only for the gene SWS2, the SK1 allele resulted in higher sporulation. These four genes were further analyzed as follows.

Bottom Line: Through reciprocal hemizygosity analysis, four genes, RAS2, PMS1, SWS2, and FKH2, located in a region of 60 kilobases on Chromosome 14, were found to be associated with sporulation efficiency.Our results provide a detailed view of genetic complexity in one "QTL region" that controls a quantitative trait and reports a single nucleotide polymorphism-trait association in wild strains.Moreover, these findings have implications on QTL identification in higher eukaryotes.

View Article: PubMed Central - PubMed

Affiliation: Institute of Plant Sciences and Genetics, Faculty of Agriculture, Hebrew University of Jerusalem, Rehovot, Israel.

ABSTRACT
Quantitative traits are conditioned by several genetic determinants. Since such genes influence many important complex traits in various organisms, the identification of quantitative trait loci (QTLs) is of major interest, but still encounters serious difficulties. We detected four linked genes within one QTL, which participate in controlling sporulation efficiency in Saccharomyces cerevisiae. Following the identification of single nucleotide polymorphisms by comparing the sequences of 145 genes between the parental strains SK1 and S288c, we analyzed the segregating progeny of the cross between them. Through reciprocal hemizygosity analysis, four genes, RAS2, PMS1, SWS2, and FKH2, located in a region of 60 kilobases on Chromosome 14, were found to be associated with sporulation efficiency. Three of the four "high" sporulation alleles are derived from the "low" sporulating strain. Two of these sporulation-related genes were verified through allele replacements. For RAS2, the causative variation was suggested to be a single nucleotide difference in the upstream region of the gene. This quantitative trait nucleotide accounts for sporulation variability among a set of ten closely related winery yeast strains. Our results provide a detailed view of genetic complexity in one "QTL region" that controls a quantitative trait and reports a single nucleotide polymorphism-trait association in wild strains. Moreover, these findings have implications on QTL identification in higher eukaryotes.

Show MeSH
Related in: MedlinePlus