Contrasting Properties of Gene-Specific Regulatory, Coding, and Copy Number Mutations in Saccharomyces cerevisiae: Frequency, Effects, and Dominance
Genetic variation within and between species can be shaped by population-level processes and mutation; however, the relative impact of "survival of the fittest" and "arrival of the fittest" on phenotypic evolution remains unclear. Assessing the influence of mutation on evolution...
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| Published in | PLoS genetics Vol. 8; no. 2; p. e1002497 |
|---|---|
| Main Authors | , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Public Library of Science
01.02.2012
Public Library of Science (PLoS) |
| Subjects | |
| Online Access | Get full text |
| ISSN | 1553-7404 1553-7390 1553-7404 |
| DOI | 10.1371/journal.pgen.1002497 |
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| Abstract | Genetic variation within and between species can be shaped by population-level processes and mutation; however, the relative impact of "survival of the fittest" and "arrival of the fittest" on phenotypic evolution remains unclear. Assessing the influence of mutation on evolution requires understanding the relative rates of different types of mutations and their genetic properties, yet little is known about the functional consequences of new mutations. Here, we examine the spectrum of mutations affecting a focal gene in Saccharomyces cerevisiae by characterizing 231 novel haploid genotypes with altered activity of a fluorescent reporter gene. 7% of these genotypes had a nonsynonymous mutation in the coding sequence for the fluorescent protein and were classified as "coding" mutants; 2% had a change in the S. cerevisiae TDH3 promoter sequence controlling expression of the fluorescent protein and were classified as "cis-regulatory" mutants; 10% contained two copies of the reporter gene and were classified as "copy number" mutants; and the remaining 81% showed altered fluorescence without a change in the reporter gene itself and were classified as "trans-acting" mutants. As a group, coding mutants had the strongest effect on reporter gene activity and always decreased it. By contrast, 50%-95% of the mutants in each of the other three classes increased gene activity, with mutants affecting copy number and cis-regulatory sequences having larger median effects on gene activity than trans-acting mutants. When made heterozygous in diploid cells, coding, cis-regulatory, and copy number mutant genotypes all had significant effects on gene activity, whereas 88% of the trans-acting mutants appeared to be recessive. These differences in the frequency, effects, and dominance among functional classes of mutations might help explain why some types of mutations are found to be segregating within or fixed between species more often than others. |
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| AbstractList | Genetic variation within and between species can be shaped by population-level processes and mutation; however, the relative impact of "survival of the fittest" and "arrival of the fittest" on phenotypic evolution remains unclear. Assessing the influence of mutation on evolution requires understanding the relative rates of different types of mutations and their genetic properties, yet little is known about the functional consequences of new mutations. Here, we examine the spectrum of mutations affecting a focal gene in Saccharomyces cerevisiae by characterizing 231 novel haploid genotypes with altered activity of a fluorescent reporter gene. 7% of these genotypes had a nonsynonymous mutation in the coding sequence for the fluorescent protein and were classified as "coding" mutants; 2% had a change in the S. cerevisiae TDH3 promoter sequence controlling expression of the fluorescent protein and were classified as "cis-regulatory" mutants;10% contained two copies of the reporter gene and were classified as "copy number" mutants; and the remaining 81% showed altered fluorescence without a change in the reporter gene itself and were classified as "frans-acting" mutants. As a group, coding mutants had the strongest effect on reporter gene activity and always decreased it. By contrast, 50%-95% of the mutants in each of the other three classes increased gene activity, with mutants affecting copy number and cis-regulatory sequences having larger median effects on gene activity than frans-acting mutants. When made heterozygous in diploid cells, coding, cis-regulatory, and copy number mutant genotypes all had significant effects on gene activity, whereas 88% of the frans-acting mutants appeared to be recessive. These differences in the frequency, effects, and dominance among functional classes of mutations might help explain why some types of mutations are found to be segregating within or fixed between species more often than others. Genetic variation within and between species can be shaped by population-level processes and mutation; however, the relative impact of "survival of the fittest" and "arrival of the fittest" on phenotypic evolution remains unclear. Assessing the influence of mutation on evolution requires understanding the relative rates of different types of mutations and their genetic properties, yet little is known about the functional consequences of new mutations. Here, we examine the spectrum of mutations affecting a focal gene in Saccharomyces cerevisiae by characterizing 231 novel haploid genotypes with altered activity of a fluorescent reporter gene. 7% of these genotypes had a nonsynonymous mutation in the coding sequence for the fluorescent protein and were classified as "coding" mutants; 2% had a change in the S. cerevisiae TDH3 promoter sequence controlling expression of the fluorescent protein and were classified as "cis-regulatory" mutants; 10% contained two copies of the reporter gene and were classified as "copy number" mutants; and the remaining 81% showed altered fluorescence without a change in the reporter gene itself and were classified as "trans-acting" mutants. As a group, coding mutants had the strongest effect on reporter gene activity and always decreased it. By contrast, 50%-95% of the mutants in each of the other three classes increased gene activity, with mutants affecting copy number and cis-regulatory sequences having larger median effects on gene activity than trans-acting mutants. When made heterozygous in diploid cells, coding, cis-regulatory, and copy number mutant genotypes all had significant effects on gene activity, whereas 88% of the trans-acting mutants appeared to be recessive. These differences in the frequency, effects, and dominance among functional classes of mutations might help explain why some types of mutations are found to be segregating within or fixed between species more often than others. Genetic variation within and between species can be shaped by population-level processes and mutation; however, the relative impact of "survival of the fittest" and "arrival of the fittest" on phenotypic evolution remains unclear. Assessing the influence of mutation on evolution requires understanding the relative rates of different types of mutations and their genetic properties, yet little is known about the functional consequences of new mutations. Here, we examine the spectrum of mutations affecting a focal gene in Saccharomyces cerevisiae by characterizing 231 novel haploid genotypes with altered activity of a fluorescent reporter gene. 7% of these genotypes had a nonsynonymous mutation in the coding sequence for the fluorescent protein and were classified as "coding" mutants; 2% had a change in the S. cerevisiae TDH3 promoter sequence controlling expression of the fluorescent protein and were classified as "cis-regulatory" mutants; 10% contained two copies of the reporter gene and were classified as "copy number" mutants; and the remaining 81% showed altered fluorescence without a change in the reporter gene itself and were classified as "trans-acting" mutants. As a group, coding mutants had the strongest effect on reporter gene activity and always decreased it. By contrast, 50%-95% of the mutants in each of the other three classes increased gene activity, with mutants affecting copy number and cis-regulatory sequences having larger median effects on gene activity than trans-acting mutants. When made heterozygous in diploid cells, coding, cis-regulatory, and copy number mutant genotypes all had significant effects on gene activity, whereas 88% of the trans-acting mutants appeared to be recessive. These differences in the frequency, effects, and dominance among functional classes of mutations might help explain why some types of mutations are found to be segregating within or fixed between species more often than others.Genetic variation within and between species can be shaped by population-level processes and mutation; however, the relative impact of "survival of the fittest" and "arrival of the fittest" on phenotypic evolution remains unclear. Assessing the influence of mutation on evolution requires understanding the relative rates of different types of mutations and their genetic properties, yet little is known about the functional consequences of new mutations. Here, we examine the spectrum of mutations affecting a focal gene in Saccharomyces cerevisiae by characterizing 231 novel haploid genotypes with altered activity of a fluorescent reporter gene. 7% of these genotypes had a nonsynonymous mutation in the coding sequence for the fluorescent protein and were classified as "coding" mutants; 2% had a change in the S. cerevisiae TDH3 promoter sequence controlling expression of the fluorescent protein and were classified as "cis-regulatory" mutants; 10% contained two copies of the reporter gene and were classified as "copy number" mutants; and the remaining 81% showed altered fluorescence without a change in the reporter gene itself and were classified as "trans-acting" mutants. As a group, coding mutants had the strongest effect on reporter gene activity and always decreased it. By contrast, 50%-95% of the mutants in each of the other three classes increased gene activity, with mutants affecting copy number and cis-regulatory sequences having larger median effects on gene activity than trans-acting mutants. When made heterozygous in diploid cells, coding, cis-regulatory, and copy number mutant genotypes all had significant effects on gene activity, whereas 88% of the trans-acting mutants appeared to be recessive. These differences in the frequency, effects, and dominance among functional classes of mutations might help explain why some types of mutations are found to be segregating within or fixed between species more often than others. Genetic variation within and between species can be shaped by population-level processes and mutation; however, the relative impact of "survival of the fittest" and "arrival of the fittest" on phenotypic evolution remains unclear. Assessing the influence of mutation on evolution requires understanding the relative rates of different types of mutations and their genetic properties, yet little is known about the functional consequences of new mutations. Here, we examine the spectrum of mutations affecting a focal gene in Saccharomyces cerevisiae by characterizing 231 novel haploid genotypes with altered activity of a fluorescent reporter gene. 7% of these genotypes had a nonsynonymous mutation in the coding sequence for the fluorescent protein and were classified as "coding" mutants; 2% had a change in the S. cerevisiae TDH3 promoter sequence controlling expression of the fluorescent protein and were classified as "cis-regulatory" mutants; 10% contained two copies of the reporter gene and were classified as "copy number" mutants; and the remaining 81% showed altered fluorescence without a change in the reporter gene itself and were classified as "trans-acting" mutants. As a group, coding mutants had the strongest effect on reporter gene activity and always decreased it. By contrast, 50%-95% of the mutants in each of the other three classes increased gene activity, with mutants affecting copy number and cis-regulatory sequences having larger median effects on gene activity than trans-acting mutants. When made heterozygous in diploid cells, coding, cis-regulatory, and copy number mutant genotypes all had significant effects on gene activity, whereas 88% of the trans-acting mutants appeared to be recessive. These differences in the frequency, effects, and dominance among functional classes of mutations might help explain why some types of mutations are found to be segregating within or fixed between species more often than others. Genetic dissection of phenotypic differences within and between species has shown that mutations affecting either the expression or function of a gene product can contribute to phenotypic evolution; mutations that alter gene copy number have also been shown to be an important source of phenotypic variation. Predicting when and why one type of mutation is more likely to underlie a phenotypic change than another remains a pressing challenge for evolution biology. Understanding the relative frequency and properties of different types of mutations will help resolve this issue. To this end, we isolated 231 mutants with altered activity of a focal gene. Mutants were classified into one of four functional classes (i.e., coding, cis-regulatory, trans-acting, or copy number) based on the location and nature of mutation(s), or lack thereof, within the focal gene. Mutant effects on focal gene activity were assessed in both haploid and diploid cells. These data identified differences in the frequency, effects, and dominance (relative to the wild-type allele) among functional classes of mutants that help explain patterns of genetic variation within and between species. Genetic variation within and between species can be shaped by population-level processes and mutation; however, the relative impact of “survival of the fittest” and “arrival of the fittest” on phenotypic evolution remains unclear. Assessing the influence of mutation on evolution requires understanding the relative rates of different types of mutations and their genetic properties, yet little is known about the functional consequences of new mutations. Here, we examine the spectrum of mutations affecting a focal gene in Saccharomyces cerevisiae by characterizing 231 novel haploid genotypes with altered activity of a fluorescent reporter gene. 7% of these genotypes had a nonsynonymous mutation in the coding sequence for the fluorescent protein and were classified as “coding” mutants; 2% had a change in the S. cerevisiae TDH3 promoter sequence controlling expression of the fluorescent protein and were classified as “ cis -regulatory” mutants; 10% contained two copies of the reporter gene and were classified as “copy number” mutants; and the remaining 81% showed altered fluorescence without a change in the reporter gene itself and were classified as “ trans -acting” mutants. As a group, coding mutants had the strongest effect on reporter gene activity and always decreased it. By contrast, 50%–95% of the mutants in each of the other three classes increased gene activity, with mutants affecting copy number and cis -regulatory sequences having larger median effects on gene activity than trans -acting mutants. When made heterozygous in diploid cells, coding, cis -regulatory, and copy number mutant genotypes all had significant effects on gene activity, whereas 88% of the trans -acting mutants appeared to be recessive. These differences in the frequency, effects, and dominance among functional classes of mutations might help explain why some types of mutations are found to be segregating within or fixed between species more often than others. Genetic dissection of phenotypic differences within and between species has shown that mutations affecting either the expression or function of a gene product can contribute to phenotypic evolution; mutations that alter gene copy number have also been shown to be an important source of phenotypic variation. Predicting when and why one type of mutation is more likely to underlie a phenotypic change than another remains a pressing challenge for evolution biology. Understanding the relative frequency and properties of different types of mutations will help resolve this issue. To this end, we isolated 231 mutants with altered activity of a focal gene. Mutants were classified into one of four functional classes (i.e., coding, cis -regulatory, trans -acting, or copy number) based on the location and nature of mutation(s), or lack thereof, within the focal gene. Mutant effects on focal gene activity were assessed in both haploid and diploid cells. These data identified differences in the frequency, effects, and dominance (relative to the wild-type allele) among functional classes of mutants that help explain patterns of genetic variation within and between species. Genetic variation within and between species can be shaped by population-level processes and mutation; however, the relative impact of "survival of the fittest" and "arrival of the fittest" on phenotypic evolution remains unclear. Assessing the influence of mutation on evolution requires understanding the relative rates of different types of mutations and their genetic properties, yet little is known about the functional consequences of new mutations. Here, we examine the spectrum of mutations affecting a focal gene in Saccharomyces cerevisiae by characterizing 231 novel haploid genotypes with altered activity of a fluorescent reporter gene. 7% of these genotypes had a nonsynonymous mutation in the coding sequence for the fluorescent protein and were classified as "coding" mutants; 2% had a change in the S. cerevisiae TDH3 promoter sequence controlling expression of the fluorescent protein and were classified as "cis-regulatory" mutants; 10% contained two copies of the reporter gene and were classified as "copy number" mutants; and the remaining 81% showed altered fluorescence without a change in the reporter gene itself and were classified as "trans-acting" mutants. As a group, coding mutants had the strongest effect on reporter gene activity and always decreased it. By contrast, 50%-95% of the mutants in each of the other three classes increased gene activity, with mutants affecting copy number and cis-regulatory sequences having larger median effects on gene activity than trans-acting mutants. When made heterozygous in diploid cells, coding, cis-regulatory, and copy number mutant genotypes all had significant effects on gene activity, whereas 88% of the trans-acting mutants appeared to be recessive. These differences in the frequency, effects, and dominance among functional classes of mutations might help explain why some types of mutations are found to be segregating within or fixed between species more often than others. |
| Audience | Academic |
| Author | Gruber, Jonathan D. Wittkopp, Patricia J. Kalay, Gizem Vogel, Kara |
| AuthorAffiliation | 2 Department of Molecular, Cellular, and Developmental Biology, University of Michigan, Ann Arbor, Michigan, United States of America 1 Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, Michigan, United States of America University of Washington, United States of America |
| AuthorAffiliation_xml | – name: 2 Department of Molecular, Cellular, and Developmental Biology, University of Michigan, Ann Arbor, Michigan, United States of America – name: 1 Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, Michigan, United States of America – name: University of Washington, United States of America |
| Author_xml | – sequence: 1 givenname: Jonathan D. surname: Gruber fullname: Gruber, Jonathan D. – sequence: 2 givenname: Kara surname: Vogel fullname: Vogel, Kara – sequence: 3 givenname: Gizem surname: Kalay fullname: Kalay, Gizem – sequence: 4 givenname: Patricia J. surname: Wittkopp fullname: Wittkopp, Patricia J. |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/22346762$$D View this record in MEDLINE/PubMed |
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| ContentType | Journal Article |
| Copyright | COPYRIGHT 2012 Public Library of Science 2012 Gruber et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Gruber JD, Vogel K, Kalay G, Wittkopp PJ (2012) Contrasting Properties of Gene-Specific Regulatory, Coding, and Copy Number Mutations in Saccharomyces cerevisiae: Frequency, Effects, and Dominance. PLoS Genet 8(2): e1002497. doi:10.1371/journal.pgen.1002497 Gruber et al. 2012 |
| Copyright_xml | – notice: COPYRIGHT 2012 Public Library of Science – notice: 2012 Gruber et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Gruber JD, Vogel K, Kalay G, Wittkopp PJ (2012) Contrasting Properties of Gene-Specific Regulatory, Coding, and Copy Number Mutations in Saccharomyces cerevisiae: Frequency, Effects, and Dominance. PLoS Genet 8(2): e1002497. doi:10.1371/journal.pgen.1002497 – notice: Gruber et al. 2012 |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 Conceived and designed the experiments: PJW JDG GK. Performed the experiments: JDG KV GK. Analyzed the data: JDG PJW KV GK. Contributed reagents/materials/analysis tools: JDG GK. Wrote the paper: PJW JDG. |
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| SubjectTerms | Biology Brewer's yeast DNA Copy Number Variations - genetics Evolution Evolution, Molecular Gene mutations Genes Genes, Dominant Genes, Recessive Genetic aspects Genetic variation Genetics Genotype Glyceraldehyde-3-Phosphate Dehydrogenase (Phosphorylating) - genetics Haploidy Heterozygote Mutation Mutation - genetics Mutation Rate Open Reading Frames - genetics Physiological aspects Promoter Regions, Genetic Proteins Regulatory Sequences, Nucleic Acid - genetics Saccharomyces cerevisiae Saccharomyces cerevisiae - genetics Saccharomyces cerevisiae Proteins - genetics |
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| Title | Contrasting Properties of Gene-Specific Regulatory, Coding, and Copy Number Mutations in Saccharomyces cerevisiae: Frequency, Effects, and Dominance |
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