A new dominant peroxiredoxin allele identified by whole-genome re-sequencing of random mutagenized yeast causes oxidant-resistance and premature aging
The combination of functional genomics with next generation sequencing facilitates new experimental strategies for addressing complex biological phenomena. Here, we report the identification of a gain-of-function allele of peroxiredoxin (thioredoxin peroxidase, Tsa1p) via whole-genome re-sequencing...
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Published in | Aging (Albany, NY.) Vol. 2; no. 8; pp. 475 - 486 |
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Main Authors | , , , , , , , , , , , |
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Abstract | The combination of functional genomics with next generation sequencing facilitates new experimental strategies for addressing complex biological phenomena. Here, we report the identification of a gain-of-function allele of peroxiredoxin (thioredoxin peroxidase, Tsa1p) via whole-genome re-sequencing of a dominantSaccharomyces cerevisiae mutant obtained by chemical mutagenesis. Yeast strain K6001, a screening system for lifespan phenotypes, was treated with ethyl methanesulfonate (EMS). We isolated an oxidative stress-resistant mutant (B7) which transmitted this phenotype in a background-independent, monogenic and dominant way. By massive parallel pyrosequencing, we generated an 38.8 fold whole-genome coverage of the strains, which differed in 12,482 positions from the reference (S288c) genome. Via a subtraction strategy, we could narrow this number to 13 total and 4 missense nucleotide variations that were specific for the mutant. Via expression in wild type backgrounds, we show that one of these mutations, exchanging a residue in the peroxiredoxin Tsa1p, was responsible for the mutant phenotype causing background-independent dominant oxidative stress-resistance. These effects were not provoked by altered Tsa1p levels, nor could they be simulated by deletion, haploinsufficiency or over-expression of the wild-type allele. Furthermore, via both a mother-enrichment technique and a micromanipulation assay, we found a robust premature aging phenotype of this oxidant-resistant strain. Thus, TSA1-B7 encodes for a novel dominant form of peroxiredoxin, and establishes a new connection between oxidative stress and aging. In addition, this study shows that the re-sequencing of entire genomes is becoming a promising alternative for the identification of functional alleles in approaches of classic molecular genetics. |
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AbstractList | The
combination of functional genomics with next generation sequencing
facilitates new experimental strategies for addressing complex biological
phenomena. Here, we report the identification of a gain-of-function allele
of peroxiredoxin (thioredoxin peroxidase, Tsa1p) via whole-genome
re-sequencing of a dominantSaccharomyces cerevisiae mutant obtained
by chemical mutagenesis. Yeast strain K6001, a screening system for
lifespan phenotypes, was treated with ethyl methanesulfonate (EMS). We
isolated an oxidative stress-resistant mutant (B7) which transmitted this
phenotype in a background-independent, monogenic and dominant way. By
massive parallel pyrosequencing, we generated an 38.8 fold whole-genome
coverage of the strains, which differed in 12,482 positions from the
reference (S288c) genome. Via a subtraction strategy, we could narrow this
number to 13 total and 4 missense nucleotide variations that were specific for
the mutant. Via expression in wild type backgrounds, we show that one of
these mutations, exchanging a residue in the peroxiredoxin Tsa1p, was
responsible for the mutant phenotype causing background-independent
dominant oxidative stress-resistance. These effects were not provoked by
altered Tsa1p levels, nor could they be simulated by deletion,
haploinsufficiency or over-expression of the wild-type allele. Furthermore,
via both a mother-enrichment technique and a micromanipulation assay, we
found a robust premature aging phenotype of this oxidant-resistant strain.
Thus, TSA1-B7 encodes for a novel dominant form of peroxiredoxin,
and establishes a new connection between oxidative stress and aging. In
addition, this study shows that the re-sequencing of entire genomes is
becoming a promising alternative for the identification of functional
alleles in approaches of classic molecular genetics. The combination of functional genomics with next generation sequencing facilitates new experimental strategies for addressing complex biological phenomena. Here, we report the identification of a gain-of-function allele of peroxiredoxin (thioredoxin peroxidase, Tsa1p) via whole-genome re-sequencing of a dominantSaccharomyces cerevisiae mutant obtained by chemical mutagenesis. Yeast strain K6001, a screening system for lifespan phenotypes, was treated with ethyl methanesulfonate (EMS). We isolated an oxidative stress-resistant mutant (B7) which transmitted this phenotype in a background-independent, monogenic and dominant way. By massive parallel pyrosequencing, we generated an 38.8 fold whole-genome coverage of the strains, which differed in 12,482 positions from the reference (S288c) genome. Via a subtraction strategy, we could narrow this number to 13 total and 4 missense nucleotide variations that were specific for the mutant. Via expression in wild type backgrounds, we show that one of these mutations, exchanging a residue in the peroxiredoxin Tsa1p, was responsible for the mutant phenotype causing background-independent dominant oxidative stress-resistance. These effects were not provoked by altered Tsa1p levels, nor could they be simulated by deletion, haploinsufficiency or over-expression of the wild-type allele. Furthermore, via both a mother-enrichment technique and a micromanipulation assay, we found a robust premature aging phenotype of this oxidant-resistant strain. Thus, TSA1-B7 encodes for a novel dominant form of peroxiredoxin, and establishes a new connection between oxidative stress and aging. In addition, this study shows that the re-sequencing of entire genomes is becoming a promising alternative for the identification of functional alleles in approaches of classic molecular genetics. |
Author | Bluemlein, Katharina Jarolim, Stefanie Grillari, Johannes Russmayer, Hannes Michel, Steve Breitenbach, Michael Kerick, Martin Krüger, Antje Lehrach, Hans Timmermann, Bernd Laun, Peter Ralser, Markus |
AuthorAffiliation | 2 Department of Cell Biology, University of Salzburg, 5020 Salzburg, Austria These authors contributed equally to this work 3 Department of Vertebrate Genomics, Max Planck Institute for Molecular Genetics, 14195 Berlin, Germany 4 Institute of Applied Microbiology, University of Natural Resources and Applied Life Sciences, 1180 Vienna, Austria 1 Next Generation Sequencing Group, Max Planck Institute for Molecular Genetics, 14195 Berlin, Germany |
AuthorAffiliation_xml | – name: 3 Department of Vertebrate Genomics, Max Planck Institute for Molecular Genetics, 14195 Berlin, Germany – name: 1 Next Generation Sequencing Group, Max Planck Institute for Molecular Genetics, 14195 Berlin, Germany – name: 4 Institute of Applied Microbiology, University of Natural Resources and Applied Life Sciences, 1180 Vienna, Austria – name: 2 Department of Cell Biology, University of Salzburg, 5020 Salzburg, Austria – name: These authors contributed equally to this work |
Author_xml | – sequence: 1 givenname: Bernd surname: Timmermann fullname: Timmermann, Bernd organization: Next Generation Sequencing Group, Max Planck Institute for Molecular Genetics, 14195 Berlin, Germany – sequence: 2 givenname: Stefanie surname: Jarolim fullname: Jarolim, Stefanie – sequence: 3 givenname: Hannes surname: Russmayer fullname: Russmayer, Hannes – sequence: 4 givenname: Martin surname: Kerick fullname: Kerick, Martin – sequence: 5 givenname: Steve surname: Michel fullname: Michel, Steve – sequence: 6 givenname: Antje surname: Krüger fullname: Krüger, Antje – sequence: 7 givenname: Katharina surname: Bluemlein fullname: Bluemlein, Katharina – sequence: 8 givenname: Peter surname: Laun fullname: Laun, Peter – sequence: 9 givenname: Johannes surname: Grillari fullname: Grillari, Johannes – sequence: 10 givenname: Hans surname: Lehrach fullname: Lehrach, Hans – sequence: 11 givenname: Michael surname: Breitenbach fullname: Breitenbach, Michael – sequence: 12 givenname: Markus surname: Ralser fullname: Ralser, Markus |
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Cites_doi | 10.18632/aging.100040 10.1186/1756-0500-1-19 10.18632/aging.100104 10.1186/jbiol61 10.1093/nar/29.9.e45 10.1016/j.femsyr.2004.06.015 10.1016/j.arr.2007.03.002 10.18632/aging.100065 10.1093/geronj/11.3.298 10.4161/cc.7.21.6965 10.18632/aging.100133 10.18632/aging.100017 10.1371/journal.pgen.1000303 10.1016/j.cmet.2007.08.011 |
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SubjectTerms | Alleles Animals Base Sequence Benzene Derivatives - toxicity Cell Proliferation Ethyl Methanesulfonate - toxicity Gene Expression Genome, Fungal Haploinsufficiency Mutagenesis Mutagens - toxicity Oxidants - toxicity Oxidative Stress - genetics Peroxidases - genetics Phenotype Saccharomyces cerevisiae - genetics Saccharomyces cerevisiae - growth & development Saccharomyces cerevisiae Proteins - genetics Sequence Analysis Sequence Analysis, DNA |
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Title | A new dominant peroxiredoxin allele identified by whole-genome re-sequencing of random mutagenized yeast causes oxidant-resistance and premature aging |
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