An evaluation of high-throughput approaches to QTL mapping in Saccharomyces cerevisiae
Dissecting the molecular basis of quantitative traits is a significant challenge and is essential for understanding complex diseases. Even in model organisms, precisely determining causative genes and their interactions has remained elusive, due in part to difficulty in narrowing intervals to single...
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| Veröffentlicht in: | Genetics (Austin) 2014-03, Vol.196 (3), p.853-865 |
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| creator | Wilkening, Stefan Lin, Gen Fritsch, Emilie S Tekkedil, Manu M Anders, Simon Kuehn, Raquel Nguyen, Michelle Aiyar, Raeka S Proctor, Michael Sakhanenko, Nikita A Galas, David J Gagneur, Julien Deutschbauer, Adam Steinmetz, Lars M |
| description | Dissecting the molecular basis of quantitative traits is a significant challenge and is essential for understanding complex diseases. Even in model organisms, precisely determining causative genes and their interactions has remained elusive, due in part to difficulty in narrowing intervals to single genes and in detecting epistasis or linked quantitative trait loci. These difficulties are exacerbated by limitations in experimental design, such as low numbers of analyzed individuals or of polymorphisms between parental genomes. We address these challenges by applying three independent high-throughput approaches for QTL mapping to map the genetic variants underlying 11 phenotypes in two genetically distant Saccharomyces cerevisiae strains, namely (1) individual analysis of >700 meiotic segregants, (2) bulk segregant analysis, and (3) reciprocal hemizygosity scanning, a new genome-wide method that we developed. We reveal differences in the performance of each approach and, by combining them, identify eight polymorphic genes that affect eight different phenotypes: colony shape, flocculation, growth on two nonfermentable carbon sources, and resistance to two drugs, salt, and high temperature. Our results demonstrate the power of individual segregant analysis to dissect QTL and address the underestimated contribution of interactions between variants. We also reveal confounding factors like mutations and aneuploidy in pooled approaches, providing valuable lessons for future designs of complex trait mapping studies. |
| doi_str_mv | 10.1534/genetics.113.160291 |
| format | Article |
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Even in model organisms, precisely determining causative genes and their interactions has remained elusive, due in part to difficulty in narrowing intervals to single genes and in detecting epistasis or linked quantitative trait loci. These difficulties are exacerbated by limitations in experimental design, such as low numbers of analyzed individuals or of polymorphisms between parental genomes. We address these challenges by applying three independent high-throughput approaches for QTL mapping to map the genetic variants underlying 11 phenotypes in two genetically distant Saccharomyces cerevisiae strains, namely (1) individual analysis of >700 meiotic segregants, (2) bulk segregant analysis, and (3) reciprocal hemizygosity scanning, a new genome-wide method that we developed. We reveal differences in the performance of each approach and, by combining them, identify eight polymorphic genes that affect eight different phenotypes: colony shape, flocculation, growth on two nonfermentable carbon sources, and resistance to two drugs, salt, and high temperature. Our results demonstrate the power of individual segregant analysis to dissect QTL and address the underestimated contribution of interactions between variants. We also reveal confounding factors like mutations and aneuploidy in pooled approaches, providing valuable lessons for future designs of complex trait mapping studies.</description><identifier>ISSN: 1943-2631</identifier><identifier>ISSN: 0016-6731</identifier><identifier>EISSN: 1943-2631</identifier><identifier>DOI: 10.1534/genetics.113.160291</identifier><identifier>PMID: 24374355</identifier><identifier>CODEN: GENTAE</identifier><language>eng</language><publisher>United States: Genetics Society of America</publisher><subject>Aneuploidy ; Chromosome Mapping ; Genetic Variation ; Genetics ; Genome, Fungal ; Genomics - methods ; Genotype & phenotype ; Investigations ; Mutation ; Phenotype ; Polymorphism ; Quantitative Trait Loci ; Saccharomyces cerevisiae ; Saccharomyces cerevisiae - genetics ; Saccharomyces cerevisiae Proteins - genetics ; Yeast</subject><ispartof>Genetics (Austin), 2014-03, Vol.196 (3), p.853-865</ispartof><rights>Copyright Genetics Society of America Mar 2014</rights><rights>Copyright © 2014 by the Genetics Society of America 2014</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c532t-ce088cb91233583d40cf60337c96752d5b5d8aa8b8f3bae25b5270f6a5dea8f63</citedby><cites>FETCH-LOGICAL-c532t-ce088cb91233583d40cf60337c96752d5b5d8aa8b8f3bae25b5270f6a5dea8f63</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,314,776,780,881,27903,27904</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/24374355$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Wilkening, Stefan</creatorcontrib><creatorcontrib>Lin, Gen</creatorcontrib><creatorcontrib>Fritsch, Emilie S</creatorcontrib><creatorcontrib>Tekkedil, Manu M</creatorcontrib><creatorcontrib>Anders, Simon</creatorcontrib><creatorcontrib>Kuehn, Raquel</creatorcontrib><creatorcontrib>Nguyen, Michelle</creatorcontrib><creatorcontrib>Aiyar, Raeka S</creatorcontrib><creatorcontrib>Proctor, Michael</creatorcontrib><creatorcontrib>Sakhanenko, Nikita A</creatorcontrib><creatorcontrib>Galas, David J</creatorcontrib><creatorcontrib>Gagneur, Julien</creatorcontrib><creatorcontrib>Deutschbauer, Adam</creatorcontrib><creatorcontrib>Steinmetz, Lars M</creatorcontrib><title>An evaluation of high-throughput approaches to QTL mapping in Saccharomyces cerevisiae</title><title>Genetics (Austin)</title><addtitle>Genetics</addtitle><description>Dissecting the molecular basis of quantitative traits is a significant challenge and is essential for understanding complex diseases. 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We reveal differences in the performance of each approach and, by combining them, identify eight polymorphic genes that affect eight different phenotypes: colony shape, flocculation, growth on two nonfermentable carbon sources, and resistance to two drugs, salt, and high temperature. Our results demonstrate the power of individual segregant analysis to dissect QTL and address the underestimated contribution of interactions between variants. We also reveal confounding factors like mutations and aneuploidy in pooled approaches, providing valuable lessons for future designs of complex trait mapping studies.</description><subject>Aneuploidy</subject><subject>Chromosome Mapping</subject><subject>Genetic Variation</subject><subject>Genetics</subject><subject>Genome, Fungal</subject><subject>Genomics - methods</subject><subject>Genotype & phenotype</subject><subject>Investigations</subject><subject>Mutation</subject><subject>Phenotype</subject><subject>Polymorphism</subject><subject>Quantitative Trait Loci</subject><subject>Saccharomyces cerevisiae</subject><subject>Saccharomyces cerevisiae - genetics</subject><subject>Saccharomyces cerevisiae Proteins - genetics</subject><subject>Yeast</subject><issn>1943-2631</issn><issn>0016-6731</issn><issn>1943-2631</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2014</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>8G5</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><sourceid>GUQSH</sourceid><sourceid>M2O</sourceid><recordid>eNqNkV2L1TAQhoMo7nr0FwgS8MabHpNMkiY3wrL4BQdEXL0NaZq2WdqkJu2B_fd2ObvL6pVX8_XMMDMvQq8p2VMB_H3vo1-CK3tKYU8lYZo-QedUc6iYBPr0kX-GXpRyTQiRWqjn6IxxqDkIcY5-XUTsj3Zc7RJSxKnDQ-iHahlyWvthXhds5zkn6wZf8JLw96sDnrZUiD0OEf-wzg02p-nGbXXnsz-GEqx_iZ51diz-1Z3doZ-fPl5dfqkO3z5_vbw4VE4AWyrniVKu0ZQBCAUtJ66TBKB2WtaCtaIRrbJWNaqDxnq2xawmnbSi9VZ1Enbow2nuvDaTb52PS7ajmXOYbL4xyQbzdyWGwfTpaEBzpbbH7dC7uwE5_V59WcwUivPjaKNPazFUMK2BKqH_AyWaUyZ5vaFv_0Gv05rj9omNoloyLvUtBSfK5VRK9t3D3pSYW4nNvcRm29ScJN663jw--aHnXlP4AwavpSI</recordid><startdate>20140301</startdate><enddate>20140301</enddate><creator>Wilkening, Stefan</creator><creator>Lin, Gen</creator><creator>Fritsch, Emilie S</creator><creator>Tekkedil, Manu M</creator><creator>Anders, Simon</creator><creator>Kuehn, Raquel</creator><creator>Nguyen, Michelle</creator><creator>Aiyar, Raeka S</creator><creator>Proctor, Michael</creator><creator>Sakhanenko, Nikita A</creator><creator>Galas, David J</creator><creator>Gagneur, Julien</creator><creator>Deutschbauer, Adam</creator><creator>Steinmetz, Lars M</creator><general>Genetics Society of America</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>3V.</scope><scope>4T-</scope><scope>4U-</scope><scope>7QP</scope><scope>7SS</scope><scope>7TK</scope><scope>7TM</scope><scope>7X2</scope><scope>7X7</scope><scope>7XB</scope><scope>88A</scope><scope>88E</scope><scope>88I</scope><scope>8AO</scope><scope>8C1</scope><scope>8FD</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>8G5</scope><scope>ABUWG</scope><scope>AEUYN</scope><scope>AFKRA</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>GUQSH</scope><scope>HCIFZ</scope><scope>K9-</scope><scope>K9.</scope><scope>LK8</scope><scope>M0K</scope><scope>M0R</scope><scope>M0S</scope><scope>M1P</scope><scope>M2O</scope><scope>M2P</scope><scope>M7N</scope><scope>M7P</scope><scope>MBDVC</scope><scope>P64</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>Q9U</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope></search><sort><creationdate>20140301</creationdate><title>An evaluation of high-throughput approaches to QTL mapping in Saccharomyces cerevisiae</title><author>Wilkening, Stefan ; Lin, Gen ; Fritsch, Emilie S ; Tekkedil, Manu M ; Anders, Simon ; Kuehn, Raquel ; Nguyen, Michelle ; Aiyar, Raeka S ; Proctor, Michael ; Sakhanenko, Nikita A ; Galas, David J ; Gagneur, Julien ; Deutschbauer, Adam ; Steinmetz, Lars M</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c532t-ce088cb91233583d40cf60337c96752d5b5d8aa8b8f3bae25b5270f6a5dea8f63</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2014</creationdate><topic>Aneuploidy</topic><topic>Chromosome Mapping</topic><topic>Genetic Variation</topic><topic>Genetics</topic><topic>Genome, Fungal</topic><topic>Genomics - 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Even in model organisms, precisely determining causative genes and their interactions has remained elusive, due in part to difficulty in narrowing intervals to single genes and in detecting epistasis or linked quantitative trait loci. These difficulties are exacerbated by limitations in experimental design, such as low numbers of analyzed individuals or of polymorphisms between parental genomes. We address these challenges by applying three independent high-throughput approaches for QTL mapping to map the genetic variants underlying 11 phenotypes in two genetically distant Saccharomyces cerevisiae strains, namely (1) individual analysis of >700 meiotic segregants, (2) bulk segregant analysis, and (3) reciprocal hemizygosity scanning, a new genome-wide method that we developed. 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| subjects | Aneuploidy Chromosome Mapping Genetic Variation Genetics Genome, Fungal Genomics - methods Genotype & phenotype Investigations Mutation Phenotype Polymorphism Quantitative Trait Loci Saccharomyces cerevisiae Saccharomyces cerevisiae - genetics Saccharomyces cerevisiae Proteins - genetics Yeast |
| title | An evaluation of high-throughput approaches to QTL mapping in Saccharomyces cerevisiae |
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