A population genomics insight into the Mediterranean origins of wine yeast domestication
The domestication of the wine yeast Saccharomyces cerevisiae is thought to be contemporary with the development and expansion of viticulture along the Mediterranean basin. Until now, the unavailability of wild lineages prevented the identification of the closest wild relatives of wine yeasts. Here,...
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Veröffentlicht in: | Molecular ecology 2015-11, Vol.24 (21), p.5412-5427 |
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creator | Almeida, Pedro Barbosa, Raquel Zalar, Polona Imanishi, Yumi Shimizu, Kiminori Turchetti, Benedetta Legras, Jean-Luc Serra, Marta Dequin, Sylvie Couloux, Arnaud Guy, Julie Bensasson, Douda Gonçalves, Paula Sampaio, José Paulo |
description | The domestication of the wine yeast Saccharomyces cerevisiae is thought to be contemporary with the development and expansion of viticulture along the Mediterranean basin. Until now, the unavailability of wild lineages prevented the identification of the closest wild relatives of wine yeasts. Here, we enlarge the collection of natural lineages and employ whole‐genome data of oak‐associated wild isolates to study a balanced number of anthropic and natural S. cerevisiae strains. We identified industrial variants and new geographically delimited populations, including a novel Mediterranean oak population. This population is the closest relative of the wine lineage as shown by a weak population structure and further supported by genomewide population analyses. A coalescent model considering partial isolation with asymmetrical migration, mostly from the wild group into the Wine group, and population growth, was found to be best supported by the data. Importantly, divergence time estimates between the two populations agree with historical evidence for winemaking. We show that three horizontally transmitted regions, previously described to contain genes relevant to wine fermentation, are present in the Wine group but not in the Mediterranean oak group. This represents a major discontinuity between the two populations and is likely to denote a domestication fingerprint in wine yeasts. Taken together, these results indicate that Mediterranean oaks harbour the wild genetic stock of domesticated wine yeasts.
See also the Perspective by Eberlein, Leducq and Landry |
doi_str_mv | 10.1111/mec.13341 |
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See also the Perspective by Eberlein, Leducq and Landry</description><identifier>ISSN: 0962-1083</identifier><identifier>EISSN: 1365-294X</identifier><identifier>DOI: 10.1111/mec.13341</identifier><identifier>PMID: 26248006</identifier><language>eng</language><publisher>England: Blackwell Publishing Ltd</publisher><subject>Agricultural sciences ; comparative genomics ; DNA, Fungal - genetics ; DNA, Ribosomal Spacer - genetics ; domestication fingerprints ; Europe ; Evolution, Molecular ; Genetic Variation ; Genetics, Population ; Genome, Fungal ; Life Sciences ; Mediterranean Region ; microbe domestication ; microbe population genomics ; Microsatellite Repeats ; Models, Genetic ; Phylogeny ; Polymorphism, Single Nucleotide ; Quercus - microbiology ; Saccharomyces cerevisiae ; Saccharomyces cerevisiae - genetics ; Sequence Analysis, DNA ; Vegetal Biology ; Vitaceae ; Wine - microbiology ; yeast molecular ecology</subject><ispartof>Molecular ecology, 2015-11, Vol.24 (21), p.5412-5427</ispartof><rights>2015 John Wiley & Sons Ltd</rights><rights>2015 John Wiley & Sons Ltd.</rights><rights>Copyright © 2015 John Wiley & Sons Ltd</rights><rights>Distributed under a Creative Commons Attribution 4.0 International License</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c5281-719a5be17f406b81e4fdd40e4fa73903d50c0d7d32fb1359c4a77c26ebcb02cc3</citedby><cites>FETCH-LOGICAL-c5281-719a5be17f406b81e4fdd40e4fa73903d50c0d7d32fb1359c4a77c26ebcb02cc3</cites><orcidid>0000-0002-4006-4389 ; 0000-0002-9114-2324</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1111%2Fmec.13341$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2Fmec.13341$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>230,314,776,780,881,1411,27901,27902,45550,45551</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/26248006$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://hal.science/hal-01837756$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Almeida, Pedro</creatorcontrib><creatorcontrib>Barbosa, Raquel</creatorcontrib><creatorcontrib>Zalar, Polona</creatorcontrib><creatorcontrib>Imanishi, Yumi</creatorcontrib><creatorcontrib>Shimizu, Kiminori</creatorcontrib><creatorcontrib>Turchetti, Benedetta</creatorcontrib><creatorcontrib>Legras, Jean-Luc</creatorcontrib><creatorcontrib>Serra, Marta</creatorcontrib><creatorcontrib>Dequin, Sylvie</creatorcontrib><creatorcontrib>Couloux, Arnaud</creatorcontrib><creatorcontrib>Guy, Julie</creatorcontrib><creatorcontrib>Bensasson, Douda</creatorcontrib><creatorcontrib>Gonçalves, Paula</creatorcontrib><creatorcontrib>Sampaio, José Paulo</creatorcontrib><title>A population genomics insight into the Mediterranean origins of wine yeast domestication</title><title>Molecular ecology</title><addtitle>Mol Ecol</addtitle><description>The domestication of the wine yeast Saccharomyces cerevisiae is thought to be contemporary with the development and expansion of viticulture along the Mediterranean basin. Until now, the unavailability of wild lineages prevented the identification of the closest wild relatives of wine yeasts. Here, we enlarge the collection of natural lineages and employ whole‐genome data of oak‐associated wild isolates to study a balanced number of anthropic and natural S. cerevisiae strains. We identified industrial variants and new geographically delimited populations, including a novel Mediterranean oak population. This population is the closest relative of the wine lineage as shown by a weak population structure and further supported by genomewide population analyses. A coalescent model considering partial isolation with asymmetrical migration, mostly from the wild group into the Wine group, and population growth, was found to be best supported by the data. Importantly, divergence time estimates between the two populations agree with historical evidence for winemaking. We show that three horizontally transmitted regions, previously described to contain genes relevant to wine fermentation, are present in the Wine group but not in the Mediterranean oak group. This represents a major discontinuity between the two populations and is likely to denote a domestication fingerprint in wine yeasts. Taken together, these results indicate that Mediterranean oaks harbour the wild genetic stock of domesticated wine yeasts.
See also the Perspective by Eberlein, Leducq and Landry</description><subject>Agricultural sciences</subject><subject>comparative genomics</subject><subject>DNA, Fungal - genetics</subject><subject>DNA, Ribosomal Spacer - genetics</subject><subject>domestication fingerprints</subject><subject>Europe</subject><subject>Evolution, Molecular</subject><subject>Genetic Variation</subject><subject>Genetics, Population</subject><subject>Genome, Fungal</subject><subject>Life Sciences</subject><subject>Mediterranean Region</subject><subject>microbe domestication</subject><subject>microbe population genomics</subject><subject>Microsatellite Repeats</subject><subject>Models, Genetic</subject><subject>Phylogeny</subject><subject>Polymorphism, Single Nucleotide</subject><subject>Quercus - microbiology</subject><subject>Saccharomyces cerevisiae</subject><subject>Saccharomyces cerevisiae - genetics</subject><subject>Sequence Analysis, DNA</subject><subject>Vegetal Biology</subject><subject>Vitaceae</subject><subject>Wine - microbiology</subject><subject>yeast molecular ecology</subject><issn>0962-1083</issn><issn>1365-294X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2015</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqNkUtv1DAUhS0EotPCgj-ALLGhi7S-dmwny-moT01hw6PqxnIcZ8YliQc7aZl_j6fTDhISEt4cyfruuefqIPQOyBGkd9xZcwSM5fACTYAJntEyv3mJJqQUNANSsD20H-MdIcAo56_RHhU0LwgRE3QzxSu_Gls9ON_jhe1950zEro9usRySDh4PS4uvbe0GG4Lure6xD26REOwb_OB6i9dWxwHXvrNxcObR6w161eg22rdPeoC-np1-mV1k88_nl7PpPDOcFpBJKDWvLMgmJ6IqwOZNXeckiZasJKzmxJBa1ow2FTBemlxLaaiwlakINYYdoMOt71K3ahVcp8Naee3UxXSuNn8ECiYlF_eQ2I9bdhX8zzFlVZ2LxrZtusqPUYFMG6gohPgPlBZCihw26Ie_0Ds_hj4dvaGkZJSR_E9OE3yMwTa7sEDUpkWVWlSPLSb2_ZPjWHW23pHPtSXgeAs8uNau_-2krk9nz5bZdsLFwf7aTejwQwnJJFffP50reVLcXgG_Vd_Yb0ZUs-0</recordid><startdate>201511</startdate><enddate>201511</enddate><creator>Almeida, Pedro</creator><creator>Barbosa, Raquel</creator><creator>Zalar, Polona</creator><creator>Imanishi, Yumi</creator><creator>Shimizu, Kiminori</creator><creator>Turchetti, Benedetta</creator><creator>Legras, Jean-Luc</creator><creator>Serra, Marta</creator><creator>Dequin, Sylvie</creator><creator>Couloux, Arnaud</creator><creator>Guy, Julie</creator><creator>Bensasson, Douda</creator><creator>Gonçalves, Paula</creator><creator>Sampaio, José Paulo</creator><general>Blackwell Publishing Ltd</general><general>Wiley</general><scope>BSCLL</scope><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>7SN</scope><scope>7SS</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>1XC</scope><orcidid>https://orcid.org/0000-0002-4006-4389</orcidid><orcidid>https://orcid.org/0000-0002-9114-2324</orcidid></search><sort><creationdate>201511</creationdate><title>A population genomics insight into the Mediterranean origins of wine yeast domestication</title><author>Almeida, Pedro ; Barbosa, Raquel ; Zalar, Polona ; Imanishi, Yumi ; Shimizu, Kiminori ; Turchetti, Benedetta ; Legras, Jean-Luc ; Serra, Marta ; Dequin, Sylvie ; Couloux, Arnaud ; Guy, Julie ; Bensasson, Douda ; Gonçalves, Paula ; Sampaio, José Paulo</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c5281-719a5be17f406b81e4fdd40e4fa73903d50c0d7d32fb1359c4a77c26ebcb02cc3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2015</creationdate><topic>Agricultural sciences</topic><topic>comparative genomics</topic><topic>DNA, Fungal - genetics</topic><topic>DNA, Ribosomal Spacer - genetics</topic><topic>domestication fingerprints</topic><topic>Europe</topic><topic>Evolution, Molecular</topic><topic>Genetic Variation</topic><topic>Genetics, Population</topic><topic>Genome, Fungal</topic><topic>Life Sciences</topic><topic>Mediterranean Region</topic><topic>microbe domestication</topic><topic>microbe population genomics</topic><topic>Microsatellite Repeats</topic><topic>Models, Genetic</topic><topic>Phylogeny</topic><topic>Polymorphism, Single Nucleotide</topic><topic>Quercus - microbiology</topic><topic>Saccharomyces cerevisiae</topic><topic>Saccharomyces cerevisiae - genetics</topic><topic>Sequence Analysis, DNA</topic><topic>Vegetal Biology</topic><topic>Vitaceae</topic><topic>Wine - microbiology</topic><topic>yeast molecular ecology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Almeida, Pedro</creatorcontrib><creatorcontrib>Barbosa, Raquel</creatorcontrib><creatorcontrib>Zalar, Polona</creatorcontrib><creatorcontrib>Imanishi, Yumi</creatorcontrib><creatorcontrib>Shimizu, Kiminori</creatorcontrib><creatorcontrib>Turchetti, Benedetta</creatorcontrib><creatorcontrib>Legras, Jean-Luc</creatorcontrib><creatorcontrib>Serra, Marta</creatorcontrib><creatorcontrib>Dequin, Sylvie</creatorcontrib><creatorcontrib>Couloux, Arnaud</creatorcontrib><creatorcontrib>Guy, Julie</creatorcontrib><creatorcontrib>Bensasson, Douda</creatorcontrib><creatorcontrib>Gonçalves, Paula</creatorcontrib><creatorcontrib>Sampaio, José Paulo</creatorcontrib><collection>Istex</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>Hyper Article en Ligne (HAL)</collection><jtitle>Molecular ecology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Almeida, Pedro</au><au>Barbosa, Raquel</au><au>Zalar, Polona</au><au>Imanishi, Yumi</au><au>Shimizu, Kiminori</au><au>Turchetti, Benedetta</au><au>Legras, Jean-Luc</au><au>Serra, Marta</au><au>Dequin, Sylvie</au><au>Couloux, Arnaud</au><au>Guy, Julie</au><au>Bensasson, Douda</au><au>Gonçalves, Paula</au><au>Sampaio, José Paulo</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>A population genomics insight into the Mediterranean origins of wine yeast domestication</atitle><jtitle>Molecular ecology</jtitle><addtitle>Mol Ecol</addtitle><date>2015-11</date><risdate>2015</risdate><volume>24</volume><issue>21</issue><spage>5412</spage><epage>5427</epage><pages>5412-5427</pages><issn>0962-1083</issn><eissn>1365-294X</eissn><abstract>The domestication of the wine yeast Saccharomyces cerevisiae is thought to be contemporary with the development and expansion of viticulture along the Mediterranean basin. Until now, the unavailability of wild lineages prevented the identification of the closest wild relatives of wine yeasts. Here, we enlarge the collection of natural lineages and employ whole‐genome data of oak‐associated wild isolates to study a balanced number of anthropic and natural S. cerevisiae strains. We identified industrial variants and new geographically delimited populations, including a novel Mediterranean oak population. This population is the closest relative of the wine lineage as shown by a weak population structure and further supported by genomewide population analyses. A coalescent model considering partial isolation with asymmetrical migration, mostly from the wild group into the Wine group, and population growth, was found to be best supported by the data. Importantly, divergence time estimates between the two populations agree with historical evidence for winemaking. We show that three horizontally transmitted regions, previously described to contain genes relevant to wine fermentation, are present in the Wine group but not in the Mediterranean oak group. This represents a major discontinuity between the two populations and is likely to denote a domestication fingerprint in wine yeasts. Taken together, these results indicate that Mediterranean oaks harbour the wild genetic stock of domesticated wine yeasts.
See also the Perspective by Eberlein, Leducq and Landry</abstract><cop>England</cop><pub>Blackwell Publishing Ltd</pub><pmid>26248006</pmid><doi>10.1111/mec.13341</doi><tpages>16</tpages><orcidid>https://orcid.org/0000-0002-4006-4389</orcidid><orcidid>https://orcid.org/0000-0002-9114-2324</orcidid></addata></record> |
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subjects | Agricultural sciences comparative genomics DNA, Fungal - genetics DNA, Ribosomal Spacer - genetics domestication fingerprints Europe Evolution, Molecular Genetic Variation Genetics, Population Genome, Fungal Life Sciences Mediterranean Region microbe domestication microbe population genomics Microsatellite Repeats Models, Genetic Phylogeny Polymorphism, Single Nucleotide Quercus - microbiology Saccharomyces cerevisiae Saccharomyces cerevisiae - genetics Sequence Analysis, DNA Vegetal Biology Vitaceae Wine - microbiology yeast molecular ecology |
title | A population genomics insight into the Mediterranean origins of wine yeast domestication |
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