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,...

Ausführliche Beschreibung

Gespeichert in:
Bibliographische Detailangaben
Veröffentlicht in:Molecular ecology 2015-11, Vol.24 (21), p.5412-5427
Hauptverfasser: 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
Format: Artikel
Sprache:eng
Schlagworte:
Online-Zugang:Volltext
Tags: Tag hinzufügen
Keine Tags, Fügen Sie den ersten Tag hinzu!
container_end_page 5427
container_issue 21
container_start_page 5412
container_title Molecular ecology
container_volume 24
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
format Article
fullrecord <record><control><sourceid>proquest_hal_p</sourceid><recordid>TN_cdi_hal_primary_oai_HAL_hal_01837756v1</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><sourcerecordid>3849129191</sourcerecordid><originalsourceid>FETCH-LOGICAL-c5281-719a5be17f406b81e4fdd40e4fa73903d50c0d7d32fb1359c4a77c26ebcb02cc3</originalsourceid><addsrcrecordid>eNqNkUtv1DAUhS0EotPCgj-ALLGhi7S-dmwny-moT01hw6PqxnIcZ8YliQc7aZl_j6fTDhISEt4cyfruuefqIPQOyBGkd9xZcwSM5fACTYAJntEyv3mJJqQUNANSsD20H-MdIcAo56_RHhU0LwgRE3QzxSu_Gls9ON_jhe1950zEro9usRySDh4PS4uvbe0GG4Lure6xD26REOwb_OB6i9dWxwHXvrNxcObR6w161eg22rdPeoC-np1-mV1k88_nl7PpPDOcFpBJKDWvLMgmJ6IqwOZNXeckiZasJKzmxJBa1ow2FTBemlxLaaiwlakINYYdoMOt71K3ahVcp8Naee3UxXSuNn8ECiYlF_eQ2I9bdhX8zzFlVZ2LxrZtusqPUYFMG6gohPgPlBZCihw26Ie_0Ds_hj4dvaGkZJSR_E9OE3yMwTa7sEDUpkWVWlSPLSb2_ZPjWHW23pHPtSXgeAs8uNau_-2krk9nz5bZdsLFwf7aTejwQwnJJFffP50reVLcXgG_Vd_Yb0ZUs-0</addsrcrecordid><sourcetype>Open Access Repository</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>1727732304</pqid></control><display><type>article</type><title>A population genomics insight into the Mediterranean origins of wine yeast domestication</title><source>MEDLINE</source><source>Wiley Online Library Journals Frontfile Complete</source><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</creator><creatorcontrib>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</creatorcontrib><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><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 &amp; Sons Ltd</rights><rights>2015 John Wiley &amp; Sons Ltd.</rights><rights>Copyright © 2015 John Wiley &amp; 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>
fulltext fulltext
identifier ISSN: 0962-1083
ispartof Molecular ecology, 2015-11, Vol.24 (21), p.5412-5427
issn 0962-1083
1365-294X
language eng
recordid cdi_hal_primary_oai_HAL_hal_01837756v1
source MEDLINE; Wiley Online Library Journals Frontfile Complete
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
url https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-01-29T14%3A24%3A14IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-proquest_hal_p&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=A%20population%20genomics%20insight%20into%20the%20Mediterranean%20origins%20of%20wine%20yeast%20domestication&rft.jtitle=Molecular%20ecology&rft.au=Almeida,%20Pedro&rft.date=2015-11&rft.volume=24&rft.issue=21&rft.spage=5412&rft.epage=5427&rft.pages=5412-5427&rft.issn=0962-1083&rft.eissn=1365-294X&rft_id=info:doi/10.1111/mec.13341&rft_dat=%3Cproquest_hal_p%3E3849129191%3C/proquest_hal_p%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=1727732304&rft_id=info:pmid/26248006&rfr_iscdi=true