A population genomics insight into the Mediterranean origins of wine yeast domestication

Pedro Almeida, Raquel Barbosa, Polona Zalar, Yumi Imanishi, Kiminori Shimizu, Benedetta Turchetti, Jean Luc Legras, Marta Serra, Sylvie Dequin, Arnaud Couloux, Julie Guy, Douda Bensasson, Paula Gonçalves, José Paulo Sampaio

Research output: Contribution to journalArticle

71 Citations (Scopus)

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.

Original languageEnglish
Pages (from-to)5412-5427
Number of pages16
JournalMolecular Ecology
Volume24
Issue number21
DOIs
Publication statusPublished - Nov 2015

Fingerprint

wine yeasts
Metagenomics
domestication
Wine
yeast
genomics
Yeasts
wines
Quercus
Population
Saccharomyces cerevisiae
viticulture
wild relatives
winemaking
Domestication
wine
Population Growth
population growth
population structure
Dermatoglyphics

Keywords

  • comparative genomics
  • domestication fingerprints
  • microbe domestication
  • microbe population genomics
  • yeast molecular ecology

Cite this

Almeida, P., Barbosa, R., Zalar, P., Imanishi, Y., Shimizu, K., Turchetti, B., ... Sampaio, J. P. (2015). A population genomics insight into the Mediterranean origins of wine yeast domestication. Molecular Ecology, 24(21), 5412-5427. https://doi.org/10.1111/mec.13341
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. / A population genomics insight into the Mediterranean origins of wine yeast domestication. In: Molecular Ecology. 2015 ; Vol. 24, No. 21. pp. 5412-5427.
@article{4645f83c5a054b47bcad02b3f70086b5,
title = "A population genomics insight into the Mediterranean origins of wine yeast domestication",
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.",
keywords = "comparative genomics, domestication fingerprints, microbe domestication, microbe population genomics, yeast molecular ecology",
author = "Pedro Almeida and Raquel Barbosa and Polona Zalar and Yumi Imanishi and Kiminori Shimizu and Benedetta Turchetti and Legras, {Jean Luc} and Marta Serra and Sylvie Dequin and Arnaud Couloux and Julie Guy and Douda Bensasson and Paula Gon{\cc}alves and Sampaio, {Jos{\'e} Paulo}",
note = "Sem PDF. FCT Portugal (PTDC/BIA-EVF/118618/2010; PTDC/AGR-ALI/118590/2010 UID/Multi/04378/2013; SFRH/BD/77390/2011) Natural Environment Research Council UK (NE/D008824/1)",
year = "2015",
month = "11",
doi = "10.1111/mec.13341",
language = "English",
volume = "24",
pages = "5412--5427",
journal = "Molecular Ecology",
issn = "0962-1083",
publisher = "Blackwell Publishing Ltd",
number = "21",

}

Almeida, P, Barbosa, R, Zalar, P, Imanishi, Y, Shimizu, K, Turchetti, B, Legras, JL, Serra, M, Dequin, S, Couloux, A, Guy, J, Bensasson, D, Gonçalves, P & Sampaio, JP 2015, 'A population genomics insight into the Mediterranean origins of wine yeast domestication', Molecular Ecology, vol. 24, no. 21, pp. 5412-5427. https://doi.org/10.1111/mec.13341

A population genomics insight into the Mediterranean origins of wine yeast domestication. / 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.

In: Molecular Ecology, Vol. 24, No. 21, 11.2015, p. 5412-5427.

Research output: Contribution to journalArticle

TY - JOUR

T1 - A population genomics insight into the Mediterranean origins of wine yeast domestication

AU - Almeida, Pedro

AU - Barbosa, Raquel

AU - Zalar, Polona

AU - Imanishi, Yumi

AU - Shimizu, Kiminori

AU - Turchetti, Benedetta

AU - Legras, Jean Luc

AU - Serra, Marta

AU - Dequin, Sylvie

AU - Couloux, Arnaud

AU - Guy, Julie

AU - Bensasson, Douda

AU - Gonçalves, Paula

AU - Sampaio, José Paulo

N1 - Sem PDF. FCT Portugal (PTDC/BIA-EVF/118618/2010; PTDC/AGR-ALI/118590/2010 UID/Multi/04378/2013; SFRH/BD/77390/2011) Natural Environment Research Council UK (NE/D008824/1)

PY - 2015/11

Y1 - 2015/11

N2 - 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.

AB - 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.

KW - comparative genomics

KW - domestication fingerprints

KW - microbe domestication

KW - microbe population genomics

KW - yeast molecular ecology

UR - http://www.scopus.com/inward/record.url?scp=84945452256&partnerID=8YFLogxK

U2 - 10.1111/mec.13341

DO - 10.1111/mec.13341

M3 - Article

VL - 24

SP - 5412

EP - 5427

JO - Molecular Ecology

JF - Molecular Ecology

SN - 0962-1083

IS - 21

ER -

Almeida P, Barbosa R, Zalar P, Imanishi Y, Shimizu K, Turchetti B et al. A population genomics insight into the Mediterranean origins of wine yeast domestication. Molecular Ecology. 2015 Nov;24(21):5412-5427. https://doi.org/10.1111/mec.13341