A population genomics insight into the Mediterranean origins of wine yeast domestication
2015
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 | Unidade de Ciencias Biomoleculares Aplicadas (UCIBIO) ; Requimte ; Universidade do Porto = University of Porto-Departamento de Química (DQ) ; Faculdade de Ciências e Tecnologia = School of Science & Technology (FCT NOVA) ; Universidade Nova de Lisboa = NOVA University Lisbon (NOVA)-Universidade Nova de Lisboa = NOVA University Lisbon (NOVA)-Faculdade de Ciências e Tecnologia = School of Science & Technology (FCT NOVA) ; Universidade Nova de Lisboa = NOVA University Lisbon (NOVA)-Universidade Nova de Lisboa = NOVA University Lisbon (NOVA)-Universidade do Porto = University of Porto-Departamento de Química (DQ) ; Faculdade de Ciências e Tecnologia = School of Science & Technology (FCT NOVA) ; Universidade Nova de Lisboa = NOVA University Lisbon (NOVA)-Universidade Nova de Lisboa = NOVA University Lisbon (NOVA)-Faculdade de Ciências e Tecnologia = School of Science & Technology (FCT NOVA) ; Universidade Nova de Lisboa = NOVA University Lisbon (NOVA)-Universidade Nova de Lisboa = NOVA University Lisbon (NOVA) | Department of Biology, Biotechnical Faculty ; University of Ljubljana | Department of Applied Material and Life Science, College of Engineering ; Kanto Gakuin University | Medical Mycology Research Center ; Chiba University | Dipartimento di Scienze Agrarie, Alimentari e Ambientali & Industrial Yeasts Collection DBVPG ; Università degli Studi di Perugia = University of Perugia (UNIPG) | Università degli Studi di Perugia = University of Perugia (UNIPG) | Sciences Pour l'Oenologie (SPO) ; Université Montpellier 1 (UM1)-Institut National de la Recherche Agronomique (INRA)-Université de Montpellier (UM)-Institut national d’études supérieures agronomiques de Montpellier (Montpellier SupAgro) | Genoscope - Centre national de séquençage [Evry] (GENOSCOPE) ; Université Paris-Saclay-Direction de Recherche Fondamentale (CEA) (DRF (CEA)) ; Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA) | Faculty of Life Sciences ; Bar-Ilan University [Israël] | 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]
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.
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