Adaptive divergence in wine yeasts and their wild relatives suggests a prominent role for introgressions and rapid evolution at noncoding sites

Pedro Almeida, Raquel Barbosa, Douda Bensasson, Paula Gonçalves, José Paulo Sampaio

Research output: Contribution to journalArticle

16 Citations (Scopus)

Abstract

In Saccharomyces cerevisiae, the main yeast in wine fermentation, the opportunity to examine divergence at the molecular level between a domesticated lineage and its wild counterpart arose recently due to the identification of the closest relatives of wine strains, a wild population associated with Mediterranean oaks. As genomic data are available for a considerable number of representatives belonging to both groups, we used population genomics to estimate the degree and distribution of nucleotide variation between wine yeasts and their closest wild relatives. We found widespread genomewide divergence, particularly at noncoding sites, which, together with above average divergence in trans-acting DNA binding proteins, may suggest an important role for divergence at the level of transcriptional regulation. Nine outlier regions putatively under strong divergent selection were highlighted by a genomewide scan under stringent conditions. Several cases of introgressions, originating in the sibling species Saccharomyces paradoxus, were also identified in the Mediterranean oak population. FZF1 and SSU1, mostly known for conferring sulphite resistance in wine yeasts, were among the introgressed genes, although not fixed. Because the introgressions detected in our study are not found in wine strains, we hypothesize that ongoing divergent ecological selection segregates the two forms between the different niches. Together, our results provide a first insight into the extent and kind of divergence between wine yeasts and their closest wild relatives.

Original languageEnglish
Pages (from-to)2167-2182
Number of pages16
JournalMolecular Ecology
Volume26
Issue number7
DOIs
Publication statusPublished - Apr 2017

Fingerprint

wine yeasts
adaptive radiation
wild relatives
introgression
Wine
yeast
Yeasts
divergence
wines
Quercus
DNA-binding proteins
Saccharomyces
sulfites
genomics
sibling species
Metagenomics
Saccharomyces cerevisiae
Sulfites
niches
nucleotides

Keywords

  • comparative population genomics
  • divergent selection
  • introgression
  • microbe adaptive evolution
  • Saccharomyces cerevisiae
  • wine yeast domestication

Cite this

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title = "Adaptive divergence in wine yeasts and their wild relatives suggests a prominent role for introgressions and rapid evolution at noncoding sites",
abstract = "In Saccharomyces cerevisiae, the main yeast in wine fermentation, the opportunity to examine divergence at the molecular level between a domesticated lineage and its wild counterpart arose recently due to the identification of the closest relatives of wine strains, a wild population associated with Mediterranean oaks. As genomic data are available for a considerable number of representatives belonging to both groups, we used population genomics to estimate the degree and distribution of nucleotide variation between wine yeasts and their closest wild relatives. We found widespread genomewide divergence, particularly at noncoding sites, which, together with above average divergence in trans-acting DNA binding proteins, may suggest an important role for divergence at the level of transcriptional regulation. Nine outlier regions putatively under strong divergent selection were highlighted by a genomewide scan under stringent conditions. Several cases of introgressions, originating in the sibling species Saccharomyces paradoxus, were also identified in the Mediterranean oak population. FZF1 and SSU1, mostly known for conferring sulphite resistance in wine yeasts, were among the introgressed genes, although not fixed. Because the introgressions detected in our study are not found in wine strains, we hypothesize that ongoing divergent ecological selection segregates the two forms between the different niches. Together, our results provide a first insight into the extent and kind of divergence between wine yeasts and their closest wild relatives.",
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AU - Gonçalves, Paula

AU - Sampaio, José Paulo

N1 - Sem PDF. Fundacao para a Ciencia e a Tecnologia, Portugal (PTDC/BIA-EVF/118618/2010; PTDC/AGR-ALI/118590/2010; UID/Multi/04378/2013; SFRH/BD/77390/2011)

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N2 - In Saccharomyces cerevisiae, the main yeast in wine fermentation, the opportunity to examine divergence at the molecular level between a domesticated lineage and its wild counterpart arose recently due to the identification of the closest relatives of wine strains, a wild population associated with Mediterranean oaks. As genomic data are available for a considerable number of representatives belonging to both groups, we used population genomics to estimate the degree and distribution of nucleotide variation between wine yeasts and their closest wild relatives. We found widespread genomewide divergence, particularly at noncoding sites, which, together with above average divergence in trans-acting DNA binding proteins, may suggest an important role for divergence at the level of transcriptional regulation. Nine outlier regions putatively under strong divergent selection were highlighted by a genomewide scan under stringent conditions. Several cases of introgressions, originating in the sibling species Saccharomyces paradoxus, were also identified in the Mediterranean oak population. FZF1 and SSU1, mostly known for conferring sulphite resistance in wine yeasts, were among the introgressed genes, although not fixed. Because the introgressions detected in our study are not found in wine strains, we hypothesize that ongoing divergent ecological selection segregates the two forms between the different niches. Together, our results provide a first insight into the extent and kind of divergence between wine yeasts and their closest wild relatives.

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