The genetic basis of natural variation in oenological traits in Saccharomyces cerevisiae

PLoS One. 2012;7(11):e49640. doi: 10.1371/journal.pone.0049640. Epub 2012 Nov 21.

Abstract

Saccharomyces cerevisiae is the main microorganism responsible for wine alcoholic fermentation. The oenological phenotypes resulting from fermentation, such as the production of acetic acid, glycerol, and residual sugar concentration are regulated by multiple genes and vary quantitatively between different strain backgrounds. With the aim of identifying the quantitative trait loci (QTLs) that regulate oenological phenotypes, we performed linkage analysis using three crosses between highly diverged S. cerevisiae strains. Segregants from each cross were used as starter cultures for 20-day fermentations, in synthetic wine must, to simulate actual winemaking conditions. Linkage analysis on phenotypes of primary industrial importance resulted in the mapping of 18 QTLs. We tested 18 candidate genes, by reciprocal hemizygosity, for their contribution to the observed phenotypic variation, and validated five genes and the chromosome II right subtelomeric region. We observed that genes involved in mitochondrial metabolism, sugar transport, nitrogen metabolism, and the uncharacterized ORF YJR030W explained most of the phenotypic variation in oenological traits. Furthermore, we experimentally validated an exceptionally strong epistatic interaction resulting in high level of succinic acid between the Sake FLX1 allele and the Wine/European MDH2 allele. Overall, our work demonstrates the complex genetic basis underlying wine traits, including natural allelic variation, antagonistic linked QTLs and complex epistatic interactions between alleles from strains with different evolutionary histories.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Acetic Acid / metabolism
  • Alcoholic Beverages
  • Alleles
  • Epistasis, Genetic
  • Evolution, Molecular
  • Fermentation
  • Food Microbiology
  • Genes, Fungal
  • Genetic Linkage
  • Genetic Variation
  • Glycerol / metabolism
  • Models, Genetic
  • Open Reading Frames
  • Phenotype
  • Quantitative Trait Loci
  • Saccharomyces cerevisiae / genetics*
  • Saccharomyces cerevisiae / physiology*
  • Wine*

Substances

  • Glycerol
  • Acetic Acid

Grant support

This work was supported by CNRS and ATIP-Avenir, Biological Sciences Research Council (BBF0152161), FONDECYT 1100509, MECESUP UCH 0604, Becas Chile, Apoyo tesis doctoral AT-24100036 and CONICYT. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.