Mapping genetic variants underlying differences in the central nitrogen metabolism in fermenter yeasts

PLoS One. 2014 Jan 21;9(1):e86533. doi: 10.1371/journal.pone.0086533. eCollection 2014.

Abstract

Different populations within a species represent a rich reservoir of allelic variants, corresponding to an evolutionary signature of withstood environmental constraints. Saccharomyces cerevisiae strains are widely utilised in the fermentation of different kinds of alcoholic beverages, such as, wine and sake, each of them derived from must with distinct nutrient composition. Importantly, adequate nitrogen levels in the medium are essential for the fermentation process, however, a comprehensive understanding of the genetic variants determining variation in nitrogen consumption is lacking. Here, we assessed the genetic factors underlying variation in nitrogen consumption in a segregating population derived from a cross between two main fermenter yeasts, a Wine/European and a Sake isolate. By linkage analysis we identified 18 main effect QTLs for ammonium and amino acids sources. Interestingly, majority of QTLs were involved in more than a single trait, grouped based on amino acid structure and indicating high levels of pleiotropy across nitrogen sources, in agreement with the observed patterns of phenotypic co-variation. Accordingly, we performed reciprocal hemizygosity analysis validating an effect for three genes, GLT1, ASI1 and AGP1. Furthermore, we detected a widespread pleiotropic effect on these genes, with AGP1 affecting seven amino acids and nine in the case of GLT1 and ASI1. Based on sequence and comparative analysis, candidate causative mutations within these genes were also predicted. Altogether, the identification of these variants demonstrate how Sake and Wine/European genetic backgrounds differentially consume nitrogen sources, in part explaining independently evolved preferences for nitrogen assimilation and representing a niche of genetic diversity for the implementation of practical approaches towards more efficient strains for nitrogen metabolism.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Alcoholic Beverages / microbiology
  • Alleles
  • Amino Acid Transport Systems, Neutral / genetics
  • Amino Acid Transport Systems, Neutral / metabolism
  • Amino Acids / genetics
  • Amino Acids / metabolism
  • Ammonium Compounds / metabolism
  • Fermentation / genetics*
  • Genetic Linkage / genetics
  • Genetic Variation / genetics*
  • Membrane Proteins / genetics
  • Membrane Proteins / metabolism
  • Nitrogen / metabolism*
  • Quantitative Trait Loci / genetics
  • Saccharomyces cerevisiae / genetics*
  • Saccharomyces cerevisiae / metabolism
  • Saccharomyces cerevisiae Proteins / genetics
  • Saccharomyces cerevisiae Proteins / metabolism
  • Wine / microbiology

Substances

  • AGP1 protein, S cerevisiae
  • ASI1 protein, S cerevisiae
  • Amino Acid Transport Systems, Neutral
  • Amino Acids
  • Ammonium Compounds
  • Membrane Proteins
  • Saccharomyces cerevisiae Proteins
  • Nitrogen

Grant support

This work was funded by grants from ATIP-Avenir, ARC (SFI20111203947) to GL and FONDECYT 1100509 to CM. FAC is supported by Conicyt (Apoyo al retorno de investigadores desde el extranjero grant number 82130010). VG is supported by FONDECYT Post-Doctoral 3120107. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.