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Title: Ecological and genetic barriers differentiate natural populations of Saccharomyces cerevisiae

Journal Article · · Molecular Biology and Evolution
 [1];  [1];  [2];  [3];  [4]
  1. Univ. of Wisconsin, Madison, WI (United States). Lab. of Genetics
  2. Great Lakes Bioenergy Research Center, Madison, WI (United States)
  3. Univ. of Wisconsin, Madison, WI (United States). Lab. of Genetics; Univ. of Georgia, Athens, GA (United States)
  4. Univ. of Wisconsin, Madison, WI (United States). Lab. of Genetics; Great Lakes Bioenergy Research Center, Madison, WI (United States)

How populations that inhabit the same geographical area become genetically differentiated is not clear. To investigate this, we characterized phenotypic and genetic differences between two populations of Saccharomyces cerevisiae that in some cases inhabit the same environment but show relatively little gene flow. We profiled stress sensitivity in a group of vineyard isolates and a group of oak-soil strains and found several niche-related phenotypes that distinguish the populations. We performed bulk-segregant mapping on two of the distinguishing traits: The vineyard-specific ability to grow in grape juice and oak-specific tolerance to the cell wall damaging drug Congo red. To implicate causal genes, we also performed a chemical genomic screen in the lab-strain deletion collection and identified many important genes that fell under quantitative trait loci peaks. One gene important for growth in grape juice and identified by both the mapping and the screen was SSU1, a sulfite-nitrite pump implicated in wine fermentations. The beneficial allele is generated by a known translocation that we reasoned may also serve as a genetic barrier. We found that the translocation is prevalent in vineyard strains, but absent in oak strains, and presents a postzygotic barrier to spore viability. Furthermore, the translocation was associated with a fitness cost to the rapid growth rate seen in oak-soil strains. Lastly, our results reveal the translocation as a dual-function locus that enforces ecological differentiation while producing a genetic barrier to gene flow in these sympatric populations.

Research Organization:
Univ. of Wisconsin, Madison, WI (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Biological and Environmental Research (BER); National Inst. of Health (NIH) (United States)
Contributing Organization:
Great Lakes Bioenergy Research Center, Madison, WI (United States)
Grant/Contract Number:
FC02-07ER64494; T32HG002760; T32GM007133-36; T32GM007133-39
OSTI ID:
1343407
Journal Information:
Molecular Biology and Evolution, Vol. 32, Issue 9; ISSN 0737-4038
Publisher:
Oxford University PressCopyright Statement
Country of Publication:
United States
Language:
English
Citation Metrics:
Cited by: 23 works
Citation information provided by
Web of Science

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Cited By (15)

Genome-wide association across Saccharomyces cerevisiae strains reveals substantial variation in underlying gene requirements for toxin tolerance journal February 2018
Patterns of Genetic Diversity and the Invasion of Commercial Starters in Saccharomyces cerevisiae Vineyard Populations of Santorini Island journal May 2020
Whole Genome Comparison Reveals High Levels of Inbreeding and Strain Redundancy Across the Spectrum of Commercial Wine Strains of Saccharomyces cerevisiae journal February 2016
Identification of the fitness determinants of budding yeast on a natural substrate journal December 2016
The genomics of wild yeast populations sheds light on the domestication of man's best (micro) friend journal October 2015
Adaptive divergence in wine yeasts and their wild relatives suggests a prominent role for introgressions and rapid evolution at noncoding sites journal March 2017
A new chromosomal rearrangement improves the adaptation of wine yeasts to sulfite journal March 2019
The SSU1 checkup, a rapid tool for detecting chromosomal rearrangements of the Saccharomyces cerevisiae chromosome XVI. An ecological and technological study on wine yeast posted_content April 2020
A unique ecological niche fosters hybridization of oak-tree and vineyard isolates of Saccharomyces cerevisiae journal November 2015
Overcoming lignocellulose‐derived microbial inhibitors: advancing the Saccharomyces cerevisiae resistance toolbox journal August 2019
Dominance of wine Saccharomyces cerevisiae strains over S. kudriavzevii in industrial fermentation competitions is related to an acceleration of nutrient uptake and utilization journal March 2019
Population genomics of yeasts: towards a comprehensive view across a broad evolutionary scale: Insights into yeast population genomics journal January 2016
Evolutionary biology through the lens of budding yeast comparative genomics journal July 2017
Fertility depression among cheese-making Penicillium roqueforti strains suggests degeneration during domestication: CHEESY DEGENERATION journal August 2016
Comparative transcriptome assembly and genome-guided profiling for Brettanomyces bruxellensis LAMAP2480 during p-coumaric acid stress journal September 2016