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Tracking alternative versions of the galactose gene network in the genus Saccharomyces and their expansion after domestication

Journal Article · · iScience
 [1];  [2];  [3];  [4];  [5];  [6];  [2];  [7];  [3];  [8];  [9];  [2];  [2]
  1. Nova School of Science and Technology, Caparica (Portugal); Universidade Nova de Lisboa
  2. Nova School of Science and Technology, Caparica (Portugal)
  3. Academia Sinica, Taipei (Taiwan)
  4. Kasetsart University, Bangkok (Thailand); Biodiversity Center Kasetsart University, Bangkok (Thailand)
  5. National Science and Technology, Development Agency (NSTDA), Pathum Thani (Thailand)
  6. University of Copenhagen (Denmark)
  7. Universidade Federal de Minas Gerais (Brazil)
  8. Vanderbilt University, Nashville, TN (United States)
  9. University of Wisconsin-Madison, WI (United States)

When Saccharomyces cerevisiae grows on mixtures of glucose and galactose, galactose utilization is repressed by glucose, and induction of the GAL gene network only occurs when glucose is exhausted. Contrary to reference GAL alleles, alternative alleles support faster growth on galactose, thus enabling distinct galactose utilization strategies maintained by balancing selection. Here, we report on new wild populations of Saccharomyces cerevisiae harboring alternative GAL versions and, for the first time, of Saccharomyces paradoxus alternative alleles. We also show that the non-functional GAL version found earlier in Saccharomyces kudriavzevii is phylogenetically related to the alternative versions, which constitutes a case of trans-specific maintenance of highly divergent alleles. Strains harboring the different GAL network variants show different levels of alleviation of glucose repression and growth proficiency on galactose. We propose that domestication involved specialization toward thriving in milk from a generalist ancestor partially adapted to galactose consumption in the plant niche.

Research Organization:
Great Lakes Bioenergy Research Center (GLBRC), Madison, WI (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Biological and Environmental Research (BER); National Science Foundation (NSF); Fundação para a Ciência e a Tecnologia (Portugal)
Grant/Contract Number:
SC0018409
OSTI ID:
2370517
Journal Information:
iScience, Journal Name: iScience Journal Issue: 2 Vol. 27; ISSN 2589-0042
Publisher:
ElsevierCopyright Statement
Country of Publication:
United States
Language:
English

References (65)

Composition of plant tissues and soil organic matter in the first stages of a vegetation succession journal March 2001
Feasting, fasting and fermenting: glucose sensing in yeast and other cells journal January 1999
Sugar and polyol compositions of some European olive fruit varieties (Olea europaea L.) suitable for table olive purposes journal March 2001
Trade-offs journal January 2014
Reverse Evolution of a Classic Gene Network in Yeast Offers a Competitive Advantage journal April 2019
Origin of Lactose Fermentation in Kluyveromyces lactis by Interspecies Transfer of a Neo-functionalized Gene Cluster during Domestication journal December 2019
Domestication of the Emblematic White Cheese-Making Fungus Penicillium camemberti and Its Diversification into Two Varieties journal November 2020
A comparative analysis of the genetic switch between not-so-distant cousins: versus journal December 2005
The Genomics of Human Local Adaptation journal June 2020
Gas chromatographic analysis of sugars and sugar-alcohols in the mesocarp, endocarp, and kernel of almond fruit journal September 1984
Strategies for cellular decision‐making journal January 2009
Remarkably ancient balanced polymorphisms in a multi-locus gene network journal February 2010
Polygenic evolution of a sugar specialization trade-off in yeast journal February 2016
Multiple recent horizontal transfers of a large genomic region in cheese making fungi journal January 2014
A Gondwanan imprint on global diversity and domestication of wine and cider yeast Saccharomyces uvarum journal June 2014
Evolution of gene network activity by tuning the strength of negative-feedback regulation journal February 2015
A framework for variation discovery and genotyping using next-generation DNA sequencing data journal April 2011
Carbon catabolite repression in bacteria: many ways to make the most out of nutrients journal August 2008
Explaining microbial genomic diversity in light of evolutionary ecology journal March 2014
The origin and adaptive evolution of domesticated populations of yeast from Far East Asia journal July 2018
Macroevolutionary diversity of traits and genomes in the model yeast genus Saccharomyces journal February 2023
Genome evolution across 1,011 Saccharomyces cerevisiae isolates journal April 2018
A yeast living ancestor reveals the origin of genomic introgressions journal November 2020
An experimental test of evolutionary trade-offs during temperature adaptation journal May 2007
Microbe domestication and the identification of the wild genetic stock of lager-brewing yeast journal August 2011
Galactose metabolic genes in yeast respond to a ratio of galactose and glucose journal January 2015
An Approximately Unbiased Test of Phylogenetic Tree Selection journal May 2002
The Early Process of Mammal Domestication in the Near East journal October 2011
SPAdes: A New Genome Assembly Algorithm and Its Applications to Single-Cell Sequencing journal May 2012
Liftoff: accurate mapping of gene annotations journal May 2021
VariScan: Analysis of evolutionary patterns from large-scale DNA sequence polymorphism data journal April 2005
Fast and accurate short read alignment with Burrows-Wheeler transform journal May 2009
Unipro UGENE: a unified bioinformatics toolkit journal February 2012
Trimmomatic: a flexible trimmer for Illumina sequence data journal April 2014
Glucose repression in Saccharomyces cerevisiae journal July 2015
Evidence of Natural Hybridization in Brazilian Wild Lineages of Saccharomyces cerevisiae journal January 2016
PAML 4: Phylogenetic Analysis by Maximum Likelihood journal April 2007
MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability journal January 2013
IQ-TREE: A Fast and Effective Stochastic Algorithm for Estimating Maximum-Likelihood Phylogenies journal November 2014
Adaptation of S. cerevisiae to Fermented Food Environments Reveals Remarkable Genome Plasticity and the Footprints of Domestication journal May 2018
Repeated Cis-Regulatory Tuning of a Metabolic Bottleneck Gene during Evolution journal May 2018
Interactive Tree Of Life (iTOL) v5: an online tool for phylogenetic tree display and annotation journal April 2021
YEASTRACT+: a portal for cross-species comparative genomics of transcription regulation in yeasts journal October 2019
Catabolite Repression journal January 1961
Microbial domestication signatures of Lactococcus lactis can be reproduced by experimental evolution journal November 2011
Surprisingly diverged populations of Saccharomyces cerevisiae in natural environments remote from human activity journal August 2012
Conceptual issues in local adaptation journal December 2004
Multidimensional Optimality of Microbial Metabolism journal May 2012
Ancient balancing selection maintains incompatible versions of the galactose pathway in yeast journal January 2021
Decoupling transcription factor expression and activity enables dimmer switch gene regulation journal April 2021
Genome-Scale Genotype-Phenotype Matching of Two Lactococcus lactis Isolates from Plants Identifies Mechanisms of Adaptation to the Plant Niche journal January 2008
Improvement of Galactose Uptake in Saccharomyces cerevisiae through Overexpression of Phosphoglucomutase: Example of Transcript Analysis as a Tool in Inverse Metabolic Engineering journal November 2005
Yeast Carbon Catabolite Repression journal June 1998
Growthcurver: an R package for obtaining interpretable metrics from microbial growth curves journal April 2016
OrthoFinder: phylogenetic orthology inference for comparative genomics journal November 2019
Adaptation, Plasticity, and Extinction in a Changing Environment: Towards a Predictive Theory journal April 2010
Different Levels of Catabolite Repression Optimize Growth in Stable and Variable Environments journal January 2014
Natural Variation in Preparation for Nutrient Depletion Reveals a Cost–Benefit Tradeoff journal January 2015
Trait Variation in Yeast Is Defined by Population History journal June 2011
Nutritional Control of Growth and Development in Yeast journal September 2012
A New System for Comparative Functional Genomics of Saccharomyces Yeasts journal July 2013
Adaptive Gene Content and Allele Distribution Variations in the Wild and Domesticated Populations of Saccharomyces cerevisiae journal February 2021
Significance of galactinol and raffinose family oligosaccharide synthesis in plants journal August 2015
Raffinose Family Oligosaccharides Act As Galactose Stores in Seeds and Are Required for Rapid Germination of Arabidopsis in the Dark journal July 2016
Revisiting the Taxonomic Synonyms and Populations of Saccharomyces cerevisiae—Phylogeny, Phenotypes, Ecology and Domestication journal June 2020

Figures / Tables (5)