A unique ecological niche fosters hybridization of oak-tree and vineyard isolates of Saccharomyces cerevisiae

Clowers, Katie J.; Will, Jessica L.; Gasch, Audrey P.

doi:10.1111/mec.13439

Title: A unique ecological niche fosters hybridization of oak-tree and vineyard isolates of Saccharomyces cerevisiae

Journal Article · Mon Nov 30 00:00:00 EST 2015 · Molecular Ecology

DOI:https://doi.org/10.1111/mec.13439· OSTI ID:1466771

Clowers, Katie J. ^[1]; Will, Jessica L. ^[1]; Gasch, Audrey P. ^[2]

Univ. of Wisconsin, Madison, WI (United States). Laboratory of Genetics
Univ. of Wisconsin, Madison, WI (United States). Laboratory of Genetics; Great Lakes Bioenergy Research Center, Madison, WI (United States)

We report that differential adaptation to distinct niches can restrict gene flow and promote population differentiation within a species. However, in some cases the distinction between niches can collapse, forming a hybrid niche with features of both environments. We previously reported that distinctions between vineyards and oak soil present an ecological barrier that restricts gene flow between lineages of Saccharomyces cerevisiae. Vineyard isolates are tolerant to stresses associated with grapes while North American oak strains are particularly tolerant to freeze–thaw cycles. Here, we report the isolation of S. cerevisiae strains from Wisconsin cherry trees, which display features common to vineyards (e.g. high sugar concentrations) and frequent freeze–thaw cycles. Genome sequencing revealed that the isolated strains are highly heterozygous and represent recent hybrids of the oak × vineyard lineages. We found that the hybrid strains are phenotypically similar to vineyard strains for some traits, but are more similar to oak strains for other traits. The cherry strains were exceptionally good at growing in cherry juice, raising the possibility that they have adapted to this niche. We performed transcriptome profiling in cherry, oak and vineyard strains and show that the cherry-tree hybrids display vineyard-like or oak-like expression, depending on the gene sets, and in some cases, the expression patterns linked back to shared stress tolerances. Allele-specific expression in these natural hybrids suggested concerted cis-regulatory evolution at sets of functionally regulated genes. In conclusion, our results raise the possibility that hybridization of the two lineages provides a genetic solution to the thriving in this unique niche.

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Research Organization:: Univ. of Wisconsin, Madison, WI (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: FC02-07ER64494

OSTI ID:: 1466771

Journal Information:: Molecular Ecology, Vol. 24, Issue 23; ISSN 0962-1083

Publisher:: WileyCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 8 works

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References (72)

MBASED: allele-specific expression detection in cancer tissues and cell lines Mayba, Oleg; Gilbert, Houston N.; Liu, Jinfeng Genome Biology, Vol. 15, Issue 8 https://doi.org/10.1186/s13059-014-0405-3	journal	August 2014
The Statistics of Bulk Segregant Analysis Using Next Generation Sequencing Magwene, Paul M.; Willis, John H.; Kelly, John K. PLoS Computational Biology, Vol. 7, Issue 11 https://doi.org/10.1371/journal.pcbi.1002255	journal	November 2011
Hybridization as an Evolutionary Stimulus Anderson, E.; Stebbins, G. L. Evolution, Vol. 8, Issue 4 https://doi.org/10.2307/2405784	journal	December 1954
Hybridization may facilitate in situ survival of endemic species through periods of climate change Becker, Matthias; Gruenheit, Nicole; Steel, Mike Nature Climate Change, Vol. 3, Issue 12 https://doi.org/10.1038/nclimate2027	journal	November 2013
Hypervariable Noncoding Sequences in Saccharomyces cerevisiae Fay, Justin C.; Benavides, Joseph A. Genetics, Vol. 170, Issue 4 https://doi.org/10.1534/genetics.105.042283	journal	June 2005
Hybridization as a Source of Variation for Adaptation to New Environments Lewontin, R. C.; Birch, L. C. Evolution, Vol. 20, Issue 3 https://doi.org/10.2307/2406633	journal	September 1966
Open source clustering software de Hoon, M. J. L.; Imoto, S.; Nolan, J. Bioinformatics, Vol. 20, Issue 9 https://doi.org/10.1093/bioinformatics/bth078	journal	February 2004
Isolation by environment Wang, Ian J.; Bradburd, Gideon S. Molecular Ecology, Vol. 23, Issue 23 https://doi.org/10.1111/mec.12938	journal	October 2014
Climate change and evolutionary adaptation Hoffmann, Ary A.; Sgrò, Carla M. Nature, Vol. 470, Issue 7335 https://doi.org/10.1038/nature09670	journal	February 2011
Saccharomyces cerevisiae: Population Divergence and Resistance to Oxidative Stress in Clinical, Domesticated and Wild Isolates Diezmann, Stephanie; Dietrich, Fred S. PLoS ONE, Vol. 4, Issue 4 https://doi.org/10.1371/journal.pone.0005317	journal	April 2009
Genetic analysis of Saccharomyces cerevisiae strains isolated from palm wine in eastern Nigeria. Comparison with other African strains Ezeronye, O. U.; Legras, J. -L. Journal of Applied Microbiology, Vol. 106, Issue 5 https://doi.org/10.1111/j.1365-2672.2008.04118.x	journal	May 2009
PLINK: A Tool Set for Whole-Genome Association and Population-Based Linkage Analyses Purcell, Shaun; Neale, Benjamin; Todd-Brown, Kathe The American Journal of Human Genetics, Vol. 81, Issue 3 https://doi.org/10.1086/519795	journal	September 2007
Variations in Stress Sensitivity and Genomic Expression in Diverse S. cerevisiae Isolates Kvitek, Daniel J.; Will, Jessica L.; Gasch, Audrey P. PLoS Genetics, Vol. 4, Issue 10 https://doi.org/10.1371/journal.pgen.1000223	journal	October 2008
A powerful and flexible statistical framework for testing hypotheses of allele-specific gene expression from RNA-seq data Skelly, D. A.; Johansson, M.; Madeoy, J. Genome Research, Vol. 21, Issue 10 https://doi.org/10.1101/gr.119784.110	journal	August 2011
Trimmomatic: a flexible trimmer for Illumina sequence data Bolger, Anthony M.; Lohse, Marc; Usadel, Bjoern Bioinformatics, Vol. 30, Issue 15 https://doi.org/10.1093/bioinformatics/btu170	journal	April 2014
Systematic screening of nuclear encoded proteins involved in the splicing metabolism of group II introns in yeast mitochondria Luban, Cornelia; Beutel, Melanie; Stahl, Ulf Gene, Vol. 354 https://doi.org/10.1016/j.gene.2005.03.023	journal	July 2005
Aquaporins in Saccharomyces: Characterization of a second functional water channel protein Carbrey, J. M.; Bonhivers, M.; Boeke, J. D. Proceedings of the National Academy of Sciences, Vol. 98, Issue 3 https://doi.org/10.1073/pnas.98.3.1000	journal	January 2001
Reproductive isolation caused by visual predation on migrants between divergent environments Nosil, Patrik Proceedings of the Royal Society of London. Series B: Biological Sciences, Vol. 271, Issue 1547 https://doi.org/10.1098/rspb.2004.2751	journal	July 2004
Genome-wide deletion mutant analysis reveals genes required for respiratory growth, mitochondrial genome maintenance and mitochondrial protein synthesis in Saccharomyces cerevisiae Merz, Sandra; Westermann, Benedikt Genome Biology, Vol. 10, Issue 9 https://doi.org/10.1186/gb-2009-10-9-r95	journal	January 2009
Evolution and Variation of the Yeast (Saccharomyces) Genome Mortimer, R. K. Genome Research, Vol. 10, Issue 4 https://doi.org/10.1101/gr.10.4.403	journal	April 2000
QTL Dissection of Lag Phase in Wine Fermentation Reveals a New Translocation Responsible for Saccharomyces cerevisiae Adaptation to Sulfite Zimmer, Adrien; Durand, Cécile; Loira, Nicolás PLoS ONE, Vol. 9, Issue 1 https://doi.org/10.1371/journal.pone.0086298	journal	January 2014
Identifying the Environmental Factors That Determine the Genetic Structure of Populations Foll, Matthieu; Gaggiotti, Oscar Genetics, Vol. 174, Issue 2 https://doi.org/10.1534/genetics.106.059451	journal	September 2006
Small- and Large-Effect Quantitative Trait Locus Interactions Underlie Variation in Yeast Sporulation Efficiency Lorenz, Kim; Cohen, Barak A. Genetics, Vol. 192, Issue 3 https://doi.org/10.1534/genetics.112.143107	journal	August 2012
Natural Populations of Saccharomyces kudriavzevii in Portugal Are Associated with Oak Bark and Are Sympatric with S. cerevisiae and S. paradoxus Sampaio, J. P.; Goncalves, P. Applied and Environmental Microbiology, Vol. 74, Issue 7 https://doi.org/10.1128/AEM.02396-07	journal	February 2008
Genomic Sequence Diversity and Population Structure of Saccharomyces cerevisiae Assessed by RAD-seq Cromie, Gareth A.; Hyma, Katie E.; Ludlow, Catherine L. G3: Genes\|Genomes\|Genetics, Vol. 3, Issue 12 https://doi.org/10.1534/g3.113.007492	journal	October 2013
Outcrossing, mitotic recombination, and life-history trade-offs shape genome evolution in Saccharomyces cerevisiae Magwene, Paul M.; Kayıkçı, Ömür; Granek, Joshua A. Proceedings of the National Academy of Sciences, Vol. 108, Issue 5 https://doi.org/10.1073/pnas.1012544108	journal	January 2011
Genetic Isolation by Environment or Distance: Which Pattern of gene flow is most Common?: Special Section Sexton, Jason P.; Hangartner, Sandra B.; Hoffmann, Ary A. Evolution, Vol. 68, Issue 1 https://doi.org/10.1111/evo.12258	journal	September 2013
Transfer and Origin of Adaptations through Natural Hybridization: Were Anderson and Stebbins Right? Arnold, Michael L. The Plant Cell, Vol. 16, Issue 3 https://doi.org/10.1105/tpc.160370	journal	March 2004
Fast and accurate long-read alignment with Burrows–Wheeler transform Li, Heng; Durbin, Richard Bioinformatics, Vol. 26, Issue 5 https://doi.org/10.1093/bioinformatics/btp698	journal	January 2010
Two Alleles of the Sulfite Resistance Genes Are Differentially Regulated in Saccharomyces cerevisiae Yuasa, Noriyuki; Nakagawa, Youji; Hayakawa, Masayuki Bioscience, Biotechnology, and Biochemistry, Vol. 69, Issue 8 https://doi.org/10.1271/bbb.69.1584	journal	January 2005
Bread, beer and wine: Yeast domestication in the Saccharomyces sensu stricto complex Sicard, Delphine; Legras, Jean-Luc Comptes Rendus Biologies, Vol. 334, Issue 3 https://doi.org/10.1016/j.crvi.2010.12.016	journal	March 2011
Ecological and Genetic Barriers Differentiate Natural Populations of Saccharomyces cerevisiae Clowers, Katie J.; Heilberger, Justin; Piotrowski, Jeff S. Molecular Biology and Evolution, Vol. 32, Issue 9 https://doi.org/10.1093/molbev/msv112	journal	May 2015
Population genomics of domestic and wild yeasts Liti, Gianni; Carter, David M.; Moses, Alan M. Nature, Vol. 458, Issue 7236 https://doi.org/10.1038/nature07743	journal	February 2009
Trait Variation in Yeast Is Defined by Population History Warringer, Jonas; Zörgö, Enikö; Cubillos, Francisco A. PLoS Genetics, Vol. 7, Issue 6 https://doi.org/10.1371/journal.pgen.1002111	journal	June 2011
Incipient Balancing Selection through Adaptive Loss of Aquaporins in Natural Saccharomyces cerevisiae Populations Will, Jessica L.; Kim, Hyun Seok; Clarke, Jessica PLoS Genetics, Vol. 6, Issue 4 https://doi.org/10.1371/journal.pgen.1000893	journal	April 2010
A framework for variation discovery and genotyping using next-generation DNA sequencing data DePristo, Mark A.; Banks, Eric; Poplin, Ryan Nature Genetics, Vol. 43, Issue 5 https://doi.org/10.1038/ng.806	journal	April 2011
Genetic Basis of Mitochondrial Function and Morphology in Saccharomyces cerevisiae Dimmer, Kai Stefan; Fritz, Stefan; Fuchs, Florian Molecular Biology of the Cell, Vol. 13, Issue 3 https://doi.org/10.1091/mbc.01-12-0588	journal	March 2002
Differential adaptation to multi-stressed conditions of wine fermentation revealed by variations in yeast regulatory networks Brion, Christian; Ambroset, Chloé; Sanchez, Isabelle BMC Genomics, Vol. 14, Issue 1 https://doi.org/10.1186/1471-2164-14-681	journal	January 2013
adegenet 1.3-1: new tools for the analysis of genome-wide SNP data Jombart, Thibaut; Ahmed, Ismaïl Bioinformatics, Vol. 27, Issue 21 https://doi.org/10.1093/bioinformatics/btr521	journal	September 2011
<i>Saccharomyces paradoxus</i> and <i>Saccharomyces cerevisiae</i> are associated with exudates of North American oaks Naumov, Gennadi I.; Naumova, Elena S.; Sniegowski, Paul D. Canadian Journal of Microbiology, Vol. 44, Issue 11 https://doi.org/10.1139/cjm-44-11-1045	journal	January 1998
edgeR: a Bioconductor package for differential expression analysis of digital gene expression data Robinson, M. D.; McCarthy, D. J.; Smyth, G. K. Bioinformatics, Vol. 26, Issue 1 https://doi.org/10.1093/bioinformatics/btp616	journal	November 2009
The 100-genomes strains, an S. cerevisiae resource that illuminates its natural phenotypic and genotypic variation and emergence as an opportunistic pathogen Strope, Pooja K.; Skelly, Daniel A.; Kozmin, Stanislav G. Genome Research, Vol. 25, Issue 5 https://doi.org/10.1101/gr.185538.114	journal	April 2015
HTSeq--a Python framework to work with high-throughput sequencing data Anders, S.; Pyl, P. T.; Huber, W. Bioinformatics, Vol. 31, Issue 2 https://doi.org/10.1093/bioinformatics/btu638	journal	September 2014
Integrative phenomics reveals insight into the structure of phenotypic diversity in budding yeast Skelly, D. A.; Merrihew, G. E.; Riffle, M. Genome Research, Vol. 23, Issue 9 https://doi.org/10.1101/gr.155762.113	journal	May 2013
MRBAYES: Bayesian inference of phylogenetic trees Huelsenbeck, J. P.; Ronquist, F. Bioinformatics, Vol. 17, Issue 8 https://doi.org/10.1093/bioinformatics/17.8.754	journal	August 2001
A genetically isolated population of Saccharomyces cerevisiae in Malaysia Naumov, G. I.; Serpova, E. V.; Naumova, E. S. Microbiology, Vol. 75, Issue 2 https://doi.org/10.1134/S0026261706020147	journal	March 2006
Microbe domestication and the identification of the wild genetic stock of lager-brewing yeast Libkind, D.; Hittinger, C. T.; Valerio, E. Proceedings of the National Academy of Sciences, Vol. 108, Issue 35 https://doi.org/10.1073/pnas.1105430108	journal	August 2011
A High-Definition View of Functional Genetic Variation from Natural Yeast Genomes Bergström, Anders; Simpson, Jared T.; Salinas, Francisco Molecular Biology and Evolution, Vol. 31, Issue 4 https://doi.org/10.1093/molbev/msu037	journal	January 2014
Mixing of vineyard and oak-tree ecotypes of Saccharomyces cerevisiae in North American vineyards Hyma, Katie E.; Fay, Justin C. Molecular Ecology, Vol. 22, Issue 11 https://doi.org/10.1111/mec.12155	journal	January 2013
The Genome Analysis Toolkit: A MapReduce framework for analyzing next-generation DNA sequencing data McKenna, A.; Hanna, M.; Banks, E. Genome Research, Vol. 20, Issue 9 https://doi.org/10.1101/gr.107524.110	journal	July 2010
Evidence for Domesticated and Wild Populations of Saccharomyces cerevisiae Fay, Justin C.; Benavides, Joseph A. PLoS Genetics, Vol. 1, Issue 1 https://doi.org/10.1371/journal.pgen.0010005	journal	January 2005
The variant call format and VCFtools Danecek, P.; Auton, A.; Abecasis, G. Bioinformatics, Vol. 27, Issue 15 https://doi.org/10.1093/bioinformatics/btr330	journal	June 2011
ECOLOGICAL REPRODUCTIVE ISOLATION OF COAST AND INLAND RACES OF MIMULUS GUTTATUS Lowry, David B.; Rockwood, R. Cotton; Willis, John H. Evolution, Vol. 62, Issue 9 https://doi.org/10.1111/j.1558-5646.2008.00457.x	journal	September 2008
Hybridization of the Habitat Anderson, Edgar Evolution, Vol. 2, Issue 1 https://doi.org/10.2307/2405610	journal	March 1948
Dosage compensation can buffer copy-number variation in wild yeast Hose, James; Yong, Chris Mun; Sardi, Maria eLife, Vol. 4 https://doi.org/10.7554/eLife.05462	journal	May 2015
A sulphite-inducible form of the sulphite efflux gene SSU1 in a Saccharomyces cerevisiae wine yeast Nardi, T.; Corich, V.; Giacomini, A. Microbiology, Vol. 156, Issue 6 https://doi.org/10.1099/mic.0.036723-0	journal	March 2010
Surprisingly diverged populations of Saccharomyces cerevisiae in natural environments remote from human activity Wang, Qi-Ming; Liu, Wan-Qiu; Liti, Gianni Molecular Ecology, Vol. 21, Issue 22 https://doi.org/10.1111/j.1365-294X.2012.05732.x	journal	August 2012
adegenet: a R package for the multivariate analysis of genetic markers Jombart, Thibaut Bioinformatics, Vol. 24, Issue 11 https://doi.org/10.1093/bioinformatics/btn129	journal	April 2008
Natural Isolates of Saccharomyces cerevisiae Display Complex Genetic Variation in Sporulation Efficiency Gerke, Justin P.; Chen, Christina T. L.; Cohen, Barak A. Genetics, Vol. 174, Issue 2 https://doi.org/10.1534/genetics.106.058453	journal	September 2006
Yeast genomic expression studies using DNA microarrays Gasch, Audrey P. Guide to Yeast Genetics and Molecular and Cell Biology - Part B https://doi.org/10.1016/S0076-6879(02)50976-9	book	January 2002
The Sequence Alignment/Map format and SAMtools Li, H.; Handsaker, B.; Wysoker, A. Bioinformatics, Vol. 25, Issue 16 https://doi.org/10.1093/bioinformatics/btp352	journal	June 2009
Hybridization of the Habitat Anderson, Edgar Evolution, Vol. 2, Issue 1 https://doi.org/10.1111/j.1558-5646.1948.tb02726.x	journal	March 1948
Hybridization as a Source of Variation for Adaptation to new Environments Lewontin, R. C.; Birch, L. C. Evolution, Vol. 20, Issue 3 https://doi.org/10.1111/j.1558-5646.1966.tb03369.x	journal	September 1966
Data from: A unique ecological niche fosters hybridization of oak-tree and vineyard isolates of Saccharomyces cerevisiae. Clowers, Katie J.; Will, Jessica L.; Gasch, Audrey P. Dryad https://doi.org/10.5061/dryad.bt5v6	dataset	January 2015
Persistence of adoptively transferred T cells with a kinetically engineered IL-2 receptor agonist Parisi, Giulia; Saco, Justin D.; Salazar, Felix B. Nature Communications, Vol. 11, Issue 1 https://doi.org/10.1038/s41467-019-12901-3	journal	January 2020
Ancestry deconvolution and partial polygenic score can improve susceptibility predictions in recently admixed individuals Marnetto, Davide; Pärna, Katri; Läll, Kristi Nature Communications, Vol. 11, Issue 1 https://doi.org/10.1038/s41467-020-15464-w	journal	April 2020
Ancient genomes reveal social and genetic structure of Late Neolithic Switzerland Furtwängler, Anja; Rohrlach, A. B.; Lamnidis, Thiseas C. Nature Communications, Vol. 11, Issue 1 https://doi.org/10.1038/s41467-020-15560-x	journal	April 2020
Production of viable chicken by allogeneic transplantation of primordial germ cells induced from somatic cells Zhao, Ruifeng; Zuo, Qisheng; Yuan, Xia Nature Communications, Vol. 12, Issue 1 https://doi.org/10.1038/s41467-021-23242-5	journal	May 2021
Species identification, phylogenetic analysis and detection of herbicide-resistant biotypes of Amaranthus based on ALS and ITS Xu, Han; Pan, Xubin; Wang, Cong Scientific Reports, Vol. 10, Issue 1 https://doi.org/10.1038/s41598-020-68541-x	journal	July 2020
Hybridization as an Evolutionary Stimulus Anderson, E.; Stebbins, G. L. Evolution, Vol. 8, Issue 4 https://doi.org/10.1111/j.1558-5646.1954.tb01504.x	journal	December 1954
Saccharomyces paradoxus and Saccharomyces cerevisiae are associated with exudates of North American oaks Naumov, Gennadi I.; Naumova, Elena S.; Sniegowski, Paul D. Canadian Journal of Microbiology, Vol. 44, Issue 11 https://doi.org/10.1139/w98-104	journal	November 1998
Characterization and functional analysis of phytoene synthase gene family in tobacco Wang, Zhaojun; Zhang, Lin; Dong, Chen BMC Plant Biology, Vol. 21, Issue 1 https://doi.org/10.1186/s12870-020-02816-3	journal	January 2021

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54 ENVIRONMENTAL SCIENCES
59 BASIC BIOLOGICAL SCIENCES
allele-specific expression
ecological divergence
environmental stress
hybridization