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Domestication reprogrammed the budding yeast life cycle

Nature Ecology & Evolution volume 6, pages 448–460 (2022)Cite this article

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Abstract

Domestication of plants and animals is the foundation for feeding the world human population but can profoundly alter the biology of the domesticated species. Here we investigated the effect of domestication on one of our prime model organisms, the yeast Saccharomyces cerevisiae, at a species-wide level. We tracked the capacity for sexual and asexual reproduction and the chronological life span across a global collection of 1,011 genome-sequenced yeast isolates and found a remarkable dichotomy between domesticated and wild strains. Domestication had systematically enhanced fermentative and reduced respiratory asexual growth, altered the tolerance to many stresses and abolished or impaired the sexual life cycle. The chronological life span remained largely unaffected by domestication and was instead dictated by clade-specific evolution. We traced the genetic origins of the yeast domestication syndrome using genome-wide association analysis and genetic engineering and disclosed causative effects of aneuploidy, gene presence/absence variations, copy number variations and single-nucleotide polymorphisms. Overall, we propose domestication to be the most dramatic event in budding yeast evolution, raising questions about how much domestication has distorted our understanding of the natural biology of this key model species.

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Fig. 1: Genomic and phenomic portraits of domesticated and wild yeast.
Fig. 2: Domestication promoted fermentative over respiratory growth.
Fig. 3: Domestication abolished or impaired yeast sporulation.
Fig. 4: Genetic control of sporulation efficiency.
Fig. 5: Domestication only weakly extended the yeast CLS.
Fig. 6: HPF1-like and WHI2 loss-of-function variants impairs yeast CLS.

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All data generated or analysed during this study are included in this article and the Supplementary Information. Source data are provided with this paper.

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Acknowledgements

We thank F. van Werven, G. Fisher and B. Llorente for the helpful discussions and B. Cohen for the kind gift of the SPS2::GFP tagged strains. This work was supported by Agence Nationale de la Recherche (ANR-15-IDEX-01, ANR-18-CE12-0004, ANR-20-CE13-0010, ANR-20-CE12-0020), Fondation pour la Recherche Médicale (EQU202003010413), CEFIPRA, Fondation ARC (no. ARCPJA32020070002320), the Swedish Research Council (2014-6547, 2014-4605, 2018-03638 and 2018-03453) and the Slovenian Research Agency (P1-0207), COFUND BoostUrCAreer programme (funded by EU Horizon 2020, Marie Curie grant agreement no. 847581, Région SUD PACA and IDEX UCAjedi).

Author information

Author notes

  1. Benjamin P. Barré

    Present address: Division of Genetics, Department of Medicine, Brigham and Women’s Hospital and Harvard Medical School, Boston, MA, USA

  2. These authors contributed equally: Matteo De Chiara, Benjamin P. Barré.

  3. These authors jointly supervised this work: Jonas Warringer, Gianni Liti.

Authors and Affiliations

  1. Université Côte d’Azur, CNRS, INSERM, IRCAN, Nice, France

    Matteo De Chiara, Benjamin P. Barré, Agurtzane Irizar, Chiara Vischioni, Sakshi Khaiwal & Gianni Liti

  2. Department of Chemistry and Molecular Biology, Gothenburg University, Gothenburg, Sweden

    Karl Persson, Simon Stenberg, Onyetugo Chioma Amadi & Jonas Warringer

  3. Department of Animal Medicine, Production and Health, University of Padova, Legnaro, Italy

    Chiara Vischioni & Cristian Taccioli

  4. Department of Microbiology, University of Nigeria, Nsukka, Nigeria

    Onyetugo Chioma Amadi

  5. Department of Molecular and Biomedical Sciences, Jožef Stefan Institute, Ljubljana, Slovenia

    Gašper Žun, Katja Doberšek & Uroš Petrovič

  6. Biotechnical Faculty, University of Ljubljana, Ljubljana, Slovenia

    Gašper Žun & Uroš Petrovič

  7. Université de Strasbourg, CNRS, GMGM UMR, Strasbourg, France

    Joseph Schacherer

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Contributions

M.D.C., B.P.B., U.P., J.W. and G.L. designed the experiments. M.D.C., B.P.B., K.P., A.I., C.V., S.K., S.S., O.C.A., G.Ž. and K.D. performed and analysed the experiments. J.S., C.T., J.W. and G.L. contributed with resources and reagents. M.D.C., B.P.B., J.W. and G.L. conceived and supervised the project. M.D.C., B.P.B., J.W. and G.L. wrote the paper.

Corresponding authors

Correspondence to Matteo De Chiara, Jonas Warringer or Gianni Liti.

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Nature Ecology & Evolution thanks José Sampaio and the other, anonymous, reviewer(s) for their contribution to the peer review of this work. Peer reviewer reports are available.

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Extended data

Extended Data Fig. 1 Wild yeast strains grow better in presence of most stresses.

Re-analysis of the asexual growth data were taken from Peter et al. 201826. a, PCA based on all data from asexual growth largely separates wild and domesticated clades. Each clade is represented by the median value for each phenotypes. b, Boxplot of asexual growth in the 16 environments in which wild (W) are superior to domesticated (D) strains. c, Boxplot of asexual growth in the five environments in which domesticated are superior to wild strains. Box: IQR. Whiskers: 1.5x IQR. Significances (1-sided Mann–Whitney is reported in Supplementary Table 2). n = 565 and 58 for, respectively, domesticated and wild isolates, with the exception of domesticated isolates in galactose, where n = 564.

Source data

Extended Data Fig. 2 Sporulation efficiency is excellent in all wild yeast clades.

a, Distribution of sporulation efficiencies after 24 h (upper panel) and 72 h (lower panel) in traditional sporulation environment (KAc) for each phylogenetic clade. Clades are ordered according to the phylogeny26, with mosaic and long branch strains at the end. Colours indicate domesticated (red) or wild (blue). The unassigned clades are left white. Box: IQR. Whiskers: 1.5x IQR. Number of data point for each boxplot are as following: Wine/European, 312; Alpechin, 12; Brazilian bioethanol, 27; Mediterranean oak, 8; French dairy, 32; African beer, 19; Mosaic beer, 12; Mixed origin, 66; Mexican agave, 7, French Guiana human, 30; Ale beer, 17; West African Cocoa beans fermentation, 12; African palm wine, 24; CHNIII, 2; CHNII, 2; CHNI, 1; Taiwanese, 3; Far East Asia, 8; Malaysian, 5; CHNV, 2; Ecuadorean, 8; Russian, 4; North American, 11; Asian islands, 7; Sake, 41; Asian fermentation, 29; Mosaic region 1, 12; Mosaic region 2, 16; Mosaic region 3, 83; Unclustered, 38. b, Distribution of the sporulation efficiency at 24 h and 72 h for the four subclades within the Wine/European clade. The S. boulardii subgroup has completely lost the ability to sporulate. Box: IQR. Whiskers: 1.5 X IQR. n = 17,10,24,29 and 232 for, respectively, Feral wine, clinical Y’ amplification, S. boulardii, Georgian and other wine isolates. c, Sporulation efficiency in water. S. cerevisiae and S. paradoxus wild strains sporulate well, S. cerevisiae domesticated strains do not. Boxplot of the distribution of asci production (only sporulating isolates, that is asci production > 0) after 8 days in water. Box: IQR. Whiskers: 1.5x IQR. n = 4, 19 and 6 for, respectively domesticated, wild and S. paradoxus. d, Fraction of S. cerevisiae domesticated, wild and S. paradoxus isolates able to sporulate (that is sporulation efficiency > 0 after 8 days) in water.

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Extended Data Fig. 3 IME1 variants control yeast sporulation variation.

a, Schematic representation of the locus of the meiotic regulator and the upstream IRT1, which overlaps the IME1 promoter. GWAS revealed that six SNPs at five sites (green stars) in the IME1 and its promoter associate to sporulation efficiency after 24 h in standard KAc. None of these correspond to the SNPs identified in Gerke et al 200944 (grey stars), which do not pass the MAF > 0.05. b, Upper panel: Distribution of IME1 GWAS sporulation hits across the sequenced strain collection (y-axis, ordered as in the tree phylogeny reported in Peter et al 201826). Several SNPs appear to be linked. Lower panel: Sporulation of strains homo- or heterozygotic for the six IME1 SNPs associated to sporulation. Box: IQR. Whiskers: 1.5x IQR. All minor SNPs, except H78R, associate to poor spore production. Number of data point for each boxplot are as following: n = 759, 44 and 47 for, respectively isolates with genotype AA, AC and CC in position −325; n = 766, 40, 44 respectively for isolates with genotype CC, CT and TT in position −181; n = 568, 5 and 184 respectively for isolates with genotype HH, HR and RR on position 78; n = 791, 30 and 29 respectively for isolates with genotype NN, NY and YY in position 311; n = 742, 5, 33, 39, 30 respectively for isolates with genotype EE, EV, VV, EG, GG in position 316. c, H78R is here restricted to a subset of domesticated clades and promotes spore production. Box: IQR. Whiskers: 1.5x IQR. n = 293, 57 and 153 respectively for domesticated isolates with genotype HH, HR and RR on position 78. d, upper panels: Inserting the C-181T variant in the strain YPS128 strongly decreased its sporulation efficiency (from 86% to 4 % asci 9 hours after meiosis induction, and from 98% to 58% after 24 h), while introducing the C allele in the CIA isolate (WT for T) increased the efficiency (from 1.7% to 22.5% asci after 24 h and from 35% to 59% asci after 168 h); bottom panels: The substitution of the R allele to the H allele massively reduced the sporulation efficiency in the isolate DBVPG6765 (from 37% to 2% asci 72 hours post-induction and from 43% to 4% 168 h). The introduction of the H78R mutation in BY4743 improved the efficiency (from 0.3% to 2% asci 72 hours post-induction and from 3.5% to 7.7% after 240 h). Time points were selected to show the maximal phenotypic effect attributed to single mutations. The asterisks indicate statistical significance (Student´s t-test).

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Extended Data Fig. 4 Loss-of-function variants in SPO12 and SPO13 trigger dyads-only spore production.

a, Sporulation efficiency after 3 days in traditional sporulation medium (KAc) and the percentage of produced asci that are dyads (x-axis), after 24 h (left panel) and 72 h (right panel). Nine strains, belonging to two clusters (indicated in green and orange) efficiently enter sporulation but interrupt the meiosis cycle after meiosis I, only producing dyads. b, Micrograph of asci produced in the strain BNL, after 72 h of sporulation, with staining of the spore wall (blue). Only dyads are produced. c, Schematic representation of the protein sequences for Spo12 and Spo13 showing the positions of homozygous loss-of-function variants that trigger dyads-only production during sporulation.

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Extended Data Fig. 5 Yeast CLS is clade specific and not strongly influenced by domestication.

Boxplots showing surviving cells (%) for each clade in each CLS condition and time point. Clades are ordered according to the phylogeny26, with mosaic and long branch strains at the end. French Dairy (5.F) and African beer (6.A) yeasts have the lowest survival (median < 30% survival after 7 days in SDC) while French Guiana (10.F), Mexican agave (09.M) and West African Cocoa (12.W) have the highest (median > 60% survival after 7 days in SDC). Among wild clades, the Taiwanese and Malaysian strains were short-living (<30% survival in SDC after 7 days), while the Far East Russian and North American oak strains all were long-living (>60% survival after 7 days in SDC). Restricting the initially available calories from 2% sugar (SDC) to 0.5% sugar (CR) extended CLS of virtually all clades, and more particularly of those with poor survival in SDC. Box: IQR. Whiskers: 1.5 X IQR. Number of data point for each boxplot are as following: Wine/European, 306; Alpechin, 12; Brazilian bioethanol, 17; Mediterranean oak, 8; French dairy, 31; African beer, 19; Mosaic beer, 9; Mixed origin, 56; Mexican agave, 7, French Guiana human, 30; Ale beer, 8; West African Cocoa beans fermentation, 12; African palm wine, 22; CHNIII, 2; CHNII, 2; CHNI, 1; Taiwanese, 3; Far East Asia, 8; Malaysian, 4; CHNV, 2; Ecuadorean, 9; Russian, 4; North American, 11; Asian islands, 8; Sake, 43; Asian fermentation, 29; Mosaic region 1, 12; Mosaic region 2, 15; Mosaic region 3, 80; Unclustered, 37.

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Extended Data Fig. 6 Aneuploidy and polyploidy effects on CLS.

For each time point and medium (SDC, which is moderately calorie restricted, or CR, which is severely caloric restricted) the distribution of the fraction of surviving cells is shown. Both aneuploidy and polyploidy are associated with a shorter CLS. Box: IQR. Whiskers: 1.5 X IQR. n = 581, 34 and 132 for, respectively, diploid euploid (EU 2 N), aneuploid diploid (AN 2 N) and polyploid euploid (EU > 2 N).

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Extended Data Fig. 7 WHI2 loss-of-function variants and HPF1-like presence associate to a short CLS.

a, Predicted loss-of-function variants in WHI2 associate to a short life span in the 1011 strain collection. Significant 2-sided Mann–Whitney results are indicated (SDC at day 7, p = 8.6e-07, CR at day 7, p = 1.4e-12, CR at day 21, p = 5.0e-03. Box: IQR. Whiskers: 1.5 X IQR. n = 747 and 60 for, respectively, isolates with a functioning allele of WHI2 and isolates with a loss-of-function in WHI2. b, The presence of HPF1-like is associated with a short life span in a calorie restricted CR medium. Significant 2-sided Mann–Whitney results are indicated (CR at day 7, p = 1.9e-09, CR at day 21, p = 8.6e-09, CR at day 35, p = 1.6e-05. Box: IQR. Whiskers: 1.5 X IQR. n = 718 and 89 for, respectively, isolates without the HPF1-like ORF and isolates with it in the 1011 strain collection.

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Extended Data Fig. 8 Correlations among life cycle traits.

Although traits of the same class (cell doubling time, yield, sporulation and CLS) broadly correlated, traits of different classes remain poorly correlated.

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Extended Data Fig. 9 Genetic variants rarely associate to more than one class of life cycle traits.

a, Only few genetic variants detected by GWAS associate to more than one class of life cycle traits and no genetic variant associate to more than two. b, Genetic variants rarely affect more than one life cycle trait (environment, time point) even within the same trait class in more than one environment or at more than one time point. Arrows indicate the position of pleiotropic exceptions discussed in the text.

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Supplementary information

Supplementary Information

Supplementary Notes 1 and 2, Fig. 1 and references.

Reporting Summary

Peer Review Information

Supplementary Tables

Supplementary Tables 1–13.

Supplementary Data

Variant matrix for GWAS generated by Plink in .bed, .bim and .fam formats. The matrix contains all biallelic positions known for the sequenced isolates with MAF > 5%, as well as LOF, presence and absence, and CNVs (for the latter, the ORFs absence has been coded as missing data).

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De Chiara, M., Barré, B.P., Persson, K. et al. Domestication reprogrammed the budding yeast life cycle. Nat Ecol Evol 6, 448–460 (2022). https://doi.org/10.1038/s41559-022-01671-9

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