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Tempo and Mode of Genome Evolution in the Budding Yeast Subphylum
Open accessAbstract
Budding yeasts (subphylum Saccharomycotina) are found in every biome and are as genetically diverse as plants or animals. To understand budding yeast evolution, we analyzed the genomes of 332 yeast species, including 220 newly sequenced ones, which represent nearly one-third of all known budding yeast diversity. Here, we establish a robust genus-level phylogeny comprising 12 major clades, infer the timescale of diversification from the Devonian period to the present, quantify horizontal gene transfer (HGT), and reconstruct the evolution of 45 metabolic traits and the metabolic toolkit of the budding yeast common ancestor (BYCA). We infer that BYCA was metabolically complex and chronicle the tempo and mode of genomic and phenotypic evolution across the subphylum, which is characterized by very low HGT levels and widespread losses of traits and the genes that control them. More generally, our results argue that reductive evolution is a major mode of evolutionary diversification.
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“In a previous study, the genomes of 343 yeast/fungi species combined with comprehensive genome annotations were publicly available 63 .”
From Deep learning-based kcat prediction enables improved enzyme-constrained model reconstruction (2022) · cites this paper as [63]
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Additional file 11 of Sex without crossing over in the yeast Saccharomycodes ludwigii
Papaioannou, I. A., Dutreux, F., Peltier, F. A., Maekawa, H., Delhomme, N., Bardhan, A., Friedrich, A., Schacherer, J., & Knop, M. (2021) · Figshare · doi:10.6084/m9.figshare.16928285
Additional file 1 of Divergent patterns of selection on metabolite levels and gene expression
Kern, A., Yang, G. X., Khosla, N. M., Ang, R. M. L., Snyder, M. P., & Fraser, H. B. (2021) · Figshare · doi:10.6084/m9.figshare.16702978
Additional file 5 of Divergent patterns of selection on metabolite levels and gene expression
Kern, A., Yang, G. X., Khosla, N. M., Ang, R. M. L., Snyder, M. P., & Fraser, H. B. (2021) · Figshare · doi:10.6084/m9.figshare.16702996
Ravn, J. L., Engqvist, M. K. M., Larsbrink, J., & Geijer, C. (2021) · Figshare · doi:10.6084/m9.figshare.14903948
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Additional file 6 of Sex without crossing over in the yeast Saccharomycodes ludwigii
Papaioannou, I. A., Dutreux, F., Peltier, F. A., Maekawa, H., Delhomme, N., Bardhan, A., Friedrich, A., Schacherer, J., & Knop, M. (2021) · Figshare · doi:10.6084/m9.figshare.16928306
Additional file 1 of Sex without crossing over in the yeast Saccharomycodes ludwigii
Papaioannou, I. A., Dutreux, F., Peltier, F. A., Maekawa, H., Delhomme, N., Bardhan, A., Friedrich, A., Schacherer, J., & Knop, M. (2021) · Figshare · doi:10.6084/m9.figshare.16928288
Ravn, J. L., Engqvist, M. K. M., Larsbrink, J., & Geijer, C. (2021) · Figshare · doi:10.6084/m9.figshare.14903954
Mühlhausen, S., Schmitt, H. D., Plessmann, U., Mienkus, P., Sternisek, P., Perl, T., Weig, M., Urlaub, H., Bader, O., & Kollmar, M. (2021) · Figshare · doi:10.6084/m9.figshare.17125700
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Self-citationBarros, K. O., Mader, M., Krause, D. J., Pangilinan, J. L., Andreopoulos, B., Lipzen, A., Mondo, S. J., Grigoriev, I. V., Rosa, C. A., Sato, T. K., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26677880
Self-citationTapia, S. M., Macías, L. G., Pérez‐Torrado, R., Daroqui, N., Manzanares, P., Querol, A., & Barrio, E. (2024) · Figshare · doi:10.6084/m9.figshare.26587956
Tapia, S. M., Macías, L. G., Pérez‐Torrado, R., Daroqui, N., Manzanares, P., Querol, A., & Barrio, E. (2024) · Figshare · doi:10.6084/m9.figshare.26587983
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Self-citationAdditional file 4 of Divergent patterns of selection on metabolite levels and gene expression
Kern, A., Yang, G. X., Khosla, N. M., Ang, R. M. L., Snyder, M. P., & Fraser, H. B. (2021) · Figshare · doi:10.6084/m9.figshare.16702993
Ravn, J. L., Engqvist, M. K. M., Larsbrink, J., & Geijer, C. (2021) · Figshare · doi:10.6084/m9.figshare.14903951
Pontes, A., Paraíso, F., Silva, M., Lagoas, C., Aires, A., Brito, P. H., Rosa, C. A., Lachance, M.-A., Sampaio, J. P., Gonçalves, C., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26727841
Self-citationTapia, S. M., Macías, L. G., Pérez‐Torrado, R., Daroqui, N., Manzanares, P., Querol, A., & Barrio, E. (2024) · Figshare · doi:10.6084/m9.figshare.26587962
Oggenfuss, U., Badet, T., & Croll, D. (2024) · Figshare · doi:10.6084/m9.figshare.26670309
Barros, K. O., Mader, M., Krause, D. J., Pangilinan, J. L., Andreopoulos, B., Lipzen, A., Mondo, S. J., Grigoriev, I. V., Rosa, C. A., Sato, T. K., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26677874
Self-citationTapia, S. M., Macías, L. G., Pérez‐Torrado, R., Daroqui, N., Manzanares, P., Querol, A., & Barrio, E. (2024) · Figshare · doi:10.6084/m9.figshare.26587989
Pontes, A., Paraíso, F., Silva, M., Lagoas, C., Aires, A., Brito, P. H., Rosa, C. A., Lachance, M.-A., Sampaio, J. P., Gonçalves, C., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26727856
Self-citationAdditional file 9 of Sex without crossing over in the yeast Saccharomycodes ludwigii
Papaioannou, I. A., Dutreux, F., Peltier, F. A., Maekawa, H., Delhomme, N., Bardhan, A., Friedrich, A., Schacherer, J., & Knop, M. (2021) · Figshare · doi:10.6084/m9.figshare.16928318
Pontes, A., Paraíso, F., Silva, M., Lagoas, C., Aires, A., Brito, P. H., Rosa, C. A., Lachance, M.-A., Sampaio, J. P., Gonçalves, C., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26727862
Self-citationMühlhausen, S., Schmitt, H. D., Plessmann, U., Mienkus, P., Sternisek, P., Perl, T., Weig, M., Urlaub, H., Bader, O., & Kollmar, M. (2021) · Figshare · doi:10.6084/m9.figshare.17125691
Tapia, S. M., Macías, L. G., Pérez‐Torrado, R., Daroqui, N., Manzanares, P., Querol, A., & Barrio, E. (2024) · Figshare · doi:10.6084/m9.figshare.26587974
Pontes, A., Paraíso, F., Silva, M., Lagoas, C., Aires, A., Brito, P. H., Rosa, C. A., Lachance, M.-A., Sampaio, J. P., Gonçalves, C., et al. (2024) · Figshare · doi:10.6084/m9.figshare.25940247
Self-citationAlva, T. R., Riera, M., & Chartron, J. W. (2021) · Figshare · doi:10.6084/m9.figshare.13620095
Additional file 2 of Sex without crossing over in the yeast Saccharomycodes ludwigii
Papaioannou, I. A., Dutreux, F., Peltier, F. A., Maekawa, H., Delhomme, N., Bardhan, A., Friedrich, A., Schacherer, J., & Knop, M. (2021) · Figshare · doi:10.6084/m9.figshare.16928291
Tapia, S. M., Macías, L. G., Pérez‐Torrado, R., Daroqui, N., Manzanares, P., Querol, A., & Barrio, E. (2024) · Figshare · doi:10.6084/m9.figshare.26587986
Pontes, A., Paraíso, F., Silva, M., Lagoas, C., Aires, A., Brito, P. H., Rosa, C. A., Lachance, M.-A., Sampaio, J. P., Gonçalves, C., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26727859
Self-citationOggenfuss, U., Badet, T., & Croll, D. (2024) · Figshare · doi:10.6084/m9.figshare.26670315
Tapia, S. M., Macías, L. G., Pérez‐Torrado, R., Daroqui, N., Manzanares, P., Querol, A., & Barrio, E. (2024) · Figshare · doi:10.6084/m9.figshare.26587953
Alva, T. R., Riera, M., & Chartron, J. W. (2021) · Figshare · doi:10.6084/m9.figshare.13620077
Pontes, A., Paraíso, F., Silva, M., Lagoas, C., Aires, A., Brito, P. H., Rosa, C. A., Lachance, M.-A., Sampaio, J. P., Gonçalves, C., et al. (2024) · Figshare · doi:10.6084/m9.figshare.25939962
Self-citationTapia, S. M., Macías, L. G., Pérez‐Torrado, R., Daroqui, N., Manzanares, P., Querol, A., & Barrio, E. (2024) · Figshare · doi:10.6084/m9.figshare.26587965
Additional file 8 of Sex without crossing over in the yeast Saccharomycodes ludwigii
Papaioannou, I. A., Dutreux, F., Peltier, F. A., Maekawa, H., Delhomme, N., Bardhan, A., Friedrich, A., Schacherer, J., & Knop, M. (2021) · Figshare · doi:10.6084/m9.figshare.16928315
Tapia, S. M., Macías, L. G., Pérez‐Torrado, R., Daroqui, N., Manzanares, P., Querol, A., & Barrio, E. (2024) · Figshare · doi:10.6084/m9.figshare.26587977
Additional file 3 of Divergent patterns of selection on metabolite levels and gene expression
Kern, A., Yang, G. X., Khosla, N. M., Ang, R. M. L., Snyder, M. P., & Fraser, H. B. (2021) · Figshare · doi:10.6084/m9.figshare.16702987
Additional file 10 of Sex without crossing over in the yeast Saccharomycodes ludwigii
Papaioannou, I. A., Dutreux, F., Peltier, F. A., Maekawa, H., Delhomme, N., Bardhan, A., Friedrich, A., Schacherer, J., & Knop, M. (2021) · Figshare · doi:10.6084/m9.figshare.16928282
Barros, K. O., Mader, M., Krause, D. J., Pangilinan, J. L., Andreopoulos, B., Lipzen, A., Mondo, S. J., Grigoriev, I. V., Rosa, C. A., Sato, T. K., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26677877
Self-citationTapia, S. M., Macías, L. G., Pérez‐Torrado, R., Daroqui, N., Manzanares, P., Querol, A., & Barrio, E. (2024) · Figshare · doi:10.6084/m9.figshare.26587968
Oggenfuss, U., Badet, T., & Croll, D. (2024) · Figshare · doi:10.6084/m9.figshare.26670312
Wadler, C. S., Wolters, J. F., Fortney, N. W., Throckmorton, K., Zhang, Y., Miller, C. R., Schneider, R. M., Wendt-Pienkowski, E., Currie, C. R., Donohue, T. J., et al. (2022) · Figshare · doi:10.6084/m9.figshare.20156792
Self-citationTapia, S. M., Macías, L. G., Pérez‐Torrado, R., Daroqui, N., Manzanares, P., Querol, A., & Barrio, E. (2024) · Figshare · doi:10.6084/m9.figshare.26587980
Additional file 2 of Divergent patterns of selection on metabolite levels and gene expression
Kern, A., Yang, G. X., Khosla, N. M., Ang, R. M. L., Snyder, M. P., & Fraser, H. B. (2021) · Figshare · doi:10.6084/m9.figshare.16702984
Pontes, A., Paraíso, F., Silva, M., Lagoas, C., Aires, A., Brito, P. H., Rosa, C. A., Lachance, M.-A., Sampaio, J. P., Gonçalves, C., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26727844
Self-citationAdditional file 7 of Sex without crossing over in the yeast Saccharomycodes ludwigii
Papaioannou, I. A., Dutreux, F., Peltier, F. A., Maekawa, H., Delhomme, N., Bardhan, A., Friedrich, A., Schacherer, J., & Knop, M. (2021) · Figshare · doi:10.6084/m9.figshare.16928309
Alva, T. R., Riera, M., & Chartron, J. W. (2021) · Figshare · doi:10.6084/m9.figshare.13620092
Barros, K. O., Mader, M., Krause, D. J., Pangilinan, J. L., Andreopoulos, B., Lipzen, A., Mondo, S. J., Grigoriev, I. V., Rosa, C. A., Sato, T. K., et al. (2024) · Figshare · doi:10.6084/m9.figshare.25157430
Self-citationAdditional file 3 of Sex without crossing over in the yeast Saccharomycodes ludwigii
Papaioannou, I. A., Dutreux, F., Peltier, F. A., Maekawa, H., Delhomme, N., Bardhan, A., Friedrich, A., Schacherer, J., & Knop, M. (2021) · Figshare · doi:10.6084/m9.figshare.16928297
Tapia, S. M., Macías, L. G., Pérez‐Torrado, R., Daroqui, N., Manzanares, P., Querol, A., & Barrio, E. (2024) · Figshare · doi:10.6084/m9.figshare.26587971
Tapia, S. M., Macías, L. G., Pérez‐Torrado, R., Daroqui, N., Manzanares, P., Querol, A., & Barrio, E. (2024) · Figshare · doi:10.6084/m9.figshare.26587959
Additional file 5 of Sex without crossing over in the yeast Saccharomycodes ludwigii
Papaioannou, I. A., Dutreux, F., Peltier, F. A., Maekawa, H., Delhomme, N., Bardhan, A., Friedrich, A., Schacherer, J., & Knop, M. (2021) · Figshare · doi:10.6084/m9.figshare.16928303
Additional file 4 of Sex without crossing over in the yeast Saccharomycodes ludwigii
Papaioannou, I. A., Dutreux, F., Peltier, F. A., Maekawa, H., Delhomme, N., Bardhan, A., Friedrich, A., Schacherer, J., & Knop, M. (2021) · Figshare · doi:10.6084/m9.figshare.16928300
Pontes, A., Paraíso, F., Silva, M., Lagoas, C., Aires, A., Brito, P. H., Rosa, C. A., Lachance, M.-A., Sampaio, J. P., Gonçalves, C., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26727847
Self-citationPontes, A., Paraíso, F., Silva, M., Lagoas, C., Aires, A., Brito, P. H., Rosa, C. A., Lachance, M.-A., Sampaio, J. P., Gonçalves, C., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26727865
Self-citationHeistinger, L., Dohm, J. C., Paes, B. G., Koizar, D., Troyer, C., Ata, Ö., Mairinger, T., & Mattanovich, D. (2022) · Figshare · doi:10.6084/m9.figshare.19654453
Barros, K. O., Mader, M., Krause, D. J., Pangilinan, J. L., Andreopoulos, B., Lipzen, A., Mondo, S. J., Grigoriev, I. V., Rosa, C. A., Sato, T. K., et al. (2024) · Figshare · doi:10.6084/m9.figshare.25157829
Self-citationPontes, A., Paraíso, F., Silva, M., Lagoas, C., Aires, A., Brito, P. H., Rosa, C. A., Lachance, M.-A., Sampaio, J. P., Gonçalves, C., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26727850
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Steenwyk, J. L., & Rokas, A. (2019) · doi:10.64628/aai.5h69gqyg5
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Belcher, L. J., & Kelly, S. L. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.01.27.702036 · Cited by 1
Haberkorn, C., Molinet, J., & Stelkens, R. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.02.02.703184
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Self-citation
Metadata
- Authors
- Shen, X.-X., Opulente, D. A., Kominek, J., Zhou, X., Steenwyk, J. L., Buh, K. V., Haase, M. A. B., Wisecaver, J. H., Wang, M., Doering, D. T., Boudouris, J. T., Schneider, R. M., Langdon, Q. K., Ohkuma, M., Endoh, R., Takashima, M., Manabe, R.-I., Čadež, N., Libkind, D., Rosa, C. A., DeVirgilio, J., Hulfachor, A. B., Groenewald, M., Kurtzman, C. P., Hittinger, C. T., & Rokas, A.
- Affiliations
- Vanderbilt University (US)
- University of Wisconsin–Madison (US)
- South China Agricultural University (CN)
- RIKEN BioResource Research Center (JP)
- RIKEN Center for Integrative Medical Sciences (JP)
- University of Ljubljana (SI)
- Consejo Nacional de Investigaciones Científicas y Técnicas (AR)
- Universidade Federal de Minas Gerais (BR)
- Agricultural Research Service (US)
- Westerdijk Fungal Biodiversity Institute (NL)
- Corresponding author
- Hittinger, Chris Todd
- Rokas, Antonis
- ORCID
- Shen, Xing-Xing
- Opulente, Dana A.
- Kominek, Jacek
- Zhou, Xiaofan
- Steenwyk, Jacob L.
- Haase, Max A.B.
- Wisecaver, Jennifer H.
- Wang, Mingshuang
- Doering, Drew T.
- Langdon, Quinn K.
- Ohkuma, Moriya
- Takashima, Masako
- Manabe, Ri-ichiroh
- Čadež, Neža
- Libkind, Diego
- Rosa, Carlos A.
- DeVirgilio, Jeremy
- Hulfachor, Amanda Beth
- Groenewald, Marizeth
- Kurtzman, Cletus P.
- Hittinger, Chris Todd
- Rokas, Antonis
- Venue
- Cell
- Publisher
- Elsevier BV
- Published
- 2018-11
- Volume
- 175
- Issue
- 6
- Pages
- 1533-1545.e20
- ISSN
- 0092-8674 (ISSN-L)
- PMC
- PMC6291210
- OpenAlex
- W2899763402
- Cited by
- 619
- References
- 112
- Citations by year
- 2026: 56 · 2025: 72 · 2024: 109 · 2023: 83 · 2022: 70 · 2021: 116 · 2020: 68 · 2019: 43 · 2018: 1
- FWCI
- 20.28
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Cell (publishedVersion)
- PubMed (publishedVersion)
- KNAW Research Portal (The Royal Netherlands Academy of Arts and Sciences) (publishedVersion, other-oa)
- LA Referencia (Red Federada de Repositorios Institucionales de Publicaciones Científicas) (publishedVersion, other-oa)
- PubMed Central (acceptedVersion)
- Data Archiving and Networked Services (DANS) (submittedVersion)
- OSTI OAI (U.S. Department of Energy Office of Scientific and Technical Information) (submittedVersion)
- CONICET Digital (CONICET) (submittedVersion, cc-by-nc-sa)
- Funders
- National Science Foundation (DEB-1442113, DEB-1442148, IOS-1401682, DGE-1256259)
- DOE Great Lakes Bioenergy Research Center (DE-FC02-07ER64494, DE-SC0018409)
- Pew Charitable Trusts
- Vilas Trust Estate
- Guggenheim
- Vanderbilt
- National Key Project for Basic Research of China (2015CB150600)
- NHGRI (5T32HG002760)
- NIH (5T32GM007133)
- CONICET (PIP 392)
- FONCyT (PICT 2542)
- Universidad Nacional del Comahue (B199)
- Conselho Nacional de Desenvolvimento Científico e Tecnológico
- Fundação de Amparo a Pesquisa do Estado de Minas Gerais
- Topics
- Life Sciences › Immunology and Microbiology › Microbiology › Yeasts and Rust Fungi Studies
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Fungal and yeast genetics research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Phylogenetic Studies
- Keywords
- Saccharomyces cerevisiae, Saccharomycotina, genome evolution, phylogeny, horizontal gene transfer, metabolic phenotypes, common ancestor, reductive evolution, gene loss
- MeSH terms
- Saccharomycetales, Phylogeny, Genome, Fungal, Evolution, Molecular, Gene Transfer, Horizontal
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