Cited by 628Yeasts and Rust Fungi StudiesFungal and yeast genetics researchGenomics and Phylogenetic Studies

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Tempo and Mode of Genome Evolution in the Budding Yeast Subphylum

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Shen, Xing-Xing, Opulente, Dana A., Kominek, Jacek, Zhou, Xiaofan, Steenwyk, Jacob L., Buh, Kelly V., Haase, Max A.B., Wisecaver, Jennifer H., Wang, Mingshuang, Doering, Drew T., Boudouris, James T., Schneider, Rachel M., Langdon, Quinn K., Ohkuma, Moriya, Endoh, Rikiya, 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·2018·Cell

DOI 10.1016/j.cell.2018.10.023PMC PMC6291210

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Abstract

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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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)
DOI: 10.1016/j.cell.2018.10.023
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: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
www.elsevier.com/open-access/userlicense/1.0/ (vor, 393 d)
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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