Molecular evidence for an ancient duplication of the entire yeast genome
Abstract
Gene duplication is an important source of evolutionary novelty. Most duplications are of just a single gene, but Ohno proposed that whole-genome duplication (polyploidy) is an important evolutionary mechanism. Many duplicate genes have been found in Saccharomyces cerevisiae, and these often seem to be phenotypically redundant. Here we show that the arrangement of duplicated genes in the S. cerevisiae genome is consistent with Ohno's hypothesis. We propose a model in which this species is a degenerate tetraploid resulting from a whole-genome duplication that occurred after the divergence of Saccharomyces from Kluyveromyces. Only a small fraction of the genes were subsequently retained in duplicate (most were deleted), and gene order was rearranged by many reciprocal translocations between chromosomes. Protein pairs derived from this duplication event make up 13% of all yeast proteins, and include pairs of transcription factors, protein kinases, myosins, cyclins and pheromones. Tetraploidy may have facilitated the evolution of anaerobic fermentation in Saccharomyces.
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PYC1 is an ohnolog of the universally conserved PYC2, resulting from the whole genome duplication event that occurred during the evolution of Saccharomycetaceae.
“PYC1 is an ohnolog of the universally conserved PYC2, resulting from the whole genome duplication (WGD) event that occurred during the evolution of Saccharomycetaceae (Wolfe and Shields 1997; Byrne and Wolfe 2005)”
From Mitochondrial retrograde control of transcription evolves with respiratory stress, metabolic adaptation, and virulence in budding yeasts (2026) · cites this paper as Wolfe and Shields 1997
Cites
Basic local alignment search tool
Altschul, S. F., Gish, W., Miller, W., Myers, E. W., & Lipman, D. J. (1990) · Journal of Molecular Biology · doi:10.1006/jmbi.1990.9999 · Cited by 98,669 · see citing works
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Initial sequencing and analysis of the human genome
International Human Genome Sequencing Consortium, Whitehead Institute for Biomedical Research, C. F. G. R., Lander, E. S., Linton, L. M., Birren, B., Nusbaum, C., Zody, M. C., Baldwin, J., Devon, K., Dewar, K., et al. (2001) · Nature · doi:10.1038/35057062 · Cited by 24,216 · see citing works
Self-citationWinzeler, E. A., Shoemaker, D. D., Astromoff, A., Liang, H., Anderson, K., Andre, B., Bangham, R., Benito, R., Boeke, J. D., Bussey, H., et al. (1999) · Science · doi:10.1126/science.285.5429.901 · Cited by 3,953 · see citing works
The economics of ribosome biosynthesis in yeast
Warner, J. R. (1999) · Trends in Biochemical Sciences · doi:10.1016/s0968-0004(99)01460-7 · Cited by 1,933 · see citing works
Whole-Genome Shotgun Assembly and Analysis of the Genome of <i>Fugu rubripes</i>
Aparicio, S., Chapman, J., Stupka, E., Putnam, N., Chia, J.-M., Dehal, P., Christoffels, A., Rash, S., Hoon, S., Smit, A., et al. (2002) · Science · doi:10.1126/science.1072104 · Cited by 1,591 · see citing works
Dujon, B., Sherman, D., Fischer, G., Durrens, P., Casaregola, S., Lafontaine, I., de Montigny, J., Marck, C., Neuvéglise, C., Talla, E., et al. (2004) · Nature · doi:10.1038/nature02579 · Cited by 1,623 · see citing works
Genome-scale approaches to resolving incongruence in molecular phylogenies.
Rokas, A., Williams, B. L., King, N., & Carroll, S. B. (2003) · Nature · doi:10.1038/nature02053 · Cited by 1,512 · see citing works
The evolutionary significance of ancient genome duplications
Van de Peer, Y., Maere, S., & Meyer, A. (2009) · Nature Reviews Genetics · doi:10.1038/nrg2600 · Cited by 1,129 · see citing works
A Recent Polyploidy Superimposed on Older Large-Scale Duplications in the <i>Arabidopsis</i> Genome
Blanc, G., Hokamp, K., & Wolfe, K. H. (2003) · Genome Research · doi:10.1101/gr.751803 · Cited by 724 · see citing works
Self-citation<em>Saccharomyces cerevisiae</em> and its industrial applications
Parapouli, M., 1 Molecular Biology laboratory, D. O. B. A. A. T., Vasileiadi, A., Afendra, A.-S., Hatziloukas, E., 2 Genetics laboratory, D. O. B. A. A. T., & equally, #. T. T. A. C. (2020) · AIMS Microbiology · doi:10.3934/microbiol.2020001 · Cited by 685 · see citing works
Highly Expressed Genes in Yeast Evolve Slowly
Pál, C., Papp, B., & Hurst, L. D. (2001) · Genetics · doi:10.1093/genetics/158.2.927 · Cited by 635 · see citing works
Candida albicans: A molecular revolution built on lessons from budding yeast
Berman, J., & Sudbery, P. E. (2002) · Nature Reviews Genetics · doi:10.1038/nrg948 · Cited by 578 · see citing works
Extensive genomic duplication during early chordate evolution
McLysaght, A., Hokamp, K., & Wolfe, K. H. (2002) · Nature Genetics · doi:10.1038/ng884 · Cited by 530 · see citing works
Self-citationGene duplication and the adaptive evolution of a classic genetic switch
Hittinger, C. T., & Carroll, S. B. (2007) · Nature · doi:10.1038/nature06151 · Cited by 439 · see citing works
Deeply conserved synteny resolves early events in vertebrate evolution
Simakov, O., Marlétaz, F., Yue, J.-X., O’Connell, B., Jenkins, J., Brandt, A., Calef, R., Tung, C.-H., Huang, T.-K., Schmutz, J., et al. (2020) · Nature Ecology & Evolution · doi:10.1038/s41559-020-1156-z · Cited by 363 · see citing works
Resurrecting ancestral alcohol dehydrogenases from yeast
Thomson, J. M., Gaucher, E. A., Burgan, M. F., De Kee, D. W., Li, T., Aris, J. P., & Benner, S. A. (2005) · Nature Genetics · doi:10.1038/ng1553 · Cited by 341 · see citing works
How good are deep phylogenetic trees?
Philippe, H., & Laurent, J. (1998) · Current Opinion in Genetics & Development · doi:10.1016/s0959-437x(98)80028-2 · Cited by 324 · see citing works
An evolutionary perspective on the Crabtree effect
Pfeiffer, T., & Morley, A. (2014) · Frontiers in Molecular Biosciences · doi:10.3389/fmolb.2014.00017 · Cited by 318 · see citing works
More than the sum of their parts: On the evolution of proteins from peptides
Söding, J., & Lupas, A. N. (2003) · BioEssays · doi:10.1002/bies.10321 · Cited by 252 · see citing works
Candida glabrata: A review of its features and resistance
Rodrigues, C. F., Silva, S., & Henriques, M. (2014) · European Journal of Clinical Microbiology & Infectious Diseases · doi:10.1007/s10096-013-2009-3 · Cited by 268 · see citing works
Transcriptional regulation of carbohydrate metabolism in the human pathogen Candida albicans
Askew, C., Sellam, A., Epp, E., Hogues, H., Mullick, A., Nantel, A., & Whiteway, M. (2009) · PLoS Pathogens · doi:10.1371/journal.ppat.1000612 · Cited by 260 · see citing works
Evolutionarily conserved gene family important for fat storage
Kadereit, B., Kumar, P., Wang, W.-J., Miranda, D., Snapp, E. L., Severina, N., Torregroza, I., Evans, T., & Silver, D. L. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0708579105 · Cited by 252 · see citing works
Scannell, D. R., Frank, A. C., Conant, G. C., Byrne, K. P., Woolfit, M., & Wolfe, K. H. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0608218104 · Cited by 235 · see citing works
Increased glycolytic flux as an outcome of whole-genome duplication in yeast
Conant, G. C., & Wolfe, K. H. (2007) · Molecular Systems Biology · doi:10.1038/msb4100170 · Cited by 222 · see citing works
Self-citationYeasts illustrate the molecular mechanisms of eukaryotic genome evolution
DUJON, B. (2006) · Trends in Genetics · doi:10.1016/j.tig.2006.05.007 · Cited by 224 · see citing works
Hagman, A., Säll, T., Compagno, C., & Piskur, J. (2013) · PLoS ONE · doi:10.1371/journal.pone.0068734 · Cited by 219 · see citing works
Phylogenetic diversity of stress signalling pathways in fungi
Nikolaou, E., Agrafioti, I., Stumpf, M., Quinn, J., Stansfield, I., & Brown, A. J. (2009) · BMC Evolutionary Biology · doi:10.1186/1471-2148-9-44 · Cited by 206 · see citing works
The <i>Candida albicans CaACE2</i> gene affects morphogenesis, adherence and virulence
Kelly, M. T., MacCallum, D. M., Clancy, S. D., Odds, F. C., Brown, A. J. P., & Butler, G. (2004) · Molecular Microbiology · doi:10.1111/j.1365-2958.2004.04185.x · Cited by 175 · see citing works
A second iron-regulatory system in yeast independent of Aft1p
Rutherford, J. C., Jaron, S., Ray, E., Brown, P. O., & Winge, D. R. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.261381198 · Cited by 153 · see citing works
Hidden in plain sight: what remains to be discovered in the eukaryotic proteome?
Wood, V., Lock, A., Harris, M. A., Rutherford, K., Bähler, J., & Oliver, S. G. (2019) · Open Biology · doi:10.1098/rsob.180241 · Cited by 132 · see citing works
A model of yeast glycolysis based on a consistent kinetic characterisation of all its enzymes
Smallbone, K., Messiha, H. L., Carroll, K. M., Winder, C. L., Malys, N., Dunn, W. B., Murabito, E., Swainston, N., Dada, J. O., Khan, F., et al. (2013) · FEBS Letters · doi:10.1016/j.febslet.2013.06.043 · Cited by 147 · see citing works
Regulation of the Hypoxic Response in Candida albicans
Synnott, J. M., Guida, A., Mulhern-Haughey, S., Higgins, D. G., & Butler, G. (2010) · Eukaryotic Cell · doi:10.1128/ec.00159-10 · Cited by 132 · see citing works
Caffrey, D. R., O'Neill, L. A. J., & Shields, D. C. (1999) · Journal of Molecular Evolution · doi:10.1007/pl00006578 · Cited by 124 · see citing works
Self-citationGenome plasticity in Candida albicans is driven by long repeat sequences
Todd, R. T., Wikoff, T. D., Forche, A., & Selmecki, A. (2019) · eLife · doi:10.7554/elife.45954 · Cited by 118 · see citing works
Baek, Y.-U., Li, M., & Davis, D. A. (2008) · Eukaryotic Cell · doi:10.1128/ec.00108-08 · Cited by 109 · see citing works
Evolutionary genomics of yeast pathogens in the Saccharomycotina
Gabaldón, T., Naranjo-Ortíz, M. A., & Marcet-Houben, M. (2016) · FEMS Yeast Research · doi:10.1093/femsyr/fow064 · Cited by 105 · see citing works
Highly variable rates of genome rearrangements between hemiascomycetous yeast lineages
Fischer, G., Rocha, E. P. C., Brunet, F., Vergassola, M., & Dujon, B. (2006) · PLoS Genetics · doi:10.1371/journal.pgen.0020032 · Cited by 101 · see citing works
Gabaldón, T., & Carreté, L. (2016) · FEMS Yeast Research · doi:10.1093/femsyr/fov110 · Cited by 99 · see citing works
Neubauer, M., Zhu, Z., Penka, M., Helmschrott, C., Wagener, N., & Wagener, J. (2015) · Molecular Microbiology · doi:10.1111/mmi.13167 · Cited by 76 · see citing works
Evolutionary principles of modular gene regulation in yeasts
Thompson, D. A., Roy, S., Chan, M., Styczynsky, M. P., Pfiffner, J., French, C., Socha, A., Thielke, A., Napolitano, S., Muller, P., et al. (2013) · eLife · doi:10.7554/elife.00603 · Cited by 78 · see citing works
Muller, H., Thierry, A., Coppée, J.-Y., Gouyette, C., Hennequin, C., Sismeiro, O., Talla, E., Dujon, B., & Fairhead, C. (2009) · Fungal Genetics and Biology · doi:10.1016/j.fgb.2008.11.006 · Cited by 78 · see citing works
Adaptation to environmental pH: integrating the Rim101 and calcineurin signal transduction pathways
Kullas, A. L., Martin, S. J., & Davis, D. (2007) · Molecular Microbiology · doi:10.1111/j.1365-2958.2007.05929.x · Cited by 75 · see citing works
Maguire, S. L., Wang, C., Holland, L. M., Brunel, F., Neuvéglise, C., Nicaud, J.-M., Zavrel, M., White, T. C., Wolfe, K. H., & Butler, G. (2014) · PLoS Genetics · doi:10.1371/journal.pgen.1004076 · Cited by 69 · see citing works
Self-citationKok, S., Nijkamp, J. F., Oud, B., Roque, F. C., Ridder, D., Daran, J.-M., Pronk, J. T., & Maris, A. J. A. (2012) · FEMS Yeast Research · doi:10.1111/j.1567-1364.2011.00787.x · Cited by 65 · see citing works
Mitochondrial stress-dependent regulation of cellular protein synthesis
Topf, U., Uszczynska-Ratajczak, B., & Chacinska, A. (2019) · Journal of Cell Science · doi:10.1242/jcs.226258 · Cited by 52 · see citing works
Evolution of ecological dominance of yeast species in high-sugar environments
Williams, K. M., Liu, P., & Fay, J. C. (2015) · Evolution · doi:10.1111/evo.12707 · Cited by 59 · see citing works
Gale, A. N., Sakhawala, R. M., Levitan, A., Sharan, R., Berman, J., Timp, W., & Cunningham, K. W. (2020) · G3 Genes|Genomes|Genetics · doi:10.1534/g3.120.401595 · Cited by 56 · see citing works
How Microbes Adapt to a Diversity of Food Niches
Papadimitriou, K., Pot, B., & Tsakalidou, E. (2015) · Current Opinion in Food Science · doi:10.1016/j.cofs.2015.01.001 · Cited by 47 · see citing works
Li, Y., Li, H., Sui, M., Li, M., Wang, J., Meng, Y., Sun, T., Liang, Q., Suo, C., Gao, X., et al. (2019) · Communications Biology · doi:10.1038/s42003-019-0419-1 · Cited by 42 · see citing works
Nespolo, R. F., Solano‐Iguaran, J. J., Paleo‐López, R., Quintero‐Galvis, J. F., Cubillos, F. A., & Bozinovic, F. (2020) · Ecology and Evolution · doi:10.1002/ece3.6208 · Cited by 9 · see citing works
Golik, P. (2024) · IUBMB Life · doi:10.1002/iub.2779 · Cited by 9 · see citing works
Ribosomal flavours: An acquired taste for specific mRNAs?
Bates, C., Hubbard, S. J., & Ashe, M. P. (2018) · Biochemical Society Transactions · doi:10.1042/bst20180160 · Cited by 8 · see citing works
Nahas, J. V., Iosue, C. L., Shaik, N. F., Selhorst, K., He, B. Z., & Wykoff, D. D. (2018) · G3 Genes Genomes Genetics · doi:10.1534/g3.118.200303 · Cited by 8 · see citing works
Łabędzka-Dmoch, K., Bui, T. H. D., Piątkowski, J., Dilling, M., Jagiełło, P., Kabza, W., & Golik, P. (2026) · Molecular Biology and Evolution · doi:10.1093/molbev/msag005 · Cited by 1 · see citing works
- Authors
- Wolfe, K. H., & Shields, D. C.
- Affiliations
- Trinity College Dublin (IE)
- Corresponding author
- Wolfe, Kenneth H.
- Venue
- Nature
- Published
- 1997-06-12
- Volume
- 387
- Issue
- 6634
- Pages
- 708-713
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- OpenAlex
- W1641544182
- Cited by
- 1,785
- References
- 1
- Citations by year
- 2026: 21 · 2025: 28 · 2024: 36 · 2023: 42 · 2022: 41 · 2021: 55 · 2020: 53 · 2019: 50 · 2018: 45 · 2017: 63 · 2016: 53 · 2015: 48 · 2014: 80 · 2013: 69 · 2012: 83
- FWCI
- 91.59
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- Funders
- Wellcome Trust
- European Commission
- Topics
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Chromosomal and Genetic Variations
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Fungal and yeast genetics research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genome Rearrangement Algorithms
- Keywords
- whole-genome duplication, polyploidy, Saccharomyces cerevisiae, tetraploidy, gene duplication, gene order, reciprocal translocation, duplicate gene retention, gene deletion, transcription factors, protein kinases, myosin, cyclins, pheromones, anaerobic fermentation
- MeSH terms
- Multigene Family, Kluyveromyces, Models, Genetic, Phylogeny, Ploidies, Saccharomyces cerevisiae, Chromosomes, Fungal, Genome, Fungal, Evolution, Molecular
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