Independent sorting-out of thousands of duplicated gene pairs in two yeast species descended from a whole-genome duplication.
Open accessAbstract
Among yeasts that underwent whole-genome duplication (WGD), Kluyveromyces polysporus represents the lineage most distant from Saccharomyces cerevisiae. By sequencing the K. polysporus genome and comparing it with the S. cerevisiae genome using a likelihood model of gene loss, we show that these species diverged very soon after the WGD, when their common ancestor contained >9,000 genes. The two genomes subsequently converged onto similar current sizes (5,600 protein-coding genes each) and independently retained sets of duplicated genes that are strikingly similar. Almost half of their surviving single-copy genes are not orthologs but paralogs formed by WGD, as would be expected if most gene pairs were resolved independently. In addition, by comparing the pattern of gene loss among K. polysporus, S. cerevisiae, and three other yeasts that diverged after the WGD, we show that the patterns of gene loss changed over time. Initially, both members of a duplicate pair were equally likely to be lost, but loss of the same gene copy in independent lineages was increasingly favored at later time points. This trend parallels an increasing restriction of reciprocal gene loss to more slowly evolving gene pairs over time and suggests that, as duplicate genes diverged, one gene copy became favored over the other. The apparent low initial sequence divergence of the gene pairs leads us to propose that the yeast WGD was probably an autopolyploidization.
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These Ty-like retrotransposon genes (Tkp5-1 to -9) were most similar to the Tkp5 protein from V. polyspora.
“These Ty-like retrotransposons genes (named here Tkp5-1 to -9) were most similar to the Tkp5 protein from V. polyspora, a yeast representing the postwhole-genome duplication lineage most divergent from S. cerevisiae (Scannell et al. 2007).”
From Comparative Genomics of Two Sequential <i>Candida glabrata</i> Clinical Isolates (2017) · cites this paper as Scannell et al. 2007
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Vakirlis, N., Sarilar, V., Drillon, G., Fleiss, A., Agier, N., Meyniel, J.-P., Blanpain, L. T., Carbone, A., Devillers, H., Dubois, K., et al. (2016) · Genome Research · doi:10.1101/gr.204420.116 · Cited by 94 · see citing works
“Yeast has exemplified the evolutionary importance of gene duplications and losses since the demonstration of an ancestral WGD in the S. cerevisiae lineage (Wolfe and Shields 1997; Fischer et al. 2001; Dietrich et al. 2004; Kellis et al. 2004; Scannell et al. 2007).”
BackgroundSémon, M., & Wolfe, K. H. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0708705105 · Cited by 97 · see citing works
“This hypothesis is supported by our laboratory’s previous work on WGD in yeast, where we found that slow-evolving genes retained their interchangeability for a longer time period after WGD than fastevolving genes (45, 46).”
ResultDRIMM-Synteny: decomposing genomes into evolutionary conserved segments
Pham, S., & Pevzner, P. A. (2010) · Bioinformatics · doi:10.1093/bioinformatics/btq465 · Cited by 97 · see citing works
“The yeast gene orders were extracted from (Kellis et al., 2004) and (Scannell et al., 2007).”
MethodNovel genes exhibit distinct patterns of function acquisition and network integration
Capra, J. A., Pollard, K. S., & Singh, M. (2010) · Genome biology · doi:10.1186/gb-2010-11-12-r127 · Cited by 89 · see citing works
“Recently, several studies have demonstrated the relevance of the scale of a duplication that copies a gene to its functional consequences [28-30].”
BackgroundComplex Nature of the Genome in a Wine Spoilage Yeast, Dekkera bruxellensis
Hellborg, L., & Piškur, J. (2009) · Eukaryotic Cell · doi:10.1128/ec.00115-09 · Cited by 86 · see citing works
“This nonrandom deletion of gene copies was also previously observed for other yeasts (31) and Arabidopsis thaliana (38).”
BackgroundZhang, Q., Guan, P.-P., Zhao, L., Ma, M., Xie, L., Li, Y., Zheng, R., Ouyang, W.-Z., Wang, S., Li, H., et al. (2020) · Molecular Plant · doi:10.1016/j.molp.2020.12.020 · Cited by 62 · see citing works
Recent allopolyploid origin of Zygosaccharomyces rouxii strain ATCC 42981
Gordon, J., & Wolfe, K. H. (2008) · Yeast · doi:10.1002/yea.1598 · Cited by 84 · see citing works
“From observations made in the Saccharomyces lineage, both on evolutionary (Scannell et al., 2007) and laboratory timescales (Antunovics et al.”
BackgroundEmery, M. L., Willis, M. M. S., Hao, Y., Barry, K., Oakgrove, K. S., Peng, Y., Schmutz, J., Lyons, E. H., Pires, J. C., Edger, P. P., et al. (2018) · PLoS Genetics · doi:10.1371/journal.pgen.1007267 · Cited by 81 · see citing works
“In previous work in yeast [15, 22, 70], we found evidence for “convergent” gene losses that were phylogenetically independent and yet more often from the same subgenome than could be explained by chance.”
BackgroundMethodInfluentialMehta, S., Li, H., Hogan, P. G., & Cunningham, K. W. (2009) · Molecular and Cellular Biology · doi:10.1128/mcb.01197-08 · Cited by 83 · see citing works
“[pSM012 and pSM015]) and Rcn1(1-172)SalI-3 (for inserts truncated before the”
BackgroundMethodInfluentialEvolutionary Capture of Viral and Plasmid DNA by Yeast Nuclear Chromosomes
Frank, A. C., & Wolfe, K. H. (2009) · Eukaryotic Cell · doi:10.1128/ec.00110-09 · Cited by 81 · see citing works
Mitochondrial inheritance in budding yeasts: towards an integrated understanding
Solieri, L. (2010) · Trends in Microbiology · doi:10.1016/j.tim.2010.08.001 · Cited by 80 · 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
“K. polysporus, the most basal post-WGD species (Scannell et al., 2007) has an intermediate phenotype between respiro-fermentative and respiratory (Figure 1A, light blue).”
BackgroundExtensive DNA-binding specificity divergence of a conserved transcription regulator
Baker, C. R., Tuch, B. B., & Johnson, A. D. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1019177108 · Cited by 75 · see citing works
“albicans αsgs were mapped across 38 genome-sequenced yeasts (10, 11, 13, 28, 46, 48).”
BackgroundThe Inside-Out Mechanism of Dicers from Budding Yeasts
Weinberg, D. E., Nakanishi, K., Patel, D. J., & Bartel, D. P. (2011) · Cell · doi:10.1016/j.cell.2011.06.021 · Cited by 73 · see citing works
Phylogenomic evolutionary surveys of subtilase superfamily genes in fungi
Li, J., Gu, F., Wu, R., Yang, J., & Zhang, K. (2017) · Scientific Reports · doi:10.1038/srep45456 · Cited by 75 · see citing works
Kienle, N., Kloepper, T. H., & Fasshauer, D. (2009) · BMC Evolutionary Biology · doi:10.1186/1471-2148-9-19 · Cited by 72 · see citing works
“In fact, it has been proposed that these lineages must have diverged and adapted to different living conditions very soon after the WGD, so that the genes retained in duplicates diverged largely independently [65].”
BackgroundAlternative Splicing and Subfunctionalization Generates Functional Diversity in Fungal Proteomes
Marshall, A. N., Montealegre, M. C., Jiménez-López, C., Lorenz, M. C., & van Hoof, A. (2013) · PLoS Genetics · doi:10.1371/journal.pgen.1003376 · Cited by 71 · see citing works
“retained different subsets of duplicated genes [9].”
Clade- and species-specific features of genome evolution in the Saccharomycetaceae
Wolfe, K. H., Armisén, D., Proux‐Wéra, E., hÉigeartaigh, S. Ó., Azam, H., Gordon, J., & Byrne, K. P. (2015) · FEMS Yeast Research · doi:10.1093/femsyr/fov035 · Cited by 64 · see citing works
Physical methods for genetic transformation of fungi and yeast
Rivera, A. L., Magaña-Ortíz, D., Gómez-Lim, M. Á., Fernández, F., & Loske, A. M. (2014) · Physics of Life Reviews · doi:10.1016/j.plrev.2014.01.007 · Cited by 64 · see citing works
Solvent Exposure Imparts Similar Selective Pressures across a Range of Yeast Proteins
Conant, G. C., & Stadler, P. F. (2009) · Molecular Biology and Evolution · doi:10.1093/molbev/msp031 · Cited by 63 · see citing works
Comparative Analysis of Chromosome Counts Infers Three Paleopolyploidies in the Mollusca
Hallinan, N., & Lindberg, D. R. (2011) · Genome Biology and Evolution · doi:10.1093/gbe/evr087 · Cited by 64 · see citing works
Lipinski, K. A., Puchta, O., Surendranath, V., Kudla, M., & Golik, P. (2011) · Molecular Biology and Evolution · doi:10.1093/molbev/msr120 · Cited by 62 · see citing works
“2003), Vanderwaltozyma polyspora (Scannell et al. 2007), Kluyveromyces lactis (Zivanovic et al.”
BackgroundComparative Genomics of Two Sequential <i>Candida glabrata</i> Clinical Isolates
Vale-Silva, L., Beaudoing, E., Tran, V. D. T., & Sanglard, D. (2017) · G3 Genes|Genomes|Genetics · doi:10.1534/g3.117.042887 · Cited by 61 · see citing works
“These Ty-like retrotransposons genes (named here Tkp5-1 to -9) were most similar to the Tkp5 protein from Vanderwaltozyma polyspora, a yeast representing the post-whole genome duplication (WGD) lineage most divergent from Saccharomyces cerevisiae (Scannell et al. 2007).”
MethodPathogenic Allodiploid Hybrids of Aspergillus Fungi
Steenwyk, J. L., Lind, A., Ries, L. N. A., dos Reis, T. F., Silva, L. P., Almeida, F. B. D. R., Bastos, R. W., Fraga‐Silva, T. F. D. C., Bonato, V. L. D., Pessoni, A. M., et al. (2020) · Current Biology · doi:10.1016/j.cub.2020.04.071 · Cited by 54 · see citing works
“For example, an ancient allodiploid hybridization event in the budding yeast lineage that includes the baker’s yeast Saccharomyces cerevisiae [9] was quickly followed by rapid gene loss in the parental genomes [53], with estimates suggesting that 10% of genes were lost in the first 10 Ma following hybridization [53].”
BackgroundFitness benefits of loss of heterozygosity in Saccharomyces hybridsPreprint
Lancaster, S. M., Payen, C., Heil, C. S., & Dunham, M. J. (2019) · Genome Research · doi:10.1101/gr.245605.118 · Cited by 57 · see citing works
“Resolution of the ancestral whole genome duplication in Saccharomyces involved loss of the majority of duplicated genes, in a process that began shortly after the initial hybridization event (Scannell et al. 2007).”
Background“Changing by doubling”, the impact of Whole Genome Duplications in the evolution of eukaryotes
Jaillon, O., Aury, J., & Wincker, P. (2008) · Comptes Rendus Biologies · doi:10.1016/j.crvi.2008.07.007 · Cited by 57 · see citing works
Muir, A. K. S., Harrison, E., & Wheals, A. E. (2011) · FEMS Yeast Research · doi:10.1111/j.1567-1364.2011.00745.x · Cited by 55 · see citing works
“Saccharomyces cerevisiae itself is probably an autopolyploid (Scannell et al., 2007) and has undergone genome evolution while maximizing its ª 2011 Federation of European Microbiological Societies FEMS Yeast Res 11 (2011) 552–563 Published by Blackwell Publishing Ltd.”
BackgroundIntron Evolution in Saccharomycetaceae
Hooks, K. B., Delneri, D., & Griffiths‐Jones, S. (2014) · Genome Biology and Evolution · doi:10.1093/gbe/evu196 · Cited by 51 · see citing works
Conant, G. C., & Wolfe, K. H. (2008) · Genetics · doi:10.1534/genetics.107.074450 · Cited by 53 · see citing works
“Probabilistic track assignment: Our original analysis assumed that every single-copy gene in a post-WGD genome could be unambiguously assigned as either a paralog or an ortholog of the corresponding genes in the other species (the ‘‘alignment’’ problem described in the Introduction; Scannell et al. 2007).”
BackgroundMethodResultInfluentialSpecialized Sugar Sensing in Diverse Fungi
Brown, V. E., Sabina, J., & Johnston, M. (2009) · Current Biology · doi:10.1016/j.cub.2009.01.056 · Cited by 50 · see citing works
“Data were compiled from references [3-8], in addition to the SGD database (www.”
Evolutionary Significance of Whole-Genome Duplication
McGrath, C., & Lynch, M. (2012) · Springer eBooks · doi:10.1007/978-3-642-31442-1_1 · Cited by 49 · see citing works
Evangelisti, A. M., & Conant, G. C. (2010) · Genome Biology and Evolution · doi:10.1093/gbe/evq067 · Cited by 46 · see citing works
“1; Scannell et al. 2006, 2007).”
BackgroundUnique genes in plants: specificities and conserved features throughout evolution
Armisén, D., Lecharny, A., & Aubourg, S. (2008) · BMC Evolutionary Biology · doi:10.1186/1471-2148-8-280 · Cited by 46 · see citing works
“Indeed, evolution is not a one-direction process and a high proportion of duplicated genes are rapidly lost [6,16,17].”
BackgroundLaere, S. D. M. V., Saerens, S., Verstrepen, K. J., Dijck, P. V., Thevelein, J. M., & Delvaux, F. R. (2008) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-008-1366-9 · Cited by 46 · see citing works
“glabrata can be explained by speciation associated with reciprocal gene loss during evolution after the WGD (Scannell et al. 2006; Scannell et al. 2007).”
BackgroundInfluentialWatching the grin fade: Tracing the effects of polyploidy on different evolutionary time scales
Mayfield‐Jones, D., Washburn, J. D., Arias, T., Edger, P. P., Pires, J. C., & Conant, G. C. (2013) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2013.02.002 · Cited by 45 · see citing works
Hayashi, A., Nagafuchi, H., Ito, I., Hirota, K., Yoshida, M., & Ozaki, S. (2009) · Modern Rheumatology · doi:10.1007/s10165-009-0151-7 · Cited by 45 · see citing works
Conant, G. C. (2014) · Molecular Biology and Evolution · doi:10.1093/molbev/msu250 · Cited by 46 · see citing works
Medina, E. M., Jones, G. W., & Fitzpatrick, D. A. (2011) · Journal of Molecular Evolution · doi:10.1007/s00239-011-9461-4 · Cited by 44 · see citing works
“polyspora has undergone a WGD (Scannell et al. 2007) and we expected it to form a monophyletic clade with the other WGD species.”
BackgroundInfluentialIntegrating Networks, Phylogenomics, and Population Genomics for the Study of Polyploidy
Blischak, P. D., Mabry, M. E., Conant, G. C., & Pires, J. C. (2018) · Annual Review of Ecology Evolution and Systematics · doi:10.1146/annurev-ecolsys-121415-032302 · Cited by 44 · see citing works
Dietrich, F. S., Voegeli, S., Kuo, S., & Philippsen, P. (2013) · G3 Genes Genomes Genetics · doi:10.1534/g3.112.002881 · Cited by 43 · see citing works
“All ORFs from the A aceri insect isolate 38 were also named following the A. gossypii nomenclature of the reference strain ATCC10895 irrespective of the translocations but adding an “ Aaceri ” prior to the systematic name.”
Evolution of the eukaryotic dynactin complex, the activator of cytoplasmic dynein
Hammesfahr, B., & Kollmar, M. (2012) · BMC Evolutionary Biology · doi:10.1186/1471-2148-12-95 · Cited by 43 · see citing works
“The absence of dynein and dynactin in Vanderwaltozyma is most likely related to the specific phenotypic feature that spores are formed by extra mitotic replications after meiosis independent of bud formation [75].”
Convergent Evolution and the Origin of Complex Phenotypes in the Age of Systems Biology
Washburn, J. D., Bird, K. A., Conant, G. C., & Pires, J. C. (2016) · International Journal of Plant Sciences · doi:10.1086/686009 · Cited by 42 · see citing works
“The majority of these duplicate genes are lost soon after the WGD event (Scannell et al. 2007).”
BackgroundThe lasting after-effects of an ancient polyploidy on the genomes of teleosts
Conant, G. C. (2020) · PLoS ONE · doi:10.1371/journal.pone.0231356 · Cited by 33 · see citing works
“These last two states model the potential for the independent parallel losses first seen in yeast [40, 61].”
BackgroundMethodAbdullaeva, Y., Ratering, S., Manirajan, B. A., Rosado-Porto, D., Schnell, S., & Cardinale, M. (2022) · Frontiers in Plant Science · doi:10.3389/fpls.2021.806915 · Cited by 41 · see citing works
Co-Evolution of Transcriptional Silencing Proteins and the DNA Elements Specifying Their Assembly
Zill, O. A., Scannell, D. R., Teytelman, L., & Rine, J. (2010) · PLoS Biology · doi:10.1371/journal.pbio.1000550 · Cited by 40 · see citing works
“Although SIR2 and SIR3 each have a paralog resulting from the whole-genome duplication (SIR2 has three additional, more ancient paralogs), neither gene has experienced subsequent duplication or loss events [27,28].”
BackgroundDynamics of Gene Loss following Ancient Whole-Genome Duplication in the Cryptic Paramecium Complex
Goût, J.-F., Hao, Y., Johri, P., Arnaiz, O., Doak, T. G., Bhullar, S., Couloux, A., Guèrin, F., Malinsky, S., Potekhin, A. A., et al. (2023) · Molecular Biology and Evolution · doi:10.1093/molbev/msad107 · Cited by 51 · see citing works
“Application of the same analysis to non-Paramecium lineages having experienced a genome duplication (Jaillon et al. 2004; Scannell et al. 2007; Berthelot et al. 2014; Session et al. 2016; Ren et al. 2018) reveals that the rate of gene loss per synonymous substitution is lower in Paramecium than in…”
InfluentialRecent advances in understanding the roles of whole genome duplications in evolution
MacKintosh, C., & Ferrier, D. E. K. (2017) · F1000Research · doi:10.12688/f1000research.11792.1 · Cited by 37 · see citing works
“…suggest that around 4000 genes still existed in duplicate when these genera were diverging from each other, with subsequent losses of different paralogues in different lineages, such that, for example, S. cerevisiae now has 551 pairs of ohnologues and Candida glabrata has 404 pairs 55,67,74 .”
BackgroundRelaxation of yeast mitochondrial functions after whole-genome duplicationPreprint
Jiang, H., Guan, W., Pinney, D., Wang, W., & Gu, Z. (2008) · Genome Research · doi:10.1101/gr.074674.107 · Cited by 36 · see citing works
“castellii occurred ∼80–90 Mya (Scannell et al. 2007).”
BackgroundGuo, W., Wu, H., Zhang, Z., Yang, C., Hu, L., Shi, X., Jian, S., Shi, S., & Huang, Y. (2017) · Frontiers in Plant Science · doi:10.3389/fpls.2017.00795 · Cited by 36 · see citing works
“Previous studies have reported a pattern of parallel paleolog retention in several different lineages (Aury et al., 2006; Schranz and Mitchell-Olds, 2006; Scannell et al., 2007; Barker et al., 2008).”
BackgroundMechanism of MRX inhibition by Rif2 at telomeres
Roisné-Hamelin, F., Pobiega, S., Jézéquel, K., Miron, S. M., Dépagne, J., Veaute, X., Busso, D., Du, M. L., Callebaut, I., Charbonnier, J., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-23035-w · Cited by 36 · see citing works
“Mutations in the F8 and R12 residues, C-terminal truncation past residue 26 and a N-terminal truncation (6-31) weaken or abolish the interaction with Rad50 (Fig.”
BackgroundInfluentialWidespread Recurrent Evolution of Genomic Features
Maeso, I., Roy, S. W., & Irimia, M. (2012) · Genome Biology and Evolution · doi:10.1093/gbe/evs022 · Cited by 36 · see citing works
Species Tree Estimation and the Impact of Gene Loss Following Whole-Genome Duplication
Xiong, H., Wang, D., Shao, C., Yang, X., Yang, J., Ma, T., Davis, C. “., Liu, L., & Xi, Z. (2022) · Systematic Biology · doi:10.1093/sysbio/syac040 · Cited by 32 · see citing works
“For example, convergent loss of paralogs has shown to be about three times more frequent than reciprocal loss of paralogs in yeasts [09:05 27/9/2022 Sysbio-OP-SYSB220040.tex] Page: 1353 1348–1361 (Scannell et al. 2006; Scannell et al. 2007).”
BackgroundPfliegler, W. P., Antunovics, Z., & Sipiczki, M. (2012) · FEMS Yeast Research · doi:10.1111/j.1567-1364.2012.00820.x · Cited by 35 · see citing works
Coate, J. E., Song, M. J., Bombarely, A., & Doyle, J. J. (2016) · New Phytologist · doi:10.1111/nph.14090 · Cited by 35 · see citing works
“Within a few million yr, however, most duplicated genes are silenced and/or removed from the genome (Lynch & Conery, 2000, 2003; Otto & Whitton, 2000; Blanc & Wolfe, 2004; Scannell et al., 2007; Moghe et al., 2014).”
Background
- Authors
- Scannell, D. R., Frank, A. C., Conant, G. C., Byrne, K. P., Woolfit, M., & Wolfe, K. H.
- Affiliations
- Trinity College Dublin (IE)
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2007-05-15
- Volume
- 104
- Issue
- 20
- Pages
- 8397-8402
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC1895961
- OpenAlex
- W2064322162
- Cited by
- 235
- References
- 30
- Citations by year
- 2026: 6 · 2025: 5 · 2024: 3 · 2023: 6 · 2022: 8 · 2021: 9 · 2020: 9 · 2019: 6 · 2018: 11 · 2017: 15 · 2016: 10 · 2015: 14 · 2014: 10 · 2013: 12 · 2012: 17
- FWCI
- 28.69
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- 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, gene loss, paralogs, orthologs, Saccharomyces cerevisiae, yeast evolution, autopolyploidization, gene family evolution, genome size reduction
- MeSH terms
- Base Sequence, Kluyveromyces, Models, Genetic, Molecular Sequence Data, Saccharomyces cerevisiae, Sequence Homology, Nucleic Acid, Time Factors, Likelihood Functions, Genome, Fungal, Conserved Sequence, Evolution, Molecular, Genes, Duplicate, Gene Duplication, Gene Order
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