A genome-wide view of the spectrum of spontaneous mutations in yeast.
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The mutation process ultimately defines the genetic features of all populations and, hence, has a bearing on a wide range of issues involving evolutionary genetics, inheritance, and genetic disorders, including the predisposition to cancer. Nevertheless, formidable technical barriers have constrained our understanding of the rate at which mutations arise and the molecular spectrum of their effects. Here, we report on the use of complete-genome sequencing in the characterization of spontaneously arising mutations in the yeast Saccharomyces cerevisiae. Our results confirm some findings previously obtained by indirect methods but also yield numerous unexpected findings, in particular a very high rate of point mutation and skewed distribution of base-substitution types in the mitochondrion, a very high rate of segmental duplication and deletion in the nuclear genome, and substantial deviations in the mutational profile among various model organisms.
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Assuming a per base mutation rate similar to that of haploid yeasts (0.33 10-9 per base per generation), each generation one would expect 0.0041 mutations in the genome.
“If we were to assume a per base mutation rate similar to that of haploid yeasts (estimated at 0.33 10-9 per base per generation) (Lynch et al., 2008), each generation one would expect 0.0041 mutations in the genome (0.33 10-9 × 12,3 106 bases in the genome = 4.1 10-3).”
From Genome Comparisons of Candida glabrata Serial Clinical Isolates Reveal Patterns of Genetic Variation in Infecting Clonal Populations (2019) · cites this paper as Lynch et al., 2008
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Cites
The Neutral Theory of Molecular Evolution
Kimura, M. (1979) · Scientific American · doi:10.1038/scientificamerican1179-98 · Cited by 7,698 · see citing works
Genome sequencing in microfabricated high-density picolitre reactors
Margulies, M., Egholm, M., Altman, W. E., Attiya, S., Bader, J. S., Bemben, L. A., Berka, J., Braverman, M. S., Chen, Y.-J., Chen, Z., et al. (2005) · Nature · doi:10.1038/nature03959 · Cited by 7,693 · see citing works
The Neutral Theory of Molecular Evolution
Kimura, M. (1983) · Cambridge University Press eBooks · doi:10.1017/cbo9780511623486 · Cited by 6,300 · see citing works
Friedberg, E. C., Walker, G. C., Siede, W., Wood, R. D., Schultz, R. A., & Ellenberger, T. (2005) · doi:10.1128/9781555816704 · Cited by 5,683 · see citing works
Drake, J. W., Charlesworth, B., Charlesworth, D., & Crow, J. F. (1998) · Genetics · doi:10.1093/genetics/148.4.1667 · Cited by 1,932 · see citing works
Strand, M. K., Prolla, T. A., Liskay, R. M., & Petes, T. D. (1993) · Nature · doi:10.1038/365274a0 · Cited by 1,077 · see citing works
The origins, patterns and implications of human spontaneous mutation
Crow, J. F. (2000) · Nature Reviews Genetics · doi:10.1038/35049558 · Cited by 928 · see citing works
Mutation Pressure and the Evolution of Organelle Genomic Architecture
Lynch, M., Koskella, B. L., & Schaack, S. (2006) · Science · doi:10.1126/science.1118884 · Cited by 597 · see citing works
Dunham, M. J., Badrane, H., Ferea, T., Adams, J., Brown, P. O., Rosenzweig, F., & Botstein, D. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.242624799 · Cited by 564 · see citing works
Widespread aneuploidy revealed by DNA microarray expression profiling
Hughes, T. R., Roberts, C. J., Dai, H. A., Jones, A. R., Meyer, M. R., Slade, D., Burchard, J., Dow, S., Ward, T. R., Kidd, M. J., et al. (2000) · Nature Genetics · doi:10.1038/77116 · Cited by 482 · see citing works
Mutation rate variation in multicellular eukaryotes: causes and consequences
Baer, C. F., Miyamoto, M. M., & Denver, D. R. (2007) · Nature Reviews Genetics · doi:10.1038/nrg2158 · Cited by 458 · see citing works
PERSPECTIVE: SPONTANEOUS DELETERIOUS MUTATION
Lynch, M., Blanchard, J. L., Houle, D., Kibota, T. T., Schultz, S. T., Vassilieva, L. L., & Willis, J. H. (1999) · Evolution · doi:10.1111/j.1558-5646.1999.tb05361.x · Cited by 454 · see citing works
Microsatellite Instability in Yeast: Dependence on the Length of the Microsatellite
Wierdl, M., Dominska, M., & Petes, T. D. (1997) · Genetics · doi:10.1093/genetics/146.3.769 · Cited by 401 · see citing works
Direct estimation of per nucleotide and genomic deleterious mutation rates in Drosophila
Liautard‐Haag, C., Dorris, M., Maside, X., Macaskill, S., Halligan, D. L., Charlesworth, B., & Keightley, P. D. (2007) · Nature · doi:10.1038/nature05388 · Cited by 396 · see citing works
Microsatellite Instability in Yeast: Dependence on Repeat Unit Size and DNA Mismatch Repair Genes
Sia, E. A., Kokoska, R. J., Dominska, M., Greenwell, P. W., & Petes, T. D. (1997) · Molecular and Cellular Biology · doi:10.1128/mcb.17.5.2851 · Cited by 392 · see citing works
The Origins of Eukaryotic Gene Structure
Lynch, M. (2005) · Molecular Biology and Evolution · doi:10.1093/molbev/msj050 · Cited by 391 · see citing works
Heterogeneous mutation processes in human microsatellite DNA sequences
Ellegren, H. (2000) · Nature Genetics · doi:10.1038/74249 · Cited by 377 · see citing works
Estimating the Per-Base-Pair Mutation Rate in the Yeast <i>Saccharomyces cerevisiae</i>
Lang, G. I., & Murray, A. W. (2008) · Genetics · doi:10.1534/genetics.107.071506 · Cited by 344 · see citing works
High mutation rate and predominance of insertions in the Caenorhabditis elegans nuclear genome
Denver, D. R., Morris, K., Lynch, M., & Thomas, W. K. (2004) · Nature · doi:10.1038/nature02697 · Cited by 340 · see citing works
Direct estimates of human per nucleotide mutation rates at 20 loci causing mendelian diseases
Kondrashov, A. S. (2002) · Human Mutation · doi:10.1002/humu.10147 · Cited by 336 · see citing works
Biased gene conversion: implications for genome and sex evolution
Marais, G. A. B. (2003) · Trends in Genetics · doi:10.1016/s0168-9525(03)00116-1 · Cited by 332 · see citing works
Genetic Properties Influencing the Evolvability of Gene Expression
Landry, C. R., Lemos, B., Rifkin, S. A., Dickinson, W. J., & Hartl, D. L. (2007) · Science · doi:10.1126/science.1140247 · Cited by 319 · see citing works
Tran, H. T., Keen, J. D., Kricker, M., Resnick, M. A., & Gordenin, D. A. (1997) · Molecular and Cellular Biology · doi:10.1128/mcb.17.5.2859 · Cited by 302 · see citing works
Rate and Pattern of Mutation at Microsatellite Loci in Maize
Vigouroux, Y., Jaqueth, J. S., Matsuoka, Y., Smith, O. S., Beavis, W. D., Smith, J. S. C., & Doebley, J. (2002) · Molecular Biology and Evolution · doi:10.1093/oxfordjournals.molbev.a004186 · Cited by 298 · see citing works
High Direct Estimate of the Mutation Rate in the Mitochondrial Genome of Caenorhabditis elegans
Denver, D. R., Morris, K., Lynch, M., Vassilieva, L. L., & Thomas, W. K. (2000) · Science · doi:10.1126/science.289.5488.2342 · Cited by 289 · see citing works
Drost, J. B., & Lee, W. R. (1995) · Environmental and Molecular Mutagenesis · doi:10.1002/em.2850250609 · Cited by 269 · see citing works
Birdsell, J. A. (2002) · Molecular Biology and Evolution · doi:10.1093/oxfordjournals.molbev.a004176 · Cited by 258 · see citing works
Instability of simple sequence DNA in Saccharomyces cerevisiae.
Henderson, S. T., & Petes, T. D. (1992) · Molecular and Cellular Biology · doi:10.1128/mcb.12.6.2749 · Cited by 237 · see citing works
Genomic Convergence toward Diploidy in Saccharomyces cerevisiae
Gerstein, A. C., Chun, H.-J. E., Grant, A., & Otto, S. P. (2006) · PLoS Genetics · doi:10.1371/journal.pgen.0020145 · Cited by 222 · see citing works
The mutation rates of di-, tri- and tetranucleotide repeats in Drosophila melanogaster
Schug, M. D., Hutter, C. M., Wetterstrand, K. A., Gaudette, M., Mackay, T. F. C., & Aquadro, C. F. (1998) · Molecular Biology and Evolution · doi:10.1093/oxfordjournals.molbev.a025901 · Cited by 222 · see citing works
Sequence-based estimation of minisatellite and microsatellite repeat variabilityPreprint
Legendre, M., Pochet, N. L. M. M., Pak, T. R., & Verstrepen, K. J. (2007) · Genome Research · doi:10.1101/gr.6554007 · Cited by 204 · see citing works
THE FITNESS EFFECTS OF SPONTANEOUS MUTATIONS IN CAENORHABDITIS ELEGANS
Vassilieva, L. L., Hook, A. M., & Lynch, M. F. (2000) · Evolution · doi:10.1111/j.0014-3820.2000.tb00557.x · Cited by 196 · see citing works
Maki, H. (2002) · Annual Review of Genetics · doi:10.1146/annurev.genet.36.042602.094806 · Cited by 191 · see citing works
Requirement of the Yeast MSH3 and MSH6 Genes for MSH2-dependent Genomic Stability
Johnson, R. E., Kovvali, G. K., Prakash, L., & Prakash, S. (1996) · Journal of Biological Chemistry · doi:10.1074/jbc.271.13.7285 · Cited by 188 · see citing works
Schlötterer, C., Ritter, R., Harr, B., & Brem, G. (1998) · Molecular Biology and Evolution · doi:10.1093/oxfordjournals.molbev.a025855 · Cited by 186 · see citing works
Marginal fitness contributions of nonessential genes in yeast
Thatcher, J. W., Shaw, J. M., & Dickinson, W. J. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.1.253 · Cited by 177 · see citing works
Spontaneous Mutations in Diploid Saccharomyces cerevisiae
Joseph, S., & Hall, D. W. (2004) · Genetics · doi:10.1534/genetics.104.033761 · Cited by 165 · see citing works
Wloch‐Salamon, D., Szafraniec, K., Borts, R. H., & Korona, R. (2001) · Genetics · doi:10.1093/genetics/159.2.441 · Cited by 163 · see citing works
Zeyl, C., & deVisser, J. A. G. M. (2001) · Genetics · doi:10.1093/genetics/157.1.53 · Cited by 156 · see citing works
Rachidi, N., Barre, P., & Blondin, B. (1999) · Molecular and General Genetics MGG · doi:10.1007/s004380050028 · Cited by 136 · see citing works
Genome-Wide Analysis of Nucleotide-Level Variation in Commonly Used Saccharomyces cerevisiae Strains
Schacherer, J., Ruderfer, D. M., Gresham, D., Dolinski, K. J., Botstein, D., & Kruglyak, L. (2007) · PLoS ONE · doi:10.1371/journal.pone.0000322 · Cited by 129 · see citing works
Allelic and ectopic recombination between Ty elements in yeast.
Kupiec, M., & Petes, T. D. (1988) · Genetics · doi:10.1093/genetics/119.3.549 · Cited by 126 · see citing works
Genetic analysis of animal development
Wilkins, A. S. (1986) · Cited by 121 · see citing works
Genetic analysis of animal development
Edgar, R. S. (1986) · Cell · doi:10.1016/0092-8674(86)90776-2 · Cited by 112 · see citing works
Gragg, H., Harfe, B. D., & Jinks-Robertson, S. (2002) · Molecular and Cellular Biology · doi:10.1128/mcb.22.24.8756-8762.2002 · Cited by 103 · see citing works
Spontaneous Loss of Heterozygosity in Diploid Saccharomyces cerevisiae Cells
Hiraoka, M., Watanabe, K., Umezu, K., & Maki, H. (2000) · Genetics · doi:10.1093/genetics/156.4.1531 · Cited by 102 · see citing works
Variation in efficiency of DNA mismatch repair at different sites in the yeast genome
Hawk, J. D., Stefanovic, L., Boyer, J. C., Petes, T. D., & Farber, R. A. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0503415102 · Cited by 97 · see citing works
Mutation and Evolution of Microsatellite Loci in Neurospora
Dettman, J. R., & Taylor, J. W. (2004) · Genetics · doi:10.1534/genetics.104.029322 · Cited by 93 · see citing works
The Rate and Spectrum of Microsatellite Mutation in Caenorhabditis elegans and Daphnia pulex
Seyfert, A. L., Cristescu, M. E., Frisse, L. A., Schaack, S., Thomas, W. K., & Lynch, M. (2008) · Genetics · doi:10.1534/genetics.107.081927 · Cited by 84 · see citing works
DNA Sequence Analysis of Spontaneous Mutagenesis in Saccharomyces cerevisiae
Kunz, B. A., Ramachandran, K., & Vonarx, E. J. (1998) · Genetics · doi:10.1093/genetics/148.4.1491 · Cited by 76 · see citing works
Denver, D. R., Morris, K., Kewalramani, A. R., Harris, K. E., Chow, A., Estes, S., Lynch, M., & Thomas, W. K. (2004) · Journal of Molecular Evolution · doi:10.1007/s00239-004-2580-4 · Cited by 71 · see citing works
Giannelli, F., Anagnostopoulos, T., & Green, P. M. (1999) · The American Journal of Human Genetics · doi:10.1086/302652 · Cited by 62 · see citing works
Instability of Simple Sequence DNA in Saccharomyces cerevisiae
Henderson, S. T., & Petes, T. D. (1992) · Molecular and Cellular Biology · doi:10.1128/mcb.12.6.2749-2757.1992 · Cited by 62 · see citing works
Baer, C. F., Phillips, N., Ostrow, D. G., Avalos, A., Blanton, D., Boggs, A. S. P., Keller, T., Levy, L. M., & Mezerhane, E. (2006) · Genetics · doi:10.1534/genetics.106.061200 · Cited by 57 · see citing works
Dickinson, W. J. (2008) · Genetics · doi:10.1534/genetics.107.080853 · Cited by 56 · see citing works
Saccharomyces cerevisiae as a Model System To Define the Chromosomal Instability Phenotype
Putnam, C. D., Pennaneach, V., & Kolodner, R. D. (2005) · Molecular and Cellular Biology · doi:10.1128/mcb.25.16.7226-7238.2005 · Cited by 55 · see citing works
Estimation of microsatellite mutation rates in Drosophila melanogaster
Vázquez, F., Pérez, T., Albornoz, J., & Domínguez, A. (2000) · Genetics Research · doi:10.1017/s0016672300004791 · Cited by 54 · see citing works
Spontaneous mutagenesis in haploid and diploid Saccharomyces cerevisiae
Ohnishi, G., Endo, K., Doi, A., Fujita, A., Daigaku, Y., Nunoshiba, T., & Yamamoto, K. (2004) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2004.10.120 · Cited by 46 · see citing works
Podlutsky, A. J. (1998) · Carcinogenesis · doi:10.1093/carcin/19.4.557 · Cited by 38 · see citing works
Rapid mutational declines of viability in Drosophila
Fry, J. D. (2001) · Genetics Research · doi:10.1017/s0016672300004882 · Cited by 31 · see citing works
Mutation frequency analysis of mononucleotide and dinucleotide repeats after oxidative stress
Yamada, N. A., Parker, J. M., & Farber, R. A. (2003) · Environmental and Molecular Mutagenesis · doi:10.1002/em.10179 · Cited by 12 · see citing works
Flagged first, then by citations
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- [18]Lynch M. The Origins of Genomic Architecture. Sunderland, MA: Sinauer; 2007. [Google Scholar]
Cited by
Sorted by citations
Evolution of the mutation rate
Lynch, M. (2010) · Trends in Genetics · doi:10.1016/j.tig.2010.05.003 · Cited by 1,138 · see citing works
The Rate and Molecular Spectrum of Spontaneous Mutations in Arabidopsis thaliana
Ossowski, S., Schneeberger, K., Lucas‐Lledó, J. I., Warthmann, N., Clark, R. M., Shaw, R. G., Weigel, D., & Lynch, M. (2009) · Science · doi:10.1126/science.1180677 · Cited by 1,148 · see citing works
Rate, molecular spectrum, and consequences of human mutation
Lynch, M. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0912629107 · Cited by 792 · see citing works
Domestication and Divergence of Saccharomyces cerevisiae Beer Yeasts
Gallone, B., Steensels, J., Prahl, T., Soriaga, L., Saels, V., Herrera-Malaver, B., Merlevede, A., Roncoroni, M., Voordeckers, K., Miraglia, L., et al. (2016) · Cell · doi:10.1016/j.cell.2016.08.020 · Cited by 679 · see citing works
Lee, H., Popodi, E., Tang, H., & Foster, P. L. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1210309109 · Cited by 681 · see citing works
Genome dynamics during experimental evolution
Barrick, J. E., & Lenski, R. E. (2013) · Nature Reviews Genetics · doi:10.1038/nrg3564 · Cited by 619 · see citing works
Total Synthesis of a Functional Designer Eukaryotic Chromosome
Annaluru, N., Muller, H., MITCHELL, L. A., Ramalingam, S., Stracquadanio, G., Richardson, S. M., Dymond, J. S., Kuang, Z., Scheifele, L. Z., Cooper, E. M., et al. (2014) · Science · doi:10.1126/science.1249252 · Cited by 547 · see citing works
Evidence That Mutation Is Universally Biased towards AT in Bacteria
Hershberg, R., & Petrov, D. (2010) · PLoS Genetics · doi:10.1371/journal.pgen.1001115 · Cited by 467 · see citing works
Gresham, D., Desai, M. M., Tucker, C. M., Jenq, H. T., Pai, D. A., Ward, A., DeSevo, C. G., Botstein, D., & Dunham, M. J. (2008) · PLoS Genetics · doi:10.1371/journal.pgen.1000303 · Cited by 482 · see citing works
Spontaneous Mutation Accumulation Studies in Evolutionary Genetics
Halligan, D. L., & Keightley, P. D. (2009) · Annual Review of Ecology Evolution and Systematics · doi:10.1146/annurev.ecolsys.39.110707.173437 · Cited by 469 · see citing works
Genome, epigenome and RNA sequences of monozygotic twins discordant for multiple sclerosis
Baranzini, S. E., Mudge, J., van Velkinburgh, J. C., Khankhanian, P., Khrebtukova, I., Miller, N. A., Zhang, L., Farmer, A. D., Bell, C. J., Kim, R. W., et al. (2010) · Nature · doi:10.1038/nature08990 · Cited by 476 · see citing works
Genomic signatures of selection at linked sites: unifying the disparity among species
Cutter, A. D., & Payseur, B. A. (2013) · Nature Reviews Genetics · doi:10.1038/nrg3425 · Cited by 465 · see citing works
Quantitative evolutionary dynamics using high-resolution lineage tracking
Levy, S. F., Blundell, J. R., Venkataram, S., Petrov, D. A., Fisher, D. S., & Sherlock, G. J. (2015) · Nature · doi:10.1038/nature14279 · Cited by 461 · see citing works
Ford, C. B., Lin, P. L., Chase, M. R., Shah, R. R., Iartchouk, O., Galagan, J., Mohaideen, N., Ioerger, T. R., Sacchettini, J. C., Lipsitch, M., et al. (2011) · Nature Genetics · doi:10.1038/ng.811 · Cited by 437 · see citing works
Precise estimates of mutation rate and spectrum in yeast
Zhu, Y. O., Siegal, M. L., Hall, D. W., & Petrov, D. A. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1323011111 · Cited by 421 · see citing works
Bet Hedging in Yeast by Heterogeneous, Age-Correlated Expression of a Stress Protectant
Levy, S. F., Ziv, N., & Siegal, M. L. (2012) · PLoS Biology · doi:10.1371/journal.pbio.1001325 · Cited by 371 · see citing works
Drift-barrier hypothesis and mutation-rate evolution
Sung, W., Ackerman, M. S., Miller, S. F., Doak, T. G., & Lynch, M. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1216223109 · Cited by 398 · see citing works
Unstable Tandem Repeats in Promoters Confer Transcriptional Evolvability
Vinces, M. D., Legendre, M., Caldara, M., Hagihara, M., & Verstrepen, K. J. (2009) · Science · doi:10.1126/science.1170097 · Cited by 372 · see citing works
Poxviruses Deploy Genomic Accordions to Adapt Rapidly against Host Antiviral Defenses
Elde, N. C., Child, S. J., Eickbush, M. T., Kitzman, J. O., Rogers, K. S., Shendure, J., Geballe, A. P., & Malik, H. S. (2012) · Cell · doi:10.1016/j.cell.2012.05.049 · Cited by 357 · see citing works
Keightley, P. D., Trivedi, U. H., Thomson, M. L., Oliver, F., Kumar, S., & Blaxter, M. (2009) · Genome Research · doi:10.1101/gr.091231.109 · Cited by 359 · see citing works
Dujon, B. (2010) · Nature Reviews Genetics · doi:10.1038/nrg2811 · Cited by 316 · see citing works
A disproportionate role for mt DNA in D obzhansky– M uller incompatibilities?
Burton, R. S., & Barreto, F. S. (2012) · Molecular Ecology · doi:10.1111/mec.12006 · Cited by 317 · see citing works
The life and death of gene families
Demuth, J. P., & Hahn, M. W. (2009) · BioEssays · doi:10.1002/bies.080085 · Cited by 313 · see citing works
Determinants of Mutation Rate Variation in the Human Germline
Ségurel, L., Wyman, M. J., & Przeworski, M. (2014) · Annual Review of Genomics and Human Genetics · doi:10.1146/annurev-genom-031714-125740 · Cited by 289 · see citing works
Keightley, P. D., Ness, R. W., Halligan, D. L., & Haddrill, P. R. (2013) · Genetics · doi:10.1534/genetics.113.158758 · Cited by 296 · see citing works
Direct Estimation of the Mitochondrial DNA Mutation Rate in Drosophila melanogaster
Liautard‐Haag, C., Coffey, N., Houle, D., Lynch, M., Charlesworth, B., & Keightley, P. D. (2008) · PLoS Biology · doi:10.1371/journal.pbio.0060204 · Cited by 296 · see citing works
On the wrong DNA track: Molecular mechanisms of repeat-mediated genome instability
Khristich, A. N., & Mirkin, S. M. (2020) · Journal of Biological Chemistry · doi:10.1074/jbc.rev119.007678 · Cited by 289 · see citing works
The on‐again, off‐again relationship between mitochondrial genomes and species boundaries
Sloan, D. B., Havird, J. C., & Sharbrough, J. (2016) · Molecular Ecology · doi:10.1111/mec.13959 · Cited by 289 · see citing works
Direct estimate of the rate of germline mutation in a birdPreprint
Smeds, L., Qvarnström, A., & Ellegren, H. (2016) · Genome Research · doi:10.1101/gr.204669.116 · Cited by 278 · see citing works
A genome-wide view of Caenorhabditis elegans base-substitution mutation processes
Denver, D. R., Dolan, P. C., Wilhelm, L., Sung, W., Lucas‐Lledó, J. I., Howe, D. K., Lewis, S. C., Okamoto, K., Thomas, W. K., Lynch, M., et al. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0904895106 · Cited by 269 · see citing works
Mechanisms of Gene Duplication and AmplificationPreprint
Reams, A. B., & Roth, J. R. (2015) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a016592 · Cited by 266 · see citing works
Genomic Plasticity of the Human Fungal Pathogen Candida albicans
Selmecki, A., Forche, A., & Berman, J. (2010) · Eukaryotic Cell · doi:10.1128/ec.00060-10 · Cited by 247 · see citing works
GinkgoandWelwitschiaMitogenomes Reveal Extreme Contrasts in Gymnosperm Mitochondrial Evolution
Guo, W., Grewe, F., Fan, W., Young, G. J., Knoop, V., Palmer, J. D., & Mower, J. P. (2016) · Molecular Biology and Evolution · doi:10.1093/molbev/msw024 · Cited by 263 · see citing works
Optimized filtering reduces the error rate in detecting genomic variants by short-read sequencing
Reumers, J., Rijk, P. D., Zhao, H., Liekens, A., Smeets, D., Cleary, J., van Loo, P., Bossche, M. V. D. V. D., Catthoor, K., Sabbe, B., et al. (2011) · Nature Biotechnology · doi:10.1038/nbt.2053 · Cited by 238 · see citing works
Species boundaries in the human pathogen Paracoccidioides
Turissini, D. A., Gómez, O. M., Teixeira, M. D. M., McEwen, J. G., & Matute, D. R. (2017) · Fungal Genetics and Biology · doi:10.1016/j.fgb.2017.05.007 · Cited by 236 · see citing works
Strong Purifying Selection at Synonymous Sites in D. melanogaster
Lawrie, D. S., Messer, P. W., Hershberg, R., & Petrov, D. A. (2013) · PLoS Genetics · doi:10.1371/journal.pgen.1003527 · Cited by 228 · see citing works
Bopp, S. E. R., Manary, M. J., Bright, A. T., Johnston, G. L., Dharia, N. V., Luna, F. L., McCormack, S., Plouffe, D., McNamara, C. W., Walker, J. R., et al. (2013) · PLoS Genetics · doi:10.1371/journal.pgen.1003293 · Cited by 221 · see citing works
Rates and Genomic Consequences of Spontaneous Mutational Events in Drosophila melanogaster
Schrider, D. R., Houle, D., Lynch, M., & Hahn, M. W. (2013) · Genetics · doi:10.1534/genetics.113.151670 · Cited by 209 · see citing works
Antibiotic treatment enhances the genome-wide mutation rate of target cells
Long, H., Miller, S. F., Strauss, C., Zhao, C., Cheng, L., Ye, Z., Griffin, K. E., Te, R., Lee, H., Chen, C., et al. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1601208113 · Cited by 204 · see citing works
Stukenbrock, E. H., Bataillon, T. M., Dutheil, J. Y., Hansen, T. T., Li, R., Zala, M., McDonald, B. A., Wang, J., & Schierup, M. H. (2011) · Genome Research · doi:10.1101/gr.118851.110 · Cited by 207 · see citing works
Altshuler, I., Demiri, B., Xu, S., Constantin, A., Yan, N. D., & Cristescu, M. E. (2011) · Integrative and Comparative Biology · doi:10.1093/icb/icr103 · Cited by 206 · see citing works
Genome-wide Consequences of Deleting Any Single Gene
Teng, X., Dayhoff-Brannigan, M., Cheng, W., Gilbert, C. E., Sing, C. N., Diny, N. L., Wheelan, S. J., Dunham, M. J., Boeke, J. D., Pineda, F. J., et al. (2013) · Molecular Cell · doi:10.1016/j.molcel.2013.09.026 · Cited by 193 · see citing works
Short tandem repeats bind transcription factors to tune eukaryotic gene expression
Horton, C. A., Alexandari, A. M., Hayes, M. G. B., Marklund, E., Schaepe, J. M., Aditham, A. K., Shah, N., Suzuki, P., Shrikumar, A., Afek, A., et al. (2023) · Science · doi:10.1126/science.add1250 · Cited by 199 · see citing works
Ma, H., Hagen, F., Stekel, D. J., Johnston, S. A., Sionov, E., Falk, R., Polacheck, I., Boekhout, T., & May, R. C. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0902963106 · Cited by 185 · see citing works
Stukenbrock, E. H., Christiansen, F., Hansen, T. T., Dutheil, J. Y., & Schierup, M. H. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1201403109 · Cited by 186 · see citing works
Global analysis of mutations driving microevolution of a heterozygous diploid fungal pathogen
Ene, I. V., Farrer, R. A., Hirakawa, M. P., Agwamba, K., Cuomo, C. A., & Bennett, R. J. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1806002115 · Cited by 155 · see citing works
“If occurring randomly, mutations will accumulate in intergenic and coding regions at frequencies proportional to their representation in the genome (39, 40, 43).”
BackgroundThe Genomic Landscape and Evolutionary Resolution of Antagonistic Pleiotropy in Yeast
Qian, W., Ma, D., Xiao, C., Wang, Z., & Zhang, J. (2012) · Cell Reports · doi:10.1016/j.celrep.2012.09.017 · Cited by 174 · see citing works
Three-stage quality control strategies for DNA re-sequencing data
Guo, Y. P., Ye, F., Sheng, Q., Clark, T. A., & Samuels, D. C. (2013) · Briefings in Bioinformatics · doi:10.1093/bib/bbt069 · Cited by 178 · see citing works
A population genomics insight into the Mediterranean origins of wine yeast domestication
Almeida, P., Barbosa, R. G., Zalar, P., Imanishi, Y., Shimizu, K., Turchetti, B., Legras, J., Serra, M. L., Dequin, S., Couloux, A., et al. (2015) · Molecular Ecology · doi:10.1111/mec.13341 · Cited by 178 · see citing works
Katju, V., & Bergthorsson, U. (2018) · Genome Biology and Evolution · doi:10.1093/gbe/evy252 · Cited by 178 · see citing works
Adaptation to High Ethanol Reveals Complex Evolutionary Pathways
Voordeckers, K., Kominek, J., Das, A. J., Espinosa‐Cantú, A., Maeyer, D. D., Arslan, A., Pee, M. V., van der Zande, E., Meert, W., Yang, Y., et al. (2015) · PLoS Genetics · doi:10.1371/journal.pgen.1005635 · Cited by 167 · see citing works
Karyotype engineering by chromosome fusion leads to reproductive isolation in yeast
Luo, J., Sun, X., Cormack, B. P., & Boeke, J. D. (2018) · Nature · doi:10.1038/s41586-018-0374-x · Cited by 174 · see citing works
Copy-number changes in evolution: rates, fitness effects and adaptive significance
Katju, V., & Bergthorsson, U. (2013) · Frontiers in Genetics · doi:10.3389/fgene.2013.00273 · Cited by 172 · see citing works
DeNovoGear: de novo indel and point mutation discovery and phasing
Ramu, A., Noordam, M. J., Schwartz, R. S., Wüster, A., Hurles, M. E., Cartwright, R. A., & Conrad, D. F. (2013) · Nature Methods · doi:10.1038/nmeth.2611 · Cited by 172 · see citing works
Local Determinants of the Mutational Landscape of the Human Genome
González-Pérez, A., Sabarinathan, R., & López-Bigas, N. (2019) · Cell · doi:10.1016/j.cell.2019.02.051 · Cited by 162 · see citing works
Extensive loss of cell-cycle and DNA repair genes in an ancient lineage of bipolar budding yeasts
Steenwyk, J. L., Opulente, D. A., Kominek, J., Shen, X.-X., Zhou, X., Labella, A. L., Bradley, N. P., Eichman, B. F., Čadež, N., Libkind, D., et al. (2019) · PLoS Biology · doi:10.1371/journal.pbio.3000255 · Cited by 162 · see citing works
Elmer, K., Fan, S.-H., Gunter, H., Jones, J. C., Boekhoff, S., Kuraku, S., & Meyer, A. (2010) · Molecular Ecology · doi:10.1111/j.1365-294x.2009.04488.x · Cited by 175 · see citing works
A Wide Extent of Inter-Strain Diversity in Virulent and Vaccine Strains of Alphaherpesviruses
SZPARA, M. L., Tafuri, Y. R., Parsons, L. R., Shamim, S. R., Verstrepen, K. J., Legendre, M., & Enquist, L. W. (2011) · PLoS Pathogens · doi:10.1371/journal.ppat.1002282 · Cited by 157 · see citing works
The genome-wide rate and spectrum of spontaneous mutations differ between haploid and diploid yeast
Sharp, N. P., Sandell, L., James, C. G., & Otto, S. P. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1801040115 · Cited by 157 · see citing works
Dopman, E. B., Robbins, P. S., & Seaman, A. (2009) · Evolution · doi:10.1111/j.1558-5646.2009.00883.x · Cited by 156 · see citing works
Expandable and reversible copy number amplification drives rapid adaptation to antifungal drugs
Todd, R. T., & Selmecki, A. (2020) · eLife · doi:10.7554/elife.58349 · Cited by 138 · see citing works
Heterogeneous polymerase fidelity and mismatch repair bias genome variation and compositionPreprint
Lujan, S. A., Clausen, A. R., Clark, A. B., MacAlpine, H. K., MacAlpine, D. M., Malc, E. P., Mieczkowski, P. A., Burkholder, A., Fargo, D. C., Gordenin, D. A., et al. (2014) · Genome Research · doi:10.1101/gr.178335.114 · Cited by 148 · see citing works
Evolution of new enzymes by gene duplication and divergence
Copley, S. D. (2020) · FEBS Journal · doi:10.1111/febs.15299 · Cited by 148 · see citing works
Selection on noise constrains variation in a eukaryotic promoter
Metzger, B. P. H., Yuan, D. C., Gruber, J. D., Duveau, F., & Wittkopp, P. J. (2015) · Nature · doi:10.1038/nature14244 · Cited by 138 · see citing works
Gene Essentiality Is a Quantitative Property Linked to Cellular Evolvability
Liu, G., Yong, M. Y. J., Yurieva, M., Srinivasan, K. G., Liu, J., Lim, J. S. Y., Poidinger, M., Wright, G. D., Zolezzi, F., Choi, H., et al. (2015) · Cell · doi:10.1016/j.cell.2015.10.069 · Cited by 145 · see citing works
Vogt, G. (2015) · Journal of Biosciences · doi:10.1007/s12038-015-9506-8 · Cited by 141 · see citing works
Pervasive Multinucleotide Mutational Events in Eukaryotes
Schrider, D. R., Hourmozdi, J., & Hahn, M. W. (2011) · Current Biology · doi:10.1016/j.cub.2011.05.013 · Cited by 144 · see citing works
Harnessing genomics for evolutionary insights
Rokas, A., & Abbot, P. (2009) · Trends in Ecology & Evolution · doi:10.1016/j.tree.2008.11.004 · Cited by 142 · see citing works
Nowrousian, M. (2010) · Eukaryotic Cell · doi:10.1128/ec.00123-10 · Cited by 141 · see citing works
Stukenbrock, E. H., Jørgensen, F. G., Zala, M., Hansen, T. T., McDonald, B. A., & Schierup, M. H. (2010) · PLoS Genetics · doi:10.1371/journal.pgen.1001189 · Cited by 137 · see citing works
Variable Glutamine-Rich Repeats Modulate Transcription Factor Activity
Gemayel, R., Chavali, S., Pougach, K., Legendre, M., Zhu, B., Boeynaems, S., van der Zande, E., Gevaert, K., Rousseau, F., Schymkowitz, J. W. H., et al. (2015) · Molecular Cell · doi:10.1016/j.molcel.2015.07.003 · Cited by 136 · see citing works
High-Resolution Mapping of Complex Traits with a Four-Parent Advanced Intercross Yeast Population
Cubillos, F. A., Parts, L., Salinas, F., Bergström, A., Scovacricchi, E., Zia, A., Illingworth, C. J. R., Mustonen, V., Ibstedt, S., Warringer, J., et al. (2013) · Genetics · doi:10.1534/genetics.113.155515 · Cited by 137 · see citing works
A regulatory role for repeated decoy transcription factor binding sites in target gene expression
Lee, T., & Maheshri, N. (2012) · Molecular Systems Biology · doi:10.1038/msb.2012.7 · Cited by 137 · see citing works
Fungal mitochondrial genomes and genetic polymorphisms
Sandor, S. R., Zhang, Y., & Xu, J. (2018) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-018-9350-5 · Cited by 136 · see citing works
Peris, D., Sylvester, K., Libkind, D., Gonçalves, P. M., Sampaio, J. P., Alexander, W. G., & Hittinger, C. T. (2014) · Molecular Ecology · doi:10.1111/mec.12702 · Cited by 133 · see citing works
Asymmetric Context-Dependent Mutation Patterns Revealed through Mutation–Accumulation Experiments
Sung, W., Ackerman, M. S., Goût, J.-F., Miller, S. F., Williams, E., Foster, P. L., & Lynch, M. (2015) · Molecular Biology and Evolution · doi:10.1093/molbev/msv055 · Cited by 134 · see citing works
Extreme mutation bias and high AT content inPlasmodium falciparum
Hamilton, W. L., Claessens, A., Otto, T. D., Kekre, M., Fairhurst, R. M., Rayner, J. C., & Kwiatkowski, D. P. (2016) · Nucleic Acids Research · doi:10.1093/nar/gkw1259 · Cited by 134 · see citing works
The Spontaneous Mutation Rate in the Fission Yeast Schizosaccharomyces pombe
Farlow, A., Long, H., Arnoux, S., Sung, W., Doak, T. G., Nordborg, M., & Lynch, M. (2015) · Genetics · doi:10.1534/genetics.115.177329 · Cited by 132 · see citing works
Ploidy and the Causes of Genomic Evolution
Gerstein, A. C., & Otto, S. P. (2009) · Journal of Heredity · doi:10.1093/jhered/esp057 · Cited by 131 · see citing works
Hong, J., & Gresham, D. (2014) · PLoS Genetics · doi:10.1371/journal.pgen.1004041 · Cited by 125 · see citing works
Recommendations for improving statistical inference in population genomics
Johri, P., Aquadro, C. F., Beaumont, M., Charlesworth, B., Excoffier, L., Eyre‐Walker, A., Keightley, P. D., Lynch, M., McVean, G., Payseur, B. A., et al. (2022) · PLoS Biology · doi:10.1371/journal.pbio.3001669 · Cited by 130 · see citing works
Estimate of the Spontaneous Mutation Rate in Chlamydomonas reinhardtii
Ness, R. W., Morgan, A. D., Colegrave, N., & Keightley, P. D. (2012) · Genetics · doi:10.1534/genetics.112.145078 · Cited by 129 · see citing works
Mutational landscape of yeast mutator strains
Serero, A., Jubin, C., Loeillet, S., Legoix-Né, P., & Nicolas, A. G. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1314423111 · Cited by 126 · see citing works
Dynamic Large-Scale Chromosomal Rearrangements Fuel Rapid Adaptation in Yeast Populations
Chang, S., Lai, H.-Y., Tung, S., & Leu, J. (2013) · PLoS Genetics · doi:10.1371/journal.pgen.1003232 · Cited by 126 · see citing works
High Spontaneous Rate of Gene Duplication in Caenorhabditis elegans
Lipinski, K. J., Farslow, J. C., Fitzpatrick, K. A., Lynch, M., Katju, V., & Bergthorsson, U. (2011) · Current Biology · doi:10.1016/j.cub.2011.01.026 · Cited by 125 · see citing works
Haploids adapt faster than diploids across a range of environments
Gerstein, A. C., CLEATHERO, L. A., Mandegar, M. A., & Otto, S. P. (2010) · Journal of Evolutionary Biology · doi:10.1111/j.1420-9101.2010.02188.x · Cited by 125 · see citing works
Single-cell copy number variant detection reveals the dynamics and diversity of adaptation
Lauer, S. L., Avecilla, G., Spealman, P., Sethia, G., Brandt, N. J., Levy, S. F., & Gresham, D. (2018) · PLoS Biology · doi:10.1371/journal.pbio.3000069 · Cited by 121 · see citing works
Lynch, M. (2008) · Molecular Biology and Evolution · doi:10.1093/molbev/msn185 · Cited by 123 · see citing works
A Modified TILLING Method for Wheat Breeding
Dong, C., Dalton‐Morgan, J., Vincent, K., & Sharp, P. J. (2009) · The Plant Genome · doi:10.3835/plantgenome2008.10.0012 · Cited by 123 · see citing works
The functional basis of adaptive evolution in chemostats
Gresham, D., & Hong, J. (2014) · FEMS Microbiology Reviews · doi:10.1111/1574-6976.12082 · Cited by 122 · see citing works
Extraordinary genome stability in the ciliate Paramecium tetraurelia
Sung, W., Tucker, A. E., Doak, T. G., Choi, E., Thomas, W. K., & Lynch, M. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1210663109 · Cited by 119 · see citing works
Genomic evidence for elevated mutation rates in highly expressed genes
Park, C., Qian, W., & Zhang, J. (2012) · EMBO Reports · doi:10.1038/embor.2012.165 · Cited by 120 · see citing works
Jarosz, D. F., Lancaster, A. K., Brown, J. C. S., & Lindquist, S. L. (2014) · Cell · doi:10.1016/j.cell.2014.07.024 · Cited by 121 · see citing works
Limits and patterns of cytomegalovirus genomic diversity in humans
Renzette, N., Pokalyuk, C., Gibson, L. L., Bhattacharjee, B., Schleiss, M. R., Hamprecht, K., Yamamoto, A. Y., Mussi‐Pinhata, M. M., Britt, W. J., Jensen, J. D., et al. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1501880112 · Cited by 120 · see citing works
The Relationship Between Relative Solvent Accessibility and Evolutionary Rate in Protein Evolution
Ramsey, D. C., Scherrer, M. P., Zhou, T., & Wilke, C. O. (2011) · Genetics · doi:10.1534/genetics.111.128025 · Cited by 118 · see citing works
Large-scale detection of in vivo transcription errors
Goût, J.-F., Thomas, W. K., Smith, Z., Okamoto, K., & Lynch, M. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1309843110 · Cited by 117 · see citing works
Experimental Evolution of Yeast for High-Temperature Tolerance
Huang, C.-J., Lu, M. J., Chang, Y.-W., & Li, W. (2018) · Molecular Biology and Evolution · doi:10.1093/molbev/msy077 · Cited by 117 · see citing works
Montooth, K. L., Meiklejohn, C. D., Abt, D. N., & Rand, D. M. (2010) · Evolution · doi:10.1111/j.1558-5646.2010.01077.x · Cited by 117 · see citing works
Whole-genome sequencing of a laboratory-evolved yeast strain
Araya, C. L., Payen, C., Dunham, M. J., & Fields, S. (2010) · BMC Genomics · doi:10.1186/1471-2164-11-88 · Cited by 113 · see citing works
High mutational rates of large-scale duplication and deletion in Daphnia pulexPreprint
Keith, N., Tucker, A. E., Jackson, C. E., Sung, W., Lucas‐Lledó, J. I., Schrider, D. R., Schaack, S., Dudycha, J. L., Ackerman, M. S., Younge, A., et al. (2015) · Genome Research · doi:10.1101/gr.191338.115 · Cited by 113 · see citing works
- Authors
- Lynch, M., Sung, W., Morris, K., Coffey, N., Landry, C. R., Dopman, E. B., Dickinson, W. J., Okamoto, K., Kulkarni, S., Hartl, D. L., & Thomas, W. K.
- Affiliations
- Indiana University Bloomington (US)
- University of New Hampshire (US)
- Harvard University (US)
- University of Utah (US)
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2008-07-08
- Volume
- 105
- Issue
- 27
- Pages
- 9272-9277
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC2453693
- OpenAlex
- W2145406188
- Cited by
- 708
- References
- 62
- Citations by year
- 2026: 16 · 2025: 23 · 2024: 24 · 2023: 34 · 2022: 29 · 2021: 56 · 2020: 35 · 2019: 39 · 2018: 42 · 2017: 40 · 2016: 44 · 2015: 46 · 2014: 47 · 2013: 51 · 2012: 42
- FWCI
- 18.53
- 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)
- Funders
- National Institutes of Health
- Natural Sciences and Engineering Research Council of Canada
- National Institute of General Medical Sciences (GM 36827, R01GM068465, R01GM036827, GM068465)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Fungal and yeast genetics research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Evolution and Genetic Dynamics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Phylogenetic Studies
- Keywords
- spontaneous mutation, mutation spectrum, Saccharomyces cerevisiae, point mutations, mitochondrial mutations, segmental duplication, deletion, mutation rate
- MeSH terms
- Base Sequence, Cell Division, DNA, Mitochondrial, Mutation, Nucleotides, Ploidies, Saccharomyces cerevisiae, Chromosomes, Fungal, Genome, Fungal, Microsatellite Repeats
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