The repertoire and dynamics of evolutionary adaptations to controlled nutrient-limited environments in yeast
Open accessAbstract
The experimental evolution of laboratory populations of microbes provides an opportunity to observe the evolutionary dynamics of adaptation in real time. Until very recently, however, such studies have been limited by our inability to systematically find mutations in evolved organisms. We overcome this limitation by using a variety of DNA microarray-based techniques to characterize genetic changes -- including point mutations, structural changes, and insertion variation -- that resulted from the experimental adaptation of 24 haploid and diploid cultures of Saccharomyces cerevisiae to growth in either glucose, sulfate, or phosphate-limited chemostats for approximately 200 generations. We identified frequent genomic amplifications and rearrangements as well as novel retrotransposition events associated with adaptation. Global nucleotide variation detection in ten clonal isolates identified 32 point mutations. On the basis of mutation frequencies, we infer that these mutations and the subsequent dynamics of adaptation are determined by the batch phase of growth prior to initiation of the continuous phase in the chemostat. We relate these genotypic changes to phenotypic outcomes, namely global patterns of gene expression, and to increases in fitness by 5-50%. We found that the spectrum of available mutations in glucose- or phosphate-limited environments combined with the batch phase population dynamics early in our experiments allowed several distinct genotypic and phenotypic evolutionary pathways in response to these nutrient limitations. By contrast, sulfate-limited populations were much more constrained in both genotypic and phenotypic outcomes. Thus, the reproducibility of evolution varies with specific selective pressures, reflecting the constraints inherent in the system-level organization of metabolic processes in the cell. We were able to relate some of the observed adaptive mutations (e.g., transporter gene amplifications) to known features of the relevant metabolic pathways, but many of the mutations pointed to genes not previously associated with the relevant physiology. Thus, in addition to answering basic mechanistic questions about evolutionary mechanisms, our work suggests that experimental evolution can also shed light on the function and regulation of individual metabolic pathways.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
C. albicans, like S. cerevisiae, generates large scale genetic variation as a means of adaptation.
“Thus, C. albicans like S. cerevisiae (Gresham et al., 2008; Pavelka et al., 2010; Yona et al., 2012; Chang et al., 2013) generates large scale genetic variation as a means of adaptation.”
From The evolution of drug resistance in clinical isolates of Candida albicans. (2015) · cites this paper as Gresham et al., 2008
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
<i>MET</i> Amplification Leads to Gefitinib Resistance in Lung Cancer by Activating ERBB3 Signaling
Engelman, J. A., Zejnullahu, K., Mitsudomi, T., Song, Y., Hyland, C., Park, J. O., Lindeman, N., Gale, C.-M., Zhao, X., Christensen, J., et al. (2007) · Science · doi:10.1126/science.1141478 · Cited by 4,496 · see citing works
Mutations of bacteria from virus sensitivity to virus resistance
Luria, S. E., & Delbrück, M. (1943) · Genetics · doi:10.1093/genetics/28.6.491 · Cited by 3,894 · see citing works
Genetic Dissection of Transcriptional Regulation in Budding Yeast
Brem, R. B., Yvert, G., Clinton, R., & Kruglyak, L. (2002) · Science · doi:10.1126/science.1069516 · Cited by 1,392 · see citing works
Effects of Aneuploidy on Cellular Physiology and Cell Division in Haploid Yeast
Torres, E. M., Sokolsky, T., Tucker, C. M., Chan, L. Y., Boselli, M., Dunham, M. J., & Amon, A. (2007) · Science · doi:10.1126/science.1142210 · Cited by 935 · see citing works
Self-citationThe fate of competing beneficial mutations in an asexual population
Gerrish, P. J., & Lenski, R. E. (1998) · Genetica · doi:10.1023/a:1017067816551 · Cited by 783 · see citing works
The fate of competing beneficial mutations in an asexual population
Gerrish, P. J., & Lenski, R. E. (1998) · Contemporary issues in genetics and evolution · doi:10.1007/978-94-011-5210-5_12 · Cited by 721 · see citing works
A genome-wide view of the spectrum of spontaneous mutations in yeast.
Lynch, M., Sung, W., Morris, K., Coffey, N., Landry, C. R., Dopman, E. B., Dickinson, W. J., Okamoto, K., Kulkarni, S., Hartl, D. L., et al. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0803466105 · Cited by 708 · see citing works
Intragenic tandem repeats generate functional variability
Verstrepen, K. J., Jansen, A., Lewitter, F., & Fink, G. R. (2005) · Nature Genetics · doi:10.1038/ng1618 · Cited by 616 · see citing works
Neigeborn, L., & Carlson, M. (1984) · Genetics · doi:10.1093/genetics/108.4.845 · Cited by 587 · 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
Self-citationCoordination of Growth Rate, Cell Cycle, Stress Response, and Metabolic Activity in Yeast
Brauer, M. J., Huttenhower, C., Airoldi, E. M., Rosenstein, R., Matese, J. C., Gresham, D., Boer, V. M., Troyanskaya, O. G., & Botstein, D. (2008) · Molecular Biology of the Cell · doi:10.1091/mbc.e07-08-0779 · Cited by 558 · see citing works
Self-citationKim, J. M., Vanguri, S., Boeke, J. D., Gabriel, A., & Voytas, D. F. (1998) · Genome Research · doi:10.1101/gr.8.5.464 · Cited by 534 · see citing works
The fate of competing beneficial mutations in an asexual population.
Gerrish, P. J., & Lenski, R. E. (1998) · PubMed · Cited by 520 · see citing works
Systematic changes in gene expression patterns following adaptive evolution in yeast
Ferea, T., Botstein, D., Brown, P. O., & Rosenzweig, R. F. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.17.9721 · Cited by 479 · 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
Herring, C. D., Raghunathan, A., Honisch, C., Patel, T., Applebee, M. K., Joyce, A. R., Albert, T. J., Blattner, F. R., van den Boom, D., Cantor, C. R., et al. (2006) · Nature Genetics · doi:10.1038/ng1906 · Cited by 381 · see citing works
Keightley, P. D., & Eyre‐Walker, A. (2007) · Genetics · doi:10.1534/genetics.107.080663 · Cited by 358 · see citing works
Adaptive Mutations in Bacteria: High Rate and Small Effects
Perfeito, L., Fernandes, L., Mota, C., & Gordo, I. (2007) · Science · doi:10.1126/science.1142284 · Cited by 336 · see citing works
Boer, V. M., de Winde, J. H., Pronk, J. T., & Piper, M. D. W. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m209759200 · Cited by 326 · see citing works
Dykhuizen, D. E., & Hartl, D. L. (1983) · Microbiological Reviews · doi:10.1128/mr.47.2.150-168.1983 · Cited by 324 · see citing works
The Speed of Evolution and Maintenance of Variation in Asexual Populations
Desai, M. M., Fisher, D. S., & Murray, A. W. (2007) · Current Biology · doi:10.1016/j.cub.2007.01.072 · Cited by 319 · see citing works
Self-citationBrown, C. J., Todd, K., & Rosenzweig, R. F. (1998) · Molecular Biology and Evolution · doi:10.1093/oxfordjournals.molbev.a026009 · Cited by 307 · see citing works
Huang, M., Rio, A.-G., Nicolas, A. G., & Kolodner, R. D. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2035018100 · Cited by 259 · see citing works
Genome-Wide Detection of Polymorphisms at Nucleotide Resolution with a Single DNA Microarray
Gresham, D., Ruderfer, D. M., Pratt, S. C., Schacherer, J., Dunham, M. J., Botstein, D., & Kruglyak, L. (2006) · Science · doi:10.1126/science.1123726 · Cited by 255 · see citing works
Self-citationDouble-strand breaks associated with repetitive DNA can reshape the genome
Argueso, J. L., Westmoreland, J. W., Mieczkowski, P. A., Gaweł, M., Petes, T. D., & Resnick, M. A. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0804529105 · Cited by 241 · see citing works
Paquin, C., & Adams, J. (1983) · Nature · doi:10.1038/302495a0 · Cited by 239 · cited 3× · see citing works
“The relative merits of haploid and diploid states with respect to adaptation have been hotly contested [6,40,46,47].”
BackgroundResultComparing whole genomes using DNA microarrays
Gresham, D., Dunham, M. J., & Botstein, D. (2008) · Nature Reviews Genetics · doi:10.1038/nrg2335 · Cited by 231 · see citing works
Self-citationExperimental Studies of Natural Selection in Bacteria
Dykhuizen, D. E. (1990) · Annual Review of Ecology and Systematics · doi:10.1146/annurev.es.21.110190.002105 · Cited by 229 · see citing works
Liu, H., Badarinarayana, V., Audino, D. C., Rappsilber, J., Mann, M., & Denis, C. L. (1998) · The EMBO Journal · doi:10.1093/emboj/17.4.1096 · Cited by 210 · see citing works
Molecular Characterization of Two High Affinity Sulfate Transporters in Saccharomyces cerevisiae
Cherest, H., Davidian, J., Thomas, D., Beneš, V., Ansorge, W. J., & Surdin-Kerjan, Y. (1997) · Genetics · doi:10.1093/genetics/145.3.627 · Cited by 206 · see citing works
Yeast Ataxin-7 links histone deubiquitination with gene gating and mRNA export
Köhler, A., Schneider, M., Cabal, G. G., Nehrbass, U., & Hurt, E. (2008) · Nature Cell Biology · doi:10.1038/ncb1733 · Cited by 204 · see citing works
Birth of a metabolic gene cluster in yeast by adaptive gene relocation
Wong, S., & Wolfe, K. H. (2005) · Nature Genetics · doi:10.1038/ng1584 · Cited by 202 · see citing works
Mutation discovery in bacterial genomes: metronidazole resistance in Helicobacter pylori
Albert, T. J., Dailidiene, D., Dailide, G., Norton, J. E., Kalia, A., Richmond, T., Molla, M. N., Singh, J., Green, R. D., & Berg, D. E. (2005) · Nature Methods · doi:10.1038/nmeth805 · Cited by 202 · see citing works
Payen, C., Koszul, R., Dujon, B., & Fischer, G. (2008) · PLoS Genetics · doi:10.1371/journal.pgen.1000175 · Cited by 200 · see citing works
Lange, H. C., & Heijnen, J. J. (2001) · Biotechnology and Bioengineering · doi:10.1002/bit.10054 · Cited by 198 · see citing works
On the Physiological Role of Casein Kinase II in Saccharomyces cerevisiae
Glover, C. V. C. (1997) · Progress in nucleic acid research and molecular biology · doi:10.1016/s0079-6603(08)61030-2 · Cited by 195 · see citing works
Comprehensive mutation identification in an evolved bacterial cooperator and its cheating ancestor
Velicer, G. J., Raddatz, G., Keller, H., Deiss, S., Lanz, C., Dinkelacker, I., & Schuster, S. C. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0510740103 · Cited by 178 · see citing works
Nutritional Homeostasis in Batch and Steady-State Culture of Yeast
Saldanha, A. J., Brauer, M. J., & Botstein, D. (2004) · Molecular Biology of the Cell · doi:10.1091/mbc.e04-04-0306 · Cited by 176 · see citing works
Self-citationThe traveling-wave approach to asexual evolution: Muller's ratchet and speed of adaptation
Rouzine, I. M., Brunet, É., & Wilke, C. O. (2007) · Theoretical Population Biology · doi:10.1016/j.tpb.2007.10.004 · Cited by 175 · 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
Rim15 and the crossroads of nutrient signalling pathways in Saccharomyces cerevisiae
Swinnen, E., Wanke, V., Roosen, J., Smets, B., Dubouloz, F., Pedruzzi, I., Cameroni, E., VIRGILIO, C. D., & Winderickx, J. (2006) · Cell Division · doi:10.1186/1747-1028-1-3 · Cited by 163 · see citing works
Dykhuizen, D. E., & Hartl, D. L. (1983) · Microbiological Reviews · doi:10.1128/mmbr.47.2.150-168.1983 · Cited by 162 · see citing works
Mieczkowski, P. A., Lemoine, F. J., & Petes, T. D. (2006) · DNA repair · doi:10.1016/j.dnarep.2006.05.027 · Cited by 154 · see citing works
An Evolutionary Advantage of Haploidy in Large Yeast Populations
Zeyl, C., Vanderford, T. H., & Carter, M. R. (2003) · Science · doi:10.1126/science.1078417 · Cited by 152 · see citing works
Recombination and the evolution of diploidy.
Otto, S. P., & Goldstein, D. B. (1992) · Genetics · doi:10.1093/genetics/131.3.745 · Cited by 149 · see citing works
Evolution of global regulatory networks during a long‐term experiment with<i>Escherichia coli</i>
Philippe, N., Crozat, E., Lenski, R. E., & Schneider, D. (2007) · BioEssays · doi:10.1002/bies.20629 · Cited by 145 · see citing works
Survey of allelic expression using EST miningPreprint
Ge, B., Gurd, S., Gaudin, T., Doré, C., Lepage, P., Harmsen, E., Hudson, T. J., & Pastinen, T. (2005) · Genome Research · doi:10.1101/gr.4023805 · Cited by 131 · 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
Self-citationProfiles of Adaptation in Two Similar Viruses
Holder, K. K., & Bull, J. J. (2001) · Genetics · doi:10.1093/genetics/159.4.1393 · Cited by 126 · see citing works
Pélosi, L., Kühn, L., Guetta, D., Garin, J., Geiselmann, J., Lenski, R. E., & Schneider, D. (2006) · Genetics · doi:10.1534/genetics.105.049619 · Cited by 110 · see citing works
Fitness effects of Ty transposition in Saccharomyces cerevisiae.
Wilke, C. M., & Adams, J. (1992) · Genetics · doi:10.1093/genetics/131.1.31 · Cited by 106 · see citing works
Delneri, D., Hoyle, D. C., Gkargkas, K., Cross, E. J. M., Rash, B. M., Zeef, L. A. H., Leong, H. S., Davey, H. M., Hayes, A., Kell, D. B., et al. (2007) · Nature Genetics · doi:10.1038/ng.2007.49 · Cited by 95 · see citing works
How the Rgt1 Transcription Factor of Saccharomyces cerevisiae Is Regulated by Glucose
Polish, J. A., Kim, J., & Johnston, M. (2004) · Genetics · doi:10.1534/genetics.104.034512 · Cited by 94 · see citing works
High Deleterious Genomic Mutation Rate in Stationary Phase of <i>Escherichia coli</i>
Loewe, L., Textor, V., & Scherer, S. (2003) · Science · doi:10.1126/science.1087911 · Cited by 85 · see citing works
Ostrowski, E. A., Woods, R. J., & Lenski, R. E. (2007) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2007.1244 · Cited by 73 · see citing works
Clonal Interference Is Alleviated by High Mutation Rates in Large Populations
Bollback, J. P., & Huelsenbeck, J. P. (2007) · Molecular Biology and Evolution · doi:10.1093/molbev/msm056 · Cited by 71 · see citing works
GOLEM: an interactive graph-based gene-ontology navigation and analysis tool
Sealfon, R. S., Hibbs, M. A., Huttenhower, C., Myers, C. L., & Troyanskaya, O. G. (2006) · BMC Bioinformatics · doi:10.1186/1471-2105-7-443 · Cited by 58 · see citing works
Maharjan, R. P., Seeto, S., & Ferenci, T. (2006) · Journal of Bacteriology · doi:10.1128/jb.01414-06 · Cited by 55 · see citing works
Global Mapping of Transposon Location
Gabriel, A., Dapprich, J., Kunkel, M. W., Gresham, D., Pratt, S. C., & Dunham, M. J. (2006) · PLoS Genetics · doi:10.1371/journal.pgen.0020212 · Cited by 54 · see citing works
Self-citationMcRobb, L. S., Seeto, S., & Ferenci, T. (2003) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2002.2295 · Cited by 49 · see citing works
Blanc, V. M., & Adams, J. (2003) · Genetics · doi:10.1093/genetics/165.3.975 · Cited by 33 · see citing works
The Role of Deleterious and Beneficial Mutations in the Evolution of Ploidy Levels
Otto, S. P. (1994) · Cited by 19 · see citing works
Experimental Studies Of Natural Selection In Bacteria
Dykhuizen, D. (1990) · Annual Review of Ecology and Systematics · doi:10.1146/annurev.ecolsys.21.1.373 · Cited by 15 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Aneuploidy confers quantitative proteome changes and phenotypic variation in budding yeast
Pavelka, N., Rancati, G., Zhu, J., Bradford, W. D., Saraf, A., Florens, L., Sanderson, B. W., Hattem, G. L., & Li, R. (2010) · Nature · doi:10.1038/nature09529 · Cited by 577 · see citing works
Chromosomal duplication is a transient evolutionary solution to stress
Yona, A. H., Manor, Y. S., Herbst, R. H., Romano, G. H., Mitchell, A., Kupiec, M., Pilpel, Y., & Dahan, O. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1211150109 · Cited by 376 · see citing works
The evolution of drug resistance in clinical isolates of Candida albicans.
Ford, C. B., Funt, J. M., Abbey, D., Issi, L., Guiducci, C., Martinez, D. A., Delorey, T., Li, B. Y., White, T. C., Cuomo, C., et al. (2015) · eLife · doi:10.7554/elife.00662 · Cited by 348 · see citing works
Gene Copy-Number Alterations: A Cost-Benefit Analysis
Tang, Y.-C., & Amon, A. (2013) · Cell · doi:10.1016/j.cell.2012.11.043 · Cited by 348 · see citing works
Selmecki, A. M., Dulmage, K., Cowen, L. E., Anderson, J. B., & Berman, J. (2009) · PLoS Genetics · doi:10.1371/journal.pgen.1000705 · Cited by 319 · 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
Hundreds of genes experienced convergent shifts in selective pressure in marine mammals
Chikina, M., Robinson, J. D., & Clark, N. L. (2016) · Molecular Biology and Evolution · doi:10.1093/molbev/msw112 · Cited by 171 · see citing works
Adaptation of<i>Saccharomyces cerevisiae</i>to saline stress through laboratory evolution
DHAR, R., SÄGESSER, R., WEIKERT, C., YUAN, J., & WAGNER, A. (2011) · Journal of Evolutionary Biology · doi:10.1111/j.1420-9101.2011.02249.x · Cited by 165 · see citing works
Evolutionary insight from whole‐genome sequencing of experimentally evolved microbes
DETTMAN, J. R., RODRIGUE, N., MELNYK, A. H., WONG, A., BAILEY, S. F., & KASSEN, R. (2012) · Molecular Ecology · doi:10.1111/j.1365-294x.2012.05484.x · Cited by 160 · see citing works
Ryall, B., Eydallin, G., & Ferenci, T. (2012) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.05028-11 · Cited by 160 · see citing works
Hunger Artists: Yeast Adapted to Carbon Limitation Show Trade-Offs under Carbon Sufficiency
Wenger, J. W., Piotrowski, J., Nagarajan, S., Chiotti, K., Sherlock, G., & Rosenzweig, F. (2011) · PLoS Genetics · doi:10.1371/journal.pgen.1002202 · Cited by 154 · 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
Bennett, R. J., Forche, A., & Berman, J. (2014) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a019604 · Cited by 118 · see citing works
Ploidy Variation in Fungi: Polyploidy, Aneuploidy, and Genome Evolution
Todd, R. T., Forche, A., & Selmecki, A. (2017) · Microbiology Spectrum · doi:10.1128/microbiolspec.funk-0051-2016 · Cited by 121 · 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
Self-citationElsemman, I. E., Rodriguez Prado, A., Grigaitis, P., Garcia Albornoz, M., Harman, V., Holman, S. W., van Heerden, J., Bruggeman, F. J., Bisschops, M. M. M., Sonnenschein, N., et al. (2022) · Nature Communications · doi:10.1038/s41467-022-28467-6 · Cited by 120 · see citing works
Wang, L., Spira, B., Zhou, Z., Feng, L., Maharjan, R. P., Li, X., Li, F., McKenzie, C., Reeves, P. R., & Ferenci, T. (2010) · Genome Biology and Evolution · doi:10.1093/gbe/evq035 · Cited by 114 · 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
Self-citationDeatherage, D. E., Traverse, C. C., Wolf, L. N., & Barrick, J. E. (2015) · Frontiers in Genetics · doi:10.3389/fgene.2014.00468 · Cited by 93 · see citing works
Evolutionary engineering of Saccharomyces cerevisiae for efficient aerobic xylose consumption
Scalcinati, G., Otero, J. M., Vleet, J. R. H., Jeffries, T. W., Olsson, L., & Nielsen, J. (2012) · FEMS Yeast Research · doi:10.1111/j.1567-1364.2012.00808.x · Cited by 89 · see citing works
Oud, B., Maris, A. J. A., Daran, J.-M., & Pronk, J. T. (2012) · FEMS Yeast Research · doi:10.1111/j.1567-1364.2011.00776.x · Cited by 82 · see citing works
The Dynamic Fungal Genome: Polyploidy, Aneuploidy and Copy Number Variation in Response to Stress
Vande Zande, P., Zhou, X., & Selmecki, A. (2023) · Annual Review of Microbiology · doi:10.1146/annurev-micro-041320-112443 · Cited by 70 · see citing works
A Double-Edged Sword: Aneuploidy is a Prevalent Strategy in Fungal Adaptation
Tsai, H.-J., & Nelliat, A. (2019) · Genes · doi:10.3390/genes10100787 · Cited by 60 · see citing works
Hickman, M. J., Spatt, D., & Winston, F. (2011) · Genetics · doi:10.1534/genetics.111.128322 · Cited by 68 · see citing works
Kok, 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
Crozat, E., Winkworth, C., Gaffe, J., Hallin, P. F., Riley, M. A., Lenski, R. E., & Schneider, D. (2010) · Molecular Biology and Evolution · doi:10.1093/molbev/msq099 · Cited by 62 · see citing works
Adamo, G. M., Lotti, M., Tamás, M. J., & Brocca, S. (2012) · Microbiology · doi:10.1099/mic.0.058024-0 · Cited by 60 · see citing works
Mba, I. E., Nweze, E. I., Eze, E. A., & Anyaegbunam, Z. K. G. (2022) · Infection, Genetics and Evolution · doi:10.1016/j.meegid.2022.105256 · Cited by 46 · see citing works
Evolutionary Dynamics of Candida albicans during <i>In Vitro</i> Evolution
Huang, M., McClellan, M., Berman, J., & Kao, K. C. (2011) · Eukaryotic Cell · doi:10.1128/ec.05168-11 · Cited by 34 · see citing works
Life-history strategies and carbon metabolism gene dosage in the<i>Nakaseomyces</i>yeasts
Legrand, J., Bolotin-Fukuhara, M., Bourgais, A., Fairhead, C., & Sicard, D. (2016) · FEMS Yeast Research · doi:10.1093/femsyr/fov112 · Cited by 8 · see citing works
Interpreting noncoding genetic variation in complex traits and human disease
Ward, L. D., & Kellis, M. (2012) · Nature Biotechnology · doi:10.1038/nbt.2422 · Cited by 6 · see citing works
- Authors
- Gresham, D., Desai, M. M., Tucker, C. M., Jenq, H. T., Pai, D. A., Ward, A., DeSevo, C. G., Botstein, D., & Dunham, M. J.
- Affiliations
- Princeton University (US)
- Corresponding author
- Botstein, David
- Dunham, Maitreya J.
- Venue
- PLoS Genetics
- Publisher
- Public Library of Science (PLoS)
- Published
- 2008-12-12
- Volume
- 4
- Issue
- 12
- Pages
- e1000303
- ISSN
- 1553-7390 (ISSN-L)
- 1553-7404
- PMC
- PMC2586090
- OpenAlex
- W2170568588
- Cited by
- 482
- References
- 63
- Citations by year
- 2026: 15 · 2025: 10 · 2024: 35 · 2023: 18 · 2022: 17 · 2021: 34 · 2020: 26 · 2019: 27 · 2018: 27 · 2017: 23 · 2016: 27 · 2015: 44 · 2014: 22 · 2013: 48 · 2012: 46
- FWCI
- 12.00
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- PLoS Genetics (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- National University of Singapore (submittedVersion, cc-by)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Figshare (submittedVersion, cc-by)
- Funders
- National Institutes of Health (GM071508, GM046406)
- National Institute of General Medical Sciences (GM071508, R37GM046406, R01GM046406, GM046406, R01GM107466, P50GM071508)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Evolution and Genetic Dynamics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Fungal and yeast genetics research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Microbial Metabolic Engineering and Bioproduction
- Keywords
- experimental evolution, Saccharomyces cerevisiae, nutrient limitation, glucose limitation, sulfate limitation, phosphate limitation, chemostat, gene amplification, retrotransposition, point mutations, gene expression, fitness, metabolic pathways
- MeSH terms
- Adaptation, Physiological, Genotype, Glucose, Molecular Sequence Data, Mutation, Phenotype, Phosphates, Saccharomyces cerevisiae, Selection, Genetic, Sulfates, Gene Deletion, Evolution, Molecular, Oligonucleotide Array Sequence Analysis, Gene Duplication, Gene Expression Profiling, Saccharomyces cerevisiae Proteins
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
