Cited by 166Evolution and Genetic DynamicsFungal and yeast genetics researchGenetics, Aging, and Longevity in Model Organisms

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Adaptation of Saccharomyces cerevisiae to saline stress through laboratory evolution

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DHAR, R., SÄGESSER, R., WEIKERT, C., YUAN, J., WAGNER, A.·2011·Journal of Evolutionary Biology

DOI 10.1111/j.1420-9101.2011.02249.x

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Abstract

Most laboratory evolution studies that characterize evolutionary adaptation genomically focus on genetically simple traits that can be altered by one or few mutations. Such traits are important, but they are few compared with complex, polygenic traits influenced by many genes. We know much less about complex traits, and about the changes that occur in the genome and in gene expression during their evolutionary adaptation. Salt stress tolerance is such a trait. It is especially attractive for evolutionary studies, because the physiological response to salt stress is well‐characterized on the molecular and transcriptome level. This provides a unique opportunity to compare evolutionary adaptation and physiological adaptation to salt stress. The yeast Saccharomyces cerevisiae is a good model system to study salt stress tolerance, because it contains several highly conserved pathways that mediate the salt stress response. We evolved three replicate lines of yeast under continuous salt (NaCl) stress for 300 generations. All three lines evolved faster growth rate in high salt conditions than their ancestor. In these lines, we studied gene expression changes through microarray analysis and genetic changes through next generation population sequencing. We found two principal kinds of gene expression changes, changes in basal expression (82 genes) and changes in regulation (62 genes). The genes that change their expression involve several well‐known physiological stress‐response genes, including CTT1, MSN4 and HLR1. Next generation sequencing revealed only one high‐frequency single‐nucleotide change, in the gene MOT2, that caused increased fitness when introduced into the ancestral strain. Analysis of DNA content per cell revealed ploidy increases in all the three lines. Our observations suggest that evolutionary adaptation of yeast to salt stress is associated with genome size increase and modest expression changes in several genes.

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1 retracted

A highly conserved kinase is an essential component for stress tolerance in yeast and plant cells
Lee, J. H., MONTAGU, M. V., & Verbruggen, N. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.10.5873 · Cited by 77
Retracted
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
MUSCLE: multiple sequence alignment with high accuracy and high throughput
Edgar, R. C. (2004) · Nucleic Acids Research · doi:10.1093/nar/gkh340 · Cited by 44,662
Finding the missing heritability of complex diseases
Manolio, T. A., Collins, F. S., Cox, N. J., Goldstein, D. B., Hindorff, L. A., Hunter, D. J., McCarthy, M. I., Ramos, E. M., Cardon, L. R., Chakravarti, A., et al. (2009) · Nature · doi:10.1038/nature08494 · Cited by 8,336
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
S ALT AND D ROUGHT S TRESS S IGNAL T RANSDUCTION IN P LANTS
Zhu, J. (2002) · Annual Review of Plant Biology · doi:10.1146/annurev.arplant.53.091401.143329 · Cited by 5,808
Genomic Expression Programs in the Response of Yeast Cells to Environmental Changes
Gasch, A. P., Spellman, P. T., Kao, C. M., Carmel-Harel, O., Eisen, M. B., Storz, G., Botstein, D., & Brown, P. O. (2000) · Molecular Biology of the Cell · doi:10.1091/mbc.11.12.4241 · Cited by 4,815
P LANT C ELLULAR AND M OLECULAR R ESPONSES TO H IGH S ALINITY
Hasegawa, P. M., Bressan, R. A., Zhu, J., & Bohnert, H. J. (2000) · Annual Review of Plant Physiology and Plant Molecular Biology · doi:10.1146/annurev.arplant.51.1.463 · Cited by 4,596
Common SNPs explain a large proportion of the heritability for human height
Yang, J., Benyamin, B., McEvoy, B. P., Gordon, S., Henders, A. K., Nyholt, D. R., Madden, P. A., Heath, A. C., Martin, N. G., Montgomery, G. W., et al. (2010) · Nature Genetics · doi:10.1038/ng.608 · Cited by 4,446
Potential etiologic and functional implications of genome-wide association loci for human diseases and traits
Hindorff, L. A., Sethupathy, P., Junkins, H. A., Ramos, E. M., Mehta, J. P., Collins, F. S., & Manolio, T. A. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0903103106 · Cited by 4,013
Plant salt tolerance
Zhu, J. (2001) · Trends in Plant Science · doi:10.1016/s1360-1385(00)01838-0 · Cited by 3,595
Mammalian Mitogen-Activated Protein Kinase Signal Transduction Pathways Activated by Stress and Inflammation
Kyriakis, J. M., & Avruch, J. (2001) · Physiological Reviews · doi:10.1152/physrev.2001.81.2.807 · Cited by 3,400
Variation and Evolution in Plants
Stebbins, G. L. (1950) · doi:10.7312/steb94536 · Cited by 2,704
A MAP Kinase Targeted by Endotoxin and Hyperosmolarity in Mammalian Cells
Han, J., Lee, J. D., Bibbs, L., & Ulevitch, R. J. (1994) · Science · doi:10.1126/science.7914033 · Cited by 2,647
Genome-wide association defines more than 30 distinct susceptibility loci for Crohn's disease
the NIDDK IBD Genetics Consortium, Barrett, J. C., the Belgian-French IBD Consortium, the Wellcome Trust Case Control Consortium, Hansoul, S., Nicolae, D. L., Cho, J. H., Duerr, R. H., Rioux, J. D., Brant, S. R., et al. (2008) · Nature Genetics · doi:10.1038/ng.175 · Cited by 2,593
Salt Tolerance Conferred by Overexpression of a Vacuolar Na + /H + Antiport in Arabidopsis
Apse, M. P., Aharon, G. S., Snedden, W. A., & Blumwald, E. (1999) · Science · doi:10.1126/science.285.5431.1256 · Cited by 1,964
Meta-analysis of genome-wide association data and large-scale replication identifies additional susceptibility loci for type 2 diabetes
Wellcome Trust Case Control Consortium, Zeggini, E., Scott, L. J., Saxena, R., Voight, B. F., Marchini, J. L., Hu, T., de Bakker, P. I., Abecasis, G. R., Almgren, P., et al. (2008) · Nature Genetics · doi:10.1038/ng.120 · Cited by 1,864
Osmotic Stress Signaling and Osmoadaptation in Yeasts
Hohmann, S. (2002) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.66.2.300-372.2002 · Cited by 1,773
Epistasis — the essential role of gene interactions in the structure and evolution of genetic systems
Phillips, P. C. (2008) · Nature Reviews Genetics · doi:10.1038/nrg2452 · Cited by 1,633
Functional analysis of oxidative stress-activated mitogen-activated protein kinase cascade in plants
Kovtun, Y., Chiu, W.-L., Tena, G., & Sheen, J. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.97.6.2940 · Cited by 1,532
Remodeling of Yeast Genome Expression in Response to Environmental Changes
Causton, H. C., Ren, B., Koh, S. S., Harbison, C. T., Kanin, E. I., Jennings, E. G., Lee, T. I., True, H. L., Lander, E. S., & Young, R. A. (2001) · Molecular Biology of the Cell · doi:10.1091/mbc.12.2.323 · Cited by 1,382
Comparison of prokaryotic diversity at offshore oceanic locations reveals a different microbiota in the Mediterranean Sea
Zaballos, M., López‐López, A., Øvreås, L., Bartual, S. G., D’Auria, G., Alba, J. C., Legault, B. A., Pushker, R., Daae, F. L., & Rodríguez‐Valera, F. (2006) · FEMS Microbiology Ecology · doi:10.1111/j.1574-6941.2006.00060.x · Cited by 1,251
An Osmosensing Signal Transduction Pathway in Yeast
Brewster, J. L., de Valoir, T., Dwyer, N. D., Winter, E., & Gustin, M. C. (1993) · Science · doi:10.1126/science.7681220 · Cited by 1,248
Cellular Memory and the Histone Code
Turner, B. M. (2002) · Cell · doi:10.1016/s0092-8674(02)01080-2 · Cited by 1,142
Epigenetic Regulation of Cellular Memory by the Polycomb and Trithorax Group Proteins
Ringrose, L., & Paro, R. (2004) · Annual Review of Genetics · doi:10.1146/annurev.genet.38.072902.091907 · Cited by 1,093
The Saccharomyces cerevisiae zinc finger proteins Msn2p and Msn4p are required for transcriptional induction through the stress response element (STRE).
Martínez‐Pastor, M. T., Marchler, G. H., Schüller, C., Marchler‐Bauer, A., Ruis, H., & Estruch, F. (1996) · The EMBO Journal · doi:10.1002/j.1460-2075.1996.tb00576.x · Cited by 1,077
K+Nutrition and Na+Toxicity: The Basis of Cellular K+/Na+Ratios
Maathuis, F. J. M. (1999) · Annals of Botany · doi:10.1006/anbo.1999.0912 · Cited by 1,031
Dynamics of adaptation and diversification: a 10,000-generation experiment with bacterial populations.
Lenski, R. E., & Travisano, M. (1994) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.91.15.6808 · Cited by 1,020
The MKK2 Pathway Mediates Cold and Salt Stress Signaling in Arabidopsis
Teige, M., Scheikl, E., Eulgem, T., Dóczi, R., Ichimura, K., Shinozaki, K., Dangl, J. L., & Hirt, H. (2004) · Molecular Cell · doi:10.1016/j.molcel.2004.06.023 · Cited by 1,002
Evolutionary changes in cis and trans gene regulation
Wittkopp, P. J., Haerum, B. K., & Clark, A. G. (2004) · Nature · doi:10.1038/nature02698 · Cited by 873
Nuclear localization of the C2H2 zinc finger protein Msn2p is regulated by stress and protein kinase A activityPreprint
Görner, W., Durchschlag, E., Martínez‐Pastor, M. T., Estruch, F., Ammerer, G., Hamilton, B., Ruis, H., & Schüller, C. (1998) · Genes & Development · doi:10.1101/gad.12.4.586 · Cited by 758
Estimation of effect size distribution from genome-wide association studies and implications for future discoveries
Park, J.-H., Wacholder, S., Gail, M. H., Peters, U., Jacobs, K. B., Chanock, S. J., & Chatterjee, N. (2010) · Nature Genetics · doi:10.1038/ng.610 · Cited by 678
Ploidy Regulation of Gene Expression
Galitski, T., Saldanha, A. J., Styles, C. A., Lander, E. S., & Fink, G. R. (1999) · Science · doi:10.1126/science.285.5425.251 · Cited by 633
The Arabidopsis thaliana proton transporters, AtNhx1 and Avp1, can function in cation detoxification in yeast
Gaxiola, R. A., Rao, R., Sherman, A., Grisafi, P. L., Alper, S. L., & Fink, G. R. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.4.1480 · Cited by 600
Genome–wide association studies provide new insights into type 2 diabetes aetiology
Frayling, T. M. (2007) · Nature Reviews Genetics · doi:10.1038/nrg2178 · Cited by 596
Mitogen and stress response pathways: MAP kinase cascades and phosphatase regulation in mammals and yeast
Waskiewicz, A. J., & Cooper, J. A. (1995) · Current Opinion in Cell Biology · doi:10.1016/0955-0674(95)80063-8 · Cited by 575
An Osmosensing Signal Transduction Pathway in Mammalian Cells
Galcheva-Gargova, Z., Dérijard, B., Wu, I., & Davis, R. J. (1994) · Science · doi:10.1126/science.8047888 · Cited by 569
Characteristic genome rearrangements in experimental evolution of Saccharomyces cerevisiae
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
Reconstitution in yeast of the Arabidopsis SOS signaling pathway for Na + homeostasis
Quintero, F. J., Ohta, M., Shi, H., Zhu, J., & Pardo, J. M. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.132092099 · Cited by 561
The Transcriptional Response of Saccharomyces cerevisiae to Osmotic Shock
Rep, M., Krantz, M., Thevelein, J. M., & Hohmann, S. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.275.12.8290 · Cited by 554
Meta-analysis of genome-wide association study data identifies additional type 1 diabetes risk loci
Cooper, J. D., Smyth, D. J., Smiles, A. M., Plagnol, V., Walker, N. M., Allen, J. E., Downes, K., Barrett, J. C., Healy, B. C., Mychaleckyj, J. C., et al. (2008) · Nature Genetics · doi:10.1038/ng.249 · Cited by 545
The HOG pathway controls osmotic regulation of transcription via the stress response element (STRE) of the Saccharomyces cerevisiae CTT1 gene.
Schüller, C., Brewster, J. L., Alexander, M. R., Gustin, M. C., & Ruis, H. (1994) · The EMBO Journal · doi:10.1002/j.1460-2075.1994.tb06758.x · Cited by 507
Redox control and oxidative stress in yeast cells
Herrero, E., Ros, J., Bellí, G., & Cabiscol, E. (2008) · Biochimica et Biophysica Acta (BBA) - General Subjects · doi:10.1016/j.bbagen.2007.12.004 · Cited by 505
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
The repertoire and dynamics of evolutionary adaptations to controlled nutrient-limited environments in yeast
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
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
Sizing up human height variation
Visscher, P. M. (2008) · Nature Genetics · doi:10.1038/ng0508-489 · Cited by 474
Msn2p, a zinc finger DNA-binding protein, is the transcriptional activator of the multistress response in Saccharomyces cerevisiae.
Schmitt, A. P., & McEntee, K. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.12.5777 · Cited by 472
Stress signaling in plants: a mitogen-activated protein kinase pathway is activated by cold and drought.
Jonak, C., Kiegerl, S., Ligterink, W., Barker, P. J., Huskisson, N. S., & Heribert Hirt, A. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.20.11274 · Cited by 469
Stress tolerance: The key to effective strains of industrial baker's yeast
Attfield, P. V. (1997) · Nature Biotechnology · doi:10.1038/nbt1297-1351 · Cited by 461
A glimpse of the mechanisms of ion homeostasis during salt stress
Serrano, R., Mulet, J. M., Ríos, G., Márquez, J. A., Fernandez-de-Larrinoa, Í., Leube, M. P., Mendizabal, I., Pascual‐Ahuir, A., Proft, M., Ros, R., et al. (1999) · Journal of Experimental Botany · doi:10.1093/jxb/50.special_issue.1023 · Cited by 427
The Transcriptional Response of Yeast to Saline Stress
Posas, F., Chambers, J. R., Heyman, J. A., Hoeffler, J. P., de Nadal, E., & Ariño, J. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.m910016199 · Cited by 423
Test of synergistic interactions among deleterious mutations in bacteria
Elena, S. F., & Lenski, R. E. (1997) · Nature · doi:10.1038/37108 · Cited by 416
A novel P‐type ATPase from yeast involved in sodium transport
Haro, R., Garcíadeblas, B., & Rodríguez‐Navarro, A. (1991) · FEBS Letters · doi:10.1016/0014-5793(91)81280-l · Cited by 361
Salt Tolerance in Plants and Microorganisms: Toxicity Targets and Defense Responses
Serrano, R. (1996) · International review of cytology · doi:10.1016/s0074-7696(08)62219-6 · Cited by 353
The protein phosphatase calcineurin is essential for NaCl tolerance of Saccharomyces cerevisiae.
Mendoza, I., Rubio, F., Rodriguez-Navarro, A., & Pardo, J. M. (1994) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(17)37038-2 · Cited by 350
Aneuploidy Underlies Rapid Adaptive Evolution of Yeast Cells Deprived of a Conserved Cytokinesis Motor
Rancati, G. I., Pavelka, N., Fleharty, B., Noll, A. C., Trimble, R., Walton, K., Perera, A. G., Staehling‐Hampton, K., Seidel, C. W., & Li, R. (2008) · Cell · doi:10.1016/j.cell.2008.09.039 · Cited by 341
CYGD: the Comprehensive Yeast Genome Database
Güldener, U. (2004) · Nucleic Acids Research · doi:10.1093/nar/gki053 · Cited by 333
Molecular characterization of clonal interference during adaptive evolution in asexual populations of Saccharomyces cerevisiae
Kao, K. C., & Sherlock, G. J. (2008) · Nature Genetics · doi:10.1038/ng.280 · Cited by 314
Osmotic Stress-Induced Gene Expression in Saccharomyces cerevisiae Requires Msn1p and the Novel Nuclear Factor Hot1p
Rep, M., Reiser, V., Gärtner, U., Thevelein, J. M., Hohmann, S., Ammerer, G., & Ruis, H. (1999) · Molecular and Cellular Biology · doi:10.1128/mcb.19.8.5474 · Cited by 283
High-resolution yeast phenomics resolves different physiological features in the saline response
Warringer, J., Ericson, E., Fernandez, L., Nerman, O., & Blomberg, A. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2435976100 · Cited by 243
Regulation of the Osmoregulatory HOG MAPK Cascade in Yeast
Saito, H. (2004) · The Journal of Biochemistry · doi:10.1093/jb/mvh135 · Cited by 240
Transcript Expression in Saccharomyces cerevisiae at High Salinity
Yale, J., & Bohnert, H. J. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m008209200 · Cited by 226
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
Stress signaling through Ca 2+ /calmodulin-dependent protein phosphatase calcineurin mediates salt adaptation in plants
Pardo, J. M., Reddy, M. P., Yang, S., Maggio, A., Huh, G., Matsumoto, T. K., Coca, M. A., D’Urzo, M. P., Koiwa, H., Yun, D., et al. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.16.9681 · Cited by 217
The NOT proteins are part of the CCR4 transcriptional complex and affect gene expression both positively and negatively
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
A search in the genome ofSaccharomyces cerevisiae for genes regulated via stress response elements
Moskvina, E., Schüller, C., Maurer, C. T. C., Mager, W. H., & Ruis, H. (1998) · Yeast · doi:10.1002/(sici)1097-0061(199808)14:11 · Cited by 204
Differential expression of two genes encoding isoforms of the ATPase involved in sodium efflux in Saccharomyces cerevisiae
Garcíadeblas, B., Rubio, F., Quintero, F. J., Bañuelos, M. A., Haro, R., & Rodríguez‐Navarro, A. (1993) · Molecular and General Genetics MGG · doi:10.1007/bf00277134 · Cited by 203
A novel and conserved salt‐induced protein is an important determinant of salt tolerance in yeast.
Gaxiola, R. A., Fernandez-de-Larrinoa, Í., Villalba, J. M., & Serrano, R. (1992) · The EMBO Journal · doi:10.1002/j.1460-2075.1992.tb05392.x · Cited by 200
A Novel Mechanism of Ion Homeostasis and Salt Tolerance in Yeast: the Hal4 and Hal5 Protein Kinases Modulate the Trk1-Trk2 Potassium Transporter
Mulet, J. M., Leube, M. P., Kron, S. J., Ríos, G., Fink, G. R., & Serrano, R. (1999) · Molecular and Cellular Biology · doi:10.1128/mcb.19.5.3328 · Cited by 197
Hsp30, the integral plasma membrane heat shock protein of Saccharmyces cerevisiae, is a stress-inducible regulator of plasma membrane H+-ATPase
Piper, P. W., Ortiz-Calderon, C., Holyoak, C. D., Coote, P. J., & Cole, M. (1997) · Cell Stress and Chaperones · doi:10.1379/1466-1268(1997)002 · Cited by 192
cDNA cloning of MAP kinase kinase reveals kinase cascade pathways in yeasts to vertebrates.
Kosako, H., Nishida, E., & Gotoh, Y. (1993) · The EMBO Journal · doi:10.1002/j.1460-2075.1993.tb05713.x · Cited by 179
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
Functional conservation between yeast and plant endosomal Na+/H+ antiporters1
Quintero, F. J., Blatt, M. R., & Pardo, J. M. (2000) · FEBS Letters · doi:10.1016/s0014-5793(00)01412-5 · Cited by 176
Arabidopsis thaliana AtHAL3: a flavoprotein related to salt and osmotic tolerance and plant growth
Espinosa‐Ruíz, A., Bellés, J. M., Serrano, R., & Culiáñez‐Macià, F. A. (1999) · The Plant Journal · doi:10.1046/j.1365-313x.1999.00626.x · Cited by 176
Tetraploid citrus rootstocks are more tolerant to salt stress than diploid
Saleh, B., Allario, T., Dambier, D., Ollitrault, P., & Morillón, R. (2008) · Comptes Rendus Biologies · doi:10.1016/j.crvi.2008.06.007 · Cited by 169
Salt Stress inDesulfovibrio vulgarisHildenborough: an Integrated Genomics Approach
Mukhopadhyay, A., He, Z., Alm, E. J., Arkin, A. P., Baidoo, E. E. K., Borglin, S. E., Chen, W., Hazen, T. C., He, Q., Holman, H. N., et al. (2006) · Journal of Bacteriology · doi:10.1128/jb.01921-05 · Cited by 168
The YeastHAL1Gene Improves Salt Tolerance of Transgenic Tomato
Gisbert, C., Rus, A. M., Bolarín, M. C., López-Coronado, J., Arrillaga, I., Montesinos, C., Caro, M., Serrano, R., & Moreno, V. (2000) · PLANT PHYSIOLOGY · doi:10.1104/pp.123.1.393 · Cited by 163
Evolution of Escherichia coli for Growth at High Temperatures
Rudolph, B., Gebendorfer, K. M., Büchner, J., & Winter, J. (2010) · Journal of Biological Chemistry · doi:10.1074/jbc.m110.103374 · Cited by 156
Regulation of Cation Transport in Saccharomyces cerevisiae by the Salt Tolerance Gene HAL3
Ferrando, A., Kron, S. J., Ríos, G., Fink, G. R., & Serrano, R. (1995) · Molecular and Cellular Biology · doi:10.1128/mcb.15.10.5470 · Cited by 154
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
High Osmolarity Glycerol (HOG) Pathway-induced Phosphorylation and Activation of 6-Phosphofructo-2-kinase Are Essential for Glycerol Accumulation and Yeast Cell Proliferation under Hyperosmotic Stress
Dihazi, H., Keßler, R., & Eschrich, K. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m312974200 · Cited by 151
Polarized localization of yeast Pbs2 depends on osmostress, the membrane protein Sho1 and Cdc42
Reiser, V., Salah, S. M., & Ammerer, G. (2000) · Nature Cell Biology · doi:10.1038/35023568 · Cited by 149
A Yeast Catabolic Enzyme Controls Transcriptional Memory
Zacharioudakis, I. M., Gligoris, T. G., & Tzamarias, D. (2007) · Current Biology · doi:10.1016/j.cub.2007.10.044 · Cited by 147
Induction of major heat-shock proteins of Saccharomyces cerevisiae, including plasma membrane Hsp30, by ethanol levels above a critical threshold
Piper, P. W., Talreja, K., Panaretou, B., Moradas‐Ferreira, P., Byrne, K. L., Praekelt, U. M., Meacock, P. A., Recnacq, M., & Boucherie, H. (1994) · Microbiology · doi:10.1099/13500872-140-11-3031 · Cited by 142
Plants use calcium to resolve salt stress
Bressan, R. A., Hasegawa, P. M., & Pardo, J. M. (1998) · Trends in Plant Science · doi:10.1016/s1360-1385(98)01331-4 · Cited by 142
The Yeast HAL2 Nucleotidase Is an in Vivo Target of Salt Toxicity
Murguía, J. R., Bellés, J. M., & Serrano, R. (1996) · Journal of Biological Chemistry · doi:10.1074/jbc.271.46.29029 · Cited by 137
Prevalent positive epistasis in Escherichia coli and Saccharomyces cerevisiae metabolic networks
He, X., Qian, W., Wang, Z., Li, Y., & Zhang, J. (2010) · Nature Genetics · doi:10.1038/ng.524 · Cited by 137
Yeast putative transcription factors involved in salt tolerance
Mendizabal, I., Rios, G., Mulet, J. M., Serrano, R., & de Larrinoa, I. F. (1998) · FEBS Letters · doi:10.1016/s0014-5793(98)00249-x · Cited by 136
MAP kinases in plant signal transduction
Jonak, C., Ligterink, W., & Hirt, H. (1999) · Cellular and Molecular Life Sciences · doi:10.1007/s000180050285 · Cited by 126
Adaptation and major chromosomal changes in populations of Saccharomyces cerevisiae
Adams, J., Puskas-Rozsa, S., Simlar, J., & Wilke, C. M. (1992) · Current Genetics · doi:10.1007/bf00351736 · Cited by 123
Control of Transcription by Cell Size
Wu, C., Rolfe, A., Gifford, D. K., & Fink, G. R. (2010) · PLoS Biology · doi:10.1371/journal.pbio.1000523 · Cited by 117
Polyubiquitination of the demethylase Jhd2 controls histone methylation and gene expressionPreprint
Mersman, D. P., Du, H., Fingerman, I. M., South, P. F., & Briggs, S. D. (2009) · Genes & Development · doi:10.1101/gad.1769209 · Cited by 117
The Yeast Ccr4-Not Complex Controls Ubiquitination of the Nascent-associated Polypeptide (NAC-EGD) Complex
Panasenko, O. O., Landrieux, E., Feuermann, M., Finka, A., Paquet, N., & Collart, M. A. (2006) · Journal of Biological Chemistry · doi:10.1074/jbc.m604986200 · Cited by 110
Xbp1, a Stress-Induced Transcriptional Repressor of the Saccharomyces cerevisiae Swi4/Mbp1 Family
Mai, B., & Breeden, L. L. (1997) · Molecular and Cellular Biology · doi:10.1128/mcb.17.11.6491 · Cited by 109
Adaptation of experimental yeast populations to stressful conditions in relation to population size
Samani, P., & Bell, G. (2010) · Journal of Evolutionary Biology · doi:10.1111/j.1420-9101.2010.01945.x · Cited by 105
Coordinated Changes in DNA Methylation and Histone Modifications Regulate Silencing/Derepression of Luteinizing Hormone Receptor Gene Transcription
Zhang, Y., Fatima, N., & Dufau, M. L. (2005) · Molecular and Cellular Biology · doi:10.1128/mcb.25.18.7929-7939.2005 · Cited by 104
Conservation and reiteration of a kinase cascade
Neiman, A. M. (1993) · Trends in Genetics · doi:10.1016/0168-9525(93)90139-9 · Cited by 103
The plasma membrane of yeast acquires a novel heat‐shock protein (hsp30) and displays a decline in proton‐pumping ATPase levels in response to both heat shock and the entry to stationary phase
Panaretou, B., & Piper, P. W. (1992) · European Journal of Biochemistry · doi:10.1111/j.1432-1033.1992.tb16968.x · Cited by 102
Phylogenetic Classification of the Mitochondrial Carrier Family ofSaccharomyces cerevisiae
Moualij, B. E., Duyckaerts, C., Lamotte‐Brasseur, J., & Sluse, F. E. (1997) · Yeast · doi:10.1002/(sici)1097-0061(199705)13:6 · Cited by 100
Genome-wide Association Studies and Human Disease
Visscher, P. M., & Montgomery, G. W. (2009) · JAMA · doi:10.1001/jama.2009.1643 · Cited by 99
Yeast Glycogen Synthase Kinase-3 Activates Msn2p-dependent Transcription of Stress Responsive Genes
Hirata, Y., Andoh, T., Asahara, T., & Kikuchi, A. (2003) · Molecular Biology of the Cell · doi:10.1091/mbc.e02-05-0247 · Cited by 97
Catalases protect cellular proteins from oxidative modification in
Lushchak, V. I., & Gospodaryov, D. V. (2005) · Cell Biology International · doi:10.1016/j.cellbi.2004.11.001 · Cited by 91
Screening and construction of Saccharomyces cerevisiae strains with improved multi-tolerance and bioethanol fermentation performance
Zheng, D., Wu, X., Tao, X.-L., Wang, P., Li, P., Chi, X., Li, Y., Yan, Q., & Zhao, Y. (2010) · Bioresource Technology · doi:10.1016/j.biortech.2010.09.122 · Cited by 88
Plant biology: The salty tale of Arabidopsis
Sanders, D. (2000) · Current Biology · doi:10.1016/s0960-9822(00)00554-6 · Cited by 85
Genetic Evidence Supports a Role for the Yeast CCR4-NOT Complex in Transcriptional Elongation
Denis, C. L., Chiang, Y. C., Cui, Y., & Chen, J. (2001) · Genetics · doi:10.1093/genetics/158.2.627 · Cited by 85
Hyperosmotic stress response and regulation of cell wall integrity in Saccharomyces cerevisiae share common functional aspects
Alonso‐Monge, R., Real, E., Wojda, I., Bebelman, J., Mager, W. H., & Siderius, M. H. (2001) · Molecular Microbiology · doi:10.1046/j.1365-2958.2001.02549.x · Cited by 85
Functional Interaction of CCR4-NOT Proteins With TATAA-Binding Protein (TBP) and Its Associated Factors in Yeast
Badarinarayana, V., Chiang, Y. C., & Denis, C. L. (2000) · Genetics · doi:10.1093/genetics/155.3.1045 · Cited by 84
Increased cell size and shortened peptidoglycan interpeptide bridge of NaCl-stressed Staphylococcus aureus and their reversal by glycine betaine
Vijaranakul, U., Nadakavukaren, M. J., DeJonge, B. L. M., Wilkinson, B. J., & Jayaswal, R. K. (1995) · Journal of Bacteriology · doi:10.1128/jb.177.17.5116-5121.1995 · Cited by 83
The genetic basis of evolutionary change in gene expression levels
Emerson, J. J., & Li, W. (2010) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2010.0005 · Cited by 72
Evolution of Penicillin-Binding Protein 2 Concentration and Cell Shape during a Long-Term Experiment withEscherichia coli
Philippe, N., Pélosi, L., Lenski, R. E., & Schneider, D. (2008) · Journal of Bacteriology · doi:10.1128/jb.01419-08 · Cited by 68
Hph1p and Hph2p, Novel Components of Calcineurin-Mediated Stress Responses in Saccharomyces cerevisiae
Heath, V. L., Shaw, S. L., Roy, S., & Cyert, M. (2004) · Eukaryotic Cell · doi:10.1128/ec.3.3.695-704.2004 · Cited by 68
EPISTASIS BETWEEN NEW MUTATIONS AND GENETIC BACKGROUND AND A TEST OF GENETIC CANALIZATION
Elena, S. F., & Lenski, R. E. (2001) · Evolution · doi:10.1111/j.0014-3820.2001.tb00824.x · Cited by 61
The Extracellular Domain of the Saccharomyces cerevisiae Sln1p Membrane Osmolarity Sensor Is Necessary for Kinase Activity
Ostrander, D. B., & Gorman, J. A. (1999) · Journal of Bacteriology · doi:10.1128/jb.181.8.2527-2534.1999 · Cited by 48
Identification and dynamics of a beneficial mutation in a long-term evolution experiment with Escherichia coli
Stanek, M. T., Cooper, T. F., & Lenski, R. E. (2009) · BMC Evolutionary Biology · doi:10.1186/1471-2148-9-302 · Cited by 42
Physiology of Polyploid Plants: Water Balance in Autotetraploid and Diploid Tomato under Low and High Salinity
Tal, M., & GARDI, I. (1976) · Physiologia Plantarum · doi:10.1111/j.1399-3054.1976.tb04000.x · Cited by 41
Characterization of Gac1p, a regulatory subunit of protein phosphatase type I involved in glycogen accumulation in Saccharomyces cerevisiae
Wu, X., Hart, H., Cheng, C., Roach, P. J., & Tatchell, K. (2001) · Molecular Genetics and Genomics · doi:10.1007/s004380100455 · Cited by 40
Structure of evolving populations of Saccharomyces cerevisiae: adaptive changes are frequently associated with sequence alterations involving mobile elements belonging to the Ty family.
Adams, J., & Oeller, P. W. (1986) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.83.18.7124 · Cited by 34
Evolution in Saccharomyces cerevisiae: Identification of Mutations Increasing Fitness in Laboratory Populations
Blanc, V. M., & Adams, J. (2003) · Genetics · doi:10.1093/genetics/165.3.975 · Cited by 33
ISC1‐encoded inositol phosphosphingolipid phospholipase C is involved in Na+/Li+ halotolerance of Saccharomyces cerevisiae
Betz, C., Zajonc, D. M., Moll, M., & Schweizer, E. (2002) · European Journal of Biochemistry · doi:10.1046/j.1432-1033.2002.03096.x · Cited by 32
Cooperative Regulation of DOG2 , Encoding 2-Deoxyglucose-6-Phosphate Phosphatase, by Snf1 Kinase and the High-Osmolarity Glycerol–Mitogen-Activated Protein Kinase Cascade in Stress Responses of Saccharomyces cerevisiae
Tsujimoto, Y., Izawa, S., & Inoue, Y. (2000) · Journal of Bacteriology · doi:10.1128/jb.182.18.5121-5126.2000 · Cited by 32
Cell Size, Shape, and Fitness in Evolving Populations of Bacteria
Lenski, R. E., & Mongold, J. A. (2000) · doi:10.1093/oso/9780195131413.003.0012 · Cited by 30
MOT2 encodes a negative regulator of gene expression that affects basal expression of pheromone-responsive genes in Saccharomyces cerevisiae.
Cade, R. M., & Errede, B. (1994) · Molecular and Cellular Biology · doi:10.1128/mcb.14.5.3139 · Cited by 28
Identification of a Calcineurin-Independent Pathway Required for Sodium Ion Stress Response in Saccharomyces cerevisiae
Ganster, R. W., McCartney, R. R., & Schmidt, M. C. (1998) · Genetics · doi:10.1093/genetics/150.1.31 · Cited by 28
HAL1 mediate salt adaptation in Arabidopsis thaliana
Yang, S., Zhao, Y. X., ZHANG, Q., Yu Ke, H. E., Zhang, H., & Luo, D. (2001) · Cell Research · doi:10.1038/sj.cr.7290079 · Cited by 26
Epistatic and Synergistic Interactions Between Circadian Clock Mutations in Neurospora crassa
Morgan, L. W., & Feldman, J. F. (2001) · Genetics · doi:10.1093/genetics/159.2.537 · Cited by 15
NaCl stress inhibits maltose fermentation by Saccharomyces cerevisiae
Trainotti, N., & Stambuk, B. U. (2001) · Biotechnology Letters · doi:10.1023/a:1012456432280 · Cited by 11
Involvement of Nst1p/YNL091w and Msl1p, a U2B″ splicing factor, in Saccharomyces cerevisiae salt tolerance
Goossens, A., Forment, J., & Serrano, R. (2002) · Yeast · doi:10.1002/yea.815 · Cited by 10
Essentials of Genomics
Benfey, P. N., & Protopapas, A. D. (2005) · Medical Entomology and Zoology · Cited by 4
Biochemistry, cell biology and molecular biology of lipids ofSaccharomyces cerevisiae
Daum, G., Lees, N. D., Bard, M., & Dickson, R. (1998) · Yeast · doi:10.1002/(sici)1097-0061(199812)14:16

Flagged first, then by citations

2 of the 132 references couldn’t be matched to a known paper.

Research works printed but not linked: 3

10.1016/S0022-2836(05)80360-2 · DOI · Paper page
Noggle R., 1946, The physiology of polyploidy in plants. I. Review of the literature, Lloydia, 9, 153
Sambrook J., 2001, Molecular Cloning: A Laboratory Manual

Sorted by citations

Adaptive laboratory evolution—Principles and applications for biotechnology
Dragosits, M., & Mattanovich, D. (2013) · Microbial Cell Factories · doi:10.1186/1475-2859-12-64 · Cited by 827
Experimental evolution
Kawecki, T. J., Lenski, R. E., Ebert, D., Hollis, B., Olivieri, I., & Whitlock, M. C. (2012) · Trends in Ecology & Evolution · doi:10.1016/j.tree.2012.06.001 · Cited by 807
Gene duplication as a mechanism of genomic adaptation to a changing environment
Kondrashov, F. A. (2012) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2012.1108 · Cited by 663
Contingency and determinism in evolution: Replaying life’s tape
Blount, Z. D., Lenski, R. E., & Losos, J. B. (2018) · Science · doi:10.1126/science.aam5979 · Cited by 590
The emergence of adaptive laboratory evolution as an efficient tool for biological discovery and industrial biotechnology
Sandberg, T. E., Salazar, M. J., Weng, L. L., Palsson, B. Ø., & Feist, A. M. (2019) · Metabolic Engineering · doi:10.1016/j.ymben.2019.08.004 · Cited by 585

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Authors: DHAR, R., SÄGESSER, R., WEIKERT, C., YUAN, J., & WAGNER, A.
Affiliations: SIB Swiss Institute of Bioinformatics (CH)
Corresponding author: WAGNER, A.
ORCID: DHAR, R.
YUAN, J.
WAGNER, A.
Venue: Journal of Evolutionary Biology
Publisher: Oxford University Press (OUP)
Published: 2011-03-07
Volume: 24
Issue: 5
Pages: 1135-1153
ISSN: 1010-061X (ISSN-L)
1420-9101
DOI: 10.1111/j.1420-9101.2011.02249.x
OpenAlex: W1805449453
Cited by: 165
References: 132
Citations by year: 2026: 5 · 2025: 8 · 2024: 9 · 2023: 18 · 2022: 9 · 2021: 10 · 2020: 22 · 2019: 8 · 2018: 8 · 2017: 9 · 2016: 4 · 2015: 12 · 2014: 16 · 2013: 14 · 2012: 9
FWCI: 8.59
Type: journal article
Language: en
Open access: green
www.zora.uzh.ch
Licence: other-oa
onlinelibrary.wiley.com/termsAndConditions#vor (vor)
Locations: Journal of Evolutionary Biology (publishedVersion)
PubMed (publishedVersion)
Zurich Open Repository and Archive (University of Zurich) (acceptedVersion, other-oa)
Zurich Open Repository and Archive (University of Zurich) (submittedVersion, other-oa)
Zurich Open Repository and Archive (University of Zurich)
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 › Aging › Genetics, Aging, and Longevity in Model Organisms
Keywords: Saccharomyces cerevisiae, salt tolerance, experimental evolution, adaptive evolution, gene expression changes, polygenic traits, CTT1, Msn4, genome size, NaCl stress, stress response genes
MeSH terms: Adaptation, Biological, Biological Evolution, Gene Amplification, Genes, Fungal, Ploidies, Saccharomyces cerevisiae, Sodium Chloride, Gene Expression Regulation, Fungal, Electrophoresis, Gel, Pulsed-Field, Gene Deletion, Sequence Analysis, DNA, Gene Duplication, Gene Expression Profiling, Salinity

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Adaptation of Saccharomyces cerevisiae to saline stress through laboratory evolution

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