Hunger artists: Yeast adapted to carbon limitation show trade-offs under carbon sufficiency

PLoS Genetics

Volumn 7, Issue 8, 2011, Pages

  Wenger, Jared W ^a   Piotrowski, Jeffrey ^b   Nagarajan, Saisubramanian ^c   Chiotti, Kami ^c   Sherlock, Gavin ^a   Rosenzweig, Frank ^c  

^a STANFORD UNIVERSITY   (United States)

^b RIKEN   (Japan)

^c UNIVERSITY OF MONTANA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARBON; GLUCOSE; MITOCHONDRIAL PROTEIN;

ARTICLE; CARBON SOURCE; CONTROLLED STUDY; EVOLUTIONARY ADAPTATION; GENE; GENE EXPRESSION REGULATION; GENE MUTATION; GENETIC ASSOCIATION; GROWTH RATE; HEXOKINASE 2 GENE; LAST COMMON ANCESTOR; MOLECULAR CLONING; MOLECULAR DYNAMICS; NONHUMAN; PHENOTYPE; POPULATION ABUNDANCE; QUORUM SENSING; SACCHAROMYCES CEREVISIAE; SEQUENCE ANALYSIS; SIGNAL TRANSDUCTION; STEADY STATE; UPREGULATION; ADAPTATION; CLUSTER ANALYSIS; ENVIRONMENT; EVOLUTION; FUNGAL GENOME; GENE EXPRESSION PROFILING; GENETICS; METABOLISM; MITOCHONDRION; MUTATION; PHYSIOLOGY; REPRODUCTIVE FITNESS; YEAST;

ADAPTATION, BIOLOGICAL; BIOLOGICAL EVOLUTION; CARBON; CLUSTER ANALYSIS; ENVIRONMENT; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, FUNGAL; GENETIC FITNESS; GENOME, FUNGAL; GLUCOSE; MITOCHONDRIA; MUTATION; SIGNAL TRANSDUCTION; YEASTS;

EID: 80052324811     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1002202     Document Type: Article

References (81)

1. Fisher RA, (1930) The Genetical Theory of Natural Selection Oxford Oxford University Press.
2. Burke MK, Dunham JP, Shahrestani P, Thornton KR, Rose MR, et al. (2010) Genome-wide analysis of a long-term evolution experiment with Drosophila. Nature 467: 587-590.
3. Elena S, Lenski R, (2003) Evolution experiments with microorganisms: the dynamics and genetic bases of adaptation. Nature Reviews Genetics 4: 457-469.
4. Goho S, Bell G, (2000) The ecology and genetics of fitness in Chlamydomonas. IX. The rate of accumulation of variation of fitness under selection. Evolution 54: 416-424.
5. Zeyl C, (2006) Experimental evolution with yeast. FEMS Yeast Research 6: 685-691.
6. Huey RB, Rosenzweig F, (2009) Laboratory Evolution Meets Catch-22. In: Garland TJ, Rose MR, editors. Experimental Evolution: Concepts, Methods, and Applications of Selection Experiments: Regents of the University of California pp. 671-702.
7. Paquin C, Adams J, (1982) Isolation of Sets of a, α, a/α, a/a and α/α isogenic strains in Saccharomyces cerevisiae. Current Genetics 6: 21-24.
8. Paquin C, Adams J, (1983) Frequency of fixation of adaptive mutations is higher in evolving diploid than haploid yeast populations. Nature 302: 495-500.
9. Paquin CE, Adams J, (1983) Relative fitness can decrease in evolving asexual populations of S. cerevisiae. Nature 306: 368-370.
10. Adams J, Paquin C, Oeller PW, Lee LW, (1985) Physiological characterization of adaptive clones in evolving populations of the yeast, Saccharomyces cerevisiae. Genetics 110: 173-185.
11. Brown C, Todd K, Rosenzweig R, (1998) Multiple duplications of yeast hexose transport genes in response to selection in a glucose-limited environment. Molecular Biology and Evolution 15: 931.
12. Kao KC, Sherlock G, (2008) Molecular characterization of clonal interference during adaptive evolution in asexual populations of Saccharomyces cerevisiae. Nat Genet 40: 1499-1504.
13. Ferea TL, Botstein D, Brown PO, Rosenzweig RF, (1999) Systematic changes in gene expression patterns following adaptive evolution in yeast. Proceedings of the National Academy of Sciences 96: 9721-9726.
14. Dunham MJ, Badrane H, Ferea T, Adams J, Brown PO, et al. (2002) Characteristic genome rearrangements in experimental evolution of Saccharomyces cerevisiae. Proceedings of the National Academy of Sciences 99: 16144-16149.
15. Harpole WS, Tilman D, (2007) Grassland species loss resulting from reduced niche dimension. Nature 446: 791-793.
16. Passy SI, (2008) Continental diatom biodiversity in stream benthos declines as more nutrients become limiting. Proceedings of the National Academy of Sciences 105: 9666-9667.
17. Tilman D, (1982) Resource competition and community structure Princeton Princeton University Press.
18. Stearns SC, (1977) The evolution of life history traits: A critique of the theory and a review of the data. Annual Review of Ecology and Systematics 8: 145-171.
19. Kassen R, (2002) The experimental evolution of specialists, generalists, and the maintenance of diversity. Journal of Evolutionary Biology 15: 173-190.
20. Kawecki TJ, (1994) Accumulation of Deleterious Mutations and the Evolutionary Cost of Being a Generalist. The American Naturalist 144: 833-838.
21. Van Tienderen PH, (1991) Evolution of Generalists and Specialists in Spatially Heterogeneous Environments. Evolution 45: 1317-1331.
22. Wilson DS, Yoshimura J, (1994) On the Coexistence of Specialists and Generalists. The American Naturalist 144: 692-707.
23. Cooper TF, Lenski RE, (2010) Experimental evolution with E. coli in diverse resource environments. I. Fluctuating environments promote divergence of replicate populations. BMC Evolutionary Biology 10: 1-10.
24. Fry JD, (1996) The Evolution of Host Specialization: Are Trade-Offs Overrated? The American Naturalist 148: S84-S107.
25. Joshi A, Thompson JN, (1995) Trade-offs and the evolution of host specialization. Evolutionary Ecology 9: 82-92.
26. Via S, Gomulkiewicz R, De Jong G, Schlichting CD, Van Tienderen PH, (1995) Adaptive phenotypic plasticity: consensus and controversy. Trends in Ecology & Evolution 10: 212-217.
27. Reboud X, Bell G, (1997) Experimental evolution in Chlamydomonas. III. Evolution of specialist and generalist types in environments that vary in space and time. Heredity 78: 507-514.
28. Whitlock M, (1996) The Red Queen Beats the Jack-of-All-Trades: The Limitations on the Evolution of Phenotypic Plasticity and Niche Breadth. The American Naturalist 148: S65-77.
29. Bell G, Reboud X, (1997) Experimental evolution in Chlamydomonas. II. Genetic variation in strongly contrasted environments. Heredity 78: 498-506.
30. Cooper V, Lenski R, (2000) The population genetics of ecological specialization in evolving Escherichia coli populations. Nature 407: 736-739.
31. Travisano M, Lenski R, (1996) Long-term experimental evolution in Escherichia coli. IV. Targets of selection and the specificity of adaptation. Genetics 143: 15-26.
32. Travisano M, Vasi F, Lenski R, (1995) Long-term experimental evolution in Escherichia coli. III. Variation among replicate populations in correlated responses to novel environments. Evolution 49: 189-200.
33. Bennett A, Lenski R, (1993) Evolutionary adaptation to temperature II. Thermal niches of experimental lines of Escherichia coli. Evolution 47: 1-12.
34. Bennett A, Lenski R, (2007) An experimental test of evolutionary trade-offs during temperature adaptation. Proceedings of the National Academy of Sciences 104: 8649-8654.
35. Bennett A, Lenski R, Mittler J, (1992) Evolutionary adaptation to temperature. I. Fitness responses of Escherichia coli to changes in its thermal environment. Evolution 46: 16-30.
36. Zhong S, Khodursky A, Dykhuizen DE, Dean AM, (2004) Evolutionary genomics of ecological specialization. Proceedings of the National Academy of Sciences 101: 11719-11724.
37. Araya CL, Payen C, Dunham MJ, Fields S, (2010) Whole-genome sequencing of a laboratory-evolved yeast strain. BMC Genomics 11: 88.
38. Gresham D, Desai M, Tucker C, Jenq H, Pai DA, et al. (2008) The Repertoire and Dynamics of Evolutionary Adaptations to Controlled Nutrient-Limited Environments in Yeast. PLoS Genet 4: e1000303 doi:10.1371/journal.pgen.1000303.
39. Gresham D, Ruderfer DM, Pratt SC, Schacherer J, Dunham MJ, et al. (2006) Genome-wide Detection of Polymorphisms at Nucleotide Resolution with a Single DNA Microarray. Science 311: 1932-1936.
40. Kinnersley MA, Holben WE, Rosenzweig F, (2009) E Unibus Plurum: Genomic Analysis of an Experimentally Evolved Polymorphism in Escherichia coli. PLoS Genet 5: e1000713 doi:10.1371/journal.pgen.1000713.
41. Chang S, Leu J, (2011) A Tradeoff Drives the Evolution of Reduced Metal Resistance in Natural Populations of Yeast. PLoS Genet 7: e1002034 doi:10.1371/journal.pgen.1002034.
42. Jansen ML, Diderich JA, Mashego M, Hassane A, de Winde JH, et al. (2005) Prolonged selection in aerobic, glucose-limited chemostat cultures of Saccharomyces cerevisiae causes a partial loss of glycolytic capacity. Microbiology 151: 1657-1669.
43. Walsh RB, Kawasaki G, Fraenkel D, (1983) Cloning of Genes That Complement Yeast Hexokinase and Glucokinase Mutants. Journal of Bacteriology 154: 1002-1004.
44. Ahuatzi D, Herrero P, de la Cera T, Moreno F, (2004) The Glucose-regulated Nuclear Localization of Hexokinase 2 in Saccharomyces cerevisiae Is Mig1-dependent. The Journal of Biological Chemistry 279: 14440-14446.
45. Palomino A, Herrero P, Moreno F, (2006) Tpk3 and Snf1 protein kinases regulate Rgt1 association with Saccharomyces cerevisiae HXK2 promoter. Nucleic Acids Research 34: 1427-1438.
46. Tusher VG, Tibshirani R, Chu G, (2001) Significance analysis of microarrays applied to the ionizing radiation response. Proceedings of the National Academy of Sciences 98: 5116-5121.
47. Bos JL, (1989) ras Oncogenes in Human Cancer: A Review. Cancer Research 49: 4682-4689.
48. Cardenas ME, Cutler NS, Lorenz MC, Di Como CJ, Heitman J, (1999) The TOR signaling cascade regulates gene expression in response to nutrients. Genes & Development 13: 3271-3279.
49. Hardwick JS, Kuruvilla FG, Tong JK, Shamji AF, Schreiber SL, (1999) Rapamycin-modulated transcription defines the subset of nutrient-sensitive signaling pathways directly controlled by the Tor proteins. Proceedings of the National Academy of Sciences 96: 14866-14870.
50. Yun J, Rago C, Cheong I, Pagliarini R, Angenendt P, et al. (2009) Glucose Deprivation Contributes to the Development of KRAS Pathway Mutations in Tumor Cells. Science 325: 1555-1559.
51. Wang Y, Pierce M, Schneper L, Güldal CG, Zhang X, et al. (2004) Ras and Gpa2 Mediate One Branch of a Redundant Glucose Signaling Pathway in Yeast. PLoS Biology 2: e128 doi:10.1371/journal.pbio.0020128.
52. Düvel K, Santhanam A, Garrett S, Schneper L, Broach JR, (2003) Multiple Roles of Tap42 in Mediating Rapamycin-Induced Transcriptional Changes in Yeast. Molecular Cell 11: 1467-1478.
53. Reinke A, Chen JC, Aronova S, Powers T, (2006) Caffeine targets TOR complex I and provides evidence for a regulatory link between the FRB and kinase domains of Tor1p. Journal of Biological Chemistry 281: 31616-31626.
54. Boyle EI, Weng S, Gollub J, Jin H, Botstein D, et al. (2004) GO::TermFinder-open source software for accessing Gene Ontology information and finding significantly enriched Gene Ontology terms associated with a list of genes. Bioinformatics 20: 3710-3715.
55. Charizanis C, Juhnke H, Krems B, Entian KD, (1999) The oxidative stress response mediated via Pos9/Skn7 is negatively regulated by the Ras/PKA pathway in Saccharomyces cerevisiae. Mol Gen Genet 261: 740-752.
56. Dejean L, Beauvoit B, Bunoust O, Guerin B, Rigoulet M, (2002) Activation of Ras cascade increases the mitochondrial enzyme content of respiratory competent yeast. Biochem Biophys Res Commun 293: 1383-1388.
57. Powers T, Walter P, (1999) Regulation of Ribosome Biogenesis by the Rapamycin-sensitive TOR-signaling Pathway in Saccharomyces cerevisiae. Molecular Biology of the Cell 10: 987-1000.
58. Kvitek DJ, Sherlock G, (2011) Reciprocal Sign Epistasis between Frequently Experimentally Evolved Adaptive Mutations Causes a Rugged Fitness Landscape. PLoS Genet 7: e1002056 doi:10.1371/journal.pgen.1002056.
59. Lang G, Murray A, (2008) Estimating the per-base-pair mutation rate in the yeast Saccharomyces cerevisiae. Genetics 178: 67-82.
60. Ellis TP, Helfenbein KG, Tzagoloff A, Dieckmann CL, (2004) Aep3p stabilizes the mitochondrial bicistronic mRNA encoding subunits 6 and 8 of the H+-translocating ATP synthase of Saccharomyces cerevisiae. Journal of Biological Chemistry 279: 15728-15733.
61. Tanaka K, Nakafuku M, Tamanoi F, Kaziro Y, Matsumoto K, et al. (1990) IRA2, a Second Gene of Saccharomyces cerevisiae that Encodes a Protein with a Domain Homologous to Mammalian ras GTPase-Activating Protein. Molecular and Cellular Biology 10: 4303-4313.
62. Kataoka T, Broek D, Wigler M, (1985) DNA Sequence and Characterization of the S. cerevisiae Gene Encoding Adenylate Cyclase. Cell 43: 493-505.
63. Castrillo JI, Zeef LA, Hoyle DC, Zhang N, Hayes A, et al. (2007) Growth control of the eukaryote cell: a systems biology study in yeast. J Biol 6: 4.
64. Loewith R, Jacinto E, Wullschleger S, Lorberg A, Crespo JL, et al. (2002) Two TOR Complexes, Only One of which Is Rapamycin Sensitive, Have Distinct Roles in Cell Growth Control. Molecular Cell 10: 457-468.
65. Robertson RP, (2004) Chronic Oxidative Stress as a Central Mechanism for Glucose Toxicity in Pancreatic Islet Beta Cells in Diabetes. Journal of Biological Chemistry 279: 42351-42354.
66. Barea F, Bonatto D, (2008) Relationships among carbohydrate intermediate metabolites and DNA damage and repair in yeast from a systems biology perspective. Mutation Research 642: 43-56.
67. Diderich JA, Schepper M, van Hoek P, Luttik MA, van Dijken JP, et al. (1999) Glucose Uptake Kinetics and Transcription of HXT Genes in Chemostat Cultures of Saccharomyces cerevisiae. Journal of Biological Chemistry 274: 15350-15359.
68. Berg JM, Tymoczko JL, Stryer L, (2007) Biochemistry New York W.H. Freeman.
69. Dykhuizen D, Dean A, (1994) Predicted fitness changes along an environmental gradient. Evolutionary Ecology 8: 524-541.
70. Elena SF, Agudelo-Romero P, Lalic J, (2009) The evolution of viruses in multi-host fitness landscapes. Open Virol J 3: 1-6.
71. Kassen R, Bell G, (1998) Experimental evolution in Chlamydomonas. IV. Selection in environments that vary through time at different scales. Heredity 80: 732-741.
72. Elena SF, Sanjuan R, (2003) Evolution. Climb every mountain? Science 302: 2074-2075.
73. Adams J, Hansche PE, (1974) Population studies in microorganisms. I. Evolution of diploidy in Saccharomyces cerevisiae. Genetics 76: 327-338.
74. Lang GI, Murray AW, Botstein D, (2009) The cost of gene expression underlies a fitness trade-off in yeast. Proceedings of the National Academy of Sciences 106: 5755-5760.
75. Treco DA, (1987) Preparation of Yeast DNA. In: Ausubel F, Brent R, Kingston R, Moore D, Seidman J, editors. Current Protocols in Molecular Biology New York John Wiley and Sons, Inc pp. 13.11.11-13.11.12.
76. Li H, Durbin R, (2009) Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25: 1754-1760.
77. Li H, Handsaker B, Wysoker A, Fennel T, Ruan J, et al. (2009) The Sequence alignment/map (SAM) format and SAMtools. Bioinformatics 25: 2078-2079.
78. Lunter G, Goodson M, (2010) Stampy: A statistical algorithm for sensitive and fast mapping of Illumina sequence reads. Genome Res doi:10.1101/gr.111120.110.
79. McKenna A, Hanna M, Banks E, Sivachenko A, Cibulskis K, et al. (2010) The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res 20: 1297-1303.
80. Depristo MA, Banks E, Poplin R, Garimella KV, Maguire JR, et al. (2011) A framework for variation discovery and genotyping using next-generation DNA sequencing data. Nat Genet in press.
81. Venkatraman ES, Olshen AB, (2007) A faster circular binary segmentation algorithm for the analysis of array CGH data. Bioinformatics 23: 657-663.