Molecular Specificity, Convergence and Constraint Shape Adaptive Evolution in Nutrient-Poor Environments

PLoS Genetics

Volumn 10, Issue 1, 2014, Pages

  Hong, Jungeui ^a   Gresham, David ^a  

^a NEW YORK UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTATION, BIOLOGICAL; ALLELES; DIPLOIDY; DIRECTED MOLECULAR EVOLUTION; GENE DOSAGE; GENETIC FITNESS; GENOTYPE; MEMBRANE TRANSPORT PROTEINS; NITROGEN; POINT MUTATION; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; TRANSCRIPTION FACTORS;

EID: 84893817979     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1004041     Document Type: Article

References (74)

1. Dean AM, Thornton JW, (2007) Mechanistic approaches to the study of evolution: the functional synthesis. Nature Reviews Genetics 8: 675-688 doi:10.1038/nrg2160.
2. Thomson JM, Gaucher EA, Burgan MF, De Kee DW, Li T, et al. (2005) Resurrecting ancestral alcohol dehydrogenases from yeast. Nature genetics 37: 630-635 doi:10.1038/ng1553.
3. Bridgham JT, Ortlund EA, Thornton JW, (2009) An epistatic ratchet constrains the direction of glucocorticoid receptor evolution. Nature 461: 515-519 doi:10.1038/nature08249.
4. Elena SF, Lenski RE, (2003) Evolution experiments with microorganisms: the dynamics and genetic bases of adaptation. Nature Reviews Genetics 4: 457-469 doi:10.1038/nrg1088.
5. Novick A, Szilard L, (1950) Description of the chemostat. Science 112: 715-716.
6. Monod J, (1950) La technique de culture continue. Théorie et applications. Ann Inst Pasteur 79: 390-410.
7. Lenski RE, Travisano M, (1994) Dynamics of adaptation and diversification: a 10,000-generation experiment with bacterial populations. Proceedings of the National Academy of Sciences 91: 6808-6814.
8. Lang GI, Botstein D, Desai MM, (2011) Genetic variation and the fate of beneficial mutations in asexual populations. Genetics 188: 647-661 doi:10.1534/genetics.111.128942.
9. Gresham D, Desai MM, Tucker CM, Jenq HT, 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.t005.
10. Gresham D, Usaite R, Germann SM, Lisby M, Botstein D, et al. (2010) Adaptation to diverse nitrogen-limited environments by deletion or extrachromosomal element formation of the GAP1 locus. Proceedings of the National Academy of Sciences 107: 18551-18556 doi:10.1073/pnas.1014023107.
11. Ferenci T, (2007) Bacterial physiology, regulation and mutational adaptation in a chemostat environment. Advances in microbial physiology 53: 169-315 doi:10.1016/S0065-2911(07)53003-1.
12. Kao KC, Sherlock G, (2008) Molecular characterization of clonal interference during adaptive evolution in asexual populations of Saccharomyces cerevisiae. Nature genetics 40: 1499-1504 doi:10.1038/ng.280.
13. 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.
14. Wenger JW, Piotrowski J, Nagarajan S, Chiotti K, Sherlock G, et al. (2011) Hunger artists: yeast adapted to carbon limitation show trade-offs under carbon sufficiency. PLoS Genet 7: e1002202 doi:10.1371/journal.pgen.1002202.
15. Magasanik B, Kaiser CA, (2002) Nitrogen regulation in Saccharomyces cerevisiae. Gene 290: 1-18 doi:10.1016/S0378-1119(02)00558-9.
16. Cooper TG, (2002) Transmitting the signal of excess nitrogen in Saccharomyces cerevisiae from the Tor proteins to the GATA factors: connecting the dots. FEMS Microbiology Reviews 26: 223-238 doi:10.1111/j.1574-6976.2002.tb00612.x.
17. Brown CJ, Todd KM, Rosenzweig RF, (1998) Multiple duplications of yeast hexose transport genes in response to selection in a glucose-limited environment. Mol Biol Evol 15: 931-942.
18. 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 of the United States of America 99: 16144-16149 doi:10.1073/pnas.242624799.
19. Zhong S, Khodursky A, Dykhuizen DE, Dean AM, (2004) Evolutionary genomics of ecological specialization. Proceedings of the National Academy of Sciences of the United States of America 101: 11719 doi:10.1073/pnas.0404397101.
20. Zhang H, Zeidler AFB, Song W, Puccia CM, Malc E, et al. (2013) Gene copy-number variation in haploid and diploid strains of the yeast Saccharomyces cerevisiae. Genetics 193: 785-801 doi:10.1534/genetics.112.146522.
21. Dorsey M, Peterson C, Bray K, Paquin CE, (1992) Spontaneous amplification of the ADH4 gene in Saccharomyces cerevisiae. Genetics 132: 943-950.
22. Rancati G, Pavelka N, Fleharty B, Noll A, Trimble R, et al. (2008) Aneuploidy underlies rapid adaptive evolution of yeast cells deprived of a conserved cytokinesis motor. Cell 135: 879-893 doi:10.1016/j.cell.2008.09.039.
23. Gerstein AC, Otto SP, (2011) Cryptic fitness advantage: diploids invade haploid populations despite lacking any apparent advantage as measured by standard fitness assays. PloS one 6: e26599 doi:10.1371/journal.pone.0026599.
24. Torres EM, Sokolsky T, Tucker CM, Chan LY, Boselli M, et al. (2007) Effects of aneuploidy on cellular physiology and cell division in haploid yeast. Science 317: 916-924 doi:10.1126/science.1142210.
25. Lynch M, Sung W, Morris K, Coffey N, Landry CR, et al. (2008) A genome-wide view of the spectrum of spontaneous mutations in yeast. Proceedings of the National Academy of Sciences of the United States of America 105: 9272-9277 doi:10.1073/pnas.0803466105.
26. Araya CL, Payen C, Dunham MJ, Fields S, (2010) Whole-genome sequencing of a laboratory-evolved yeast strain. BMC Genomics 11: 88 doi:10.1186/1471-2164-11-88.
27. Dettman JR, Rodrigue N, Melnyk AH, Wong A, Bailey SF, et al. (2012) Evolutionary insight from whole-genome sequencing of experimentally evolved microbes. Mol Ecol 21: 2058-2077 doi:10.1111/j.1365-294X.2012.05484.x.
28. Notley-McRobb L, Seeto S, Ferenci T, (2003) The influence of cellular physiology on the initiation of mutational pathways in Escherichia coli populations. Proc Biol Sci 270: 843-848 doi:10.1098/rspb.2002.2295.
29. Herron MD, Doebeli M, (2013) Parallel Evolutionary Dynamics of Adaptive Diversification in Escherichia coli. PLoS Biol 11: e1001490 doi:10.1371/journal.pbio.1001490.
30. Maharjan R, Seeto S, Notley-McRobb L, Ferenci T, (2006) Clonal adaptive radiation in a constant environment. Science 313: 514-517 doi:10.1126/science.1129865.
31. Maharjan RP, Ferenci T, Reeves PR, Li Y, Liu B, et al. (2012) The multiplicity of divergence mechanisms in a single evolving population. Genome Biology 13: R41 doi:10.1186/gb-2012-13-6-r41.
32. Jin N, Chow CY, Liu L, Zolov SN, Bronson R, et al. (2008) VAC14 nucleates a protein complex essential for the acute interconversion of PI3P and PI(3,5)P(2) in yeast and mouse. The EMBO Journal 27: 3221-3234 doi:10.1038/emboj.2008.248.
33. Notley-McRobb L, King T, Ferenci T, (2002) rpoS mutations and loss of general stress resistance in Escherichia coli populations as a consequence of conflict between competing stress responses. Journal of bacteriology 184: 806-811 doi:10.1128/JB.184.3.806-811.2002.
34. Scherens B, Feller A, Vierendeels F, Messenguy F, Dubois E, (2006) Identification of direct and indirect targets of the Gln3 and Gat1 activators by transcriptional profiling in response to nitrogen availability in the short and long term. FEMS Yeast Research 6: 777-791 doi:10.1111/j.1567-1364.2006.00060.x.
35. Roberg KJ, Bickel S, Rowley N, Kaiser CA, (1997) Control of amino acid permease sorting in the late secretory pathway of Saccharomyces cerevisiae by SEC13, LST4, LST7 and LST8. Genetics 147: 1569-1584.
36. Costanzo M, Baryshnikova A, Bellay J, Kim Y, Spear ED, et al. (2010) The Genetic Landscape of a Cell. Science 327: 425-431 doi:10.1126/science.1180823.
37. Paquin C, Adams J, (1983) Frequency of fixation of adaptive mutations is higher in evolving diploid than haploid yeast populations. Nature 302: 495-500.
38. Paquin CE, Adams J, (1983) Relative fitness can decrease in evolving asexual populations of S. cerevisiae. Nature 306: 368-370.
39. 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 doi:10.1073/pnas.96.17.9721.
40. 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 doi:10.1126/science.1123726.
41. Kubitschek HE, (1970) Introduction to research with continuous cultures. Prentice Hall pp. 195.
42. Rudge SA, Anderson DM, Emr SD, (2004) Vacuole size control: regulation of PtdIns(3,5)P2 levels by the vacuole-associated Vac14-Fig4 complex, a PtdIns(3,5)P2-specific phosphatase. Molecular Biology of the Cell 15: 24-36 doi:10.1091/mbc.E03-05-0297.
43. Dove SK, McEwen RK, Mayes A, Hughes DC, Beggs JD, et al. (2002) Vac14 controls PtdIns (3, 5) P2 synthesis and Fab1-dependent protein trafficking to the multivesicular body. Curr Biol 12: 885-893 doi:10.1016/S0960-9822(02)00891-6.
44. Weisman LS, (2003) Yeast vacuole inheritance and dynamics. Annu Rev Genet 37: 435-460 doi:10.1146/annurev.genet.37.050203.103207.
45. Li SC, Kane PM, (2009) The yeast lysosome-like vacuole: endpoint and crossroads. Biochim Biophys Acta 1793: 650-663 doi:10.1016/j.bbamcr.2008.08.003.
46. Cardenas ME, Cutler NS, Lorenz MC, Di Como CJ, Heitman J, (1999) The TOR signaling cascade regulates gene expression in response to nutrients. Genes Dev 13: 3271-3279 doi:10.1101/gad.13.24.3271.
47. Tamanoi F, (2011) Ras signaling in yeast. Genes Cancer 2: 210-215 doi:10.1177/1947601911407322.
48. Cameroni E, Hulo N, Roosen J, Winderickx J, De Virgilio C, (2004) The novel yeast PAS kinase Rim15 orchestrates G0-associated antioxidant defense mechanisms. Cell Cycle 3: 460-466 doi:10.4161/cc.3.4.791.
49. Swinnen E, Wanke V, Roosen J, Smets B, Dubouloz F, et al. (2006) Rim15 and the crossroads of nutrient signalling pathways in Saccharomyces cerevisiae. Cell Div 1: 3 doi:10.1186/1747-1028-1-3.
50. Ferenci T, (2003) What is driving the acquisition of mutS and rpoS polymorphisms in Escherichia coli? Trends Microbiol 11: 457-461 doi:10.1016/j.tim.2003.08.003.
51. Wang L, Spira B, Zhou Z, Feng L, Maharjan RP, et al. (2010) Divergence involving global regulatory gene mutations in an Escherichia coli population evolving under phosphate limitation. Genome Biol Evol 2: 478-487 doi:10.1093/gbe/evq035.
52. Dunn B, Paulish T, Stanbery A, Piotrowski J, Koniges G, et al. (2013) Recurrent Rearrangement during Adaptive Evolution in an Interspecific Yeast Hybrid Suggests a Model for Rapid Introgression. PLoS Genet 9: e1003366 doi:10.1371/journal.pgen.1003366.
53. Rubio-Texeira M, Kaiser CA, (2006) Amino acids regulate retrieval of the yeast general amino acid permease from the vacuolar targeting pathway. Molecular Biology of the Cell 17: 3031-3050 doi:10.1091/mbc.E05-07-0669.
54. Lee M-C, Marx CJ, (2013) Synchronous waves of failed soft sweeps in the laboratory: remarkably rampant clonal interference of alleles at a single locus. Genetics 193: 943-952 doi:10.1534/genetics.112.148502.
55. Gerke J, Lorenz K, Cohen B, (2009) Genetic interactions between transcription factors cause natural variation in yeast. Science 323: 498-501 doi:10.1126/science.1166426.
56. Steiner CC, Weber JN, Hoekstra HE, (2007) Adaptive variation in beach mice produced by two interacting pigmentation genes. PLoS Biol 5: e219 doi:10.1371/journal.pbio.0050219.g001.
57. Hittinger CT, Gonçalves P, Sampaio JP, Dover J, Johnston M, et al. (2010) Remarkably ancient balanced polymorphisms in a multi-locus gene network. Nature 464: 54-58 doi:10.1038/nature08791.
58. Gietz RD, Schiestl RH, (2007) High-efficiency yeast transformation using the LiAc/SS carrier DNA/PEG method. Nature protocols 2: 31-34 doi:10.1038/nprot.2007.13.
59. Brauer MJ, Huttenhower C, Airoldi EM, Rosenstein R, Matese JC, et al. (2008) Coordination of Growth Rate, Cell Cycle, Stress Response, and Metabolic Activity in Yeast. Molecular Biology of the Cell 19: 352-367 doi:10.1091/mbc.E07-08-0779.
60. Kahm M, Hasenbrink G, Lichtenberg-Fraté H, Ludwig J, Kschischo M, (2010) grofit: fitting biological growth curves with R. Journal of Statistical Software 33: 1-21.
61. Venkatraman ES, Olshen AB, (2007) A faster circular binary segmentation algorithm for the analysis of array CGH data. Bioinformatics 23: 657-663 doi:10.1093/bioinformatics/btl646.
62. Li H, Durbin R, (2010) Fast and accurate long-read alignment with Burrows-Wheeler transform. Bioinformatics 26: 589-595 doi:10.1093/bioinformatics/btp698.
63. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, et al. (2009) The Sequence Alignment/Map format and SAMtools. Bioinformatics 25: 2078-2079 doi:10.1093/bioinformatics/btp352.
64. Albers CA, Lunter G, MacArthur DG, McVean G, Ouwehand WH, et al. (2011) Dindel: accurate indel calls from short-read data. Genome Res 21: 961-973 doi:10.1101/gr.112326.110.
65. Wei Z, Wang W, Hu P, Lyon GJ, Hakonarson H, (2011) SNVer: a statistical tool for variant calling in analysis of pooled or individual next-generation sequencing data. Nucleic Acids Research 39: e132 doi:10.1093/nar/gkr599.
66. Andréasson C, Neve EPA, Ljungdahl PO, (2004) Four permeases import proline and the toxic proline analogue azetidine-2-carboxylate into yeast. Yeast 21: 193-199 doi:10.1002/yea.1052.
67. Schure EG, Riel NA, Verrips CT, (2000) The role of ammonia metabolism in nitrogen catabolite repression in Saccharomyces cerevisiae. FEMS Microbiology Reviews 24: 67-83 doi:10.1111/j.1574-6976.2000.tb00533.x.
68. Lõoke M, Kristjuhan K, Kristjuhan A, (2011) Extraction of genomic DNA from yeasts for PCR-based applications. BioTechniques 50: 325-328 doi:10.2144/000113672.
69. Ge B, Gurd S, Gaudin T, Dore C, Lepage P, et al. (2005) Survey of allelic expression using EST mining. Genome Res 15: 1584-1591 doi:10.1101/gr.4023805.
70. Julius D, Blair L, Brake A, Sprague G, Thorner J, (1983) Yeast alpha factor is processed from a larger precursor polypeptide: the essential role of a membrane-bound dipeptidyl aminopeptidase. Cell 32: 839-852.
71. Godard P, Urrestarazu A, Vissers S, Kontos K, Bontempi G, et al. (2007) Effect of 21 different nitrogen sources on global gene expression in the yeast Saccharomyces cerevisiae. Molecular and Cellular Biology 27: 3065-3086 doi:10.1128/MCB.01084-06.
72. Arnold K, Kiefer F, Kopp J, Battey JND, Podvinec M, et al. (2009) The Protein Model Portal. J Struct Funct Genomics 10: 1-8 doi:10.1007/s10969-008-9048-5.
73. Drotschmann K, (1999) Mutator phenotypes of yeast strains heterozygous for mutations in the MSH2 gene. Proceedings of the National Academy of Sciences 96: 2970-2975 doi:10.1073/pnas.96.6.2970.
74. Barrick JE, Lenski RE, (2009) Genome-wide mutational diversity in an evolving population of Escherichia coli. Cold Spring Harb Symp Quant Biol 74: 119-129 doi:10.1101/sqb.2009.74.018.