The Dynamics of Diverse Segmental Amplifications in Populations of Saccharomyces cerevisiae Adapting to Strong Selection

G3: Genes, Genomes, Genetics

Volumn 4, Issue 3, 2014, Pages 399-409

  Payen, Celia ^a   Di Rienzi, Sara C ^a,b   Ong, Giang T ^a   Pogachar, Jamie L ^a   Sanchez, Joseph C ^a   Sunshine, Anna B ^a   Raghuraman, M K ^a   Brewer, Bonita J ^a   Dunham, Maitreya J ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

^b Department of Obstetrics Gynecology   (United States)

Author keywords

Amplification; Clonal; Evolution; Evolutionary; Experimental; Gene; Genomics; Interference; Inverted; Sequencing; Triplication; Whole genome

Indexed keywords

CATION; SULFATE;

ARTICLE; CLONE; COMPARATIVE GENOMIC HYBRIDIZATION; CULTURE MEDIUM; DYNAMICS; EVOLUTIONARY ADAPTATION; GEL ELECTROPHORESIS; GENE AMPLIFICATION; GENE MUTATION; GENE SEQUENCE; MICROBIAL POPULATION DYNAMICS; NONHUMAN; SACCHAROMYCES CEREVISIAE; SUL1 GENE; YEAST;

CLONAL INTERFERENCE; EVOLUTIONARY GENOMICS; EXPERIMENTAL EVOLUTION; GENE AMPLIFICATION; INVERTED TRIPLICATION; WHOLE GENOME SEQUENCING;

ADAPTATION, BIOLOGICAL; ANION TRANSPORT PROTEINS; DNA, FUNGAL; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; KINETICS; MUTATION; NUCLEIC ACID CONFORMATION; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SELECTION, GENETIC; SEQUENCE ANALYSIS, DNA;

EID: 84897008356     PISSN: None     EISSN: 21601836     Source Type: Journal    
DOI: 10.1534/g3.113.009365     Document Type: Article

References (54)

1. Adamo G.M., Lotti M., Tam M.J.ás, and S. Brocca, 2012 Amplification of the CUP1 gene is associated with evolution of copper tolerance in Saccharomyces cerevisiae. Microbiology 158: 2325-2335.
2. Andersson D.I., Slechta E.S., and J. R. Roth, 1998 Evidence that gene amplification underlies adaptive mutability of the bacterial lac operon. Science 282: 1133-1135.
3. Araya C.L., Payen C., Dunham M.J., and S. Fields, 2010 Whole-genome sequencing of a laboratory-evolved yeast strain. BMC Genomics 11: 88.
4. Barrick J.E., Yu D.S., Yoon S.H., Jeong H., Oh T.K. et al., 2009 Genome evolution and adaptation in a long-term experiment with Escherichia coli. Nature 461: 1243-1247.
5. Blount Z.D., Barrick J.E., Davidson C.J., and R. E. Lenski, 2012 Genomic analysis of a key innovation in an experimental Escherichia coli population. Nature 489: 513-518.
6. Brewer B.J., Payen C., Raghuraman M.K., and M. J. Dunham, 2011 Origindependent inverted-repeat amplification: a replication-based model for generating palindromic amplicons. PLoS Genet. 7: e1002016.
7. Brown C.J., Todd K.M., and R. F. Rosenzweig, 1998 Multiple duplications of yeast hexose transport genes in response to selection in a glucoselimited environment. Mol. Biol. Evol. 15: 931-942.
8. Burke M.K., 2012 How does adaptation sweep through the genome? Insights from long-term selection experiments. Proc. Roy. Soc. B. 279: 5029-5038.
9. Cakar Z.P., Seker U.O., Tamerler C., M. Sonderegger, and U. Sauer, 2005 Evolutionary engineering of multiple-stress resistant Saccharomyces cerevisiae. FEMS Yeast Res. 5: 569-578.
10. Cherest, H., Davidian J.C., Thomas D., V. Benes, W. Ansorge et al., 1997 Molecular characterization of two high affinity sulfate transporters in Saccharomyces cerevisiae. Genetics 145: 627-635.
11. Chou H.H., and C. J. Marx, 2012 Optimization of gene expression through divergent mutational paths. Cell Rep 1: 133-140.
12. Desai M.M., Fisher D.S., and A.W. Murray, 2007 The speed of evolution and maintenance of variation in asexual populations. Curr. Biol. 17: 385-394.
13. de Visser, G J.A.M., Zeyl C.W., Gerrish P.J., Blanchard J.L., and R. E. Lenski, 1999 Diminishing returns from mutation supply rate in asexual populations. Science 283: 404-406.
14. Di Rienzi S.C., Lancaster K.C., Lindstrom R., L. Rolczynski, Raghuraman M.K. et al., 2011 Genetic, genomic, and molecular tools for studying the protoploid yeast, L. waltii. Yeast 28: 137-151.
15. Dunham M.J., Badrane H., T. Ferea, Adams J., Brown P.O. et al., 2002 Characteristic genome rearrangements in experimental evolution of Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 99: 16144-16149.
16. Gerrish P.J., and R. E. Lenski, 1998 The fate of competing beneficial mutations in an asexual population. Genetica 102-103: 127-144.
17. Giaever, G., Chu A.M., Ni L., C. Connelly, L. Riles et al., 2002 Functional profiling of the Saccharomyces cerevisiae genome. Nature 418: 387-391.
18. Gresham, D., Desai M.M., Tucker C.M., Jenq H.T., Pai D.A. et al., 2008 The repertoire and dynamics of evolutionary adaptations to controlled nutrient-limited environments in yeast. PLoS Genet. 4: e1000303.
19. Gresham, D., Usaite R., Germann S.M., Lisby M., D. Botstein et al., 2010 Adaptation to diverse nitrogen-limited environments by deletion or extrachromosomal element formation of the GAP1 locus. Proc. Natl. Acad. Sci. USA 107: 18551-18556.
20. Guimaraes P.M., Teixeira J.A., and L. Domingues, 2008 Fermentation of high concentrations of lactose to ethanol by engineered flocculent Saccharomyces cerevisiae. Biotechnol. Lett. 30: 1953-1958.
21. Hach, F., Hormozdiari F., C. Alkan, Birol I., Eichler E.E. et al., 2010 mrsFAST: a cache-oblivious algorithm for short-read mapping. Nat. Methods 7: 576-577.
22. Herron M.D., and M. Doebeli, 2013 Parallel evolutionary dynamics of adaptive diversification in Escherichia coli. PLoS Biol. 11: e1001490.
23. Ho C.H., Magtanong L., Barker S.L., Gresham D., S. Nishimura et al., 2009 A molecular barcoded yeast ORF library enables mode-of-action analysis of bioactive compounds. Nat. Biotechnol. 27: 369-377.
24. Hoffman C.S., and F. Winston, 1987 A ten-minute DNA preparation from yeast efficiently releases autonomous plasmids for transformation of Escherichia coli. Gene 57: 267-272.
25. Huberman J.A., Spotila L.D., Nawotka K.A., el S.M.-Assouli, and L. R. Davis, 1987 The in vivo replication origin of the yeast 2mm plasmid. Cell 51: 473-481.
26. Kao K.C., and G. Sherlock, 2008 Molecular characterization of clonal interference during adaptive evolution in asexual populations of Saccharomyces cerevisiae. Nat. Genet. 40: 1499-1504.
27. Karakoc, E., Alkan C., O B.J.'Roak, Dennis M.Y., L. Vives et al., 2011 Detection of structural variants and indels within exome data. Nat. Methods 9: 176-178.
28. Kohler, A., Schneider M., Cabal G.G., Nehrbass U., and E. Hurt, 2008 Yeast Ataxin-7 links histone deubiquitination with gene gating and mRNA export. Nat. Cell Biol. 10: 707-715.
29. Koszul, R., Caburet S., B. Dujon, and G. Fischer, 2004 Eucaryotic genome evolution through the spontaneous duplication of large chromosomal segments. EMBO J. 23: 234-243.
30. Koszul, R., Dujon B., and G. Fischer, 2006 Stability of large segmental duplications in the yeast genome. Genetics 172: 2211-2222.
31. Kugelberg, E., Kofoid E., Andersson D.I., Lu Y., J. Mellor et al., 2010 The tandem inversion duplication in Salmonella enterica: selection drives unstable precursors to final mutation types. Genetics 185: 65-80.
32. Lang G.I., Rice D.P., Hickman M.J., Sodergren E., Weinstock G.M. et al., 2013 Pervasive genetic hitchhiking and clonal interference in forty evolving yeast populations. Nature 500: 571-574.
33. Lee M.C., and C. J. Marx, 2012 Repeated, selection-driven genome reduction of accessory genes in experimental populations. PLoS Genet. 8: e1002651.
34. Lee M.C., and C. J. Marx, 2013 Synchronous waves of failed soft sweeps in the laboratory: remarkably rampant clonal interference of alleles at a single locus. Genetics 193: 943-952.
35. Li, H., and R. Durbin, 2009 Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25: 1754-1760.
36. Li, H., Handsaker B., A. Wysoker, Fennell T., J. Ruan et al., 2009 The Sequence Alignment/Map format and SAMtools. Bioinformatics 25: 2078-2079.
37. Miller A.W., Befort C., Kerr E.O., and M. J. Dunham, 2013 Design and use of multiplexed chemostat arrays. J. Vis. Exp. Feb 23: e50262.
38. Miller C.R., Joyce P., and H. A. Wichman, 2011 Mutational effects and population dynamics during viral adaptation challenge current models. Genetics 187: 185-202.
39. Notley-McRobb, L., and T. Ferenci, 2000 Experimental analysis of molecular events during mutational periodic selections in bacterial evolution. Genetics 156: 1493-1501.
40. Pashkova, N., Gakhar L., Winistorfer S.C., Sunshine A.B., M. Rich et al., 2013 The yeast Alix homolog Bro1 functions as a ubiquitin receptor for protein sorting into multivesicular endosomes. Dev. Cell. 25: 5202533.
41. Payen, C., Koszul R., B. Dujon, and G. Fischer, 2008 Segmental duplications arise from Pol32-dependent repair of broken forks through two alternative replication-based mechanisms. PLoS Genet. 4: e1000175.
42. Pryde F.E., and E. J. Louis, 1997 Saccharomyces cerevisiae telomeres. A review. Biochemistry (Mosc) 62: 1232-1241.
43. Robinson J.T., Thorvaldsdottir H., W. Winckler, Guttman M., Lander E.S. et al., 2011 Integrative genomics viewer. Nat. Biotechnol. 29: 24-26.
44. Sonti R.V., and J. R. Roth, 1989 Role of gene duplications in the adaptation of Salmonella typhimurium to growth on limiting carbon sources. Genetics 123: 19-28.
45. Stoebel D.M., Hokamp K., Last M.S., and C. J. Dorman, 2009 Compensatory evolution of gene regulation in response to stress by Escherichia coli lacking RpoS. PLoS Genet. 5: e1000671.
46. Tanaka, H., Bergstrom D.A., Yao M.C., and S. J. Tapscott, 2005 Widespread and nonrandom distribution of DNA palindromes in cancer cells provides a structural platform for subsequent gene amplification. Nat. Genet. 37: 320-327.
47. Tang Y.C., and A. Amon, 2013 Gene copy-number alterations: a costbenefit analysis. Cell 152: 394-405.
48. Tenaillon, O., A. Rodriguez-Verdugo, Gaut R.L., McDonald P., Bennett A.F. et al., 2012 The molecular diversity of adaptive convergence. Science 335: 457-461.
49. van Maris A.J., Winkler A.A., Kuyper M., de W.T. Laat, van J.P. Dijken et al., 2007 Development of efficient xylose fermentation in Saccharomyces cerevisiae: xylose isomerase as a key component. Adv. Biochem. Eng. Biotechnol. 108: 179-204.
50. Wahl L.M., and D. C. Krakauer, 2000 Models of experimental evolution: the role of genetic chance and selective necessity. Genetics 156: 1437- 1448.
51. Woods, R., Schneider D., Winkworth C.L., Riley M.A., and R. E. Lenski, 2006 Tests of parallel molecular evolution in a long-term experiment with Escherichia coli. Proc. Natl. Acad. Sci. USA 103: 9107-9112.
52. Yona A.H., Manor Y.S., Herbst R.H., Romano G.H., A. Mitchell et al., 2012 Chromosomal duplication is a transient evolutionary solution to stress. Proc. Natl. Acad. Sci. USA 109: 21010-21015.
53. Zhang, E., and T. Ferenci, 1999 OmpF changes and the complexity of Escherichia coli adaptation to prolonged lactose limitation. FEMS Microbiol. Lett. 176: 395-401.
54. Zhong, S., Khodursky A., Dykhuizen D.E., and A. M. Dean, 2004 Evolutionary genomics of ecological specialization. Proc. Natl. Acad. Sci. USA 101: 11719-11724.