Ancient Evolutionary Trade-Offs between Yeast Ploidy States

PLoS Genetics

Volumn 9, Issue 3, 2013, Pages

  Zörgö, Enikö ^a,b   Chwialkowska, Karolina ^b   Gjuvsland, Arne B ^a   Garré, Elena ^b   Sunnerhagen, Per ^b   Liti, Gianni ^c   Blomberg, Anders ^b   Omholt, Stig W ^d   Warringer, Jonas ^a,b  

^a NORWEGIAN UNIVERSITY OF LIFE SCIENCES   (Norway)

^b UNIVERSITY OF GOTHENBURG   (Sweden)

^c UNIVERSITY OF NICE SOPHIA ANTIPOLIS   (France)

^d NORWEGIAN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Norway)

Author keywords

[No Author keywords available]

Indexed keywords

CARRIER PROTEIN; ENA PROTEIN; FUNGAL PROTEIN; LITHIUM ION; NHA1 PROTEIN; TOXIN; UNCLASSIFIED DRUG;

ARTICLE; CELL SIZE; CONTROLLED STUDY; DIPLOIDY; ENVIRONMENTAL FACTOR; GENE LOCUS; GENE MAPPING; GENE MUTATION; GENETIC SELECTION; GENETIC VARIABILITY; GENOTYPE; HAPLOIDY; MATING; MITOSIS; MOLECULAR EVOLUTION; MOLECULAR GENETICS; NONHUMAN; NUTRIENT; NUTRIENT RESTRICTION; PHENOTYPE; PLOIDY; REPRODUCTION; SACCHAROMYCES; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES PARADOXUS;

BIOLOGICAL EVOLUTION; CELL SIZE; CHROMOSOMES; COPPER; DIPLOIDY; ECOLOGY; EVOLUTION, MOLECULAR; GENE-ENVIRONMENT INTERACTION; GENES, MATING TYPE, FUNGAL; GENOTYPE; HAPLOIDY; LITHIUM; REPRODUCTION; SACCHAROMYCES CEREVISIAE;

ENA; EUKARYOTA; SACCHAROMYCES PARADOXUS;

EID: 84875992955     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1003388     Document Type: Article

References (69)

1. Blanc G, Wolfe KH, (2004) Widespread paleopolyploidy in model plant species inferred from age distributions of duplicate genes. Plant Cell 16: 1667-1678.
2. Bowers JE, Chapman BA, Rong J, Paterson AH, (2003) Unravelling angiosperm genome evolution by phylogenetic analysis of chromosomal duplication events. Nature 422: 433-438.
3. Dehal P, Boore JL, (2005) Two rounds of whole genome duplication in the ancestral vertebrate. PLoS Biol 3: e314 doi:10.1371/journal.pbio.0030314.
4. Freeling M, Thomas BC, (2006) Gene-balanced duplications, like tetraploidy, provide predictable drive to increase morphological complexity. Genome Res 16: 805-814.
5. Kellis M, Birren BW, Lander ES, (2004) Proof and evolutionary analysis of ancient genome duplication in the yeast Saccharomyces cerevisiae. Nature 428: 617-624.
6. Haldane JBS (1932) The causes of evolution. Princeton (NJ): Reprinted in 1990 by Princeton University Press.
7. Gregory TR (2004) The evolution of the genome. San Diego (CA): Elsevier.
8. Zhimulev IF, Belyaeva ES, Semeshin VF, Koryakov DE, Demakov SA, et al. (2004) Polytene chromosomes: 70 years of genetic research. Int Rev Cytol 241: 203-275.
9. Davoli T, de Lange T, (2011) The causes and consequences of polyploidy in normal development and cancer. Annu Rev Cell Dev Biol 27: 585-610.
10. Gerstein AC, Otto SP, (2009) Ploidy and the causes of genomic evolution. J Hered 100: 571-581.
11. Haldane JBS, (1937) The Effect of Variation of Fitness. The American Naturalist 71: 337-349.
12. Anderson JB, Sirjusingh C, Ricker N, (2004) Haploidy, diploidy and evolution of antifungal drug resistance in Saccharomyces cerevisiae. Genetics 168: 1915-1923.
13. Orr HA, Otto SP, (1994) Does diploidy increase the rate of adaptation? Genetics 136: 1475-1480.
14. Zeyl C, Vanderford T, Carter M, (2003) An evolutionary advantage of haploidy in large yeast populations. Science 299: 555-558.
15. Weiss RL, Kukora JR, Adams J, (1975) The relationship between enzyme activity, cell geometry, and fitness in Saccharomyces cerevisiae. Proc Natl Acad Sci U S A 72: 794-798.
16. Adams J, Hansche PE, (1974) Population studies in microorganisms. I. Evolution of diploidy in Saccharomyces cerevisiae. Genetics 76: 327-338.
17. Lewis WM, (1985) Nutrient scarcity as an evolutionary cause of haploidy. The American Naturalist 125: 692-701.
18. Mable BK, (2001) Ploidy evolution in the yeast Saccharomyces cerevisiae: a test of the nutrient limitation hypothesis. Journal of Evolutionary Biology 14: 157-170.
19. Neiman AM, (2011) Sporulation in the budding yeast Saccharomyces cerevisiae. Genetics 189: 737-765.
20. Dujon B, (2010) Yeast evolutionary genomics. Nat Rev Genet 11: 512-524.
21. Liti G, Carter DM, Moses AM, Warringer J, Parts L, et al. (2009) Population genomics of domestic and wild yeasts. Nature 458: 337-341.
22. Warringer J, Zorgo E, Cubillos FA, Zia A, Gjuvsland A, et al. (2011) Trait variation in yeast is defined by population history. PLoS Genet 7: e1002111 doi:10.1371/journal.pgen.1002111.
23. Ruderfer DM, Pratt SC, Seidel HS, Kruglyak L, (2006) Population genomic analysis of outcrossing and recombination in yeast. Nat Genet 38: 1077-1081.
24. Tsai IJ, Bensasson D, Burt A, Koufopanou V, (2008) Population genomics of the wild yeast Saccharomyces paradoxus: Quantifying the life cycle. Proc Natl Acad Sci U S A 105: 4957-4962.
25. Mable BK, Otto SP, (2001) Masking and purging mutations following EMS treatment in haploid, diploid and tetraploid yeast (Saccharomyces cerevisiae). Genet Res 77: 9-26.
26. Arino J, Ramos J, Sychrova H, (2010) Alkali metal cation transport and homeostasis in yeasts. Microbiol Mol Biol Rev 74: 95-120.
27. Galitski T, Saldanha AJ, Styles CA, Lander ES, Fink GR, (1999) Ploidy regulation of gene expression. Science 285: 251-254.
28. de Godoy LM, Olsen JV, Cox J, Nielsen ML, Hubner NC, et al. (2008) Comprehensive mass-spectrometry-based proteome quantification of haploid versus diploid yeast. Nature 455: 1251-1254.
29. Jorgensen P, Nishikawa JL, Breitkreutz BJ, Tyers M, (2002) Systematic identification of pathways that couple cell growth and division in yeast. Science 297: 395-400.
30. Nelson MA, (1996) Mating systems in ascomycetes: a romp in the sac. Trends Genet 12: 69-74.
31. Xiao L, Grove A, (2009) Coordination of Ribosomal Protein and Ribosomal RNA Gene Expression in Response to TOR Signaling. Curr Genomics 10: 198-205.
32. Jung PP, Fritsch ES, Blugeon C, Souciet JL, Potier S, et al. (2011) Ploidy influences cellular responses to gross chromosomal rearrangements in Saccharomyces cerevisiae. BMC Genomics 12: 331.
33. Knop M, (2006) Evolution of the hemiascomycete yeasts: on life styles and the importance of inbreeding. Bioessays 28: 696-708.
34. Gerstein AC, Chun HJ, Grant A, Otto SP, (2006) Genomic convergence toward diploidy in Saccharomyces cerevisiae. PLoS Genet 2: e145 doi:10.1371/journal.pgen.0020145.
35. 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.
36. 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. Proc Natl Acad Sci U S A 105: 9272-9277.
37. Zorgo E, Gjuvsland A, Cubillos FA, Louis EJ, Liti G, et al. (2012) Life history shapes trait heredity by accumulation of loss-of-function alleles in yeast. Mol Biol Evol 29: 1781-1789.
38. Hillenmeyer ME, Fung E, Wildenhain J, Pierce SE, Hoon S, et al. (2008) The Chemical Genomic Portrait of Yeast: Uncovering a Phenotype for All Genes. Science 320: 362-365.
39. Coluccio AE, Rodriguez RK, Kernan MJ, Neiman AM, (2008) The yeast spore wall enables spores to survive passage through the digestive tract of Drosophila. PLoS ONE 3: e2873 doi:10.1371/journal.pone.0002873.
40. Ezov TK, Boger-Nadjar E, Frenkel Z, Katsperovski I, Kemeny S, et al. (2006) Molecular-genetic biodiversity in a natural population of the yeast Saccharomyces cerevisiae from "Evolution Canyon": microsatellite polymorphism, ploidy and controversial sexual status. Genetics 174: 1455-1468.
41. Ohnishi G, Endo K, Doi A, Fujita A, Daigaku Y, et al. (2004) Spontaneous mutagenesis in haploid and diploid Saccharomyces cerevisiae. Biochem Biophys Res Commun 325: 928-933.
42. Dickinson WJ, (2008) Synergistic fitness interactions and a high frequency of beneficial changes among mutations accumulated under relaxed selection in Saccharomyces cerevisiae. Genetics 178: 1571-1578.
43. Deutschbauer AM, Jaramillo DF, Proctor M, Kumm J, Hillenmeyer ME, et al. (2005) Mechanisms of haploinsufficiency revealed by genome-wide profiling in yeast. Genetics 169: 1915-1925.
44. Korona R, (1999) Unpredictable fitness transitions between haploid and diploid strains of the genetically loaded yeast Saccharomyces cerevisiae. Genetics 151: 77-85.
45. Westmoreland TJ, Wickramasekara SM, Guo AY, Selim AL, Winsor TS, et al. (2009) Comparative genome-wide screening identifies a conserved doxorubicin repair network that is diploid specific in Saccharomyces cerevisiae. PLoS ONE 4: e5830 doi:10.1371/journal.pone.0005830.
46. Wilson DM 3rd, Sofinowski TM, McNeill DR, (2003) Repair mechanisms for oxidative DNA damage. Front Biosci 8: d963-981.
47. Li XC, Tye BK, (2011) Ploidy dictates repair pathway choice under DNA replication stress. Genetics 187: 1031-1040.
48. Storchova Z, Breneman A, Cande J, Dunn J, Burbank K, et al. (2006) Genome-wide genetic analysis of polyploidy in yeast. Nature 443: 541-547.
49. Haber JE, (2012) Mating-type genes and MAT switching in Saccharomyces cerevisiae. Genetics 191: 33-64.
50. Chant J, (1996) Generation of cell polarity in yeast. Curr Opin Cell Biol 8: 557-565.
51. Ke N, Irwin PA, Voytas DF, (1997) The pheromone response pathway activates transcription of Ty5 retrotransposons located within silent chromatin of Saccharomyces cerevisiae. Embo J 16: 6272-6280.
52. Frank-Vaillant M, Marcand S, (2001) NHEJ regulation by mating type is exercised through a novel protein, Lif2p, essential to the ligase IV pathway. Genes Dev 15: 3005-3012.
53. Kegel A, Sjostrand JO, Astrom SU, (2001) Nej1p, a cell type-specific regulator of nonhomologous end joining in yeast. Curr Biol 11: 1611-1617.
54. Gerstein AC, (2013) Mutational effects depend on ploidy level: all else is not equal. Biol Lett 9: 20120614.
55. Wieland J, Nitsche AM, Strayle J, Steiner H, Rudolph HK, (1995) The PMR2 gene cluster encodes functionally distinct isoforms of a putative Na+ pump in the yeast plasma membrane. Embo J 14: 3870-3882.
56. Chan YH, Marshall WF, (2010) Scaling properties of cell and organelle size. Organogenesis 6: 88-96.
57. Jorgensen P, Edgington NP, Schneider BL, Rupes I, Tyers M, et al. (2007) The size of the nucleus increases as yeast cells grow. Mol Biol Cell 18: 3523-3532.
58. McLaughlan JM, Liti G, Sharp S, Maslowska A, Louis EJ, (2012) Apparent Ploidy Effects on Silencing Are Post-Transcriptional at HML and Telomeres in Saccharomyces cerevisiae. PLoS ONE 7: e39044 doi:10.1371/journal.pone.0039044.
59. Ehrenreich IM, Bloom J, Torabi N, Wang X, Jia Y, et al. (2012) Genetic architecture of highly complex chemical resistance traits across four yeast strains. PLoS Genet 8: e1002570 doi:10.1371/journal.pgen.1002570.
60. Parts L, Cubillos FA, Warringer J, Jain K, Salinas F, et al. (2011) Revealing the genetic structure of a trait by sequencing a population under selection. Genome Res 21: 1131-1138.
61. Cubillos FA, Louis EJ, Liti G, (2009) Generation of a large set of genetically tractable haploid and diploid Saccharomyces strains. FEMS Yeast Res 9: 1217-1225.
62. Warringer J, Anevski D, Liu B, Blomberg A, (2008) Chemogenetic fingerprinting by analysis of cellular growth dynamics. BMC Chem Biol 8: 3.
63. Warringer J, Blomberg A, (2003) Automated screening in environmental arrays allows analysis of quantitative phenotypic profiles in Saccharomyces cerevisiae. Yeast 20: 53-67.
64. Benjamini Y, Hochberg Y, (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society 57: 289-300.
65. Eisen MB, Spellman PT, Brown PO, Botstein D, (1998) Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci U S A 95: 14863-14868.
66. Liti G, Louis EJ, (2003) NEJ1 prevents NHEJ-dependent telomere fusions in yeast without telomerase. Mol Cell 11: 1373-1378.
67. Springer M, Weissman JS, Kirschner MW, (2010) A general lack of compensation for gene dosage in yeast. Mol Syst Biol 6: 368.
68. Haase SB, Reed SI, (2002) Improved flow cytometric analysis of the budding yeast cell cycle. Cell Cycle 1: 132-136.
69. Lopes CA, Barrio E, Querol A, (2010) Natural hybrids of S. cerevisiae x S. kudriavzevii share alleles with European wild populations of Saccharomyces kudriavzevii. FEMS Yeast Res 10: 412-421.