Ancient Evolutionary Trade-Offs between Yeast Ploidy States
The number of chromosome sets contained within the nucleus of eukaryotic organisms is a fundamental yet evolutionarily poorly characterized genetic variable of life. Here, we mapped the impact of ploidy on the mitotic fitness of baker's yeast and its never domesticated relative Saccharomyces paradoxus across wide swaths of their natural genotypic and phenotypic space. Surprisingly, environment-specific influences of ploidy on reproduction were found to be the rule rather than the exception. These ploidy–environment interactions were well conserved across the 2 billion generations separating the two species, suggesting that they are the products of strong selection. Previous hypotheses of generalizable advantages of haploidy or diploidy in ecological contexts imposing nutrient restriction, toxin exposure, and elevated mutational loads were rejected in favor of more fine-grained models of the interplay between ecology and ploidy. On a molecular level, cell size and mating type locus composition had equal, but limited, explanatory power, each explaining 12.5%–17% of ploidy–environment interactions. The mechanism of the cell size–based superior reproductive efficiency of haploids during Li+ exposure was traced to the Li+ exporter ENA. Removal of the Ena transporters, forcing dependence on the Nha1 extrusion system, completely altered the effects of ploidy on Li+ tolerance and evoked a strong diploid superiority, demonstrating how genetic variation at a single locus can completely reverse the relative merits of haploidy and diploidy. Taken together, our findings unmasked a dynamic interplay between ploidy and ecology that was of unpredicted evolutionary importance and had multiple molecular roots.
Vyšlo v časopise:
Ancient Evolutionary Trade-Offs between Yeast Ploidy States. PLoS Genet 9(3): e32767. doi:10.1371/journal.pgen.1003388
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1003388
Souhrn
The number of chromosome sets contained within the nucleus of eukaryotic organisms is a fundamental yet evolutionarily poorly characterized genetic variable of life. Here, we mapped the impact of ploidy on the mitotic fitness of baker's yeast and its never domesticated relative Saccharomyces paradoxus across wide swaths of their natural genotypic and phenotypic space. Surprisingly, environment-specific influences of ploidy on reproduction were found to be the rule rather than the exception. These ploidy–environment interactions were well conserved across the 2 billion generations separating the two species, suggesting that they are the products of strong selection. Previous hypotheses of generalizable advantages of haploidy or diploidy in ecological contexts imposing nutrient restriction, toxin exposure, and elevated mutational loads were rejected in favor of more fine-grained models of the interplay between ecology and ploidy. On a molecular level, cell size and mating type locus composition had equal, but limited, explanatory power, each explaining 12.5%–17% of ploidy–environment interactions. The mechanism of the cell size–based superior reproductive efficiency of haploids during Li+ exposure was traced to the Li+ exporter ENA. Removal of the Ena transporters, forcing dependence on the Nha1 extrusion system, completely altered the effects of ploidy on Li+ tolerance and evoked a strong diploid superiority, demonstrating how genetic variation at a single locus can completely reverse the relative merits of haploidy and diploidy. Taken together, our findings unmasked a dynamic interplay between ploidy and ecology that was of unpredicted evolutionary importance and had multiple molecular roots.
Zdroje
1. BlancG, WolfeKH (2004) Widespread paleopolyploidy in model plant species inferred from age distributions of duplicate genes. Plant Cell 16: 1667–1678.
2. BowersJE, ChapmanBA, RongJ, PatersonAH (2003) Unravelling angiosperm genome evolution by phylogenetic analysis of chromosomal duplication events. Nature 422: 433–438.
3. DehalP, BooreJL (2005) Two rounds of whole genome duplication in the ancestral vertebrate. PLoS Biol 3: e314 doi:10.1371/journal.pbio.0030314
4. FreelingM, ThomasBC (2006) Gene-balanced duplications, like tetraploidy, provide predictable drive to increase morphological complexity. Genome Res 16: 805–814.
5. KellisM, BirrenBW, LanderES (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. ZhimulevIF, BelyaevaES, SemeshinVF, KoryakovDE, DemakovSA, et al. (2004) Polytene chromosomes: 70 years of genetic research. Int Rev Cytol 241: 203–275.
9. DavoliT, de LangeT (2011) The causes and consequences of polyploidy in normal development and cancer. Annu Rev Cell Dev Biol 27: 585–610.
10. GersteinAC, OttoSP (2009) Ploidy and the causes of genomic evolution. J Hered 100: 571–581.
11. HaldaneJBS (1937) The Effect of Variation of Fitness. The American Naturalist 71: 337–349.
12. AndersonJB, SirjusinghC, RickerN (2004) Haploidy, diploidy and evolution of antifungal drug resistance in Saccharomyces cerevisiae. Genetics 168: 1915–1923.
13. OrrHA, OttoSP (1994) Does diploidy increase the rate of adaptation? Genetics 136: 1475–1480.
14. ZeylC, VanderfordT, CarterM (2003) An evolutionary advantage of haploidy in large yeast populations. Science 299: 555–558.
15. WeissRL, KukoraJR, AdamsJ (1975) The relationship between enzyme activity, cell geometry, and fitness in Saccharomyces cerevisiae. Proc Natl Acad Sci U S A 72: 794–798.
16. AdamsJ, HanschePE (1974) Population studies in microorganisms. I. Evolution of diploidy in Saccharomyces cerevisiae. Genetics 76: 327–338.
17. LewisWM (1985) Nutrient scarcity as an evolutionary cause of haploidy. The American Naturalist 125: 692–701.
18. MableBK (2001) Ploidy evolution in the yeast Saccharomyces cerevisiae: a test of the nutrient limitation hypothesis. Journal of Evolutionary Biology 14: 157–170.
19. NeimanAM (2011) Sporulation in the budding yeast Saccharomyces cerevisiae. Genetics 189: 737–765.
20. DujonB (2010) Yeast evolutionary genomics. Nat Rev Genet 11: 512–524.
21. LitiG, CarterDM, MosesAM, WarringerJ, PartsL, et al. (2009) Population genomics of domestic and wild yeasts. Nature 458: 337–341.
22. WarringerJ, ZorgoE, CubillosFA, ZiaA, GjuvslandA, et al. (2011) Trait variation in yeast is defined by population history. PLoS Genet 7: e1002111 doi:10.1371/journal.pgen.1002111
23. RuderferDM, PrattSC, SeidelHS, KruglyakL (2006) Population genomic analysis of outcrossing and recombination in yeast. Nat Genet 38: 1077–1081.
24. TsaiIJ, BensassonD, BurtA, KoufopanouV (2008) Population genomics of the wild yeast Saccharomyces paradoxus: Quantifying the life cycle. Proc Natl Acad Sci U S A 105: 4957–4962.
25. MableBK, OttoSP (2001) Masking and purging mutations following EMS treatment in haploid, diploid and tetraploid yeast (Saccharomyces cerevisiae). Genet Res 77: 9–26.
26. ArinoJ, RamosJ, SychrovaH (2010) Alkali metal cation transport and homeostasis in yeasts. Microbiol Mol Biol Rev 74: 95–120.
27. GalitskiT, SaldanhaAJ, StylesCA, LanderES, FinkGR (1999) Ploidy regulation of gene expression. Science 285: 251–254.
28. de GodoyLM, OlsenJV, CoxJ, NielsenML, HubnerNC, et al. (2008) Comprehensive mass-spectrometry-based proteome quantification of haploid versus diploid yeast. Nature 455: 1251–1254.
29. JorgensenP, NishikawaJL, BreitkreutzBJ, TyersM (2002) Systematic identification of pathways that couple cell growth and division in yeast. Science 297: 395–400.
30. NelsonMA (1996) Mating systems in ascomycetes: a romp in the sac. Trends Genet 12: 69–74.
31. XiaoL, GroveA (2009) Coordination of Ribosomal Protein and Ribosomal RNA Gene Expression in Response to TOR Signaling. Curr Genomics 10: 198–205.
32. JungPP, FritschES, BlugeonC, SoucietJL, PotierS, et al. (2011) Ploidy influences cellular responses to gross chromosomal rearrangements in Saccharomyces cerevisiae. BMC Genomics 12: 331.
33. KnopM (2006) Evolution of the hemiascomycete yeasts: on life styles and the importance of inbreeding. Bioessays 28: 696–708.
34. GersteinAC, ChunHJ, GrantA, OttoSP (2006) Genomic convergence toward diploidy in Saccharomyces cerevisiae. PLoS Genet 2: e145 doi:10.1371/journal.pgen.0020145
35. GersteinAC, OttoSP (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. LynchM, SungW, MorrisK, CoffeyN, LandryCR, 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. ZorgoE, GjuvslandA, CubillosFA, LouisEJ, LitiG, et al. (2012) Life history shapes trait heredity by accumulation of loss-of-function alleles in yeast. Mol Biol Evol 29: 1781–1789.
38. HillenmeyerME, FungE, WildenhainJ, PierceSE, HoonS, et al. (2008) The Chemical Genomic Portrait of Yeast: Uncovering a Phenotype for All Genes. Science 320: 362–365.
39. ColuccioAE, RodriguezRK, KernanMJ, NeimanAM (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. EzovTK, Boger-NadjarE, FrenkelZ, KatsperovskiI, KemenyS, 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. OhnishiG, EndoK, DoiA, FujitaA, DaigakuY, et al. (2004) Spontaneous mutagenesis in haploid and diploid Saccharomyces cerevisiae. Biochem Biophys Res Commun 325: 928–933.
42. DickinsonWJ (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. DeutschbauerAM, JaramilloDF, ProctorM, KummJ, HillenmeyerME, et al. (2005) Mechanisms of haploinsufficiency revealed by genome-wide profiling in yeast. Genetics 169: 1915–1925.
44. KoronaR (1999) Unpredictable fitness transitions between haploid and diploid strains of the genetically loaded yeast Saccharomyces cerevisiae. Genetics 151: 77–85.
45. WestmorelandTJ, WickramasekaraSM, GuoAY, SelimAL, WinsorTS, 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. WilsonDM3rd, SofinowskiTM, McNeillDR (2003) Repair mechanisms for oxidative DNA damage. Front Biosci 8: d963–981.
47. LiXC, TyeBK (2011) Ploidy dictates repair pathway choice under DNA replication stress. Genetics 187: 1031–1040.
48. StorchovaZ, BrenemanA, CandeJ, DunnJ, BurbankK, et al. (2006) Genome-wide genetic analysis of polyploidy in yeast. Nature 443: 541–547.
49. HaberJE (2012) Mating-type genes and MAT switching in Saccharomyces cerevisiae. Genetics 191: 33–64.
50. ChantJ (1996) Generation of cell polarity in yeast. Curr Opin Cell Biol 8: 557–565.
51. KeN, IrwinPA, VoytasDF (1997) The pheromone response pathway activates transcription of Ty5 retrotransposons located within silent chromatin of Saccharomyces cerevisiae. Embo J 16: 6272–6280.
52. Frank-VaillantM, MarcandS (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. KegelA, SjostrandJO, AstromSU (2001) Nej1p, a cell type-specific regulator of nonhomologous end joining in yeast. Curr Biol 11: 1611–1617.
54. GersteinAC (2013) Mutational effects depend on ploidy level: all else is not equal. Biol Lett 9: 20120614.
55. WielandJ, NitscheAM, StrayleJ, SteinerH, RudolphHK (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. ChanYH, MarshallWF (2010) Scaling properties of cell and organelle size. Organogenesis 6: 88–96.
57. JorgensenP, EdgingtonNP, SchneiderBL, RupesI, TyersM, et al. (2007) The size of the nucleus increases as yeast cells grow. Mol Biol Cell 18: 3523–3532.
58. McLaughlanJM, LitiG, SharpS, MaslowskaA, LouisEJ (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. EhrenreichIM, BloomJ, TorabiN, WangX, JiaY, 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. PartsL, CubillosFA, WarringerJ, JainK, SalinasF, et al. (2011) Revealing the genetic structure of a trait by sequencing a population under selection. Genome Res 21: 1131–1138.
61. CubillosFA, LouisEJ, LitiG (2009) Generation of a large set of genetically tractable haploid and diploid Saccharomyces strains. FEMS Yeast Res 9: 1217–1225.
62. WarringerJ, AnevskiD, LiuB, BlombergA (2008) Chemogenetic fingerprinting by analysis of cellular growth dynamics. BMC Chem Biol 8: 3.
63. WarringerJ, BlombergA (2003) Automated screening in environmental arrays allows analysis of quantitative phenotypic profiles in Saccharomyces cerevisiae. Yeast 20: 53–67.
64. BenjaminiY, HochbergY (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society 57: 289–300.
65. EisenMB, SpellmanPT, BrownPO, BotsteinD (1998) Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci U S A 95: 14863–14868.
66. LitiG, LouisEJ (2003) NEJ1 prevents NHEJ-dependent telomere fusions in yeast without telomerase. Mol Cell 11: 1373–1378.
67. SpringerM, WeissmanJS, KirschnerMW (2010) A general lack of compensation for gene dosage in yeast. Mol Syst Biol 6: 368.
68. HaaseSB, ReedSI (2002) Improved flow cytometric analysis of the budding yeast cell cycle. Cell Cycle 1: 132–136.
69. LopesCA, BarrioE, QuerolA (2010) Natural hybrids of S. cerevisiae x S. kudriavzevii share alleles with European wild populations of Saccharomyces kudriavzevii. FEMS Yeast Res 10: 412–421.
Štítky
Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
2013 Číslo 3
- Je „freeze-all“ pro všechny? Odborníci na fertilitu diskutovali na virtuálním summitu
- Gynekologové a odborníci na reprodukční medicínu se sejdou na prvním virtuálním summitu
Najčítanejšie v tomto čísle
- Fine Characterisation of a Recombination Hotspot at the Locus and Resolution of the Paradoxical Excess of Duplications over Deletions in the General Population
- Molecular Networks of Human Muscle Adaptation to Exercise and Age
- Recurrent Rearrangement during Adaptive Evolution in an Interspecific Yeast Hybrid Suggests a Model for Rapid Introgression
- Genome-Wide Association Study and Gene Expression Analysis Identifies as a Predictor of Response to Etanercept Therapy in Rheumatoid Arthritis