#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Mechanisms of Chromosome Number Evolution in Yeast


The whole-genome duplication (WGD) that occurred during yeast evolution changed the basal number of chromosomes from 8 to 16. However, the number of chromosomes in post-WGD species now ranges between 10 and 16, and the number in non-WGD species (Zygosaccharomyces, Kluyveromyces, Lachancea, and Ashbya) ranges between 6 and 8. To study the mechanism by which chromosome number changes, we traced the ancestry of centromeres and telomeres in each species. We observe only two mechanisms by which the number of chromosomes has decreased, as indicated by the loss of a centromere. The most frequent mechanism, seen 8 times, is telomere-to-telomere fusion between two chromosomes with the concomitant death of one centromere. The other mechanism, seen once, involves the breakage of a chromosome at its centromere, followed by the fusion of the two arms to the telomeres of two other chromosomes. The only mechanism by which chromosome number has increased in these species is WGD. Translocations and inversions have cycled telomere locations, internalizing some previously telomeric genes and creating novel telomeric locations. Comparison of centromere structures shows that the length of the CDEII region is variable between species but uniform within species. We trace the complete rearrangement history of the Lachancea kluyveri genome since its common ancestor with Saccharomyces and propose that its exceptionally low level of rearrangement is a consequence of the loss of the non-homologous end joining (NHEJ) DNA repair pathway in this species.


Vyšlo v časopise: Mechanisms of Chromosome Number Evolution in Yeast. PLoS Genet 7(7): e32767. doi:10.1371/journal.pgen.1002190
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1002190

Souhrn

The whole-genome duplication (WGD) that occurred during yeast evolution changed the basal number of chromosomes from 8 to 16. However, the number of chromosomes in post-WGD species now ranges between 10 and 16, and the number in non-WGD species (Zygosaccharomyces, Kluyveromyces, Lachancea, and Ashbya) ranges between 6 and 8. To study the mechanism by which chromosome number changes, we traced the ancestry of centromeres and telomeres in each species. We observe only two mechanisms by which the number of chromosomes has decreased, as indicated by the loss of a centromere. The most frequent mechanism, seen 8 times, is telomere-to-telomere fusion between two chromosomes with the concomitant death of one centromere. The other mechanism, seen once, involves the breakage of a chromosome at its centromere, followed by the fusion of the two arms to the telomeres of two other chromosomes. The only mechanism by which chromosome number has increased in these species is WGD. Translocations and inversions have cycled telomere locations, internalizing some previously telomeric genes and creating novel telomeric locations. Comparison of centromere structures shows that the length of the CDEII region is variable between species but uniform within species. We trace the complete rearrangement history of the Lachancea kluyveri genome since its common ancestor with Saccharomyces and propose that its exceptionally low level of rearrangement is a consequence of the loss of the non-homologous end joining (NHEJ) DNA repair pathway in this species.


Zdroje

1. JWIJBaldiniAWardDCReedersSTWellsRA 1991 Origin of human chromosome 2: an ancestral telomere-telomere fusion. Proc Natl Acad Sci U S A 88 9051 9055

2. HillierLWGravesTAFultonRSFultonLAPepinKH 2005 Generation and annotation of the DNA sequences of human chromosomes 2 and 4. Nature 434 724 731

3. LuoMCDealKRAkhunovEDAkhunovaARAndersonOD 2009 Genome comparisons reveal a dominant mechanism of chromosome number reduction in grasses and accelerated genome evolution in Triticeae. Proc Natl Acad Sci U S A

4. International Brachypodium Initiative 2010 Genome sequencing and analysis of the model grass Brachypodium distachyon. Nature 463 763 768

5. GuerraCEKabackDB 1999 The role of centromere alignment in meiosis I segregation of homologous chromosomes in Saccharomyces cerevisiae. Genetics 153 1547 1560

6. MalikHSHenikoffS 2009 Major evolutionary transitions in centromere complexity. Cell 138 1067 1082

7. DernburgAF 2001 Here, there, and everywhere: kinetochore function on holocentric chromosomes. J Cell Biol 153 F33 38

8. FleigUBeinhauerJDHegemannJH 1995 Functional selection for the centromere DNA from yeast chromosome VIII. Nucleic Acids Res 23 922 924

9. HieterPPridmoreDHegemannJHThomasMDavisRW 1985 Functional selection and analysis of yeast centromeric DNA. Cell 42 913 921

10. KennaMAmayaEBloomK 1988 Selective excision of the centromere chromatin complex from Saccharomyces cerevisiae. J Cell Biol 107 9 15

11. BensassonDZarowieckiMBurtAKoufopanouV 2008 Rapid evolution of yeast centromeres in the absence of drive. Genetics 178 2161 2167

12. SanyalKBaumMCarbonJ 2004 Centromeric DNA sequences in the pathogenic yeast Candida albicans are all different and unique. Proc Natl Acad Sci U S A 101 11374 11379

13. LynchDBLogueMEButlerGWolfeKH 2010 Chromosomal G+C content evolution in yeasts: systematic interspecies differences, and GC-poor troughs at centromeres. Genome Biol Evol 2 572 583

14. BlackburnEHGallJG 1978 A tandemly repeated sequence at the termini of the extrachromosomal ribosomal RNA genes in Tetrahymena. J Mol Biol 120 33 53

15. McClintockB 1939 The Behavior in Successive Nuclear Divisions of a Chromosome Broken at Meiosis. Proc Natl Acad Sci U S A 25 405 416

16. BoscoGHaberJE 1998 Chromosome break-induced DNA replication leads to nonreciprocal translocations and telomere capture. Genetics 150 1037 1047

17. CechTR 2004 Beginning to understand the end of the chromosome. Cell 116 273 279

18. de BruinDKantrowSMLiberatoreRAZakianVA 2000 Telomere folding is required for the stable maintenance of telomere position effects in yeast. Mol Cell Biol 20 7991 8000

19. LydallD 2003 Hiding at the ends of yeast chromosomes: telomeres, nucleases and checkpoint pathways. J Cell Sci 116 4057 4065

20. WeinertT 2005 Do telomeres ask checkpoint proteins: “gimme shelter-in”? Dev Cell 9 725 726

21. de BruinDZamanZLiberatoreRAPtashneM 2001 Telomere looping permits gene activation by a downstream UAS in yeast. Nature 409 109 113

22. ChanSWBlackburnEH 2003 Telomerase and ATM/Tel1p protect telomeres from nonhomologous end joining. Mol Cell 11 1379 1387

23. RayARungeKW 1999 The yeast telomere length counting machinery is sensitive to sequences at the telomere-nontelomere junction. Mol Cell Biol 19 31 45

24. RungeKWZakianVA 1989 Introduction of extra telomeric DNA sequences into Saccharomyces cerevisiae results in telomere elongation. Mol Cell Biol 9 1488 1497

25. CohnMMcEachernMJBlackburnEH 1998 Telomeric sequence diversity within the genus Saccharomyces. Curr Genet 33 83 91

26. KurtzmanCP 2011 Discussion of teleomorphic and anamorphic ascomycetous yeasts and yeast-like taxa. BoekhoutT The Yeasts, a Taxonomic Study. 5 ed Amsterdam Elsevier 293 307

27. DietrichFSVoegeliSBrachatSLerchAGatesK 2004 The Ashbya gossypii genome as a tool for mapping the ancient Saccharomyces cerevisiae genome. Science 304 304 307

28. DujonBShermanDFischerGDurrensPCasaregolaS 2004 Genome evolution in yeasts. Nature 430 35 44

29. GoffeauABarrellBGBusseyHDavisRWDujonB 1996 Life with 6000 genes. Science 274 546, 563–547

30. KellisMBirrenBWLanderES 2004 Proof and evolutionary analysis of ancient genome duplication in the yeast Saccharomyces cerevisiae. Nature 428 617 624

31. KellisMPattersonNEndrizziMBirrenBLanderES 2003 Sequencing and comparison of yeast species to identify genes and regulatory elements. Nature 423 241 254

32. ScannellDRFrankACConantGCByrneKPWoolfitM 2007 Independent sorting-out of thousands of duplicated gene pairs in two yeast species descended from a whole-genome duplication. Proc Natl Acad Sci U S A 104 8397 8402

33. SoucietJLDujonBGaillardinCJohnstonMBaretPV 2009 Comparative genomics of protoploid Saccharomycetaceae. Genome Res 19 1696 1709

34. WolfeKHShieldsDC 1997 Molecular evidence for an ancient duplication of the entire yeast genome. Nature 387 708 713

35. WolfeKH 2006 Comparative genomics and genome evolution in yeasts. Philos Trans R Soc Lond B Biol Sci 361 403 412

36. GordonJLByrneKPWolfeKH 2009 Additions, losses, and rearrangements on the evolutionary route from a reconstructed ancestor to the modern Saccharomyces cerevisiae genome. PLoS Genet 5 e1000485 doi:10.1371/journal.pgen.1000485

37. SpirekMYangJGrothCPetersenRFLangkjaerRB 2003 High-rate evolution of Saccharomyces sensu lato chromosomes. FEMS Yeast Res 3 363 373

38. PetersenRFNilsson-TillgrenTPiskurJ 1999 Karyotypes of Saccharomyces sensu lato species. Int J Syst Bacteriol 49 Pt 4 1925 1931

39. ByrneKPWolfeKH 2005 The Yeast Gene Order Browser: combining curated homology and syntenic context reveals gene fate in polyploid species. Genome Res 15 1456 1461

40. EllenbergerTTomkinsonAE 2008 Eukaryotic DNA ligases: structural and functional insights. Annu Rev Biochem 77 313 338

41. TsengHMTomkinsonAE 2004 Processing and joining of DNA ends coordinated by interactions among Dnl4/Lif1, Pol4, and FEN-1. J Biol Chem 279 47580 47588

42. WilsonTELieberMR 1999 Efficient processing of DNA ends during yeast nonhomologous end joining. Evidence for a DNA polymerase beta (Pol4)-dependent pathway. J Biol Chem 274 23599 23609

43. KegelASjostrandJOAstromSU 2001 Nej1p, a cell type-specific regulator of nonhomologous end joining in yeast. Curr Biol 11 1611 1617

44. ValenciaMBenteleMVazeMBHerrmannGKrausE 2001 NEJ1 controls non-homologous end joining in Saccharomyces cerevisiae. Nature 414 666 669

45. DecottigniesA 2007 Microhomology-mediated end joining in fission yeast is repressed by pku70 and relies on genes involved in homologous recombination. Genetics 176 1403 1415

46. MaJLKimEMHaberJELeeSE 2003 Yeast Mre11 and Rad1 proteins define a Ku-independent mechanism to repair double-strand breaks lacking overlapping end sequences. Mol Cell Biol 23 8820 8828

47. LeeKLeeSE 2007 Saccharomyces cerevisiae Sae2- and Tel1-dependent single-strand DNA formation at DNA break promotes microhomology-mediated end joining. Genetics 176 2003 2014

48. de ClareMPirPOliverSG 2011 Haploinsufficiency and the sex chromosomes from yeasts to humans. BMC Biol 9 15

49. BaileyTLElkanC 1994 Fitting a mixture model by expectation maximization to discover motifs in biopolymers. Proc Int Conf Intell Syst Mol Biol 2 28 36

50. CliftenPFFultonRSWilsonRKJohnstonM 2006 After the duplication: gene loss and adaptation in Saccharomyces genomes. Genetics 172 863 872

51. PobiegaSMarcandS 2010 Dicentric breakage at telomere fusions. Genes Dev 24 720 733

52. HughesTRRobertsCJDaiHJonesARMeyerMR 2000 Widespread aneuploidy revealed by DNA microarray expression profiling. Nat Genet 25 333 337

53. DelneriDColsonIGrammenoudiSRobertsINLouisEJ 2003 Engineering evolution to study speciation in yeasts. Nature 422 68 72

54. PolakovaSBlumeCZarateJAMentelMJorck-RambergD 2009 Formation of new chromosomes as a virulence mechanism in yeast Candida glabrata. Proc Natl Acad Sci U S A 106 2688 2693

55. HubermanJAPridmoreRDJägerDZonneveldBPhilippsenP 1986 Centromeric DNA from Saccharomyces uvarum is functional in Saccharomyces cerevisiae. Chromosoma 94 162 168

56. YamaneSKarashimaHMatsuzakiHHatanoTFukuiS 1999 Isolation of centromeric DNA from Saccharomyces bayanus. J Gen Appl Microbiol 45 89 92

57. KitadaKYamaguchiEHamadaKArisawaM 1997 Structural analysis of a Candida glabrata centromere and its functional homology to the Saccharomyces cerevisiae centromere. Curr Genet 31 122 127

58. PribylovaLStraubM-LSychrovaHde MontignyJ 2007 Characterisation of Zygosaccharomyces rouxii centromeres and construction of first Z. rouxii centromeric vectors. Chromosome Res 15 439 445

59. HeusJJZonneveldBJSteensmaHYvan den BergJA 1993 The consensus sequence of Kluyveromyces lactis centromeres shows homology to functional centromeric DNA from Saccharomyces cerevisiae. Mol Gen Genet 236 355 362

60. BellochCBarrioEGarciaMDQuerolA 1998 Inter- and intraspecific chromosome pattern variation in the yeast genus Kluyveromyces. Yeast 14 1341 1354

61. HegemannJHFleigUN 1993 The centromere of budding yeast. Bioessays 15 451 460

62. HegemannJHSheroJHCottarelGPhilippsenPHieterP 1988 Mutational analysis of centromere DNA from chromosome VI of Saccharomyces cerevisiae. Mol Cell Biol 8 2523 2535

63. NiedenthalRStollRHegemannJH 1991 In vivo characterization of the Saccharomyces cerevisiae centromere DNA element I, a binding site for the helix-loop-helix protein CPF1. Mol Cell Biol 11 3545 3553

64. JehnBNiedenthalRHegemannJH 1991 In vivo analysis of the Saccharomyces cerevisiae centromere CDEIII sequence: requirements for mitotic chromosome segregation. Mol Cell Biol 11 5212 5221

65. KetelCWangHSMcClellanMBouchonvilleKSelmeckiA 2009 Neocentromeres form efficiently at multiple possible loci in Candida albicans. PLoS Genet 5 e1000400 doi:10.1371/journal.pgen.1000400

66. DiedeSJGottschlingDE 1999 Telomerase-mediated telomere addition in vivo requires DNA primase and DNA polymerases alpha and delta. Cell 99 723 733

67. KramerKMHaberJE 1993 New telomeres in yeast are initiated with a highly selected subset of TG1-3 repeats. Genes Dev 7 2345 2356

68. PutnamCDPennaneachVKolodnerRD 2004 Chromosome healing through terminal deletions generated by de novo telomere additions in Saccharomyces cerevisiae. Proc Natl Acad Sci U S A 101 13262 13267

69. MyungKDattaAKolodnerRD 2001 Suppression of spontaneous chromosomal rearrangements by S phase checkpoint functions in Saccharomyces cerevisiae. Cell 104 397 408

70. WyrickJJHolstegeFCJenningsEGCaustonHCShoreD 1999 Chromosomal landscape of nucleosome-dependent gene expression and silencing in yeast. Nature 402 418 421

71. LoneyERInglisPWSharpSPrydeFEKentNA 2009 Repressive and non-repressive chromatin at native telomeres in Saccharomyces cerevisiae. Epigenetics Chromatin 2 18

72. MartinAMPouchnikDJWalkerJLWyrickJJ 2004 Redundant roles for histone H3 N-terminal lysine residues in subtelomeric gene repression in Saccharomyces cerevisiae. Genetics 167 1123 1132

73. BatadaNNHurstLD 2007 Evolution of chromosome organization driven by selection for reduced gene expression noise. Nat Genet 39 945 949

74. PalCPappBLercherMJ 2006 An integrated view of protein evolution. Nat Rev Genet 7 337 348

75. DrummondDABloomJDAdamiCWilkeCOArnoldFH 2005 Why highly expressed proteins evolve slowly. Proc Natl Acad Sci U S A 102 14338 14343

76. PalCPappBHurstLD 2001 Highly expressed genes in yeast evolve slowly. Genetics 158 927 931

77. PalCPappBHurstLD 2003 Genomic function: Rate of evolution and gene dispensability. Nature 421 496 497; discussion 497–498

78. KentWJBaertschRHinrichsAMillerWHausslerD 2003 Evolution's cauldron: duplication, deletion, and rearrangement in the mouse and human genomes. Proc Natl Acad Sci U S A 100 11484 11489

79. MyungKChenCKolodnerRD 2001 Multiple pathways cooperate in the suppression of genome instability in Saccharomyces cerevisiae. Nature 411 1073 1076

80. MieczkowskiPAMieczkowskaJODominskaMPetesTD 2003 Genetic regulation of telomere-telomere fusions in the yeast Saccharomyces cerevisae. Proc Natl Acad Sci U S A 100 10854 10859

81. LitiGLouisEJ 2003 NEJ1 prevents NHEJ-dependent telomere fusions in yeast without telomerase. Mol Cell 11 1373 1378

82. GreenwoodJCooperJP 2009 Trapping Rap1 at the telomere to prevent chromosome end fusions. EMBO J 28 3277 3278

83. PennaneachVPutnamCDKolodnerRD 2006 Chromosome healing by de novo telomere addition in Saccharomyces cerevisiae. Mol Microbiol 59 1357 1368

84. ButlerGKennyCFaganAKurischkoCGaillardinC 2004 Evolution of the MAT locus and its Ho endonuclease in yeast species. Proc Natl Acad Sci U S A 101 1632 1637

85. DelneriDColsonIGrammenoudiSRobertsINLouisEJ 2003 Engineering evolution to study speciation in yeasts. Nature 422 68 72

86. De SchutterKLinYCTielsPVan HeckeAGlinkaS 2009 Genome sequence of the recombinant protein production host Pichia pastoris. Nat Biotechnol 27 561 566

87. ButlerGRasmussenMDLinMFSantosMASakthikumarS 2009 Evolution of pathogenicity and sexual reproduction in eight Candida genomes. Nature 459 657 662

88. HedtkeSMTownsendTMHillisDM 2006 Resolution of phylogenetic conflict in large data sets by increased taxon sampling. Syst Biol 55 522 529

Štítky
Genetika Reprodukčná medicína

Článok vyšiel v časopise

PLOS Genetics


2011 Číslo 7
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Aktuální možnosti diagnostiky a léčby litiáz
nový kurz
Autori: MUDr. Tomáš Ürge, PhD.

Všetky kurzy
Prihlásenie
Zabudnuté heslo

Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.

Prihlásenie

Nemáte účet?  Registrujte sa

#ADS_BOTTOM_SCRIPTS#