Factors enforcing the species boundary between the human pathogens Cryptococcus neoformans and Cryptococcus deneoformans


Autoři: Shelby J. Priest aff001;  Marco A. Coelho aff001;  Verónica Mixão aff002;  Shelly Applen Clancey aff001;  Yitong Xu aff004;  Sheng Sun aff001;  Toni Gabaldón aff002;  Joseph Heitman aff001
Působiště autorů: Department of Molecular Genetics and Microbiology, Duke University Medical Center, Durham, North Carolina, United States of America aff001;  Life Sciences Department, Barcelona Supercomputing Center, Barcelona, Spain aff002;  Institute for Research in Biomedicine, Barcelona Institute of Science and Technology, Barcelona, Spain aff003;  Program in Cell and Molecular Biology, Duke University Medical Center, Durham, North Carolina, United States of America aff004;  Catalan Institution for Research and Advanced Studies (ICREA), Barcelona, Spain aff005
Vyšlo v časopise: Factors enforcing the species boundary between the human pathogens Cryptococcus neoformans and Cryptococcus deneoformans. PLoS Genet 17(1): e1008871. doi:10.1371/journal.pgen.1008871
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pgen.1008871

Souhrn

Hybridization has resulted in the origin and variation in extant species, and hybrids continue to arise despite pre- and post-zygotic barriers that limit their formation and evolutionary success. One important system that maintains species boundaries in prokaryotes and eukaryotes is the mismatch repair pathway, which blocks recombination between divergent DNA sequences. Previous studies illuminated the role of the mismatch repair component Msh2 in blocking genetic recombination between divergent DNA during meiosis. Loss of Msh2 results in increased interspecific genetic recombination in bacterial and yeast models, and increased viability of progeny derived from yeast hybrid crosses. Hybrid isolates of two pathogenic fungal Cryptococcus species, Cryptococcus neoformans and Cryptococcus deneoformans, are isolated regularly from both clinical and environmental sources. In the present study, we sought to determine if loss of Msh2 would relax the species boundary between C. neoformans and C. deneoformans. We found that crosses between these two species in which both parents lack Msh2 produced hybrid progeny with increased viability and high levels of aneuploidy. Whole-genome sequencing revealed few instances of recombination among hybrid progeny and did not identify increased levels of recombination in progeny derived from parents lacking Msh2. Several hybrid progeny produced structures associated with sexual reproduction when incubated alone on nutrient-rich medium in light, a novel phenotype in Cryptococcus. These findings represent a unique, unexpected case where rendering the mismatch repair system defective did not result in increased meiotic recombination across a species boundary. This suggests that alternative pathways or other mismatch repair components limit meiotic recombination between homeologous DNA and enforce species boundaries in the basidiomycete Cryptococcus species.

Klíčová slova:

Aneuploidy – Cryptococcus – Cryptococcus neoformans – Genomics – Heterozygosity – Homologous recombination – Single nucleotide polymorphisms – Genetic hybrids


Zdroje

1. Arnold ML, Bulger MR, Burke JM, Hempel AL, Williams H, Arnold ML, et al. Natural hybridization: how low can you go and still be important? Ecology. 1999;80: 371–381. doi: 10.1890/0012-9658(1999)080[0371:NHHLCY]2.0.CO;2

2. Goulet BE, Roda F, Hopkins R. Hybridization in plants: old ideas, new techniques. Plant Physiol. 2017;173: 65–78. doi: 10.1104/pp.16.01340 27895205

3. Vallejo-Marin M, Hiscock SJ. Hybridization and hybrid speciation under global change. New Phytol. 2016;211: 1170–1187. doi: 10.1111/nph.14004 27214560

4. Fu C, Coelho MA, David-Palma M, Priest SJ, Heitman J. Genetic and genomic evolution of sexual reproduction: echoes from LECA to the fungal kingdom. Curr Opin Genet Dev. 2019;58–59: 70–75. doi: 10.1016/j.gde.2019.07.008 31473482

5. Lu A, Clark S, Modrich P. Methyl-directed repair of DNA base-pair mismatches in vitro. DNA Repair (Amst). 1983;80: 4639–4643. doi: 10.1073/pnas.80.15.4639 6308634

6. Grilley M, Holmes J, Yashar B, Modrich P. Mechanisms of DNA-mismatch correction. Mutat Res. 1990;236: 253–267. doi: 10.1016/0921-8777(90)90009-t 2144613

7. Harfe BD, Jinks-Robertson S. Mismatch repair proteins and mitotic genome stability. Mutat Res. 2000;451: 151–167. doi: 10.1016/s0027-5107(00)00047-6 10915870

8. Rayssiguier C, Thaler DS, Radman M. The barrier to recombination between Escherichia coli and Salmonella typhimurium is disrupted in mismatch-repair mutants. Nature. 1989;342: 396–401. doi: 10.1038/342396a0 2555716

9. Greig D, Leu J-Y. Natural history of budding yeast. Curr Biol. 2009;19: 886–890. doi: 10.1016/j.cub.2009.07.037 19825346

10. Hunter N, Chambers SR, Louis EJ, Borts RH. The mismatch repair system contributes to meiotic sterility in an interspecific yeast hybrid. EMBO J. 1996;15: 1726–1733. doi: 10.1002/j.1460-2075.1996.tb00518.x 8612597

11. Chambers SR, Hunter N, Louis EJ, Borts RH. The mismatch repair system reduces meiotic homeologous recombination and stimulates recombination-dependent chromosome loss. Mol Cell Biol. 1996;16: 6110–6120. doi: 10.1128/mcb.16.11.6110 8887641

12. Lamichhaney S, Han F, Webster MT, Andersson L, Grant BR, Grant PR. Rapid hybrid speciation in Darwin’s finches. Science. 2018;359: 224–228. doi: 10.1126/science.aao4593 29170277

13. Kelso J, Prufer K. Ancient humans and the origin of modern humans. Curr Opin Genet Dev. 2014;29: 133–138. doi: 10.1016/j.gde.2014.09.004 25286439

14. Darwin C. What Mr. Darwin saw in his voyage round the world in the ship “Beagle.” New York, NY: Harper & Brothers; 1880. doi: 10.5962/bhl.title.27538

15. Coyne JA, Orr HA. Speciation. Sunderland, MA: Sinauer Associates; 2004.

16. Dietrich FS, Voegeli S, Brachat S, Lerch A, Gates K, Steiner S, et al. The Ashbya gossypii genome as a tool for mapping the ancient Saccharomyces cerevisiae genome. Science. 2004;304: 304–7. doi: 10.1126/science.1095781 15001715

17. Wolfe KH. Origin of the yeast whole-genome duplication. PLoS Biol. 2015;13: e1002221. doi: 10.1371/journal.pbio.1002221 26252643

18. Marcet-Houben M, Gabaldón T. Beyond the whole-genome duplication: phylogenetic evidence for an ancient interspecies hybridization in the baker’s yeast lineage. PLoS Biol. 2015;13: 26252497. doi: 10.1371/journal.pbio.1002220 26252497

19. Stukenbrock EH, Christiansen FB, Hansen TT, Dutheil JY, Schierup MH. Fusion of two divergent fungal individuals led to the recent emergence of a unique widespread pathogen species. Proc Natl Acad Sci. 2012;109: 10954–10959. doi: 10.1073/pnas.1201403109 22711811

20. Pryszcz LP, Németh T, Saus E, Ksiezopolska E, Hegedusova E, Nosek J, et al. The genomic aftermath of hybridization in the opportunistic pathogen Candida metapsilosis. PLoS Genet. 2015;11: e1005626. doi: 10.1371/journal.pgen.1005626 26517373

21. Mixão V, Hansen AP, Saus E, Boekhout T, Lass-florl C, Gabaldón T. Whole-genome sequencing of the opportunistic yeast pathogen Candida inconspicua uncovers its hybrid origin. Front Genet. 2019;10: 383. doi: 10.3389/fgene.2019.00383 31105748

22. Mixão V, Gabaldón T. Hybridization and emergence of virulence in opportunistic human yeast pathogens. Yeast. 2018;35: 5–20. doi: 10.1002/yea.3242 28681409

23. Rajasingham R, Smith RM, Park BJ, Jarvis JN, Govender NP, Chiller TM, et al. Global burden of disease of HIV-associated cryptococcal meningitis: an updated analysis. Lancet Infect Dis. 2017;17: 873–881. doi: 10.1016/S1473-3099(17)30243-8 28483415

24. Hagen F, Khayhan K, Theelen B, Kolecka A, Polacheck I, Sionov E, et al. Recognition of seven species in the Cryptococcus gattii/Cryptococcus neoformans species complex. Fungal Genet Biol. 2015;78: 16–48. doi: 10.1016/j.fgb.2015.02.009 25721988

25. Farrer RA, Chang M, Davis MJ, van Dorp L, Yang D, Shea T, et al. A new lineage of Cryptococcus gattii (VGV) discovered in the Central Zambezian Miombo Woodlands. mBio. 2019;10: e02306–19. doi: 10.1128/mBio.02306-19 31719178

26. Xu J, Vilgalys R, Mitchell TG. Multiple gene genealogies reveal recent dispersion and hybridization in the human pathogenic fungus Cryptococcus neoformans. Mol Ecol. 2000;9: 1471–1481. doi: 10.1046/j.1365-294x.2000.01021.x 11050543

27. Kavanaugh LA, Fraser JA, Dietrich FS. Recent evolution of the human pathogen Cryptococcus neoformans by intervarietal transfer of a 14-gene fragment. Mol Biol Evol. 2004;23: 1879–1890. doi: 10.1093/molbev/msl070 16870684

28. Loftus BJ, Fung E, Roncaglia P, Rowley D, Amedeo P, Vamathevan J, et al. The genome of the basidiomycetous yeast and human pathogen Cryptococcus neoformans. Science. 2005;307: 1321–1324. doi: 10.1126/science.1103773 15653466

29. Janbon G, Ormerod KL, Paulet D, Byrnes EJ, Yadav V, Chatterjee G, et al. Analysis of the genome and transcriptome of Cryptococcus neoformans var. grubii reveals complex RNA expression and microevolution leading to virulence attenuation. PLoS Genet. 2014;10: e1004261. doi: 10.1371/journal.pgen.1004261 24743168

30. Martinez LR, Garcia-Rivera J, Casadevall A. Cryptococcus neoformans var. neoformans (serotype D) strains are more susceptible to heat than C. neoformans var. grubii (serotype A) strains. J Clin Microbiol. 2001;39: 3365–3367. doi: 10.1128/jcm.39.9.3365-3367.2001 11526180

31. Feldmesser M, Kress Y, Casadevall A. Dynamic changes in the morphology of Cryptococcus neoformans during murine pulmonary infection. Microbiology. 2001;147: 2355–2365. doi: 10.1099/00221287-147-8-2355 11496012

32. Desnos-Ollivier M, Patel S, Raoux-Barbot D, Heitman J, Dromer F, The French Cryptococcosis Study Group. Cryptococcosis serotypes impact outcome and provide evidence of Cryptococcus neoformans speciation. mBio. 2015;6: e00311–15. doi: 10.1128/mBio.00311-15 26060271

33. Casadevall A, Perfect JR. Cryptococcus neoformans. Washington, DC: ASM Press; 1998.

34. Dromer F, Mathoulin-Pelissier S, Launay O, Lortholary O, The French Cryptocococcosis Study Group. Determinants of disease presentation and outcome during cryptococcosis: the Crypto A/D study. PLOS Med. 2007;4: e21. doi: 10.1371/journal.pmed.0040021 17284154

35. Chayakulkeeree M, Perfect JR. Cryptococcosis. Infect Dis Clin North Am. 2006;20: 507–544. doi: 10.1016/j.idc.2006.07.001 16984867

36. Sun S, Coelho MA, David-Palma M, Priest SJ, Heitman J. The evolution of sexual reproduction and the mating-type locus: links to pathogenesis of Cryptococcus human pathogenic fungi. Annu Rev Genet. 2019;53: 417–444. doi: 10.1146/annurev-genet-120116-024755 31537103

37. Litvintseva AP, Kestenbaum L, Vilgalys R, Mitchell TG. Comparative analysis of environmental and clinical populations of Cryptococcus neoformans. J Clin Microbiol. 2005;43: 556–564. doi: 10.1128/JCM.43.2.556-564.2005 15695645

38. Cogliati M, Esposto MC, Clarke DL, Wickes BL, Viviani MA. Origin of Cryptococcus neoformans var. neoformans diploid strains. J Clin Microbiol. 2001;39: 3889–3894. doi: 10.1128/JCM.39.11.3889-3894.2001 11682503

39. Frases S, Ferrer C, Sanchez M, Colom-Valiente MF. Molecular epidemiology of isolates of the Cryptococcus neoformans species complex from Spain. Rev Iberoam Micol. 2009;26: 112–117. doi: 10.1016/S1130-1406(09)70021-X 19631160

40. Maduro AP, Mansinho K, Teles F, Silva I, Meyer W, Martins ML, et al. Insights on the genotype distribution among Cryptococcus neoformans and C. gattii Portuguese clinical isolates. Curr Microbiol. 2014;68: 199–203. doi: 10.1007/s00284-013-0452-0 24077953

41. Lengeler KB, Cox GM, Heitman J. Serotype AD strains of Cryptococcus neoformans are diploid or aneuploid and are heterozygous at the mating-type locus. Infect Immun. 2001;69: 115–122. doi: 10.1128/IAI.69.1.115-122.2001 11119496

42. Sun S, Xu J. Chromosomal rearrangements between serotype A and D strains in Cryptococcus neoformans. PLoS One. 2009;4: e5524. doi: 10.1371/journal.pone.0005524 19436753

43. Lin X, Litvintseva AP, Nielsen K, Patel S, Floyd A, Mitchell TG, et al. αADα hybrids of Cryptococcus neoformans: evidence of same-sex mating in nature and hybrid fitness. PLoS Genet. 2007;3: 1975–1990. doi: 10.1371/journal.pgen.0030186 17953489

44. Kwon-Chung KJ, Varma A. Do major species concepts support one, two or more species within Cryptococcus neoformans? FEMS Yeast Res. 2006;6: 574–587. doi: 10.1111/j.1567-1364.2006.00088.x 16696653

45. Li W, Averette AF, Desnos-Ollivier M, Ni M, Dromer F, Heitman J. Genetic diversity and genomic plasticity of Cryptococcus neoformans AD hybrid strains. G3. 2012;2: 83–97. doi: 10.1534/g3.111.001255 22384385

46. Sun S, Xu J. Genetic analyses of a hybrid cross between Serotypes A and D strains of the human pathogenic fungus Cryptococcus neoformans. Genetics. 2007;177: 1475–1486. doi: 10.1534/genetics.107.078923 17947421

47. Vogan AA, Khankhet J, Xu J. Evidence for mitotic recombination within the basidia of a hybrid cross of Cryptococcus neoformans. PLoS One. 2013;8: e62790. doi: 10.1371/journal.pone.0062790 23690954

48. Samarasinghe H, Vogan A, Pum N, Xu J. Patterns of allele distribution in a hybrid population of the Cryptococcus neoformans species complex. Mycoses. 2019;63: 275–283. doi: 10.1111/myc.13040 31774582

49. Billmyre RB, Clancey SA, Heitman J. Natural mismatch repair mutations mediate phenotypic diversity and drug resistance in Cryptococcus deuterogattii. eLife. 2017;6: e28802. doi: 10.7554/eLife.28802 28948913

50. Boyce KJ, Wang Y, Verma S, Shakya VPS, Xue C, Idnurm A. Mismatch repair of DNA replication errors contributes to microevolution in the pathogenic fungus Cryptococcus neoformans. mBio. 2017;8: e00595–17. doi: 10.1128/mBio.00595-17 28559486

51. Liu OW, Chun CD, Chow ED, Chen C, Madhani HD, Noble SM. Systematic genetic analysis of virulence in the human fungal pathogen Cryptococcus neoformans. Cell. 2008;135: 174–188. doi: 10.1016/j.cell.2008.07.046 18854164

52. Billmyre RB, Clancey SA, Li LX, Doering TL, Heitman J. 5-fluorocytosine resistance is associated with hypermutation and alterations in capsule biosynthesis in Cryptococcus. Nat Commun. 2020;11: 127. doi: 10.1038/s41467-019-13890-z 31913284

53. Tran HT, Keen JD, Kricker M, Resnick MA, Gordenin DA. Hypermutability of homonucleotide runs in mismatch repair and DNA polymerase proofreading yeast mutants. Mol Cell Biol. 1997;17: 2859–2865. doi: 10.1128/mcb.17.5.2859 9111358

54. Alani E, Reenan RAG, Kolodner RD. Interaction between mismatch repair and genetic recombination in Saccharomyces cerevisiae. Genetics. 1994;137: 19–39. 8056309

55. Zhai B, Zhu P, Foyle D, Upadhyay S, Idnurm A, Lin X. Congenic strains of the filamentous form of Cryptococcus neoformans for studies of fungal morphogenesis and virulence. Infect Immun. 2013;81: 2626–2637. doi: 10.1128/IAI.00259-13 23670559

56. Fu C, Thielhelm TP, Heitman J. Unisexual reproduction promotes competition for mating partners in the global human fungal pathogen Cryptococcus deneoformans. PLOS Genet. 2019;15: e1008394. doi: 10.1371/journal.pgen.1008394 31536509

57. Hsueh Y-P, Idnurm A, Heitman J. Recombination hotspots flank the Cryptococcus mating-type locus: implications for the evolution of a fungal sex chromosome. PLOS Genet. 2006;2: e184. doi: 10.1371/journal.pgen.0020184 17083277

58. Alspaugh JA, Perfect JR, Heitman J. Cryptococcus neoformans mating and virulence are regulated by the G-protein α subunit GPA1 and cAMP. Genes Dev. 1997;11: 3206–3217. doi: 10.1101/gad.11.23.3206 9389652

59. Idnurm A, Heitman J. Light controls growth and development via a conserved pathway in the fungal kingdom. PLoS Biol. 2005;3: e95. doi: 10.1371/journal.pbio.0030095 15760278

60. Heitman J, Kozel TR, Kwon-Chung KJ, Perfect JR, Casadevall A, editors. Cryptococcus: From Human Pathogen to Model Yeast. Washington, DC: ASM Press; 2011.

61. Li F, Upadhyaya NM, Sperschneider J, Matny O, Nguyen-Phuc H, Mago R, et al. Emergence of the Ug99 lineage of the wheat stem rust pathogen through somatic hybridisation. Nat Commun. 2019;10: 5068. doi: 10.1038/s41467-019-12927-7 31699975

62. Parry EM, Cox BS. The tolerance of aneuploidy in yeast. Genet Res. 1970;16: 333–340. doi: 10.1017/s0016672300002597 5512257

63. Greig D, Borts RH, Louis EJ, Travisano M. Epistasis and hybrid sterility in Saccharomyces. Proc R Soc B Biol Sci. 2002;269: 1167–1171. doi: 10.1098/rspb.2002.1989 12061961

64. Feretzaki M, Heitman J. Genetic circuits that govern bisexual and unisexual reproduction in Cryptococcus neoformans. PLoS Genet. 2013;9: e1003688. doi: 10.1371/journal.pgen.1003688 23966871

65. Lin X, Hull CM, Heitman J. Sexual reproduction between partners of the same mating type in Cryptococcus neoformans. Nature. 2005;434: 1017–1021. doi: 10.1038/nature03448 15846346

66. Vogan AA, Xu J. Evidence for genetic incompatibilities associated with post-zygotic reproductive isolation in the human fungal pathogen Cryptococcus neoformans. Genome. 2014;57: 335–344. doi: 10.1139/gen-2014-0077 25187972

67. Rizki A, Lundblad V. Defects in mismatch repair promote telomerase-independent proliferation. Nature. 2001;411: 713–716. doi: 10.1038/35079641 11395777

68. Yadav V, Sun S, Coelho MA, Heitman J. Centromere scission drives chromosome shuffling and reproductive isolation. Proc Natl Acad Sci. 2020;117: 7917–7928. doi: 10.1073/pnas.1918659117 32193338

69. Sun S, Billmyre RB, Mieczkowski PA, Heitman J. Unisexual reproduction drives meiotic recombination and phenotypic and karyotypic plasticity in Cryptococcus neoformans. PLOS Genet. 2014;10: e1004849. doi: 10.1371/journal.pgen.1004849 25503976

70. Roth C, Sun S, Billmyre RB, Heitman J, Magwene PM. A high-resolution map of meiotic recombination in Cryptococcus deneoformans demonstrates decreased recombination in unisexual reproduction. Genetics. 2018;209: 567–578. doi: 10.1534/genetics.118.300996 29625994

71. Chen W, Jinks-Robertson S. The role of the mismatch repair machinery in regulating mitotic and meiotic recombination between diverged sequences in yeast. Genetics. 1999;151: 1299–1313. 10101158

72. Datta A, Adjiri A, New L, Crouse GF, Jinks-Robertson S. Mitotic crossovers between diverged sequences are regulated by mismatch repair proteins in Saccharomyces cerevisiae. Mol Cell Biol. 1996;16: 1085–1093. doi: 10.1128/mcb.16.3.1085 8622653

73. Datta A, Hendrix M, Lipsitch M, Jinks-Robertson S. Dual roles for DNA sequence identity and the mismatch repair system in the regulation of mitotic crossing-over in yeast. Proc Natl Acad Sci. 1997;94: 9757–9762. doi: 10.1073/pnas.94.18.9757 9275197

74. Elliott B, Jasin M. Repair of double-strand breaks by homologous recombination in mismatch repair-defective mammalian cells. Mol Cell Biol. 2001;21: 2671–2682. doi: 10.1128/MCB.21.8.2671-2682.2001 11283247

75. Anand R, Beach A, Li K, Haber J. Rad51-mediated double-strand break repair and mismatch correction of divergent substrates. Nature. 2017;544: 377–380. doi: 10.1038/nature22046 28405019

76. Peterson SE, Keeney S, Jasin M. Mechanistic insight into crossing over during mouse meiosis ll. Mol Cell. 2020;78: 1252–1263. doi: 10.1016/j.molcel.2020.04.009 32362315

77. Bozdag GO, Ono J, Denton JA, Karakoc E, Hunter N, Leu J-Y, et al. Engineering recombination between diverged yeast species reveals genetic incompatibilities. bioRxiv. 2019. doi: 10.1101/755165

78. Rogers DW, Mcconnell E, Ono J, Greig D. Spore-autonomous fluorescent protein expression identifies meiotic chromosome mis-segregation as the principal cause of hybrid sterility in yeast. PLoS Biol. 2018;16: e2005066. doi: 10.1371/journal.pbio.2005066 30419022

79. Tay YD, Sidebotham JM, Wu L. Mph1 requires mismatch repair-independent and -dependent functions of MutSα to regulate crossover formation during homologous recombination repair. Nucleic Acids Res. 2010;38: 1889–1901. doi: 10.1093/nar/gkp1199 20047969

80. Kwon-Chung KJ, Edman JC, Wickes BL. Genetic association of mating types and virulence in Cryptococcus neoformans. Infect Immun. 1992;60: 602–605. doi: 10.1128/IAI.60.2.602-605.1992 1730495

81. Toffaletti DL, Rude TH, Johnston SA, Durack DT, Perfecrl JR. Gene transfer in Cryptococcus neoformans by use of biolistic delivery of DNA. J Bacteriol. 1993;175: 1405–1411. doi: 10.1128/jb.175.5.1405-1411.1993 8444802

82. Nielsen K, Cox GM, Wang P, Toffaletti DL, Perfect JR, Heitman J. Sexual cycle of Cryptococcus neoformans var. grubii and virulence of congenic a and α Isolates. Infect Immun. 2003;71: 4831–4841. doi: 10.1128/iai.71.9.4831-4841.2003 12933823

83. Radchenko EA, McGinty RJ, Aksenova AY, Neil AJ, Mirkin SM. Quantitative analysis of the rates for repeat-mediated genome instability in a yeast experimental system. Methods Mol Biol. 2018;1672: 421–438. doi: 10.1007/978-1-4939-7306-4_29 29043640

84. Sun S, Priest SJ, Heitman J. Cryptococcus neoformans: mating and genetic crosses. Curr Protoc Microbiol. 2019;53: e75. doi: 10.1002/cpmc.75 30661293

85. Pitkin JW, Panaccione DG, Walton JD. A putative cyclic peptide efflux pump encoded by the TOXA gene of the plant-pathogenic fungus Cochliobolus carbonurn. Microbiology. 1996;142: 1557–1565. doi: 10.1099/13500872-142-6-1557 8704997

86. Hua W, Vogan A, Xu J. Genotypic and phenotypic analyses of two ‘“isogenic”‘ strains of the human fungal pathogen Cryptococcus neoformans var. neoformans. Mycopathologia. 2019;184: 195–212. doi: 10.1007/s11046-019-00328-9 30891668

87. Grabherr MG, Russell P, Meyer M, Mauceli E, Alföldi J, Di Palma F, et al. Genome-wide synteny through highly sensitive sequence alignment: Satsuma. Bioinformatics. 2010;26: 1145–1151. doi: 10.1093/bioinformatics/btq102 20208069

88. Darling ACE, Mau B, Blattner FR, Perna NT. Mauve: multiple alignment of conserved genomic sequence with rearrangements. Genome Res. 2004;14: 1394–1403. doi: 10.1101/gr.2289704 15231754

89. Cabanettes F, Klopp C. D-GENIES: dot plot large genomes in an interactive, efficient and simple way. PeerJ. 2018;6: e4958. doi: 10.7717/peerj.4958 29888139

90. Li H. Minimap2: pairwise alignment for nucleotide sequences. Bioinformatics. 2018;34: 3094–3100. doi: 10.1093/bioinformatics/bty191 29750242

91. Langdon QK, Peris D, Kyle B, Hittinger CT. sppIDer: a species identification tool to investigate hybrid genomes with high-throughput sequencing. Mol Biol Evol. 2018;35: 2835–2849. doi: 10.1093/molbev/msy166 30184140

92. Robinson JT, Thorvaldsdottir H, Winckler W, Guttman M, Lander ES, Getz G, et al. Integrative genomics viewer. Nat Biotechnol. 2011;29: 24–26. doi: 10.1038/nbt.1754 21221095

93. Li H. Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM. arXiv Prepr. 2013; 1303.3997v2.

94. Depristo MA, Banks E, Poplin RE, Garimella K V, Maguire JR, Hartl C, et al. A framework for variation discovery and genotyping using next-generation DNA sequencing data. Nat Genet. 2011;43: 491–498. doi: 10.1038/ng.806 21478889

95. Mckenna A, Hanna M, Banks E, Sivachenko A, Cibulskis K, Kernytsky A, et al. The genome analysis toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res. 2010;20: 1297–1303. doi: 10.1101/gr.107524.110 20644199

96. Cingolani P, Platts A, Wang LL, Coon M, Nguyen T, Wang L, et al. A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff. Fly. 2012;6: 80–92. doi: 10.4161/fly.19695 22728672

97. Koren A, Ben-Aroya S, Steinlauf R, Kupiec M. Pitfalls of the synthetic lethality screen in Saccharomyces cerevisiae: an improved design. Curr Genet. 2003;43: 62–69. doi: 10.1007/s00294-003-0373-8 12684846

98. Paluszynski JP, Klassen R, Meinhardt F. Genetic prerequisites for additive or synergistic actions of 5-fluorocytosine and fluconazole in baker’s yeast. Microbiology. 2008;154: 3154–3164. doi: 10.1099/mic.0.2008/020107-0 18832321

99. Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 2014;30: 2114–2120. doi: 10.1093/bioinformatics/btu170 24695404

100. Pegueroles C, Mixão V, Carrete L, Molina M, Gabaldón T. HaploTypo: a variant-calling pipeline for phased genomes. Bioinformatics. 2020;36: 2569–2571. doi: 10.1093/bioinformatics/btz933 31834373

101. Quinlan AR, Hall IM. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics. 2010;26: 841–842. doi: 10.1093/bioinformatics/btq033 20110278

102. Goodwin TJD, Poulter RTM. The diversity of retrotransposons in the yeast Cryptococcus neoformans. Yeast. 2001;18: 865–880. doi: 10.1002/yea.733 11427969

103. Idnurm A. A tetrad analysis of the basidiomycete fungus Cryptococcus neoformans. Genetics. 2010;185: 153–163. doi: 10.1534/genetics.109.113027 20157004

104. Fraser JA, Huang JC, Pukkila-Worley R, Alspaugh JA, Mitchell TG, Heitman J. Chromosomal translocation and segmental duplication in Cryptococcus neoformans. Eukaryot Cell. 2005;4: 401–406. doi: 10.1128/EC.4.2.401-406.2005 15701802


Článek vyšel v časopise

PLOS Genetics


2021 Číslo 1
Nejčtenější tento týden
Nejčtenější v tomto čísle
Kurzy

Zvyšte si kvalifikaci online z pohodlí domova

Důležitost adherence při depresivním onemocnění
nový kurz
Autoři: MUDr. Eliška Bartečková, Ph.D.

Koncepce osteologické péče pro gynekology a praktické lékaře
Autoři: MUDr. František Šenk

Sekvenční léčba schizofrenie
Autoři: MUDr. Jana Hořínková, Ph.D.

Hypertenze a hypercholesterolémie – synergický efekt léčby
Autoři: prof. MUDr. Hana Rosolová, DrSc.

Multidisciplinární zkušenosti u pacientů s diabetem
Autoři: Prof. MUDr. Martin Haluzík, DrSc., prof. MUDr. Vojtěch Melenovský, CSc., prof. MUDr. Vladimír Tesař, DrSc.

Všechny kurzy
Přihlášení
Zapomenuté heslo

Zadejte e-mailovou adresu, se kterou jste vytvářel(a) účet, budou Vám na ni zaslány informace k nastavení nového hesla.

Přihlášení

Nemáte účet?  Registrujte se