#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Evolution of Ty1 copy number control in yeast by horizontal transfer and recombination


Autoři: Wioletta Czaja aff001;  Douda Bensasson aff002;  Hyo Won Ahn aff001;  David J. Garfinkel aff001;  Casey M. Bergman aff003
Působiště autorů: Department of Biochemistry and Molecular Biology, University of Georgia, Athens, Georgia, United States of America aff001;  Institute of Bioinformatics and Department of Plant Biology, University of Georgia, Athens, Georgia, United States of America aff002;  Institute of Bioinformatics and Department of Genetics, University of Georgia, Athens, Georgia, United States of America aff003
Vyšlo v časopise: Evolution of Ty1 copy number control in yeast by horizontal transfer and recombination. PLoS Genet 16(2): e32767. doi:10.1371/journal.pgen.1008632
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pgen.1008632

Souhrn

Transposable elements constitute a large fraction of most eukaryotic genomes. Insertion of mobile DNA sequences typically has deleterious effects on host fitness, and thus diverse mechanisms have evolved to control mobile element proliferation. Mobility of the Ty1 retrotransposon in Saccharomyces yeasts is regulated by copy number control (CNC) mediated by a self-encoded restriction factor derived from the Ty1 gag capsid gene that inhibits virus-like particle function. Here, we survey a panel of wild and human-associated strains of S. cerevisiae and S. paradoxus to investigate how genomic Ty1 content influences variation in Ty1 mobility. We observe high levels of mobility for a tester element with a gag sequence from the canonical Ty1 subfamily in permissive strains that either lack full-length Ty1 elements or only contain full-length copies of the Ty1’ subfamily that have a divergent gag sequence. In contrast, low levels of canonical Ty1 mobility are observed in restrictive strains carrying full-length Ty1 elements containing a canonical gag sequence. Phylogenomic analysis of full-length Ty1 elements revealed that Ty1’ is the ancestral subfamily present in wild strains of S. cerevisiae, and that canonical Ty1 in S. cerevisiae is a derived subfamily that acquired gag from S. paradoxus by horizontal transfer and recombination. Our results provide evidence that variation in the ability of S. cerevisiae and S. paradoxus strains to repress canonical Ty1 transposition via CNC is regulated by the genomic content of different Ty1 subfamilies, and that self-encoded forms of transposon control can spread across species boundaries by horizontal transfer.

Klíčová slova:

Multiple alignment calculation – Phylogenetic analysis – Phylogenetics – Saccharomyces cerevisiae – Sequence alignment – Sequence analysis – Transposable elements – Gag genes


Zdroje

1. Chenais B, Caruso A, Hiard S, Casse N. The impact of transposable elements on eukaryotic genomes: from genome size increase to genetic adaptation to stressful environments. Gene. 2012;509: 7–15. doi: 10.1016/j.gene.2012.07.042 22921893

2. Mita P, Boeke JD. How retrotransposons shape genome regulation. Curr Opin Genet Dev. 2016;37: 90–100. doi: 10.1016/j.gde.2016.01.001 26855260

3. Voytas DF, Boeke JD. Ty1 and Ty5 of Saccharomyces cerevisiae. 2002; 631–662. doi: 10.1128/9781555817954.ch26

4. Curcio MJ, Lutz S, Lesage P. The Ty1 LTR-retrotransposon of budding yeast, Saccharomyces cerevisiae. Microbiol Spectr. 2015;3: 1–35.

5. Sandmeyer S, Patterson K, Bilanchone V. Ty3, a position-specific retrotransposon in budding yeast. Microbiol Spectr. 2015;3: MDNA3-0057–2014. doi: 10.1128/microbiolspec.MDNA3-0057-2014 26104707

6. Goffeau A, Barrell BG, Bussey H, Davis RW, Dujon B, Feldmann H, et al. Life with 6000 genes. Science. 1996;274: 546, 563–7. doi: 10.1126/science.274.5287.546 8849441

7. Kim JM, Vanguri S, Boeke JD, Gabriel A, Voytas DF. Transposable elements and genome organization: a comprehensive survey of retrotransposons revealed by the complete Saccharomyces cerevisiae genome sequence. Genome Res. 1998;8: 464–478. doi: 10.1101/gr.8.5.464 9582191

8. Jordan IK, McDonald JF. Evidence for the role of recombination in the regulatory evolution of Saccharomyces cerevisiae Ty elements. Journal of Molecular Evolution. 1998;47: 14–20. doi: 10.1007/pl00006358 9664692

9. Jordan IK, McDonald JF. Tempo and mode of Ty element evolution in Saccharomyces cerevisiae. Genetics. 1999;151: 1341–51. 10101161

10. Promislow DE, Jordan IK, McDonald JF. Genomic demography: a life-history analysis of transposable element evolution. Proc Biol Sci. 1999;266: 1555–60. doi: 10.1098/rspb.1999.0815 10467744

11. Neuveglise C, Feldmann H, Bon E, Gaillardin C, Casaregola S. Genomic evolution of the long terminal repeat retrotransposons in hemiascomycetous yeasts. Genome Research. 2002;12: 930–43. doi: 10.1101/gr.219202 12045146

12. Liti G, Carter DM, Moses AM, Warringer J, Parts L, James SA, et al. Population genomics of domestic and wild yeasts. Nature. 2009;458: 337–41. doi: 10.1038/nature07743 19212322

13. Carr M, Bensasson D, Bergman CM. Evolutionary genomics of transposable elements in Saccharomyces cerevisiae. PLoS ONE. 2012;7: e50978. doi: 10.1371/journal.pone.0050978 23226439

14. Bleykasten-Grosshans C, Friedrich A, Schacherer J. Genome-wide analysis of intraspecific transposon diversity in yeast. BMC Genomics. 2013;14: 399. doi: 10.1186/1471-2164-14-399 23768249

15. Menconi G, Battaglia G, Grossi R, Pisanti N, Marangoni R. Mobilomics in Saccharomyces cerevisiae strains. BMC Bioinformatics. 2013;14: 102. doi: 10.1186/1471-2105-14-102 23514613

16. Istace B, Friedrich A, d’Agata L, Faye S, Payen E, Beluche O, et al. De novo assembly and population genomic survey of natural yeast isolates with the Oxford Nanopore MinION sequencer. Gigascience. 2017;6: 1–13. doi: 10.1093/gigascience/giw018 28369459

17. Nelson MG, Linheiro RS, Bergman CM. McClintock: an integrated pipeline for detecting transposable element insertions in whole-genome shotgun sequencing data. G3. 2017;7: 2749–2762. doi: 10.1534/g3.117.040915

18. Yue J-X, Li J, Aigrain L, Hallin J, Persson K, Oliver K, et al. Contrasting evolutionary genome dynamics between domesticated and wild yeasts. Nat Genet. 2017;49: 913–924. doi: 10.1038/ng.3847 28416820

19. Bergman CM. Horizontal transfer and proliferation of Tsu4 in Saccharomyces paradoxus. Mobile DNA. 2018;9: 18. doi: 10.1186/s13100-018-0122-7 29942366

20. Peter J, Chiara MD, Friedrich A, Yue J-X, Pflieger D, Bergstrom A, et al. Genome evolution across 1,011 Saccharomyces cerevisiae isolates. Nature. 2018;556: 339–344. doi: 10.1038/s41586-018-0030-5 29643504

21. Wilke CM, Maimer E, Adams J. The population biology and evolutionary significance of Ty elements in Saccharomyces cerevisiae. Genetica. 1992;86: 155–73. doi: 10.1007/bf00133718 1334907

22. Liti G, Peruffo A, James SA, Roberts IN, Louis EJ. Inferences of evolutionary relationships from a population survey of LTR-retrotransposons and telomeric-associated sequences in the Saccharomyces sensu stricto complex. Yeast. 2005;22: 177–92. doi: 10.1002/yea.1200 15704235

23. Jordan IK, McDonald JF. Phylogenetic perspective reveals abundant Ty1/Ty2 hybrid elements in the Saccharomyces cerevisiae genome. Mol Biol Evol. 1999;16: 419–422. doi: 10.1093/oxfordjournals.molbev.a026123 10331268

24. Bridier-Nahmias A, Tchalikian-Cosson A, Baller JA, Menouni R, Fayol H, Flores A, et al. Retrotransposons. An RNA polymerase III subunit determines sites of retrotransposon integration. Science. 2015;348: 585–588. doi: 10.1126/science.1259114 25931562

25. Cheung S, Ma L, Chan PHW, Hu H-L, Mayor T, Chen H-T, et al. Ty1 Integrase Interacts with RNA Polymerase III-specific Subcomplexes to Promote Insertion of Ty1 Elements Upstream of Polymerase (Pol) III-transcribed Genes. J Biol Chem. 2016;291: 6396–6411. doi: 10.1074/jbc.M115.686840 26797132

26. Friedli M, Trono D. The developmental control of transposable elements and the evolution of higher species. Annu Rev Cell Dev Biol. 2015;31: 429–451. doi: 10.1146/annurev-cellbio-100814-125514 26393776

27. Goodier JL. Restricting retrotransposons: a review. Mob DNA. 2016;7: 16. doi: 10.1186/s13100-016-0070-z 27525044

28. Drinnenberg IA, Weinberg DE, Xie KT, Mower JP, Wolfe KH, Fink GR, et al. RNAi in budding yeast. Science. 2009;326: 544–550. doi: 10.1126/science.1176945 19745116

29. Shen X-X, Opulente DA, Kominek J, Zhou X, Steenwyk JL, Buh KV, et al. Tempo and Mode of Genome Evolution in the Budding Yeast Subphylum. Cell. 2018;175: 1533–1545.e20. doi: 10.1016/j.cell.2018.10.023 30415838

30. Garfinkel DJ, Nyswaner K, Wang J, Cho J-Y. Post-transcriptional cosuppression of Ty1 retrotransposition. Genetics. 2003;165: 83–99. 14504219

31. Garfinkel DJ, Tucker JM, Saha A, Nishida Y, Pachulska-Wieczorek K, Błaszczyk L, et al. A self-encoded capsid derivative restricts Ty1 retrotransposition in Saccharomyces. Curr Genet. 2016;62: 321–329. doi: 10.1007/s00294-015-0550-6 26650614

32. Saha A, Mitchell JA, Nishida Y, Hildreth JE, Ariberre JA, Gilbert WV, et al. A trans-dominant form of Gag restricts Ty1 retrotransposition and mediates copy number control. J Virol. 2015;89: 3922–3938. doi: 10.1128/JVI.03060-14 25609815

33. Ahn HW, Tucker JM, Arribere JA, Garfinkel DJ. Ribosome biogenesis modulates Ty1 copy number control in Saccharomyces cerevisiae. Genetics. 2017;207: 1441–1456. doi: 10.1534/genetics.117.300388 29046400

34. Nishida Y, Pachulska-Wieczorek K, Błaszczyk L, Saha A, Gumna J, Garfinkel DJ, et al. Ty1 retrovirus-like element Gag contains overlapping restriction factor and nucleic acid chaperone functions. Nucleic Acids Res. 2015;43: 7414–7431. doi: 10.1093/nar/gkv695 26160887

35. Tucker JM, Larango ME, Wachsmuth LP, Kannan N, Garfinkel DJ. The Ty1 Retrotransposon Restriction Factor p22 Targets Gag. PLOS Genet. 2015;11: e1005571. doi: 10.1371/journal.pgen.1005571 26451601

36. Tucker JM, Garfinkel DJ. Ty1 escapes restriction by the self-encoded factor p22 through mutations in capsid. Mobile Genetic Elements. 2016;6: e1154639. doi: 10.1080/2159256X.2016.1154639 27141327

37. Moore SP, Liti G, Stefanisko KM, Nyswaner KM, Chang C, Louis EJ, et al. Analysis of a Ty1-less variant of Saccharomyces paradoxus: the gain and loss of Ty1 elements. Yeast. 2004;21: 649–60. doi: 10.1002/yea.1129 15197730

38. Garfinkel DJ. Genome evolution mediated by Ty elements in Saccharomyces. Cytogenet Genome Res. 2005;110: 63–9. doi: 10.1159/000084939 16093659

39. Curcio MJ, Garfinkel DJ. Single-step selection for Ty1 element retrotransposition. Proc Natl Acad Sci USA. 1991;88: 936–940. doi: 10.1073/pnas.88.3.936 1846969

40. Atwood A, Choi J, Levin HL. The application of a homologous recombination assay revealed amino acid residues in an LTR-retrotransposon that were critical for integration. J Virol. 1998;72: 1324–1333. 9445033

41. Curcio MJ, Kenny AE, Moore S, Garfinkel DJ, Weintraub M, Gamache ER, et al. S-phase checkpoint pathways stimulate the mobility of the retrovirus-like transposon Ty1. Mol Cell Biol. 2007;27: 8874–8885. doi: 10.1128/MCB.01095-07 17923678

42. Khatri I, Tomar R, Ganesan K, Prasad GS, Subramanian S. Complete genome sequence and comparative genomics of the probiotic yeast Saccharomyces boulardii. Sci Rep. 2017;7: 371. doi: 10.1038/s41598-017-00414-2 28336969

43. Naseeb S, Alsammar H, Burgis T, Donaldson I, Knyazev N, Knight C, et al. Whole genome sequencing, de novo assembly and phenotypic profiling for the new budding yeast species Saccharomyces jurei. G3. 2018;8: 2967–2977. doi: 10.1534/g3.118.200476 30097472

44. Cubillos FA, Louis EJ, Liti G. Generation of a large set of genetically tractable haploid and diploid Saccharomyces strains. FEMS Yeast Research. 2009;9: 1217–1225. doi: 10.1111/j.1567-1364.2009.00583.x 19840116

45. Boeke JD, Garfinkel DJ, Styles CA, Fink GR. Ty elements transpose through an RNA intermediate. Cell. 1985;40: 491–500. doi: 10.1016/0092-8674(85)90197-7 2982495

46. Garfinkel DJ, Boeke JD, Fink GR. Ty element transposition: reverse transcriptase and virus-like particles. Cell. 1985;42: 507–517. doi: 10.1016/0092-8674(85)90108-4 2411424

47. Boeke JD, Eichinger D, Castrillon D, Fink GR. The Saccharomyces cerevisiae genome contains functional and nonfunctional copies of transposon Ty1. Mol Cell Biol. 1988;8: 1432–1442. doi: 10.1128/mcb.8.4.1432 2837641

48. Sharon G, Burkett TJ, Garfinkel DJ. Efficient homologous recombination of Ty1 element cDNA when integration is blocked. Mol Cell Biol. 1994;14: 6540–6551. doi: 10.1128/mcb.14.10.6540 7523854

49. Almeida P, Barbosa R, Zalar P, Imanishi Y, Shimizu K, Turchetti B, et al. A population genomics insight into the Mediterranean origins of wine yeast domestication. Mol Ecol. 2015;24: 5412–5427. doi: 10.1111/mec.13341 26248006

50. Diezmann S, Dietrich FS. Saccharomyces cerevisiae: Population Divergence and Resistance to Oxidative Stress in Clinical, Domesticated and Wild Isolates. PLOS ONE. 2009;4: e5317. doi: 10.1371/journal.pone.0005317 19390633

51. Kellis M, Patterson N, Endrizzi M, Birren B, Lander ES. Sequencing and comparison of yeast species to identify genes and regulatory elements. Nature. 2003;423: 241–54. doi: 10.1038/nature01644 12748633

52. Belcourt MF, Farabaugh PJ. Ribosomal frameshifting in the yeast retrotransposon Ty: tRNAs induce slippage on a 7 nucleotide minimal site. Cell. 1990;62: 339–352. doi: 10.1016/0092-8674(90)90371-k 2164889

53. Matsuda E, Garfinkel DJ. Posttranslational interference of Ty1 retrotransposition by antisense RNAs. PNAS. 2009;106: 15657–15662. doi: 10.1073/pnas.0908305106 19721006

54. Liti G, Ba ANN, Blythe M, Müller CA, Bergström A, Cubillos FA, et al. High quality de novo sequencing and assembly of the Saccharomyces arboricolus genome. BMC Genomics. 2013;14: 69. doi: 10.1186/1471-2164-14-69 23368932

55. Best S, Le Tissier P, Towers G, Stoye JP. Positional cloning of the mouse retrovirus restriction gene Fv1. Nature. 1996;382: 826–829. doi: 10.1038/382826a0 8752279

56. Murcia PR, Arnaud F, Palmarini M. The transdominant endogenous retrovirus enJS56A1 associates with and blocks intracellular trafficking of Jaagsiekte sheep retrovirus Gag. J Virol. 2007;81: 1762–1772. doi: 10.1128/JVI.01859-06 17135320

57. Morillon A, Bénard L, Springer M, Lesage P. Differential Effects of Chromatin and Gcn4 on the 50-Fold Range of Expression among Individual Yeast Ty1 Retrotransposons. Molecular and Cellular Biology. 2002;22: 2078–2088. doi: 10.1128/MCB.22.7.2078-2088.2002 11884596

58. Liti G, Barton DBH, Louis EJ. Sequence diversity, reproductive isolation and species concepts in Saccharomyces. Genetics. 2006;174: 839–850. doi: 10.1534/genetics.106.062166 16951060

59. Doniger SW, Kim HS, Swain D, Corcuera D, Williams M, Yang S-P, et al. A catalog of neutral and deleterious polymorphism in yeast. PLoS Genet. 2008;4: e1000183. doi: 10.1371/journal.pgen.1000183 18769710

60. Strope PK, Skelly DA, Kozmin SG, Mahadevan G, Stone EA, Magwene PM, et al. The 100-genomes strains, an S. cerevisiae resource that illuminates its natural phenotypic and genotypic variation and emergence as an opportunistic pathogen. Genome Res. 2015;25: 762–774. doi: 10.1101/gr.185538.114 25840857

61. Barbosa R, Almeida P, Safar SVB, Santos RO, Morais PB, Nielly-Thibault L, et al. Evidence of natural hybridization in Brazilian wild lineages of Saccharomyces cerevisiae. Genome Biol Evol. 2016;8: 317–329. doi: 10.1093/gbe/evv263 26782936

62. Almeida P, Barbosa R, Bensasson D, Goncalves P, Sampaio JP. Adaptive divergence in wine yeasts and their wild relatives suggests a prominent role for introgressions and rapid evolution at noncoding sites. Mol Ecol. 2017;26: 2167–2182. doi: 10.1111/mec.14071 28231394

63. Fay JC, Liu P, Ong GT, Dunham MJ, Cromie GA, Jeffery EW, et al. A polyploid admixed origin of beer yeasts derived from European and Asian wine populations. PLOS Biology. 2019;17: e3000147. doi: 10.1371/journal.pbio.3000147 30835725

64. Wang Q-M, Liu W-Q, Liti G, Wang S-A, Bai F-Y. Surprisingly diverged populations of Saccharomyces cerevisiae in natural environments remote from human activity. Mol Ecol. 2012;21: 5404–5417. doi: 10.1111/j.1365-294X.2012.05732.x

65. Skelly DA, Merrihew GE, Riffle M, Connelly CF, Kerr EO, Johansson M, et al. Integrative phenomics reveals insight into the structure of phenotypic diversity in budding yeast. Genome Res. 2013;23: 1496–1504. doi: 10.1101/gr.155762.113 23720455

66. Bergstrom A, Simpson JT, Salinas F, Barre B, Parts L, Zia A, et al. A high-definition view of functional genetic variation from natural yeast genomes. Mol Biol Evol. 2014;31: 872–888. doi: 10.1093/molbev/msu037 24425782

67. Marsit S, Mena A, Bigey F, Sauvage F-X, Couloux A, Guy J, et al. Evolutionary advantage conferred by an eukaryote-to-eukaryote gene transfer event in wine yeasts. Mol Biol Evol. 2015;32: 1695–1707. doi: 10.1093/molbev/msv057 25750179

68. Song G, Dickins BJA, Demeter J, Engel S, Gallagher J, Choe K, et al. AGAPE (Automated Genome Analysis PipelinE) for pan-genome analysis of Saccharomyces cerevisiae. PLoS ONE. 2015;10: e0120671. doi: 10.1371/journal.pone.0120671 25781462

69. Barbosa R, Pontes A, Santos RO, Montandon GG, de Ponzzes-Gomes CM, Morais PB, et al. Multiple Rounds of Artificial Selection Promote Microbe Secondary Domestication—The Case of Cachaça Yeasts. Genome Biol Evol. 2018;10: 1939–1955. doi: 10.1093/gbe/evy132 29982460

70. Duan S-F, Han P-J, Wang Q-M, Liu W-Q, Shi J-Y, Li K, et al. The origin and adaptive evolution of domesticated populations of yeast from Far East Asia. Nature Communications. 2018;9: 2690. doi: 10.1038/s41467-018-05106-7 30002370

71. Kang K, Bergdahl B, Machado D, Dato L, Han T-L, Li J, et al. Linking genetic, metabolic, and phenotypic diversity among Saccharomyces cerevisiae strains using multi-omics associations. Gigascience. 2019;8: giz015. doi: 10.1093/gigascience/giz015 30715293

72. Ramazzotti M, Stefanini I, Paola MD, Filippo CD, Rizzetto L, Berná L, et al. Population genomics reveals evolution and variation of Saccharomyces cerevisiae in the human and insects gut. Environmental Microbiology. 2019;21: 50–71. doi: 10.1111/1462-2920.14422 30246283

73. Alani E, Cao L, Kleckner N. A method for gene disruption that allows repeated use of URA3 selection in the construction of multiply disrupted yeast strains. Genetics. 1987;116: 541–545. doi: 10.1534/genetics.112.541.test 3305158

74. Voth WP, Jiang YW, Stillman DJ. New “marker swap” plasmids for converting selectable markers on budding yeast gene disruptions and plasmids. Yeast. 2003;20: 985–993. doi: 10.1002/yea.1018 12898713

75. Lee BS, Lichtenstein CP, Faiola B, Rinckel LA, Wysock W, Curcio MJ, et al. Posttranslational inhibition of Ty1 retrotransposition by nucleotide excision repair/transcription factor TFIIH subunits Ssl2p and Rad3p. Genetics. 1998;148: 1743–1761. 9560391

76. Guthrie C, Fink GR, editors. Guide to yeast genetics and molecular biology. Spi edition. San Diego, Calif.: Academic Press; 1991.

77. Gietz RD, Schiestl RH. High-efficiency yeast transformation using the LiAc/SS carrier DNA/PEG method. Nat Protoc. 2007;2: 31–34. doi: 10.1038/nprot.2007.13 17401334

78. Gietz RD, Schiestl RH. Quick and easy yeast transformation using the LiAc/SS carrier DNA/PEG method. Nat Protoc. 2007;2: 35–37. doi: 10.1038/nprot.2007.14 17401335

79. Curcio MJ, Hedge A-M, Boeke JD, Garfinkel DJ. Ty RNA levels determine the spectrum of retrotransposition events that activate gene expression in Saccharomyces cerevisiae. Molec Gen Genet. 1990;220: 213–221. doi: 10.1007/bf00260484 2157950

80. Castellon-Vogel MA, Menawat AS. A method to disperse aggregates of a flocculent yeast for photometric analysis. Biotechnol Prog. 1990;6: 135–141. doi: 10.1021/bp00002a007

81. Rhoads A, Au KF. PacBio Sequencing and Its Applications. Genomics, Proteomics & Bioinformatics. 2015;13: 278–289. doi: 10.1016/j.gpb.2015.08.002 26542840

82. Gurevich A, Saveliev V, Vyahhi N, Tesler G. QUAST: quality assessment tool for genome assemblies. Bioinformatics. 2013;29: 1072–1075. doi: 10.1093/bioinformatics/btt086 23422339

83. Kurtz S, Phillippy A, Delcher AL, Smoot M, Shumway M, Antonescu C, et al. Versatile and open software for comparing large genomes. Genome Biol. 2004;5: R12. doi: 10.1186/gb-2004-5-2-r12 14759262

84. 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

85. Katoh K, Kuma K, Toh H, Miyata T. MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Res. 2005;33: 511–8. doi: 10.1093/nar/gki198 15661851

86. Gouy M, Guindon S, Gascuel O. SeaView version 4: A multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Mol Biol Evol. 2010;27: 221–4. doi: 10.1093/molbev/msp259 19854763

87. Schliep KP. phangorn: phylogenetic analysis in R. Bioinformatics. 2011;27: 592–593. doi: 10.1093/bioinformatics/btq706 21169378

88. Brown SDJ, Collins RA, Boyer S, Lefort M-C, Malumbres‐Olarte J, Vink CJ, et al. Spider: An R package for the analysis of species identity and evolution, with particular reference to DNA barcoding. Molecular Ecology Resources. 2012;12: 562–565. doi: 10.1111/j.1755-0998.2011.03108.x 22243808

89. Gascuel O. BIONJ: an improved version of the NJ algorithm based on a simple model of sequence data. Mol Biol Evol. 1997;14: 685–695. doi: 10.1093/oxfordjournals.molbev.a025808 9254330

90. Paradis E, Claude J, Strimmer K. APE: Analyses of phylogenetics and evolution in R language. Bioinformatics. 2004;20: 289–290. doi: 10.1093/bioinformatics/btg412 14734327

91. Bryant D, Moulton V. Neighbor-Net: An Agglomerative Method for the Construction of Phylogenetic Networks. Mol Biol Evol. 2004;21: 255–265. doi: 10.1093/molbev/msh018 14660700

92. Huson DH, Bryant D. Application of phylogenetic networks in evolutionary studies. Mol Biol Evol. 2006;23: 254–267. doi: 10.1093/molbev/msj030 16221896

93. Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics. 2014;30: 1312–1313. doi: 10.1093/bioinformatics/btu033 24451623

94. Loytynoja A, Goldman N. Phylogeny-aware gap placement prevents errors in sequence alignment and evolutionary analysis. Science. 2008;320: 1632–1635. doi: 10.1126/science.1158395 18566285

95. Yang Z. PAML 4: Phylogenetic Analysis by Maximum Likelihood. Mol Biol Evol. 2007;24: 1586–1591. doi: 10.1093/molbev/msm088 17483113

96. Huerta-Cepas J, Serra F, Bork P. ETE 3: Reconstruction, analysis, and visualization of phylogenomic data. Mol Biol Evol. 2016;33: 1635–1638. doi: 10.1093/molbev/msw046 26921390

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

98. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, et al. The Sequence Alignment/Map format and SAMtools. Bioinformatics. 2009;25: 2078–2079. doi: 10.1093/bioinformatics/btp352 19505943

99. Wickham H. ggplot2: Elegant Graphics for Data Analysis. 2nd ed. Springer International Publishing; 2016. doi: 10.1007/978-3-319-24277-4


Článek vyšel v časopise

PLOS Genetics


2020 Číslo 2
Nejčtenější tento týden
Nejčtenější v tomto čísle
Kurzy

Zvyšte si kvalifikaci online z pohodlí domova

Hypertenze a hypercholesterolémie – synergický efekt léčby
nový kurz
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.

Úloha kombinovaných preparátů v léčbě arteriální hypertenze
Autoři: prof. MUDr. Martin Haluzík, DrSc.

Halitóza
Autoři: MUDr. Ladislav Korábek, CSc., MBA

Terapie roztroušené sklerózy v kostce
Autoři: MUDr. Dominika Šťastná, Ph.D.

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

#ADS_BOTTOM_SCRIPTS#