Long transposon-rich centromeres in an oomycete reveal divergence of centromere features in Stramenopila-Alveolata-Rhizaria lineages


Autoři: Yufeng Fang aff001;  Marco A. Coelho aff001;  Haidong Shu aff002;  Klaas Schotanus aff001;  Bhagya C. Thimmappa aff003;  Vikas Yadav aff001;  Han Chen aff002;  Ewa P. Malc aff004;  Jeremy Wang aff004;  Piotr A. Mieczkowski aff004;  Brent Kronmiller aff005;  Brett M. Tyler aff005;  Kaustuv Sanyal aff003;  Suomeng Dong aff002;  Minou Nowrousian aff006;  Joseph Heitman aff001
Působiště autorů: Department of Molecular Genetics and Microbiology, Duke University Medical Center, Durham, North Carolina, United States of America aff001;  College of Plant Protection, Nanjing Agricultural University, Nanjing, China aff002;  Molecular Biology and Genetics Unit, Jawaharlal Nehru Centre for Advanced Scientific Research, Bangalore, India aff003;  Department of Genetics, University of North Carolina, Chapel Hill, North Carolina, United States of America aff004;  Center for Genome Research and Biocomputing and Department of Botany and Plant Pathology, Oregon State University, Corvallis, Oregon, United States of America aff005;  Lehrstuhl fuer Molekulare und Zellulaere Botanik, Ruhr-Universitaet Bochum, Bochum, Germany aff006
Vyšlo v časopise: Long transposon-rich centromeres in an oomycete reveal divergence of centromere features in Stramenopila-Alveolata-Rhizaria lineages. PLoS Genet 16(3): e32767. doi:10.1371/journal.pgen.1008646
Kategorie: Research Article
doi: 10.1371/journal.pgen.1008646

Souhrn

Centromeres are chromosomal regions that serve as platforms for kinetochore assembly and spindle attachments, ensuring accurate chromosome segregation during cell division. Despite functional conservation, centromere DNA sequences are diverse and often repetitive, making them challenging to assemble and identify. Here, we describe centromeres in an oomycete Phytophthora sojae by combining long-read sequencing-based genome assembly and chromatin immunoprecipitation for the centromeric histone CENP-A followed by high-throughput sequencing (ChIP-seq). P. sojae centromeres cluster at a single focus at different life stages and during nuclear division. We report an improved genome assembly of the P. sojae reference strain, which enabled identification of 15 enriched CENP-A binding regions as putative centromeres. By focusing on a subset of these regions, we demonstrate that centromeres in P. sojae are regional, spanning 211 to 356 kb. Most of these regions are transposon-rich, poorly transcribed, and lack the histone modification H3K4me2 but are embedded within regions with the heterochromatin marks H3K9me3 and H3K27me3. Strikingly, we discovered a Copia-like transposon (CoLT) that is highly enriched in the CENP-A chromatin. Similar clustered elements are also found in oomycete relatives of P. sojae, and may be applied as a criterion for prediction of oomycete centromeres. This work reveals a divergence of centromere features in oomycetes as compared to other organisms in the Stramenopila-Alveolata-Rhizaria (SAR) supergroup including diatoms and Plasmodium falciparum that have relatively short and simple regional centromeres. Identification of P. sojae centromeres in turn also advances the genome assembly.

Klíčová slova:

Centromeres – Genomic libraries – Heterochromatin – Multiple alignment calculation – Oomycetes – Sequence alignment – Sequence assembly tools – Transposable elements


Zdroje

1. Kursel LE, Malik HS. Centromeres. Curr Biol. 2016;26(12):R487–R90. Epub 2016/06/22. doi: 10.1016/j.cub.2016.05.031 27326706.

2. Stimpson KM, Sullivan BA. Epigenomics of centromere assembly and function. Curr Opin Cell Biol. 2010;22(6):772–80. Epub 2010/08/03. doi: 10.1016/j.ceb.2010.07.002 20675111.

3. Buscaino A, Allshire R, Pidoux A. Building centromeres: home sweet home or a nomadic existence? Curr Opin Genet Dev. 2010;20(2):118–26. Epub 2010/03/09. doi: 10.1016/j.gde.2010.01.006 20206496.

4. Wang N, Dawe RK. Centromere size and its relationship to haploid formation in plants. Mol Plant. 2018;11(3):398–406. Epub 2017/12/27. doi: 10.1016/j.molp.2017.12.009 29277426.

5. Black BE, Foltz DR, Chakravarthy S, Luger K, Woods VL Jr, Cleveland DW. Structural determinants for generating centromeric chromatin. Nature. 2004;430(6999):578–82. Epub 2004/07/30. doi: 10.1038/nature02766 15282608.

6. Guse A, Carroll CW, Moree B, Fuller CJ, Straight AF. In vitro centromere and kinetochore assembly on defined chromatin templates. Nature. 2011;477(7364):354–8. Epub 2011/08/30. doi: 10.1038/nature10379 21874020.

7. Steiner FA, Henikoff S. Holocentromeres are dispersed point centromeres localized at transcription factor hotspots. Elife. 2014;3:e02025. Epub 2014/04/10. doi: 10.7554/eLife.02025 24714495.

8. Comai L, Maheshwari S, Marimuthu MPA. Plant centromeres. Curr Opin Plant Biol. 2017;36:158–67. Epub 2017/04/16. doi: 10.1016/j.pbi.2017.03.003 28411416.

9. McNulty SM, Sullivan BA. Alpha satellite DNA biology: finding function in the recesses of the genome. Chromosome Res. 2018;26(3):115–38. Epub 2018/07/06. doi: 10.1007/s10577-018-9582-3 29974361.

10. Jin W, Melo JR, Nagaki K, Talbert PB, Henikoff S, Dawe RK, et al. Maize centromeres: organization and functional adaptation in the genetic background of oat. Plant Cell. 2004;16(3):571–81. Epub 2004/02/20. doi: 10.1105/tpc.018937 14973167.

11. Smith KM, Galazka JM, Phatale PA, Connolly LR, Freitag M. Centromeres of filamentous fungi. Chromosome Res. 2012;20(5):635–56. Epub 2012/07/04. doi: 10.1007/s10577-012-9290-3 22752455.

12. Yadav V, Sreekumar L, Guin K, Sanyal K. Five pillars of centromeric chromatin in fungal pathogens. PLoS Pathog. 2018;14(8):e1007150. Epub 2018/08/24. doi: 10.1371/journal.ppat.1007150 30138484.

13. Yadav V, Sun S, Billmyre RB, Thimmappa BC, Shea T, Lintner R, et al. RNAi is a critical determinant of centromere evolution in closely related fungi. Proc Natl Acad Sci U S A. 2018;115(12):3108–13. Epub 2018/03/07. doi: 10.1073/pnas.1713725115 29507212.

14. Smith KM, Phatale PA, Sullivan CM, Pomraning KR, Freitag M. Heterochromatin is required for normal distribution of Neurospora crassa CenH3. Mol Cell Biol. 2011;31(12):2528–42. Epub 2011/04/21. doi: 10.1128/MCB.01285-10 21505064.

15. Schotanus K, Soyer JL, Connolly LR, Grandaubert J, Happel P, Smith KM, et al. Histone modifications rather than the novel regional centromeres of Zymoseptoria tritici distinguish core and accessory chromosomes. Epigenet Chromatin. 2015;8(1):41. Epub 2015/10/03. doi: 10.1186/s13072-015-0033-5 26430472.

16. Sanyal K, Baum M, Carbon J. Centromeric DNA sequences in the pathogenic yeast Candida albicans are all different and unique. Proc Natl Acad Sci U S A. 2004;101(31):11374–9. Epub 2004/07/24. doi: 10.1073/pnas.0404318101 15272074.

17. Hoeijmakers WA, Flueck C, Francoijs KJ, Smits AH, Wetzel J, Volz JC, et al. Plasmodium falciparum centromeres display a unique epigenetic makeup and cluster prior to and during schizogony. Cell Microbiol. 2012;14(9):1391–401. Epub 2012/04/18. doi: 10.1111/j.1462-5822.2012.01803.x 22507744.

18. Diner RE, Noddings CM, Lian NC, Kang AK, McQuaid JB, Jablanovic J, et al. Diatom centromeres suggest a mechanism for nuclear DNA acquisition. Proc Natl Acad Sci U S A. 2017;114(29):E6015–E24. Epub 2017/07/05. doi: 10.1073/pnas.1700764114 28673987.

19. Brooks CF, Francia ME, Gissot M, Croken MM, Kim K, Striepen B. Toxoplasma gondii sequesters centromeres to a specific nuclear region throughout the cell cycle. Proc Natl Acad Sci U S A. 2011;108(9):3767–72. Epub 2011/02/16. doi: 10.1073/pnas.1006741108 21321216.

20. Yadav V, Yang F, Reza MH, Liu S, Valent B, Sanyal K, et al. Cellular dynamics and genomic identity of centromeres in cereal blast fungus. mBio. 2019;10(4):e01581–19. Epub 2019/08/01. doi: 10.1128/mBio.01581-19 31363034.

21. Navarro-Mendoza MI, Perez-Arques C, Panchal S, Nicolas FE, Mondo SJ, Ganguly P, et al. Early diverging fungus Mucor circinelloides lacks centromeric histone CENP-A and displays a mosaic of point and regional centromeres. Curr Biol. 2019;29(22):3791–802 e6. Epub 2019/11/05. doi: 10.1016/j.cub.2019.09.024 31679929.

22. Chang CH, Chavan A, Palladino J, Wei X, Martins NMC, Santinello B, et al. Islands of retroelements are major components of Drosophila centromeres. PLoS Biol. 2019;17(5):e3000241. Epub 2019/05/16. doi: 10.1371/journal.pbio.3000241 31086362.

23. Lan T, Renner T, Ibarra-Laclette E, Farr KM, Chang TH, Cervantes-Perez SA, et al. Long-read sequencing uncovers the adaptive topography of a carnivorous plant genome. Proc Natl Acad Sci U S A. 2017;114(22):E4435–E41. Epub 2017/05/17. doi: 10.1073/pnas.1702072114 28507139.

24. Jain M, Olsen HE, Turner DJ, Stoddart D, Bulazel KV, Paten B, et al. Linear assembly of a human centromere on the Y chromosome. Nat Biotechnol. 2018;36(4):321–3. Epub 2018/03/20. doi: 10.1038/nbt.4109 29553574.

25. Keeling PJ, Burki F. Progress towards the Tree of Eukaryotes. Curr Biol. 2019;29(16):R808–R17. Epub 2019/08/21. doi: 10.1016/j.cub.2019.07.031 31430481.

26. Tyler BM, Tripathy S, Zhang X, Dehal P, Jiang RH, Aerts A, et al. Phytophthora genome sequences uncover evolutionary origins and mechanisms of pathogenesis. Science. 2006;313(5791):1261–6. Epub 2006/09/02. doi: 10.1126/science.1128796 16946064.

27. Grattepanche JD, Walker LM, Ott BM, Paim Pinto DL, Delwiche CF, Lane CE, et al. Microbial diversity in the eukaryotic SAR clade: Illuminating the darkness between morphology and molecular data. Bioessays. 2018;40(4):e1700198. Epub 2018/03/08. doi: 10.1002/bies.201700198 29512175.

28. Erwin DC, Ribeiro OK. Phytophthora diseases worldwide: American Phytopathological Society (APS Press); 1996.

29. Jiang RH, Tyler BM. Mechanisms and evolution of virulence in oomycetes. Annu Rev Phytopathol. 2012;50:295–318. Epub 2012/08/28. doi: 10.1146/annurev-phyto-081211-172912 22920560.

30. Savary S, Willocquet L, Pethybridge SJ, Esker P, McRoberts N, Nelson A. The global burden of pathogens and pests on major food crops. Nat Ecol Evol. 2019;3(3):430–9. Epub 2019/02/06. doi: 10.1038/s41559-018-0793-y 30718852.

31. Fang Y, Cui L, Gu B, Arredondo F, Tyler BM. Efficient genome editing in the oomycete Phytophthora sojae using CRISPR/Cas9. Curr Protoc Microbiol. 2017;44:21A 1.1–A.1 6. Epub 2017/02/07. doi: 10.1002/cpmc.25 28166383.

32. Judelson HS, Coffey MD, Arredondo FR, Tyler BM. Transformation of the oomycete pathogen Phytophthora-megasperma f.sp. glycinea occurs by DNA integration into single or multiple chromosomes. Curr Genet. 1993;23(3):211–8. Epub 1993/03/01. doi: 10.1007/bf00351498 8382110.

33. Fang Y, Tyler BM. Efficient disruption and replacement of an effector gene in the oomycete Phytophthora sojae using CRISPR/Cas9. Mol Plant Pathol. 2016;17(1):127–39. Epub 2015/10/29. doi: 10.1111/mpp.12318 26507366.

34. McGowan J, Fitzpatrick DA. Genomic, network, and phylogenetic analysis of the oomycete effector arsenal. mSphere. 2017;2(6):e00408–17. Epub 2017/12/05. doi: 10.1128/mSphere.00408-17 29202039.

35. Tyler BM, Gijzen M. The Phytophthora sojae genome sequence: foundation for a revolution. Genomics of plant-associated fungi and oomycetes: dicot pathogens: Springer; 2014. p. 133–57.

36. Malar CM, Yuzon JD, Das S, Das A, Panda A, Ghosh S, et al. Haplotype-phased genome assembly of virulent Phytophthora ramorum isolate ND886 facilitated by long-read sequencing reveals effector polymorphisms and copy number variation. Mol Plant Microbe Interact. 2019;32(8):1047–60. Epub 2019/02/23. doi: 10.1094/MPMI-08-18-0222-R 30794480.

37. Fletcher K, Gil J, Bertier LD, Kenefick A, Wood KJ, Zhang L, et al. Genomic signatures of heterokaryosis in the oomycete pathogen Bremia lactucae. Nat Commun. 2019;10(1):2645. Epub 2019/06/16. doi: 10.1038/s41467-019-10550-0 31201315.

38. van Hooff JJ, Tromer E, van Wijk LM, Snel B, Kops GJ. Evolutionary dynamics of the kinetochore network in eukaryotes as revealed by comparative genomics. EMBO Rep. 2017;18(9):1559–71. Epub 2017/06/24. doi: 10.15252/embr.201744102 28642229.

39. Fulneckova J, Sevcikova T, Fajkus J, Lukesova A, Lukes M, Vlcek C, et al. A broad phylogenetic survey unveils the diversity and evolution of telomeres in eukaryotes. Genome Biol Evol. 2013;5(3):468–83. Epub 2013/02/12. doi: 10.1093/gbe/evt019 23395982.

40. Tooley PW, Carras MM. Separation of chromosomes of Phytophthora species using CHEF gel electrophoresis. Experimental Mycology. 1992;16(3):188–96. doi: 10.1016/0147-5975(92)90027-O

41. Sansome E, Brasier C. Polyploidy associated with varietal differentiation in the megasperma complex of Phytophthora. Transactions of the British Mycological Society. 1974;63(3):461–IN11.

42. Sullivan BA, Karpen GH. Centromeric chromatin exhibits a histone modification pattern that is distinct from both euchromatin and heterochromatin. Nature Structural & Molecular Biology. 2004;11(11):1076–83. doi: 10.1038/nsmb845 15475964

43. Jiang RHY, Dawe AL, Weide R, van Staveren M, Peters S, Nuss DL, et al. Elicitin genes in Phytophthora infestans are clustered and interspersed with various transposon-like elements. Molecular Genetics and Genomics. 2005;273(1):20–32. doi: 10.1007/s00438-005-1114-0 15702346

44. Basnayake S, Maclean DJ, Whisson SC, Drenth A. Identification and occurrence of the LTR-Copia-like retrotransposon, PSCR and other Copia-like elements in the genome of Phytophthora sojae. Curr Genet. 2009;55(5):521–36. Epub 2009/07/31. doi: 10.1007/s00294-009-0263-9 19641921.

45. Bao W, Kojima KK, Kohany O. Repbase Update, a database of repetitive elements in eukaryotic genomes. Mob DNA. 2015;6(1):11. Epub 2015/06/06. doi: 10.1186/s13100-015-0041-9 26045719.

46. Henikoff S, Ahmad K, Malik HS. The centromere paradox: stable inheritance with rapidly evolving DNA. Science. 2001;293(5532):1098–102. Epub 2001/08/11. doi: 10.1126/science.1062939 11498581.

47. Volpe TA, Kidner C, Hall IM, Teng G, Grewal SI, Martienssen RA. Regulation of heterochromatic silencing and histone H3 lysine-9 methylation by RNAi. Science. 2002;297(5588):1833–7. Epub 2002/08/24. doi: 10.1126/science.1074973 12193640.

48. Li XY, Wang XF, He K, Ma YQ, Su N, He H, et al. High-resolution mapping of epigenetic modifications of the rice genome uncovers interplay between DNA methylation, histone methylation, and gene expression. Plant Cell. 2008;20(2):259–76. doi: 10.1105/tpc.107.056879 18263775

49. Allshire RC, Karpen GH. Epigenetic regulation of centromeric chromatin: old dogs, new tricks? Nat Rev Genet. 2008;9(12):923–37. Epub 2008/11/13. doi: 10.1038/nrg2466 19002142.

50. Blower MD, Sullivan BA, Karpen GH. Conserved organization of centromeric chromatin in flies and humans. Dev Cell. 2002;2(3):319–30. Epub 2002/03/07. doi: 10.1016/s1534-5807(02)00135-1 11879637.

51. Scott KC, Merrett SL, Willard HF. A heterochromatin barrier partitions the fission yeast centromere into discrete chromatin domains. Curr Biol. 2006;16(2):119–29. Epub 2006/01/25. doi: 10.1016/j.cub.2005.11.065 16431364.

52. Allshire RC, Madhani HD. Ten principles of heterochromatin formation and function. Nat Rev Mol Cell Biol. 2018;19(4):229–44. Epub 2017/12/14. doi: 10.1038/nrm.2017.119 29235574.

53. Greaves IK, Rangasamy D, Ridgway P, Tremethick DJ. H2A.Z contributes to the unique 3D structure of the centromere. Proc Natl Acad Sci U S A. 2007;104(2):525–30. Epub 2006/12/30. doi: 10.1073/pnas.0607870104 17194760.

54. Friedman S, Freitag M. Evolving centromeres and kinetochores. Advances in genetics. 98: Elsevier; 2017. p. 1–41. doi: 10.1016/bs.adgen.2017.07.001 28942791

55. Brown JD, O’Neill RJ. The evolution of centromeric DNA sequences. In: John Wiley & Sons Ltd, editor. eLS. John Wiley & Sons, Ltd: Chichester, UK; 2014. doi: 10.1002/9780470015902.a0020827.pub2

56. Yin L, Wang Q, Ning F, Zhu X, Zuo Y, Shan W. Identification of a repetitive sequence element for DNA fingerprinting in Phytophthora sojae. Wei Sheng Wu Xue Bao. 2010;50(4):524–9. Epub 2010/06/22. 20560357.

57. Xiao J, Miao M, Gao K, Xiang G, Yang S, Dong S, et al. Genetic diversity of Phytophthora sojae in China based on RFLP. Scientia Agricultura Sinica. 2011;44(20):4190–8.

58. Cao MD, Nguyen SH, Ganesamoorthy D, Elliott AG, Cooper MA, Coin LJ. Scaffolding and completing genome assemblies in real-time with nanopore sequencing. Nat Commun. 2017;8:14515. Epub 2017/02/22. doi: 10.1038/ncomms14515 28218240.

59. Boetzer M, Pirovano W. SSPACE-LongRead: scaffolding bacterial draft genomes using long read sequence information. BMC Bioinformatics. 2014;15(1):211. doi: 10.1186/1471-2105-15-211 24950923

60. Warren RL, Yang C, Vandervalk BP, Behsaz B, Lagman A, Jones SJ, et al. LINKS: Scalable, alignment-free scaffolding of draft genomes with long reads. Gigascience. 2015;4(1):35. Epub 2015/08/06. doi: 10.1186/s13742-015-0076-3 26244089.

61. Compton DA. Mechanisms of aneuploidy. Curr Opin Cell Biol. 2011;23(1):109–13. Epub 2010/09/03. doi: 10.1016/j.ceb.2010.08.007 20810265.

62. Todd RT, Forche A, Selmecki A. Ploidy variation in fungi: polyploidy, aneuploidy, and genome evolution. Microbiol Spectr. 2017;5(4):599–618. Epub 2017/07/29. doi: 10.1128/microbiolspec.FUNK-0051-2016 28752816.

63. Elliott M, Yuzon J, C MM, Tripathy S, Bui M, Chastagner GA, et al. Characterization of phenotypic variation and genome aberrations observed among Phytophthora ramorum isolates from diverse hosts. BMC Genomics. 2018;19(1):320. Epub 2018/05/04. doi: 10.1186/s12864-018-4709-7 29720102.

64. Dobrowolski MP, Tommerup IC, Blakeman HD, O’Brien PA. Non-Mendelian inheritance revealed in a genetic analysis of sexual progeny of Phytophthora cinnamomi with microsatellite markers. Fungal Genet Biol. 2002;35(3):197–212. Epub 2002/04/04. doi: 10.1006/fgbi.2001.1319 11929210.

65. Kasuga T, Bui M, Bernhardt E, Swiecki T, Aram K, Cano LM, et al. Host-induced aneuploidy and phenotypic diversification in the sudden oak death pathogen Phytophthora ramorum. BMC Genomics. 2016;17(1):385. Epub 2016/05/22. doi: 10.1186/s12864-016-2717-z 27206972.

66. van der Lee T, Testa A, Robold A, van’t Klooster J, Govers F. High-density genetic linkage maps of Phytophthora infestans reveal trisomic progeny and chromosomal rearrangements. Genetics. 2004;167(4):1643–61. Epub 2004/09/03. doi: 10.1534/genetics.104.029652 15342505.

67. Hu J, Shrestha S, Zhou Y, Mudge J, Liu X, Lamour K. Dynamic Extreme Aneuploidy (DEA) in the vegetable pathogen Phytophthora capsici and the potential for rapid asexual evolution. PLoS One. 2020;15(1):e0227250. Epub 2020/01/08. doi: 10.1371/journal.pone.0227250 31910244.

68. Lin L, Ye W, Wu J, Xuan M, Li Y, Gao J, et al. The MADS-box transcription factor PsMAD1 is involved in zoosporogenesis and pathogenesis of Phytophthora sojae. Front Microbiol. 2018;9(2259):2259. Epub 2018/10/16. doi: 10.3389/fmicb.2018.02259 30319576.

69. Fang Y, Jang HS, Watson GW, Wellappili DP, Tyler BM. Distinctive nuclear localization signals in the oomycete Phytophthora sojae. Front Microbiol. 2017;8:10. Epub 2017/02/18. doi: 10.3389/fmicb.2017.00010 28210240.

70. Gent JI, Wang N, Dawe RK. Stable centromere positioning in diverse sequence contexts of complex and satellite centromeres of maize and wild relatives. Genome Biol. 2017;18(1):121. Epub 2017/06/24. doi: 10.1186/s13059-017-1249-4 28637491.

71. Quinlan AR, Hall IM. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics. 2010;26(6):841–2. Epub 2010/01/30. doi: 10.1093/bioinformatics/btq033 20110278.

72. Smit A, Hubley R, Green P. RepeatMasker Open-4.0. 2013–2015. 2015.

73. Cantarel BL, Korf I, Robb SMC, Parra G, Ross E, Moore B, et al. MAKER: An easy-to-use annotation pipeline designed for emerging model organism genomes. Genome Res. 2008;18:188–96. doi: 10.1101/gr.6743907 18025269

74. Haas BJ, Kamoun S, Zody MC, Jiang RHY, Handsaker RE, Cano LM, et al. Genome sequence and analysis of the Irish potato famine pathogen Phytophthora infestans. Nature. 2009;461:393–8. doi: 10.1038/nature08358 19741609

75. Lagesen K, Hallin P, Rodland EA, Staerfeldt HH, Rognes T, Ussery DW. RNAmmer: consistent and rapid annotation of ribosomal RNA genes. Nucleic Acids Res. 2007;35(9):3100–8. Epub 2007/04/25. doi: 10.1093/nar/gkm160 17452365.

76. Lowe TM, Chan PP. tRNAscan-SE On-line: integrating search and context for analysis of transfer RNA genes. Nucleic Acids Res. 2016;44(W1):W54–7. Epub 2016/05/14. doi: 10.1093/nar/gkw413 27174935.

77. Krzywinski M, Schein J, Birol I, Connors J, Gascoyne R, Horsman D, et al. Circos: an information aesthetic for comparative genomics. Genome Res. 2009;19(9):1639–45. Epub 2009/06/23. doi: 10.1101/gr.092759.109 19541911.

78. Jain C, Koren S, Dilthey A, Phillippy AM, Aluru S. A fast adaptive algorithm for computing whole-genome homology maps. Bioinformatics. 2018;34(17):i748–i56. Epub 2018/11/14. doi: 10.1093/bioinformatics/bty597 30423094.

79. Okonechnikov K, Golosova O, Fursov M, team U. Unipro UGENE: a unified bioinformatics toolkit. Bioinformatics. 2012;28(8):1166–7. Epub 2012/03/01. doi: 10.1093/bioinformatics/bts091 22368248.

80. Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol. 2013;30(4):772–80. Epub 2013/01/19. doi: 10.1093/molbev/mst010 23329690.

81. Capella-Gutierrez S, Silla-Martinez JM, Gabaldon T. trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics. 2009;25(15):1972–3. Epub 2009/06/10. doi: 10.1093/bioinformatics/btp348 19505945.

82. Nguyen LT, Schmidt HA, von Haeseler A, Minh BQ. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol. 2015;32(1):268–74. Epub 2014/11/06. doi: 10.1093/molbev/msu300 25371430.

83. Hoang DT, Chernomor O, Von Haeseler A, Minh BQ, Vinh LS. UFBoot2: improving the ultrafast bootstrap approximation. Molecular Biology and Evolution. 2017;35(2):518–22.

84. Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol. 2010;59(3):307–21. Epub 2010/06/09. doi: 10.1093/sysbio/syq010 20525638.

85. Letunic I, Bork P. Interactive Tree Of Life (iTOL) v4: recent updates and new developments. Nucleic Acids Res. 2019;47(W1):W256–W9. Epub 2019/04/02. doi: 10.1093/nar/gkz239 30931475.

86. Wicker T, Sabot F, Hua-Van A, Bennetzen JL, Capy P, Chalhoub B, et al. A unified classification system for eukaryotic transposable elements. Nat Rev Genet. 2007;8(12):973–82. Epub 2007/11/07. doi: 10.1038/nrg2165 17984973.

87. Xiong Y, Eickbush TH. Origin and evolution of retroelements based upon their reverse-transcriptase sequences. Embo J. 1990;9(10):3353–62. doi: 10.1002/j.1460-2075.1990.tb07536.x 1698615

88. Kumar S, Stecher G, Suleski M, Hedges SB. TimeTree: A resource for timelines, timetrees, and divergence times. Mol Biol Evol. 2017;34(7):1812–9. Epub 2017/04/08. doi: 10.1093/molbev/msx116 28387841.

89. Mikheenko A, Prjibelski A, Saveliev V, Antipov D, Gurevich A. Versatile genome assembly evaluation with QUAST-LG. Bioinformatics. 2018;34(13):i142–i50. Epub 2018/06/29. doi: 10.1093/bioinformatics/bty266 29949969.

90. Li H. Minimap2: pairwise alignment for nucleotide sequences. Bioinformatics. 2018;34(18):3094–100. Epub 2018/05/12. doi: 10.1093/bioinformatics/bty191 29750242.

91. Sović I, Šikić M, Wilm A, Fenlon SN, Chen S, Nagarajan N. Fast and sensitive mapping of nanopore sequencing reads with GraphMap. Nat Commun. 2016;7:11307. doi: 10.1038/ncomms11307 27079541

92. Marcais G, Delcher AL, Phillippy AM, Coston R, Salzberg SL, Zimin A. MUMmer4: A fast and versatile genome alignment system. PLoS Comput Biol. 2018;14(1):e1005944. Epub 2018/01/27. doi: 10.1371/journal.pcbi.1005944 29373581.


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PLOS Genetics


2020 Číslo 3

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