Single-molecule real-time sequencing combined with optical mapping yields completely finished fungal genome

mBio

Volumn 6, Issue 4, 2015, Pages

  Faino, Luigi ^a   Seidl, Michael F ^a   Datema, Erwin ^b   Van Den Berg, Grardy C M ^a   Janssen, Antoine ^b   Wittenberg, Alexander H J ^b   Thomma, Bart P H J ^a  

^a WAGENINGEN UNIVERSITY   (Netherlands)

^b KEYGENE N V   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; CHROMATIN ASSEMBLY AND DISASSEMBLY; CONTROLLED STUDY; DNA TEMPLATE; EVOLUTIONARY DEVELOPMENTAL BIOLOGY; FUNGAL GENOME; FUNGAL STRAIN; GENE SEQUENCE; HYBRID GENE; NEXT GENERATION SEQUENCING; NONHUMAN; OPTICAL MAPPING; PACBIO GENE; PRIORITY JOURNAL; PROTEIN ASSEMBLY; SINGLE MOLECULE REAL TIME SEQUENCING; TELOMERE; TRANSPOSON; VERTICILLIUM DAHLIAE; CHROMOSOMAL MAPPING; DNA SEQUENCE; GENETICS; GENOMICS; HIGH THROUGHPUT SEQUENCING; PROCEDURES; RESTRICTION MAPPING; VERTICILLIUM;

TRANSPOSON;

CHROMOSOME MAPPING; DNA TRANSPOSABLE ELEMENTS; GENOME, FUNGAL; GENOMICS; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; OPTICAL RESTRICTION MAPPING; SEQUENCE ANALYSIS, DNA; TELOMERE; VERTICILLIUM;

EID: 84940872323     PISSN: 21612129     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.00936-15     Document Type: Article

References (59)

1. Koboldt DC, Steinberg KM, Larson DE, Wilson RK, Mardis ER. 2013. The next-generation sequencing revolution and its impact on genomics. Cell 155:27-38. http://dx.doi.org/10.1016/j.cell.2013.09.006.
2. Metzker ML. 2010. Sequencing technologies—the next generation. Nat Rev Genet 11:31-46. http://dx.doi.org/10.1038/nrg2626.
3. Schatz MC, Delcher AL, Salzberg SL. 2010. Assembly of large genomes using second-generation sequencing. Genome Res 20:1165-1173. http://dx.doi.org/10.1101/gr.101360.109.
4. Chain PS, Grafham DV, Fulton RS, Fitzgerald MG, Hostetler J, Muzny D, Ali J, Birren B, Bruce DC, Buhay C, Cole JR, Ding Y, Dugan S, Field D, Garrity GM, Gibbs R, Graves T, Han CS, Harrison SH, Highlander S, Hugenholtz P, Khouri HM, Kodira CD, Kolker E, Kyrpides NC, Lang D, Lapidus A, Malfatti SA, Markowitz V, Metha T, Nelson KE, Parkhill J, Pitluck S, Qin X, Read TD, Schmutz J, Sozhamannan S, Sterk P, Strausberg RL, Sutton G, Thomson NR, Tiedje JM, Weinstock G, Wollam A, Genomic Standards Consortium Human Microbiome Proj- ect Jumpstart Consortium, Detter JC. 2009. Genome project standards in a new era of sequencing. Science 326:236-237.
5. Treangen TJ, Salzberg SL. 2012. Repetitive DNA and next-generation sequencing: computational challenges and solutions. Nat Rev Genet 13: 36-46. http://dx.doi.org/10.1038/nrg3117.
6. Ashton PM, Nair S, Dallman T, Rubino S, Rabsch W, Mwaigwisya S, Wain J, O’Grady J. 2015. MinION nanopore sequencing identifies the position and structure of a bacterial antibiotic resistance island. Nat Bio- technol 33:296-300. http://dx.doi.org/10.1038/nbt.3103.
7. Laszlo AH, Derrington IM, Ross BC, Brinkerhoff H, Adey A, Nova IC, Craig JM, Langford KW, Samson JM, Daza R, Doering K, Shendure J, Gundlach JH. 2014. Decoding long nanopore sequencing reads of natural DNA. Nat Biotechnol 32:829-833. http://dx.doi.org/10.1038/nbt.2950.
8. Huddleston J, Ranade S, Malig M, Antonacci F, Chaisson M, Hon L, Sudmant PH, Graves TA, Alkan C, Dennis MY, Wilson RK, Turner SW, Korlach J, Eichler EE. 2014. Reconstructing complex regions of genomes using long-read sequencing technology. Genome Res 24:688-696. http://dx.doi.org/10.1101/gr.168450.113.
9. Powers JG, Weigman VJ, Shu J, Pufky JM, Cox D, Hurban P. 2013. Efficient and accurate whole genome assembly and methylome profiling of E. coli. BMC Genomics 14:675. http://dx.doi.org/10.1186/1471-2164-14-675.
10. Kim KE, Peluso P, Babayan P, Yeadon PJ, Yu C, Fisher WW, Chin C-S, Rapicavoli NA, Rank DR, Li J, Catcheside DE, Celniker SE, Phillippy AM, Bergman CM, Landolin JM. 2014. Long-read, whole-genome shotgun sequence data for five model organisms. Sci Data 1:140045. http://dx.doi.org/10.1038/sdata.2014.45.
11. English AC, Richards S, Han Y, Wang M, Vee V, Qu J, Qin X, Muzny DM, Reid JG, Worley KC, Gibbs RA. 2012. Mind the gap: upgrading genomes with Pacific Biosciences RS long-read sequencing technology. PLoS One 7:e47768. http://dx.doi.org/10.1371/journal.pone.0047768.
12. Chin CS, Alexander DH, Marks P, Klammer AA, Drake J, Heiner C, Clum A, Copeland A, Huddleston J, Eichler EE, Turner SW, Korlach J. 2013. Nonhybrid, finished microbial genome assemblies from long-read SMRT sequencing data. Nat Methods 10:563-569. http://dx.doi.org/10.1038/nmeth.2474.
13. Levy-Sakin M, Ebenstein Y. 2013. Beyond sequencing: optical mapping of DNA in the age of nanotechnology and nanoscopy. Curr Opin Biotechnol 24:690-698. http://dx.doi.org/10.1016/j.copbio.2013.01.009.
14. Dong Y, Xie M, Jiang Y, Xiao N, Du X, Zhang W, Tosser-Klopp G, Wang J, Yang S, Liang J, Chen W, Chen J, Zeng P, Hou Y, Bian C, Pan S, Li Y, Liu X, Wang W, Servin B, Sayre B, Zhu B, Sweeney D, Moore R, Nie W, Shen Y, Zhao R, Zhang G, Li J, Faraut T, Womack J, Zhang Y, Kijas J, Cockett N, Xu X, Zhao S, Wang J, Wang W. 2013. Sequencing and automated whole-genome optical mapping of the genome of a do- mestic goat (Capra hircus). Nat Biotechnol 31:135-141. http://dx.doi.org/10.1038/nbt.2478.
15. Shearer LA, Anderson LK, de Jong H, Smit S, Goicoechea JL, Roe BA, Hua A, Giovannoni JJ, Stack SM. 2014. Fluorescence in situ hybridiza- tion and optical mapping to correct scaffold arrangement in the tomato genome. G3 (Bethesda) 4:1395-1405. http://dx.doi.org/10.1534/g3.114.011197.
16. Raffaele S, Kamoun S. 2012. Genome evolution in filamentous plant pathogens: why bigger can be better. Nat Rev Microbiol 10:417-430. http://dx.doi.org/10.1038/nrmicro2790.
17. Bickhart DM, Liu GE. 2014. The challenges and importance of structural variation detection in livestock. Front Genet 5:37. http://dx.doi.org/10.3389/fgene.2014.00037.
18. Seidl MF, Thomma BPHJ. 2014. Sex or no sex: evolutionary adaptation occurs regardless. Bioessays 36:335-345. http://dx.doi.org/10.1002/ bies.201300155.
19. Chaisson MJ, Huddleston J, Dennis MY, Sudmant PH, Malig M, Hormozdiari F, Antonacci F, Surti U, Sandstrom R, Boitano M, Landolin JM, Stamatoyannopoulos JA, Hunkapiller MW, Korlach J, Eichler EE. 2015. Resolving the complexity of the human genome using single-molecule sequencing. Nature 517:608-611. http://dx.doi.org/10.1038/nature13907.
20. Faino L, Thomma BPHJ. 2014. Get your high-quality low-cost genome sequence. Trends Plant Sci 19:288-291. http://dx.doi.org/10.1016/j.tplants.2014.02.003.
21. Koren S, Harhay GP, Smith TP, Bono JL, Harhay DM, McVey SD, Radune D, Bergman NH, Phillippy AM. 2013. Reducing assembly complexity of microbial genomes with single-molecule sequencing. Genome Biol 14:R101. http://dx.doi.org/10.1186/gb-2013-14-9-r101.
22. de Jonge R, Bolton MD, Kombrink A, van den Berg GC, Yadeta KA, Thomma BPHJ. 2013. Extensive chromosomal reshuffling drives evolution of virulence in an asexual pathogen. Genome Res 23:1271-1282. http://dx.doi.org/10.1101/gr.152660.112.
23. Klosterman SJ, Subbarao KV, Kang S, Veronese P, Gold SE, Thomma BPHJ, Chen Z, Henrissat B, Lee YH, Park J, Garcia-Pedrajas MD, Barbara DJ, Anchieta A, de Jonge R, Santhanam P, Maruthachalam K, Atallah Z, Amyotte SG, Paz Z, Inderbitzin P, Hayes RJ, Heiman DI, Young S, Zeng Q, Engels R, Galagan J, Cuomo CA, Dobinson KF, Ma LJ. 2011. Comparative genomics yields insights into niche adaptation of plant vascular wilt pathogens. PLoS Pathog 7:e1002137. http://dx.doi.org/10.1371/journal.ppat.1002137.
24. De Jonge R, van Esse HP, Maruthachalam K, Bolton MD, Santhanam P, Saber MK, Zhang Z, Usami T, Lievens B, Subbarao KV, Thomma BP. 2012. To matoimmune receptorVe1 recognizes effect or of multiple fungal pathogensun covered by genomeand RNA sequencing. Proc Natl Acad Sci USA 109:5110-5115. http://dx.doi.org/10.1073/pnas.1119623109.
25. Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS, Lesin VM, Nikolenko SI, Pham S, Prjibelski AD, Pyshkin AV, Sirotkin AV, Vyahhi N, Tesler G, Alekseyev MA, Pevzner PA. 2012. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 19:455-477.
26. Seidl MF, Faino L, Shi-Kunne X, van den Berg GC, Bolton MD, Thomma BPHJ. 2015. The genome of the saprophytic fungus Verticillium tricorpus reveals a complex effector repertoire resembling that of its pathogenic relatives. Mol Plant Microbe Interact 28:362-373. http://dx.doi.org/10.1094/MPMI-06-14-0173-R.
27. Tritt A, Eisen JA, Facciotti MT, Darling AE. 2012. An integrated pipeline for de novo assembly of microbial genomes. PLoS One 7:e42304. http://dx.doi.org/10.1371/journal.pone.0042304.
28. Berlin K, Koren S, Chin C-S, Drake JP, Landolin JM, Phillippy AM. 2015. Assembling large genomes with single-molecule sequencing and locality-sensitive hashing. Nat Biotechnol 33:623-630. http://dx.doi.org/10.1038/nbt.3238.
29. Chaisson MJ, Tesler G. 2012. Mapping single molecule sequencing reads using basic local alignment with successive refinement (BLASR): application and theory. BMC Bioinformatics 13:238. http://dx.doi.org/10.1186/1471-2105-13-238.
30. Bulatovic M, Heijstek MW, van Dijkhuizen EHP, Wulffraat NM, Pluijm SMF, de Jonge R. 2012. Prediction of clinical non-response to methotrexate treatment in juvenile idiopathic arthritis. Ann Rheum Dis 71:1484-1489.
31. Gurevich A, Saveliev V, Vyahhi N, Tesler G. 2013. QUAST: quality assessment tool for genome assemblies. Bioinformatics 29:1072-1075. http://dx.doi.org/10.1093/bioinformatics/btt086.
32. Spanu PD, Abbott JC, Amselem J, Burgis TA, Soanes DM, Stüber K, VerLorenvan Themaat E, Brown JK, Butcher SA, Gurr SJ, Lebrun MH, Ridout CJ, Schulze-Lefert P, Talbot NJ, Ahmadinejad N, Ametz C, Barton GR, Benjdia M, Bidzinski P, Bindschedler LV, Both M, Brewer MT, Cadle-Davidson L, Cadle-Davidson MM, Collemare J, Cramer R, Frenkel O, Godfrey D, Harriman J, Hoede C, King BC, Klages S, Kleemann J, Knoll D, Koti PS, Kreplak J, Lopez-Ruiz FJ, Lu X, Maekawa T, Mahanil S, Micali C, Milgroom MG, Montana G, Noir S, O’Connell RJ, Oberhaensli S, Parlange F, Pedersen C, Quesneville H, Reinhardt R, Rott M, et al. 2010. Genome expansion and gene loss in powdery mildew fungi reveal tradeoffs in extreme parasitism. Science 330: 1543-1546. http://dx.doi.org/10.1126/science.1194573.
33. Amyotte SG, Tan X, Pennerman K, delMar Jimenez-Gasco M, Klosterman SJ, Ma L-J, Dobinson KF, Veronese P. 2012. Transposable elements in phytopathogenic Verticillium spp.: insights into genome evolution and inter- and intra-specific diversification. BMC Genomics 13:314. http://dx.doi.org/10.1186/1471-2164-13-314.
34. Wicker T, Sabot F, Hua-Van A, Bennetzen JL, Capy P, Chalhoub B, Flavell A, Leroy P, Morgante M, Panaud O, Paux E, SanMiguel P, Schulman AH. 2007. A unified classification system for eukaryotic trans- posable elements. Nat Rev Genet 8:973-982. http://dx.doi.org/10.1038/nrg2165.
35. Havecker ER, Gao X, Voytas DF. 2004. The diversity of LTR retrotransposons. Genome Biol 5:225. http://dx.doi.org/10.1186/gb-2004-5-6-225.
36. Chénais B, Caruso A, Hiard S, Casse N. 2012. The impact of transposable elements on eukaryotic genomes: from genome size increase to genetic adaptation to stressful environments. Gene 509:7-15. http://dx.doi.org/10.1016/j.gene.2012.07.042.
37. Pritham EJ. 2009. Transposable elements and factors influencing their success in eukaryotes. J Hered 100:648-655. http://dx.doi.org/10.1093/jhered/esp065.
38. Grandaubert J, Lowe RG, Soyer JL, Schoch CL, Vande Wouw AP, Fudal I, Robbertse B, Lapalu N, Links MG, Ollivier B, Linglin J, Barbe V, Mangenot S, Cruaud C, Borhan H, Howlett BJ, Balesdent MH, Rouxel T. 2014. Transposable element-assisted evolution and adaptation to host plant within the Leptosphaeria maculans-Leptosphaeria biglobosa species complex of fungal pathogens. BMC Genomics 15:891. http://dx.doi.org/10.1186/1471-2164-15-891.
39. Daboussi MJ, Capy P. 2003. Transposable elements in filamentous fungi. Annu Rev Microbiol 57:275-299. http://dx.doi.org/10.1146/annurev.micro.57.030502.091029.
40. McCoy RC, Taylor RW, Blauwkamp TA, Kelley JL, Kertesz M, Pushkarev D, Petrov DA, Fiston-Lavier AS. 2014. Illumina, TruSeq synthetic long-reads empower de novo assembly and resolve complex, highly-repetitive transposable elements. PLoS One 9:e106689.
41. Voskoboynik A, Neff NF, Sahoo D, Newman AM, Pushkarev D, Koh W, Passarelli B, Fan HC, Mantalas GL, Palmeri KJ, Ishizuka KJ, Gissi C, Griggio F, Ben-Shlomo R, Corey DM, Penland L, White RA, III, Weissman IL, Quake SR. 2013. The genome sequence of the colonial chordate, Botryllus schlosseri. Elife 2:e00569. http://dx.doi.org/10.7554/eLife.00569.
42. Liao YC, Lin SH, Lin HH. 2015. Completing bacterial genome assemblies:strategyandperformancecomparisons. SciRep 5:8747. http://dx.doi.org/10.1038/srep08747.
43. Nagarajan N, Read TD, Pop M. 2008. Scaffolding and validation of bacterial genome assemblies using optical restriction maps. Bioinformatics 24:1229-1235. http://dx.doi.org/10.1093/bioinformatics/btn102.
44. Ma LJ, van der Does HC, Borkovich KA, Coleman JJ, Daboussi MJ, Di Pietro A, Dufresne M, Freitag M, Grabherr M, Henrissat B, Houterman PM, Kang S, Shim WB, Woloshuk C, Xie X, Xu JR, Antoniw J, Baker SE, Bluhm BH, Breakspear A, Brown DW, Butchko RA, Chapman S, Coulson R, Coutinho PM, Danchin EG, Diener A, Gale LR, Gardiner DM, Goff S, Hammond-Kosack KE, Hilburn K, Hua-Van A, Jonkers W, Kazan K, Kodira CD, Koehrsen M, Kumar L, Lee YH, Li L, Manners JM, Miranda-Saavedra D, Mukherjee M, Park G, Park J, Park SY, Proctor RH, Regev A, Ruiz-Roldan MC, Sain D, Sakthikumar S, et al. 2010. Comparative genomics reveals mobile pathogenicity chromosomes in Fusarium. Nature 464:367-373. http://dx.doi.org/10.1038/nature08850.
45. Zhou S, Wei F, Nguyen J, Bechner M, Potamousis K, Goldstein S, Pape L, Mehan MR, Churas C, Pasternak S, Forrest DK, Wise R, Ware D, Wing RA, Waterman MS, Livny M, Schwartz DC. 2009. A single molecule scaffold for the maize genome. PLoS Genet 5:e1000711. http://dx.doi.org/10.1371/journal.pgen.1000711.
46. Nowak MD, Russo G, Schlapbach R, Huu CN, Lenhard M, Conti E. 2015. The draft genome of Primula veris yields insights into the molecular basis of heterostyly. Genome Biol 16:12. http://dx.doi.org/10.1186/s13059-014-0567-z.
47. Chamala S, Chanderbali AS, Der JP, Lan T, Walts B, Albert VA, dePamphilis CW, Leebens-Mack J, Rounsley S, Schuster SC, Wing RA, Xiao N, Moore R, Soltis PS, Soltis DE, Barbazuk WB. 2013. Assembly and validation of the genome of the nonmodel basal angiosperm Amborella. Science 342:1516-1517. http://dx.doi.org/10.1126/science.1241130.
48. Janbon G, Ormerod KL, Paulet D, Byrnes EJ III, Yadav V, Chatterjee G, Mullapudi N, Hon CC, Billmyre RB, Brunel F, Bahn YS, Chen W, Chen Y, Chow EW, Coppée JY, Floyd-Averette A, Gaillardin C, Gerik KJ, Goldberg J, Gonzalez-Hilarion S, Gujja S, Hamlin JL, Hsueh YP, Ianiri G, Jones S, Kodira CD, Kozubowski L, Lam W, Marra M, Mesner LD, Mieczkowski PA, Moyrand F, Nielsen K, Proux C, Rossignol T, Schein JE, Sun S, Wollschlaeger C, Wood IA, Zeng Q, Neuveglise C, Newlon CS, Perfect JR, Lodge, Idnurm A, Stajich JE, Kronstad JW, Sanyal K, Heitman J, Fraser JA, Cuomo CA, Dietrich FS. 2014. Analysis of the genome and transcriptome of Cryptococcus neoformans var. grubii reveals complex RNA expression and microevolution leading to virulence attenuation. PLoS Genet 10:e1004261. http://dx.doi.org/10.1371/journal.pgen.1004261.
49. Berka RM, Grigoriev IV, Otillar R, Salamov A, Grimwood J, Reid I, Ishmael N, John T, Darmond C, Moisan MC, Henrissat B, Coutinho PM, Lombard V, Natvig DO, Lindquist E, Schmutz J, Lucas S, Harris P, Powlowski J, Bellemare A, Taylor D, Butler G, de Vries RP, Allijn IE, van den Brink J, Ushinsky S, Storms R, Powell AJ, Paulsen IT, Elbourne LD, Baker SE, Magnuson J, Laboissiere S, Clutterbuck AJ, Martinez D, Wogulis M, de Leon AL, Rey MW, Tsang A. 2011. Comparative genomic analysis of the thermophilic biomass-degrading fungi Myceliophthora thermophila and Thielavia terrestris. Nat Biotechnol 29:922-927. http://dx.doi.org/10.1038/nbt.1976.
50. Goodwin SB, M’Barek SB, Dhillon B, Wittenberg AH, Crane CF, Hane JK, Foster AJ, Van der Lee TA, Grimwood J, Aerts A, Antoniw J, Bailey A, Bluhm B, Bowler J, Bristow J, van der Burgt A, Canto-Canché B, Churchill AC, Conde-Ferràez L, Cools HJ, Coutinho PM, Csukai M, Dehal P, De Wit P, Donzelli B, van de Geest HC, van Ham RC, Hammond-Kosack KE, Henrissat B, Kilian A, Kobayashi AK, Koopmann E, Kourmpetis Y, Kuzniar A, Lindquist E, Lombard V, Maliepaard C, Martins N, Mehrabi R, Nap JP, Ponomarenko A, Rudd JJ, Salamov A, Schmutz J, Schouten HJ, Shapiro H, Stergiopoulos I, Torriani SF, Tu H, de Vries RP, Waalwijk C, et al. 2011. Finished genome of the fungal wheat pathogen Mycosphaerella graminicolarevealsdispensomestructure,chromosomeplasticity,andstealth pathogenesis. PLoS Genet 7:e1002070. http://dx.doi.org/10.1371/journal.pgen.1002070.
51. Dhillon B, Gill N, Hamelin RC, Goodwin SB. 2014. The landscape of transposable elements in the finished genome of the fungal wheat patho- gen Mycosphaerella graminicola. BMC Genomics 15:1132. http://dx.doi.org/10.1186/1471-2164-15-1132.
52. Travers KJ, Chin CS, Rank DR, Eid JS, Turner SW. 2010. A flexible and efficient template format for circular consensus sequencing and SNP detection. NucleicAcidsRes 38: e159. http://dx.doi.org/10.1093/nar/gkq543.
53. Benson G. 1999. Tandem repeats finder: a program to analyze DNA se- quences. Nucleic Acids Res 27:573-580. http://dx.doi.org/10.1093/nar/27.2.573.
54. Smit AFA, Hubley R, Green P. 2006. RepeatMasker Open-3.0. 1996-2010. http://www.repeatmasker.org.
55. Xu Z, Wang H. 2007. LTR_FINDER: an efficient tool for the prediction of full-length LTR retrotransposons. Nucleic Acids Res 35:W265-W268. http://dx.doi.org/10.1093/nar/gkm286.
56. Price AL, Jones NC, Pevzner PA. 2005. De novo identification of repeat families in large genomes. Bioinformatics 21(Suppl 1):i351-i358. http://dx.doi.org/10.1093/bioinformatics/bti1018.
57. Jurka J, Kapitonov VV, Pavlicek A, Klonowski P, Kohany O, Walichie- wicz J. 2005. Repbase update, a database of eukaryotic repetitive elements. Cytogenet Genome Res 110:462-467. http://dx.doi.org/10.1159/000084979.
58. Langmead B, Trapnell C, Pop M, Salzberg SL. 2009. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10:R25. http://dx.doi.org/10.1186/gb-2009-10-3-r25.
59. Garrison E, Marth G. 2012. Haplotype-based variant detection from short-read sequencing. arXiv:1207.3907 (q-bio.GN). http://arxiv.org/abs/1207.3907v1.