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The Third Revolution in Sequencing Technology

van Dijk, Erwin L., Jaszczyszyn, Yan, Naquin, Delphine, Thermes, Claude·2018·Trends in Genetics
DOI 10.1016/j.tig.2018.05.008
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Abstract

Forty years ago the advent of Sanger sequencing was revolutionary as it allowed complete genome sequences to be deciphered for the first time. A second revolution came when next-generation sequencing (NGS) technologies appeared, which made genome sequencing much cheaper and faster. However, NGS methods have several drawbacks and pitfalls, most notably their short reads. Recently, third-generation/long-read methods appeared, which can produce genome assemblies of unprecedented quality. Moreover, these technologies can directly detect epigenetic modifications on native DNA and allow whole-transcript sequencing without the need for assembly. This marks the third revolution in sequencing technology. Here we review and compare the various long-read methods. We discuss their applications and their respective strengths and weaknesses and provide future perspectives.

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Research works printed but not linked: 70

  1. Maxam, 1977, A new method for sequencing DNA, Proc. Natl. Acad. Sci. U. S. A., 74, 560, 10.1073/pnas.74.2.560 · DOI
  2. Sanger, 1977, DNA sequencing with chain-terminating inhibitors, Proc. Natl. Acad. Sci. U. S. A., 74, 5463, 10.1073/pnas.74.12.5463 · DOI · Paper page
  3. Lander, 2001, Initial sequencing and analysis of the human genome, Nature, 409, 860, 10.1038/35057062 · DOI · Paper page
  4. Schloss, 2008, How to get genomes at one ten-thousandth the cost, Nat. Biotechnol., 26, 1113, 10.1038/nbt1008-1113 · DOI
  5. van Dijk, 2014, Ten years of next-generation sequencing technology, Trends Genet., 30, 418, 10.1016/j.tig.2014.07.001 · DOI
  6. Goodwin, 2016, Coming of age: ten years of next-generation sequencing technologies, Nat. Rev. Genet., 17, 333, 10.1038/nrg.2016.49 · DOI · Paper page
  7. Salzberg, 2005, Beware of mis-assembled genomes, Bioinformatics, 21, 4320, 10.1093/bioinformatics/bti769 · DOI
  8. Weischenfeldt, 2013, Phenotypic impact of genomic structural variation: insights from and for human disease, Nat. Rev. Genet., 14, 125, 10.1038/nrg3373 · DOI
  9. Tewhey, 2011, The importance of phase information for human genomics, Nat. Rev. Genet., 12, 215, 10.1038/nrg2950 · DOI
  10. Schadt, 2010, A window into third-generation sequencing, Hum. Mol. Genet., 19, R227, 10.1093/hmg/ddq416 · DOI
  11. Pushkarev, 2009, Single-molecule sequencing of an individual human genome, Nat. Biotechnol., 27, 847, 10.1038/nbt.1561 · DOI
  12. Eid, 2009, Real-time DNA sequencing from single polymerase molecules, Science, 323, 133, 10.1126/science.1162986 · DOI · Paper page
  13. Jain, 2015, Improved data analysis for the MinION nanopore sequencer, Nat. Methods, 12, 351, 10.1038/nmeth.3290 · DOI
  14. Voskoboynik, 2013, The genome sequence of the colonial chordate, Botryllus schlosseri, Elife, 2, 10.7554/eLife.00569 · DOI
  15. Zheng, 2016, Haplotyping germline and cancer genomes with high-throughput linked-read sequencing, Nat. Biotechnol., 34, 303, 10.1038/nbt.3432 · DOI
  16. Chu, 2017, Innovations and challenges in detecting long read overlaps: an evaluation of the state-of-the-art, Bioinformatics, 33, 1261, 10.1093/bioinformatics/btw811 · DOI
  17. Travers, 2010, A flexible and efficient template format for circular consensus sequencing and SNP detection, Nucleic Acids Res., 38, e159, 10.1093/nar/gkq543 · DOI
  18. Deamer, 2016, Three decades of nanopore sequencing, Nat. Biotechnol., 34, 518, 10.1038/nbt.3423 · DOI · Paper page
  19. Manrao, 2012, Reading DNA at single-nucleotide resolution with a mutant MspA nanopore and phi29 DNA polymerase, Nat. Biotechnol., 30, 349, 10.1038/nbt.2171 · DOI
  20. Brown, 2016, Nanopore development at Oxford Nanopore, Nat. Biotechnol., 34, 810, 10.1038/nbt.3622 · DOI
  21. Jain, 2018, Nanopore sequencing and assembly of a human genome with ultra-long reads, Nat. Biotechnol., 36, 338, 10.1038/nbt.4060 · DOI · Paper page
  22. Jain, 2017, MinION Analysis and Reference Consortium: phase 2 data release and analysis of R9.0 chemistry, F1000Res., 6, 760, 10.12688/f1000research.11354.1 · DOI · Paper page
  23. Li, 2016, INC-seq: accurate single molecule reads using nanopore sequencing, Gigascience, 5, 34, 10.1186/s13742-016-0140-7 · DOI
  24. Marks, 2017, Resolving the full spectrum of human genome variation using linked-reads, BioRxiv
  25. Genovese, 2013, Using population admixture to help complete maps of the human genome, Nat. Genet., 45, 406, 10.1038/ng.2565 · DOI
  26. Schmidt, 2016, Disease-associated repeat instability and mismatch repair, DNA Repair (Amst.), 38, 117, 10.1016/j.dnarep.2015.11.008 · DOI
  27. Chaisson, 2015, Resolving the complexity of the human genome using single-molecule sequencing, Nature, 517, 608, 10.1038/nature13907 · DOI
  28. Seo, 2016, De novo assembly and phasing of a Korean human genome, Nature, 538, 243, 10.1038/nature20098 · DOI
  29. Quick, 2015, Rapid draft sequencing and real-time nanopore sequencing in a hospital outbreak of Salmonella, Genome Biol., 16, 114, 10.1186/s13059-015-0677-2 · DOI
  30. Loman, 2015, A complete bacterial genome assembled de novo using only nanopore sequencing data, Nat. Methods, 12, 733, 10.1038/nmeth.3444 · DOI
  31. Tyson, 2018, MinION-based long-read sequencing and assembly extends the Caenorhabditis elegans reference genome, Genome Res., 28, 266, 10.1101/gr.221184.117 · DOI
  32. Michael, 2018, High contiguity Arabidopsis thaliana genome assembly with a single nanopore flow cell, Nat. Commun., 9, 541, 10.1038/s41467-018-03016-2 · DOI
  33. Giordano, 2017, De novo yeast genome assemblies from MinION, PacBio and MiSeq platforms, Sci. Rep., 7, 3935, 10.1038/s41598-017-03996-z · DOI
  34. Rudd, 2004, Analysis of the centromeric regions of the human genome assembly, Trends Genet., 20, 529, 10.1016/j.tig.2004.08.008 · DOI
  35. Jain, 2017, Linear assembly of a human Y centromere using nanopore long reads, BioRxiv
  36. McCoy, 2014, Illumina TruSeq synthetic long-reads empower de novo assembly and resolve complex, highly-repetitive transposable elements, PLoS One, 9, 10.1371/journal.pone.0106689 · DOI
  37. Li, 2015, Illumina synthetic long read sequencing allows recovery of missing sequences even in the “finished” C. elegans genome, Sci. Rep., 5, 10814, 10.1038/srep10814 · DOI
  38. Hulse-Kemp, 2018, Reference quality assembly of the 3.5-Gb genome of Capsicum annuum from a single linked-read library, Hortic. Res., 5, 4, 10.1038/s41438-017-0011-0 · DOI
  39. Porubsky, 2017, Dense and accurate whole-chromosome haplotyping of individual genomes, Nat. Commun., 8, 129, 10.1038/s41467-017-01389-4 · DOI
  40. Hui, 2017, Universal haplotype-based noninvasive prenatal testing for single gene diseases, Clin. Chem., 63, 513, 10.1373/clinchem.2016.268375 · DOI
  41. Lam, 2012, Genome mapping on nanochannel arrays for structural variation analysis and sequence assembly, Nat. Biotechnol., 30, 771, 10.1038/nbt.2303 · DOI
  42. Burton, 2013, Chromosome-scale scaffolding of de novo genome assemblies based on chromatin interactions, Nat. Biotechnol., 31, 1119, 10.1038/nbt.2727 · DOI · Paper page
  43. Mascher, 2017, A chromosome conformation capture ordered sequence of the barley genome, Nature, 544, 427, 10.1038/nature22043 · DOI · Paper page
  44. Bickhart, 2017, Single-molecule sequencing and chromatin conformation capture enable de novo reference assembly of the domestic goat genome, Nat. Genet., 49, 643, 10.1038/ng.3802 · DOI
  45. Steijger, 2013, Assessment of transcript reconstruction methods for RNA-seq, Nat. Methods, 10, 1177, 10.1038/nmeth.2714 · DOI · Paper page
  46. Kalsotra, 2011, Functional consequences of developmentally regulated alternative splicing, Nat. Rev. Genet., 12, 715, 10.1038/nrg3052 · DOI · Paper page
  47. Tilgner, 2014, Defining a personal, allele-specific, and single-molecule long-read transcriptome, Proc. Natl. Acad. Sci. U. S. A., 111, 9869, 10.1073/pnas.1400447111 · DOI · Paper page
  48. Wang, 2016, Unveiling the complexity of the maize transcriptome by single-molecule long-read sequencing, Nat. Commun., 7, 11708, 10.1038/ncomms11708 · DOI
  49. Lagarde, 2017, High-throughput annotation of full-length long noncoding RNAs with capture long-read sequencing, Nat. Genet., 49, 1731, 10.1038/ng.3988 · DOI
  50. Weirather, 2017, Comprehensive comparison of Pacific Biosciences and Oxford Nanopore Technologies and their applications to transcriptome analysis, F1000Res., 6, 100, 10.12688/f1000research.10571.2 · DOI
  51. Garalde, 2018, Highly parallel direct RNA sequencing on an array of nanopores, Nat. Methods, 15, 201, 10.1038/nmeth.4577 · DOI
  52. Smith, 2017, Reading canonical and modified nucleotides in 16S ribosomal RNA using nanopore direct RNA sequencing, BioRxiv
  53. Tilgner, 2015, Comprehensive transcriptome analysis using synthetic long-read sequencing reveals molecular co-association of distant splicing events, Nat. Biotechnol., 33, 736, 10.1038/nbt.3242 · DOI · Paper page
  54. Tilgner, 2018, Microfluidic isoform sequencing shows widespread splicing coordination in the human transcriptome, Genome Res., 28, 231, 10.1101/gr.230516.117 · DOI · Paper page
  55. Bierne, 2012, Epigenetics and bacterial infections, Cold Spring Harb. Perspect. Med., 2, 10.1101/cshperspect.a010272 · DOI
  56. Greer, 2015, DNA methylation on N6-adenine in C. elegans, Cell, 161, 868, 10.1016/j.cell.2015.04.005 · DOI
  57. Murray, 2012, The methylomes of six bacteria, Nucleic Acids Res., 40, 11450, 10.1093/nar/gks891 · DOI
  58. Ichikawa, 2017, Centromere evolution and CpG methylation during vertebrate speciation, Nat. Commun., 8, 1833, 10.1038/s41467-017-01982-7 · DOI
  59. Rand, 2017, Mapping DNA methylation with high-throughput nanopore sequencing, Nat. Methods, 14, 411, 10.1038/nmeth.4189 · DOI · Paper page
  60. Simpson, 2017, Detecting DNA cytosine methylation using nanopore sequencing, Nat. Methods, 14, 407, 10.1038/nmeth.4184 · DOI
  61. Euskirchen, 2017, Same-day genomic and epigenomic diagnosis of brain tumors using real-time nanopore sequencing, Acta Neuropathol., 134, 691, 10.1007/s00401-017-1743-5 · DOI
  62. Pootakham, 2017, High resolution profiling of coral-associated bacterial communities using full-length 16S rRNA sequence data from PacBio SMRT sequencing system, Sci. Rep., 7, 2774, 10.1038/s41598-017-03139-4 · DOI
  63. Shin, 2016, Analysis of the mouse gut microbiome using full-length 16S rRNA amplicon sequencing, Sci. Rep., 6, 29681, 10.1038/srep29681 · DOI
  64. Kuleshov, 2016, Synthetic long-read sequencing reveals intraspecies diversity in the human microbiome, Nat. Biotechnol., 34, 64, 10.1038/nbt.3416 · DOI
  65. Merker, 2018, Long-read genome sequencing identifies causal structural variation in a Mendelian disease, Genet. Med., 20, 159, 10.1038/gim.2017.86 · DOI
  66. Quick, 2016, Real-time, portable genome sequencing for Ebola surveillance, Nature, 530, 228, 10.1038/nature16996 · DOI
  67. Faria, 2016, Mobile real-time surveillance of Zika virus in Brazil, Genome Med., 8, 97, 10.1186/s13073-016-0356-2 · DOI · Paper page
  68. Stoddart, 2010, Multiple base-recognition sites in a biological nanopore: two heads are better than one, Angew. Chem. Int. Ed. Engl., 49, 556, 10.1002/anie.200905483 · DOI
  69. Larkin, 2017, Length-independent DNA packing into nanopore zero-mode waveguides for low-input DNA sequencing, Nat. Nanotechnol., 12, 1169, 10.1038/nnano.2017.176 · DOI
  70. Kolmogorov, 2017, Single-molecule protein identification by sub-nanopore sensors, PLoS Comput. Biol., 13, 10.1371/journal.pcbi.1005356 · DOI

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Metadata

Authors
van Dijk, E. L., Jaszczyszyn, Y., Naquin, D., & Thermes, C.
Venue
Trends in Genetics
Publisher
Elsevier BV
Published
2018-09
Volume
34
Issue
9
Pages
666-681
ISSN
0168-9525
DOI
10.1016/j.tig.2018.05.008
Cited by
1,057
References
6
Language
en
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