Cited by 1,057

The DOI matches its Crossref record; 6 of the 6 references it cites were found in a registry or an index.

The Third Revolution in Sequencing Technology

van Dijk, Erwin L., Jaszczyszyn, Yan, Naquin, Delphine, Thermes, Claude·2018·Trends in Genetics

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.

Overview

Integrity signals

Registry

Crossref · 10.1016/j.tig.2018.05.008

Cites

6 of 6 references verified0 citation errors · 0 not checkable

Statistics

Recomputing p-values needs the paper’s full text.

Verification

Claims the paper makes

This paper’s full text isn’t openly available, so its claims and self-check weren’t run. The registry and citation checks still apply.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Citations

Cites

Flagged first, then by citations

Show all 6 references

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

Cited by

Sorted by citations

See all 1,057

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
Cited by
1,057
References
6
Language
en

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review