CoChat
Sign Up
Cited by 3,097Genomics and Phylogenetic StudiesChromosomal and Genetic VariationsGenomic variations and chromosomal abnormalities

Towards complete and error-free genome assemblies of all vertebrate species

Open access
Rhie, Arang, McCarthy, Shane A., Fedrigo, Olivier, Damas, Joana, Formenti, Giulio, Koren, Sergey, Uliano-Silva, Marcela, Chow, William +119 more·2021·Nature
DOI 10.1038/s41586-021-03451-0PMC PMC8081667

Published version of a preprint

Open this paper in CoChat — free accountOpen PDF

Abstract

High-quality and complete reference genome assemblies are fundamental for the application of genomics to biology, disease, and biodiversity conservation. However, such assemblies are available for only a few non-microbial species 1–4 . To address this issue, the international Genome 10K (G10K) consortium 5,6 has worked over a five-year period to evaluate and develop cost-effective methods for assembling highly accurate and nearly complete reference genomes. Here we present lessons learned from generating assemblies for 16 species that represent six major vertebrate lineages. We confirm that long-read sequencing technologies are essential for maximizing genome quality, and that unresolved complex repeats and haplotype heterozygosity are major sources of assembly error when not handled correctly. Our assemblies correct substantial errors, add missing sequence in some of the best historical reference genomes, and reveal biological discoveries. These include the identification of many false gene duplications, increases in gene sizes, chromosome rearrangements that are specific to lineages, a repeated independent chromosome breakpoint in bat genomes, and a canonical GC-rich pattern in protein-coding genes and their regulatory regions. Adopting these lessons, we have embarked on the Vertebrate Genomes Project (VGP), an international effort to generate high-quality, complete reference genomes for all of the roughly 70,000 extant vertebrate species and to help to enable a new era of discovery across the life sciences.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1038/s41586-021-03451-0

Cites

8 of 8 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

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?

  • Thousands of newly sequenced chromosome-scale genomes are rapidly filling phylogenetic gaps of animal diversity.

    “thousands of newly sequenced chromosome-scale genomes are rapidly filling phylogenetic gaps of animal diversity”

    From Topological Approaches in Animal Comparative Genomics (2026) · cites this paper as [1]

    The Vertebrate Genomes Project section describes a plan to sequence representatives across vertebrate orders, families and genera, supporting the idea of filling phylogenetic gaps. But the Abstract reports assemblies for 16 species, while the thousands of additional genomes are future goals—not newly sequenced genomes already filling gaps across animal diversity. Page numbers are unavailable in our copy. (LLM, conf=0.85)

    Experimental — accuracy not yet measured

  • Genome sequencing and assembly have become increasingly affordable and computationally tractable thanks to long-read sequencing technologies, DNA proximity ligation sequencing techniques, and genome sequencing consortia.

    “Genome sequencing and assembly have become increasingly affordable and computationally tractable thanks to the development of long-read sequencing technologies like the Pacific Biosciences and Oxford Nanopore platforms (52); the development of DNA proximity ligation sequencing techniques, like Hi-C, for genome scaffolding (53–55); and the efforts of genome sequencing consortia (1, 2, 4, 56)”

    From Topological Approaches in Animal Comparative Genomics (2026) · cites this paper as [1]

    The Main section identifies the G10K consortium and describes its work evaluating sequencing and assembly approaches; the Vertebrate Genomes Project section describes plans to scale genome production using improved technology and computational infrastructure. The paper also says sequencing became more affordable, but it does not establish that consortium efforts themselves made sequencing and assembly more affordable or computationally tractable. The citations for long-read platforms and Hi-C are attached to other parts of the citing sentence. (LLM, conf=0.78)

    Experimental — accuracy not yet measured

  • TOGA provides a general strategy to cope with the annotation and orthology inference bottleneck.

    “With the tree of life becoming more densely populated with genomes, thanks to great efforts of large-scale projects and numerous laboratories (26–28, 39), TOGA provides a general strategy to cope with the annotation and orthology inference bottleneck.”

    From Integrating gene annotation with orthology inference at scale (2023) · cites this paper as [26]

  • Comparative genomic analyses usually test for correlations between traits.

    “Comparative genomic analyses usually test for correlations between traits.”

    From A phylogenetic approach to comparative genomics (2025) · cites this paper as [80]

    The Methods > Curation passage describes comparative genomics used to check assembly structure, while Fig. 2 reports correlations among genome and assembly measures. Neither passage says that comparative genomic analyses usually test correlations between traits; searches for that formulation and for trait or phenotype correlations found no supporting passage in our copy. (LLM, conf=0.74)

    Experimental — accuracy not yet measured

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 95

  1. [1]International Human Genome Sequencing Consortium Initial sequencing and analysis of the human genome Nature 2001 409 860 921 11237011
  2. [2]Sulston J The C. elegans genome sequencing project: a beginning Nature 1992 356 37 41 1538779
  3. [4]Howe K The zebrafish reference genome sequence and its relationship to the human genome Nature 2013 496 498 503 23594743 PMC3703927
  4. [5]Genome 10K Community of Scientists Genome 10K: a proposal to obtain whole-genome sequence for 10,000 vertebrate species J. Hered. 2009 100 659 674 19892720 PMC2877544
  5. [6]Koepfli K-P Paten B the Genome 10K Community of Scientists O’Brien SJ The Genome 10K Project: a way forward Annu. Rev. Anim. Biosci. 2015 3 57 111 25689317 PMC5837290
  6. [7]Venter JC The sequence of the human genome Science 2001 291 1304 1351 11181995
  7. [8]Adams MD The genome sequence of Drosophila melanogaster Science 2000 287 2185 2195 10731132
  8. [9]Shendure J Ji H Next-generation DNA sequencing Nat. Biotechnol. 2008 26 1135 1145 18846087
  9. [10]Yin Z-T Revisiting avian ‘missing’ genes from de novo assembled transcripts BMC Genomics 2019 20 4 30611188 PMC6321700
  10. [11]Korlach J De novo PacBio long-read and phased avian genome assemblies correct and add to reference genes generated with intermediate and short reads Gigascience 2017 6 1 16 29020750 PMC5632298
  11. [12]Kelley DR Salzberg SL Detection and correction of false segmental duplications caused by genome mis-assembly Genome Biol. 2010 11 R28 20219098 PMC2864568
  12. [13]Roach MJ Schmidt SA Borneman AR Purge Haplotigs: allelic contig reassignment for third-gen diploid genome assemblies BMC Bioinformatics 2018 19 460 30497373 PMC6267036
  13. [14]Guan D Identifying and removing haplotypic duplication in primary genome assemblies Bioinformatics 2020 36 2896 2898 31971576 PMC7203741
  14. [15]Bradnam KR Assemblathon 2: evaluating de novo methods of genome assembly in three vertebrate species Gigascience 2013 2 10 23870653 PMC3844414
  15. [16]Zhang G Comparative genomics reveals insights into avian genome evolution and adaptation Science 2014 346 1311 1320 25504712 PMC4390078
  16. [17]Chin C-S Phased diploid genome assembly with single-molecule real-time sequencing Nat. Methods 2016 13 1050 1054 27749838 PMC5503144
  17. [18]Bresler G Bresler M Tse D Optimal assembly for high throughput shotgun sequencing BMC Bioinformatics 2013 14 S18 23902516 PMC3706340
  18. [19]Warren WC The genome of a songbird Nature 2010 464 757 762 20360741 PMC3187626
  19. [20]Koren, S. et al. De novo assembly of haplotype-resolved genomes with trio binning. Nat. Biotechnol. (2018). PMC6476705 30346939
  20. [21]Koren S Phillippy AM Simpson JT Loman NJ Loose M Reply to ‘Errors in long-read assemblies can critically affect protein prediction’ Nat. Biotechnol. 2019 37 127 128 30670797
  21. [22]Vollger MR Long-read sequence and assembly of segmental duplications Nat. Methods 2019 16 88 94 30559433 PMC6382464
  22. [23]Rhie A Walenz BP Koren S Phillippy AM Merqury: reference-free quality, completeness, and phasing assessment for genome assemblies Genome Biol. 2020 21 245 32928274 PMC7488777
  23. [24]Waterhouse RM BUSCO applications from quality assessments to gene prediction and phylogenomics Mol. Biol. Evol. 2018 35 543 548 29220515 PMC5850278
  24. [25]Howe K Significantly improving the quality of genome assemblies through curation Gigascience 2021 10 giaa153 33420778 PMC7794651
  25. [26]Zhou, Y. et al. Platypus and echidna genomes reveal mammalian biology and evolution. Nature10.1038/s41586-020-03039-0 (2021). PMC8081666 33408411
  26. [27]Kim, J. et al. False gene and chromosome losses affected by assembly and sequence errors. Preprint at 10.1101/2021.04.09.438906 (2021). · DOI
  27. [28]Lewin HA Graves JAM Ryder OA Graphodatsky AS O’Brien SJ Precision nomenclature for the new genomics Gigascience 2019 8 giz086 31437278 PMC6705538
  28. [29]Kronenberg, Z. N. et al. Extended haplotype phasing of de novo genome assemblies with FALCON-Phase. Nat. Commun. 10.1038/s41467-020-20536-y (2021). PMC8081726 33911078 · DOI
  29. [30]Ewing B Hillier L Wendl MC Green P Base-calling of automated sequencer traces using phred. I. Accuracy assessment Genome Res. 1998 8 175 185 9521921
  30. [31]Tomaszkiewicz M Medvedev P Makova KD Y and W chromosome assemblies: approaches and discoveries Trends Genet. 2017 33 266 282 28236503
  31. [32]Kolesnikov AA Gerasimov ES Diversity of mitochondrial genome organization Biochem. (Mosc.) 2012 77 1424 1435 23379519
  32. [33]Formenti, G. et al. Complete vertebrate mitogenomes reveal widespread repeats and gene duplications. Genome Biol. (in the press). PMC8082918 33910595
  33. [34]Harrison GLA Four new avian mitochondrial genomes help get to basic evolutionary questions in the late cretaceous Mol. Biol. Evol. 2004 21 974 983 14739240
  34. [35]Zhao H The complete mitochondrial genome of the Anabas testudineus (Perciformes, Anabantidae) Mitochondrial DNA A DNA Mapp. Seq. Anal. 2016 27 1005 1007 24960569
  35. [36]Suzuki A How the kinetochore couples microtubule force and centromere stretch to move chromosomes Nat. Cell Biol. 2016 18 382 392 26974660 PMC4814359
  36. [38]Robinson R For mammals, loss of yolk and gain of milk went hand in hand PLoS Biol. 2008 6 e77 20076706 PMC2267822
  37. [39]Brandl K Yip1 domain family, member 6 (Yipf6) mutation induces spontaneous intestinal inflammation in mice Proc. Natl Acad. Sci. USA 2012 109 12650 12655 22802641 PMC3412000
  38. [40]Malmstrøm M Evolution of the immune system influences speciation rates in teleost fishes Nat. Genet. 2016 48 1204 1210 27548311
  39. [41]Japundžić-Žigon N Lozić M Šarenac O Murphy D Vasopressin & oxytocin in control of the cardiovascular system: an updated review Curr. Neuropharmacol. 2020 18 14 33 31544693 PMC7327933
  40. [42]Cataldo I Azhari A Esposito G A review of oxytocin and arginine-vasopressin receptors and their modulation of autism spectrum disorder Front. Mol. Neurosci. 2018 11 27 29487501 PMC5816822
  41. [44]Ko, B. J. et al. Widespread false gene gains caused by duplication errors in genome assemblies. Preprint at 10.1101/2021.04.09.438957 (2021). PMC9516828 36167596 · DOI
  42. [45]Lemaire S Characterizing the interplay between gene nucleotide composition bias and splicing Genome Biol. 2019 20 259 31783898 PMC6883713
  43. [46]Zhang L Kasif S Cantor CR Broude NE GC/AT-content spikes as genomic punctuation marks Proc. Natl Acad. Sci. USA 2004 101 16855 16860 15548610 PMC534751
  44. [47]Jarvis ED Global view of the functional molecular organization of the avian cerebrum: mirror images and functional columns J. Comp. Neurol. 2013 521 3614 3665 23818122 PMC4145244
  45. [48]Kubikova L Wada K Jarvis ED Dopamine receptors in a songbird brain J. Comp. Neurol. 2010 518 741 769 20058221 PMC2904815
  46. [49]Sémon M Wolfe KH Rearrangement rate following the whole-genome duplication in teleosts Mol. Biol. Evol. 2007 24 860 867 17218642
  47. [50]Jebb D Six reference-quality genomes reveal evolution of bat adaptations Nature 2020 583 578 584 32699395 PMC8075899
  48. [52]Warren WC A new chicken genome assembly provides insight into avian genome structure G3 (Bethesda) 2017 7 109 117 27852011 PMC5217101
  49. [54]Rodriguez-Agudo D StarD5: an ER stress protein regulates plasma membrane and intracellular cholesterol homeostasis J. Lipid Res. 2019 60 1087 1098 31015253 PMC6547630
  50. [55]Kim J Reconstruction and evolutionary history of eutherian chromosomes Proc. Natl Acad. Sci. USA 2017 114 E5379 E5388 28630326 PMC5502614
  51. [56]Lin B Dutta B Fraser IDC Systematic investigation of multi-TLR sensing identifies regulators of sustained gene activation in macrophages Cell Syst. 2017 5 25 37.e3 28750197 PMC5584636
  52. [57]Theofanopoulou, C., Gedman, G. L., Cahill, J. A., Boeckx, C. & Jarvis, E. D. Universal nomenclature for oxytocin-vasotocin ligand and receptor families. Nature10.1038/s41586-020-03040-7 (2021). PMC8081664 33911268
  53. [58]Ocampo Daza D Haitina T Reconstruction of the carbohydrate 6-O sulfotransferase gene family evolution in vertebrates reveals novel member, CHST16, lost in amniotes Genome Biol. Evol. 2020 12 993 1012 32652010 PMC7353957
  54. [59]Damas J Broad host range of SARS-CoV-2 predicted by comparative and structural analysis of ACE2 in vertebrates Proc. Natl Acad. Sci. USA 2020 117 22311 22322 32826334 PMC7486773
  55. [60]Dussex, N. et al. Population genomics reveals the impact of long-term small population size in the critically endangered kākāpō. Cell Genom. (in the press). PMC9903828 36777713
  56. [61]Teeling EC Bat biology, genomes, and the Bat1K project: to generate chromosome-level genomes for all living bat species Annu. Rev. Anim. Biosci. 2018 6 23 46 29166127
  57. [62]Lewin HA Earth BioGenome Project: sequencing life for the future of life Proc. Natl Acad. Sci. USA 2018 115 4325 4333 29686065 PMC5924910
  58. [63]Jarvis ED Whole-genome analyses resolve early branches in the tree of life of modern birds Science 2014 346 1320 1331 25504713 PMC4405904
  59. [64]Li S Genomic signatures of near-extinction and rebirth of the crested ibis and other endangered bird species Genome Biol. 2014 15 557 25496777 PMC4290368
  60. [65]Koren S Phillippy AM One chromosome, one contig: complete microbial genomes from long-read sequencing and assembly Curr. Opin. Microbiol. 2015 23 110 120 25461581
  61. [66]Jenjaroenpun P Complete genomic and transcriptional landscape analysis using third-generation sequencing: a case study of Saccharomyces cerevisiae CEN.PK113-7D Nucleic Acids Res. 2018 46 e38 29346625 PMC5909453
  62. [67]Tyson JR MinION-based long-read sequencing and assembly extends the Caenorhabditis elegans reference genome Genome Res. 2018 28 266 274 29273626 PMC5793790
  63. [68]Miga KH Telomere-to-telomere assembly of a complete human X chromosome Nature 2020 585 79 84 32663838 PMC7484160
  64. [69]Logsdon, G. A. et al. The structure, function and evolution of a complete human chromosome 8. Nature10.1038/s41586-021-03420-7 (2021). PMC8099727 33828295
  65. [70]Beçak, M. L., Beçak, W., Roberts, F. L., Shoffner, R. N. & Volpe, P. (eds.) Chromosome Atlas: Fish, Amphibians, Reptiles, and Birds Vol. 2 (Springer, 1973).
  66. [71]Vurture GW GenomeScope: fast reference-free genome profiling from short reads Bioinformatics 2017 33 2202 2204 28369201 PMC5870704
  67. [72]Kumar S Stecher G Suleski M Hedges SB TimeTree: a resource for timelines, timetrees, and divergence times Mol. Biol. Evol. 2017 34 1812 1819 28387841
  68. [73]Ondov BD Mash: fast genome and metagenome distance estimation using MinHash Genome Biol. 2016 17 132 27323842 PMC4915045
  69. [75]Morgulis A Gertz EM Schäffer AA Agarwala R WindowMasker: window-based masker for sequenced genomes Bioinformatics 2006 22 134 141 16287941
  70. [76]Chin C-S Nonhybrid, finished microbial genome assemblies from long-read SMRT sequencing data Nat. Methods 2013 10 563 569 23644548
  71. [77]Koren S Canu: scalable and accurate long-read assembly via adaptive k-mer weighting and repeat separation Genome Res. 2017 27 722 736 28298431 PMC5411767
  72. [78]Weisenfeld NI Kumar V Shah P Church DM Jaffe DB Direct determination of diploid genome sequences Genome Res. 2017 27 757 767 28381613 PMC5411770
  73. [79]Ghurye J Integrating Hi-C links with assembly graphs for chromosome-scale assembly PLoS Comput. Biol. 2019 15 e1007273 31433799 PMC6719893
  74. [80]Lieberman-Aiden E Comprehensive mapping of long-range interactions reveals folding principles of the human genome Science 2009 326 289 293 19815776 PMC2858594
  75. [81]Luo R SOAPdenovo2: an empirically improved memory-efficient short-read de novo assembler Gigascience 2012 1 18 23587118 PMC3626529
  76. [82]English AC Mind the gap: upgrading genomes with Pacific Biosciences RS long-read sequencing technology PLoS ONE 2012 7 e47768 23185243 PMC3504050
  77. [83]Bishara A Read clouds uncover variation in complex regions of the human genome Genome Res. 2015 25 1570 1580 26286554 PMC4579342
  78. [84]Walker BJ Pilon: an integrated tool for comprehensive microbial variant detection and genome assembly improvement PLoS ONE 2014 9 e112963 25409509 PMC4237348
  79. [85]Garrison, E. & Marth, G. Haplotype-based variant detection from short-read sequencing. Preprint at http://arxiv.org/abs/1207.3907 (2012). · arXiv
  80. [86]Jain C Koren S Dilthey A Phillippy AM Aluru S A fast adaptive algorithm for computing whole-genome homology maps Bioinformatics 2018 34 i748 i756 30423094 PMC6129286
  81. [90]Li H Minimap2: pairwise alignment for nucleotide sequences Bioinformatics 2018 34 3094 3100 29750242 PMC6137996
  82. [91]Chaisson MJ Tesler G Mapping single molecule sequencing reads using basic local alignment with successive refinement (BLASR): application and theory BMC Bioinformatics 2012 13 238 22988817 PMC3572422
  83. [93]Dierckxsens N Mardulyn P Smits G NOVOPlasty: de novo assembly of organelle genomes from whole genome data Nucleic Acids Res. 2017 45 e18 28204566 PMC5389512
  84. [94]Soorni A Haak D Zaitlin D Bombarely A Organelle_PBA, a pipeline for assembling chloroplast and mitochondrial genomes from PacBio DNA sequencing data BMC Genomics 2017 18 49 28061749 PMC5219736
  85. [95]Chow W gEVAL — a web-based browser for evaluating genome assemblies Bioinformatics 2016 32 2508 2510 27153597 PMC4978925
  86. [96]Durand NC Juicebox provides a visualization system for Hi-C contact maps with unlimited zoom Cell Syst. 2016 3 99 101 27467250 PMC5596920
  87. [97]Kerpedjiev P HiGlass: web-based visual exploration and analysis of genome interaction maps Genome Biol. 2018 19 125 30143029 PMC6109259
  88. [98]Camacho C BLAST+: architecture and applications BMC Bioinformatics 2009 10 421 20003500 PMC2803857
  89. [99]Harris, R. S. Improved Pairwise Alignment of Genomic DNA. Thesis, Pennsylvania State Univ. (2007).
  90. [100]Kent WJ Baertsch R Hinrichs A Miller W Haussler D Evolution’s cauldron: duplication, deletion, and rearrangement in the mouse and human genomes Proc. Natl Acad. Sci. USA 2003 100 11484 11489 14500911 PMC208784
  91. [101]Kolmogorov M Raney B Paten B Pham S Ragout—a reference-assisted assembly tool for bacterial genomes Bioinformatics 2014 30 i302 i309 24931998 PMC4058940
  92. [102]Farré M Novel insights into chromosome evolution in birds, archosaurs, and reptiles Genome Biol. Evol. 2016 8 2442 2451 27401172 PMC5010900
  93. [104]Tarailo-Graovac M Chen N Using RepeatMasker to identify repetitive elements in genomic sequences Curr. Protoc. Bioinformatics 2009 25 4.10.1 4.10.14 19274634
  94. [105]Krumsiek J Arnold R Rattei T Gepard: a rapid and sensitive tool for creating dotplots on genome scale Bioinformatics 2007 23 1026 1028 17309896
  95. [107]Kurtz S Versatile and open software for comparing large genomes Genome Biol. 2004 5 R12 14759262 PMC395750

Cited by

Sorted by citations

Authors
Rhie, A., McCarthy, S. A., Fedrigo, O., Damas, J., Formenti, G., Koren, S., Uliano-Silva, M., Chow, W., Fungtammasan, A., Kim, J., Lee, C., Ko, B. J., Chaisson, M., Gedman, G. L., Cantin, L. J., Thibaud-Nissen, F., Haggerty, L., Bista, I., Smith, M., Haase, B., Mountcastle, J., Winkler, S., Paez, S., Howard, J., Vernes, S. C., Lama, T. M., Grutzner, F., Warren, W. C., Balakrishnan, C. N., Burt, D., George, J. M., Biegler, M. T., Iorns, D., Digby, A., Eason, D., Robertson, B., Edwards, T., Wilkinson, M., Turner, G., Meyer, A., Kautt, A. F., Franchini, P., Detrich, H. W., Svardal, H., Wagner, M., Naylor, G. J. P., Pippel, M., Malinsky, M., Mooney, M., Simbirsky, M., Hannigan, B. T., Pesout, T., Houck, M., Misuraca, A., Kingan, S. B., Hall, R., Kronenberg, Z., Sović, I., Dunn, C., Ning, Z., Hastie, A., Lee, J., Selvaraj, S., Green, R. E., Putnam, N. H., Gut, I., Ghurye, J., Garrison, E., Sims, Y., Collins, J., Pelan, S., Torrance, J., Tracey, A., Wood, J., Dagnew, R. E., Guan, D., London, S. E., Clayton, D. F., Mello, C. V., Friedrich, S. R., Lovell, P. V., Osipova, E., Al-Ajli, F. O., Secomandi, S., Kim, H., Theofanopoulou, C., Hiller, M., Zhou, Y., Harris, R. S., Makova, K. D., Medvedev, P., Hoffman, J., Masterson, P., Clark, K., Martin, F., Howe, K., Flicek, P., Walenz, B. P., Kwak, W., Clawson, H., Diekhans, M., Nassar, L., Paten, B., Kraus, R. H. S., Crawford, A. J., Gilbert, M. T. P., Zhang, G., Venkatesh, B., Murphy, R. W., Koepfli, K.-P., Shapiro, B., Johnson, W. E., Di Palma, F., Marques-Bonet, T., Teeling, E. C., Warnow, T., Graves, J. M., Ryder, O. A., Haussler, D., O’Brien, S. J., Korlach, J., Lewin, H. A., Howe, K., Myers, E. W., Durbin, R., Phillippy, A. M., & Jarvis, E. D.
Affiliations
  • National Institutes of Health (US)
  • University of Cambridge (GB)
  • Rockefeller University (US)
  • University of California, Davis (US)
  • Wellcome Sanger Institute (GB)
  • DNAnexus (United States) (US)
  • Seoul National University (KR)
  • University of Southern California (US)
  • European Bioinformatics Institute (GB)
  • Max Planck Institute of Molecular Cell Biology and Genetics (DE)
  • University of St Andrews (GB)
  • University of Massachusetts Amherst (US)
  • University of Missouri (US)
  • East Carolina University (US)
  • Clemson University (US)
  • Department of Conservation (NZ)
  • University of Otago (NZ)
  • University of Arizona (US)
  • Natural History Museum (GB)
  • Bangor University (GB)
  • University of Konstanz (DE)
  • Harvard University (US)
  • Northeastern University (US)
  • Naturalis Biodiversity Center (NL)
  • University of Graz (AT)
  • Florida Museum of Natural History (US)
  • Center for Systems Biology Dresden (DE)
  • University of Basel (CH)
  • University of California, Santa Cruz (US)
  • Zoological Society of San Diego (US)
  • Pacific Biosciences (United States) (US)
  • BioNano Genomics (United States) (US)
  • Arima Genomics (United States) (US)
  • Universitat Pompeu Fabra (ES)
  • Dovetail Genomics (United States) (US)
  • Harbin Institute of Technology (CN)
  • University of Chicago (US)
  • Oregon Health & Science University (US)
  • Max Planck Institute for the Physics of Complex Systems (DE)
  • Monash University Malaysia (MY)
  • University of Milan (IT)
  • Goethe University Frankfurt (DE)
  • BGI Group (China) (CN)
  • Pennsylvania State University (US)
  • Universidad de Los Andes (CO)
  • University of Copenhagen (DK)
  • Agency for Science, Technology and Research (SG)
  • Royal Ontario Museum (CA)
  • Smithsonian Conservation Biology Institute (US)
  • Howard Hughes Medical Institute (US)
  • Smithsonian Institution (US)
  • University College Dublin (IE)
  • University of Illinois Urbana-Champaign (US)
  • La Trobe University (AU)
  • ITMO University (RU)
  • Institute of the Environment (US)
Corresponding author
  • Howe, Kevin
  • Howe, Kerstin
  • Myers, Eugene W.
  • Durbin, Richard
  • Phillippy, Adam M.
  • Jarvis, Erich D.
ORCID
Venue
Nature
Publisher
Springer Science and Business Media LLC
Published
2021-04-28
Volume
592
Issue
7856
Pages
737-746
ISSN
  • 0028-0836 (ISSN-L)
  • 1476-4687
DOI
10.1038/s41586-021-03451-0
PMC
PMC8081667
OpenAlex
W3159728495
Cited by
3,097
References
8
Citations by year
2026: 680 · 2025: 702 · 2024: 724 · 2023: 615 · 2022: 221 · 2021: 133 · 2020: 19 · 2019: 1 · 2012: 1
FWCI
134.98
Type
journal article
Language
en
Open access
Licence
Locations
  • Nature (publishedVersion, cc-by)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc-nd)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • Research at the University of Copenhagen (University of Copenhagen) (publishedVersion, cc-by)
  • Informationszentrum Lebenswissenschaften (ZB MED) (submittedVersion, cc-by)
  • Smith ScholarWorks (Smith College) (submittedVersion)
  • RePEc: Research Papers in Economics (submittedVersion)
  • The Scholarship East Carolina University's Institutional Repository (East Carolina University) (submittedVersion)
  • Archivio Istituzionale della Ricerca (Universita Degli Studi Di Milano) (submittedVersion, other-oa)
  • Dipòsit Digital de Documents de la UAB (Universitat Autònoma de Barcelona) (submittedVersion, cc-by)
  • Dipòsit Digital de Documents de la UAB (Universitat Autònoma de Barcelona) (submittedVersion, other-oa)
  • DIGITAL.CSIC (Spanish National Research Council (CSIC)) (submittedVersion, cc-by)
  • UnitusOpen (Tuscia University) (submittedVersion, public-domain)
  • eScholarship (California Digital Library) (submittedVersion)
  • eScholarship (California Digital Library) (submittedVersion, cc-by)
  • Figshare (submittedVersion, cc-by)
  • IRIS Research product catalog (Sapienza University of Rome) (submittedVersion, cc-by)
  • KOPS (University of Konstanz) (submittedVersion, cc-by)
  • NORA - Norwegian Open Research Archives (submittedVersion, other-oa)
  • Repositori digital de la UPF (Universitat Pompeu Fabra) (submittedVersion, cc-by)
  • Radboud Repository (Radboud University) (submittedVersion)
  • St Andrews Research Repository (St Andrews Research Repository) (submittedVersion, cc-by)
  • Bangor University Research Portal (Bangor University) (submittedVersion, other-oa)
  • Apollo (University of Cambridge) (submittedVersion, cc-by)
  • Radboud Repository (Radboud University) (submittedVersion, other-oa)
  • Apollo
  • Apollo (cc-by)
  • La Trobe University (cc-by)
Funders
  • National Science Foundation (1457541, 0132032, 1458652, 1444167, 1456612)
  • Villum Fonden (00025900)
  • Wellcome Trust (R01HG010485, 108749/Z/15/Z, WT207492, 207492/Z/17/Z, 207492/A/17/Z, WT206194, WT108749, WT218328/B/19/Z, /Z/15/Z, WT108749/Z/15/Z, 108749)
  • Oxford Nanopore Technologies
  • European Molecular Biology Laboratory
  • UK Research and Innovation (MR/T021985/1)
  • Centres de Recerca de Catalunya (GRC 2017 SGR 880)
  • European Commission (864203, 750747, HORIZON2020, 681396)
  • National Research Foundation (DNRF143)
  • Deutsche Forschungsgemeinschaft (418083601)
  • Danmarks Grundforskningsfond (DNRF143)
  • Monash University
  • University of Queensland
  • Irish Research Council
  • Bundesministerium für Bildung und Forschung (01IS18026C)
  • Generalitat de Catalunya (2017-SGR, BFU2017-86471-P, CEX2018-000792-M, GRC 2017 SGR 880, 864203, 681396)
  • Hessisches Ministerium für Wissenschaft und Kunst
  • Korea Health Industry Development Institute (HI17C2098)
  • Max-Planck-Gesellschaft (BFU2017-86471-P)
  • Monash University Malaysia
  • Korea Institute of Marine Science and Technology promotion (20180430)
  • Leibniz-Institut für Zoo- und Wildtierforschung
  • National Institutes of Health (WT108749/Z/15/Z)
  • Directorate for Biological Sciences (1458652, 1456612, 1457541)
  • Directorate for Geosciences (2324998, 1955368, 1444167, 0132032)
  • Biotechnology and Biological Sciences Research Council (BBS/E/T/000PR9817, BBS/E/T/000PR9818, BBS/E/T/000PR9819)
  • Australian Research Council (BFU2017-86471-P, 681396, CEX2018-000792-M, GRC 2017 SGR 880, 864203)
  • Leibniz-Gemeinschaft
  • Agencia Estatal de Investigación (864203, 681396, #CEX2018-000792-M, GRC 2017 SGR 880, BFU2017-86471-P)
  • National Key Research and Development Program of China (2017YFC0907503, 2017YFC1201201, 2018YFC0910504)
  • Biomedical Research Council
  • National Human Genome Research Institute (R44HG008118, U41HG002371, R01HG010485, U41HG007234, U24HG007234, ZIAHG200398)
  • National Institute on Deafness and Other Communication Disorders (R21DC014432, DC014432)
  • National Institute of General Medical Sciences (R01GM130691)
  • U.S. National Library of Medicine (ZIHLM200888)
  • Walter Reed Army Institute of Research
  • FP7 Ideas: European Research Council (311000)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Phylogenetic Studies
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Chromosomal and Genetic Variations
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genomic variations and chromosomal abnormalities
Keywords
long-read sequencing, gene duplication, chromosomal rearrangements, bat genome, reference genome
MeSH terms
Animals, Birds, Haplotypes, Sex Chromosomes, Vertebrates, Gene Library, Sequence Alignment, Genome, Sequence Analysis, DNA, Genomics, Genome, Mitochondrial, Molecular Sequence Annotation, High-Throughput Nucleotide Sequencing, Genome Size

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