Evaluation of GRCh38 and de novo haploid genome assemblies demonstrates the enduring quality of the reference assembly

Genome Research

Volumn 27, Issue 5, 2017, Pages 849-864

  Schneider, Valerie A ^a   Graves Lindsay, Tina ^b   Howe, Kerstin ^c   Bouk, Nathan ^a   Chen, Hsiu Chuan ^a   Kitts, Paul A ^a   Murphy, Terence D ^a   Pruitt, Kim D ^a   Thibaud Nissen, Françoise ^a   Albracht, Derek ^b   Fulton, Robert S ^b   Kremitzki, Milinn ^b   Magrini, Vincent ^b,j   Markovic, Chris ^b   McGrath, Sean ^b   Steinberg, Karyn Meltz ^b   Auger, Kate ^c   Chow, William ^c   Collins, Joanna ^c   Harden, Glenn ^c   Hubbard, Timothy ^c,k   Pelan, Sarah ^c   Simpson, Jared T ^c,l,m   Threadgold, Glen ^c   Torrance, James ^c   Wood, Jonathan M ^c   Clarke, Laura ^d   Koren, Sergey ^e   Boitano, Matthew ^f   Peluso, Paul ^f   Li, Heng ^g   Chin, Chen Shan ^f   Phillippy, Adam M ^e   Durbin, Richard ^c   Wilson, Richard K ^b   Flicek, Paul ^d   Eichler, Evan E ^h,i   Church, Deanna M ^a,n   more..

^a NATIONAL INSTITUTES OF HEALTH   (United States)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^d EUROPEAN BIOINFORMATICS INSTITUTE   (United Kingdom)

^e NATIONAL HUMAN GENOME RESEARCH INSTITUTE   (United States)

^f PACIFIC BIOSCIENCES   (United States)

^g BROAD INSTITUTE OF MIT AND HARVARD   (United States)

^h UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

ⁱ UNIVERSITY OF WASHINGTON   (United States)

^j NATIONWIDE CHILDREN S HOSPITAL   (United States)

^k KING'S COLLEGE LONDON   (United Kingdom)

^l ONTARIO INSTITUTE FOR CANCER RESEARCH   (Canada)

^m UNIVERSITY OF TORONTO   (Canada)

ⁿ NONE   (United States)

more..

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; GENE MAPPING; GENE SEQUENCE; HAPLOTYPE; PRIORITY JOURNAL; CONTIG MAPPING; DNA SEQUENCE; GENETIC POLYMORPHISM; GENOMICS; HAPLOIDY; HUMAN; HUMAN GENOME; PROCEDURES; SOFTWARE; STANDARD; STANDARDS;

CONTIG MAPPING; GENOME, HUMAN; GENOMICS; HAPLOIDY; HAPLOTYPES; HUMANS; POLYMORPHISM, GENETIC; REFERENCE STANDARDS; SEQUENCE ANALYSIS, DNA; SOFTWARE;

EID: 85019127944     PISSN: 10889051     EISSN: 15495469     Source Type: Journal    
DOI: 10.1101/gr.213611.116     Document Type: Article

References (73)

1. The 1000 Genomes Project Consortium. 2010. A map of human genome variation from population-scale sequencing. Nature 467: 1061-1073.
2. The 1000 Genomes Project Consortium. 2012. An integrated map of genetic variation from 1,092 human genomes. Nature 491: 56-65.
3. The 1000 Genomes Project Consortium. 2015. A global reference for human genetic variation. Nature 526: 68-74.
4. Antonacci F, Dennis MY, Huddleston J, Sudmant PH, Steinberg KM, Rosenfeld JA, Miroballo M, Graves TA, Vives L, Malig M, et al. 2014. Palindromic GOLGA8 core duplicons promote chromosome 15q13.3 microdeletion and evolutionary instability. Nat Genet 46: 1293-1302.
5. Bailey JA, Yavor AM, Massa HF, Trask BJ, Eichler EE. 2001. Segmental duplications: organization and impact within the current human genome project assembly. Genome Res 11: 1005-1017.
6. Berlin K, Koren S, Chin CS, Drake JP, Landolin JM, Phillippy AM. 2015. Assembling large genomes with single-molecule sequencing and locality-sensitive hashing. Nat Biotechnol 33: 623-630.
7. Bradnam KR, Fass JN, Alexandrov A, Baranay P, Bechner M, Birol I, Boisvert S, Chapman JA, Chapuis G, Chikhi R, et al. 2013. Assemblathon 2: evaluating de novo methods of genome assembly in three vertebrate species. Gigascience 2: 10.
8. Cao H,WuH, Luo R, Huang S, Sun Y, Tong X, Xie Y, Liu B, Yang H, Zheng H, et al. 2015. De novo assembly of a haplotype-resolved human genome. Nat Biotechnol 33: 617-622.
9. Chaisson MJP, Huddleston J, Dennis MY, Sudmant PH, Malig M, Hormozdiari F, Antonacci F, Surti U, Sandstrom R, Boitano M, et al. 2015a. Resolving the complexity of the human genome using singlemolecule sequencing. Nature 517: 608-611.
10. Chaisson MJP, Wilson RK, Eichler EE. 2015b. Genetic variation and the de novo assembly of human genomes. Nat Rev Genet 16: 627-640.
11. Chin CS, Alexander DH, Marks P, Klammer AA, Drake J, Heiner C, Clum A, Copeland A, Huddleston J, Eichler EE, et al. 2013. Nonhybrid, finished microbial genome assemblies from long-read SMRT sequencing data. Nat Methods 10: 563-569.
12. Chin CS, Peluso P, Sedlazeck FJ, Nattestad M, Concepcion GT, Clum A, Dunn C, O'Malley R, Figueroa-Balderas R, Morales-Cruz A, et al. 2016. Phased diploid genome assembly with single-molecule real-time sequencing. Nat Methods 13: 1050-1054.
13. Church DM, Schneider VA, Graves T, Auger K, Cunningham F, Bouk N, Chen HC, Agarwala R, McLaren WM, Ritchie GR, et al. 2011. Modernizing reference genome assemblies. PLoS Biol 9: e1001091.
14. Church DM, Schneider VA, Steinberg KM, Schatz MC, Quinlan AR, Chin CS, Kitts PA, Aken B, Marth GT, Hoffman MM, et al. 2015. Extending reference assembly models. Genome Biol 16: 13.
15. Dennis MY, Nuttle X, Sudmant PH, Antonacci F, Graves TA, Nefedov M, Rosenfeld JA, Sajjadian S, Malig M, Kotkiewicz H, et al. 2012. Evolution of human-specific neural SRGAP2 genes by incomplete segmental duplication. Cell 149: 912-922.
16. Dilthey A, Cox C, Iqbal Z, Nelson MR, McVean G. 2015. Improved genome inference in the MHC using a population reference graph. Nat Genet 47: 682-688.
17. Earl D, Bradnam K, St John J, Darling A, Lin D, Fass J, Yu HO, Buffalo V, Zerbino DR, Diekhans M, et al. 2011. Assemblathon 1: a competitive assessment of de novo short read assembly methods. Genome Res 21: 2224-2241.
18. English AC, Salerno WJ, Hampton OA, Gonzaga-Jauregui C, Ambreth S, Ritter DI, Beck CR, Davis CF, Dahdouli M, Ma S, et al. 2015. Assessing structural variation in a personal genome-towards a human reference diploid genome. BMC Genomics 16: 286.
19. Falconer E, Hills M, Naumann U, Poon SS, Chavez EA, Sanders AD, Zhao Y, Hirst M, Lansdorp PM. 2012. DNA template strand sequencing of singlecells maps genomic rearrangements at high resolution. Nat Methods 9: 1107-1112.
20. Fan JB, Surti U, Taillon-Miller P, Hsie L, Kennedy GC, Hoffner L, Ryder T, Mutch DG, Kwok PY. 2002. Paternal origins of complete hydatidiform moles proven by whole genome single-nucleotide polymorphism haplotyping. Genomics 79: 58-62.
21. Florea L, Souvorov A, Kalbfleisch TS, Salzberg SL. 2011. Genome assembly has a major impact on gene content: a comparison of annotation in two Bos taurus assemblies. PLoS One 6: e21400.
22. Fritz MHY, Leinonen R, Cochrane G, Birney E. 2011. Efficient storage of high throughput DNA sequencing data using reference-based compression. Genome Res 21: 734-740.
23. Genovese G, Handsaker RE, Li H, Altemose N, Lindgren AM, Chambert K, Pasaniuc B, Price AL, Reich D, Morton CC, et al. 2013a. Using population admixture to help complete maps of the human genome. Nat Genet 45: 406-414.
24. Genovese G, Handsaker RE, Li H, Kenny EE, McCarroll SA. 2013b. Mapping the human reference genome's missing sequence by three-way admixture in Latino genomes. Am J Hum Genet 93: 411-421.
25. Green RE, Krause J, Briggs AW, Maricic T, Stenzel U, Kircher M, Patterson N, Li H, Zhai W, Fritz MH, et al. 2010. A draft sequence of the Neandertal genome. Science 328: 710-722.
26. Harrow J, Frankish A, Gonzalez JM, Tapanari E, Diekhans M, Kokocinski F, Aken BL, Barrell D, Zadissa A, Searle S, et al. 2012. GENCODE: the reference human genome annotation for The ENCODE Project. Genome Res 22: 1760-1774.
27. Hickey G, Paten B, Earl D, Zerbino D, Haussler D. 2013. HAL: a hierarchical format for storing and analyzing multiple genome alignments. Bioinformatics 29: 1341-1342.
28. Horton R, Gibson R, Coggill P, Miretti M, Allcock RJ, Almeida J, Forbes S, Gilbert JG, Halls K, Harrow JL, et al. 2008. Variation analysis and gene annotation of eight MHC haplotypes: the MHC Haplotype Project. Immunogenetics 60: 1-18.
29. Howe K, Wood JM. 2015. Using optical mapping data for the improvement of vertebrate genome assemblies. Gigascience 4: 10.
30. Huddleston J, Ranade S, Malig M, Antonacci F, Chaisson M, Hon L, Sudmant PH, Graves TA, Alkan C, Dennis MY, et al. 2014. Reconstructing complex regions of genomes using long-read sequencing technology. Genome Res 24: 688-696.
31. The International HapMap Consortium. 2005. A haplotype map of the human genome. Nature 437: 1299-1320.
32. International Human Genome Sequencing Consortium. 2001. Initial sequencing and analysis of the human genome. Nature 409: 860-921.
33. International Human Genome Sequencing Consortium. 2004. Finishing the euchromatic sequence of the human genome. Nature 431: 931-945.
34. Kidd JM, Cooper GM, Donahue WF, Hayden HS, Sampas N, Graves T, Hansen N, Teague B, Alkan C, Antonacci F, et al. 2008. Mapping and sequencing of structural variation from eight human genomes. Nature 453: 56-64.
35. Kitts PA, Church DM, Thibaud-Nissen F, Choi J, Hem V, Sapojnikov V, Smith RG, Tatusova T, Xiang C, Zherikov A, et al. 2016. Assembly: a resource for assembled genomes at NCBI. Nucleic Acids Res 44: D73-D80.
36. Landrum MJ, Lee JM, Riley GR, Jang W, Rubinstein WS, Church DM, Maglott DR. 2014. ClinVar: public archive of relationships among sequence variation and human phenotype. Nucleic Acids Res 42: D980-D985.
37. Levy S, Sutton G, Ng PC, Feuk L, Halpern AL, Walenz BP, Axelrod N, Huang J, Kirkness EF, Denisov G, et al. 2007. The diploid genome sequence of an individual human. PLoS Biol 5: e254.
38. Li H. 2013. Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM. arXiv: 1303.3997.
39. Li H. 2014. Toward better understanding of artifacts in variant calling from high-coverage samples. Bioinformatics 30: 2843-2851.
40. Li H. 2015. FermiKit: assembly-based variant calling for Illumina resequencing data. Bioinformatics 31: 3694-3696.
41. Li R, Li Y, Zheng H, Luo R, Zhu H, Li Q, Qian W, Ren Y, Tian G, Li J, et al. 2010. Building the sequence map of the human pan-genome. Nat Biotechnol 28: 57-63.
42. Matsuno H, Ohi K, Hashimoto R, Yamamori H, Yasuda Y, Fujimoto M, Yano-Umeda S, Saneyoshi T, Takeda M, Hayashi Y. 2015. A naturally occurring null variant of theNMDAtype glutamate receptor NR3B subunit is a risk factor of schizophrenia. PLoS One 10: e0116319.
43. McKenna A, Hanna M, Banks E, Sivachenko A, Cibulskis K, Kernytsky A, Garimella K, Altshuler D, Gabriel S, Daly M, et al. 2010. The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res 20: 1297-1303.
44. Miga KH, Newton Y, Jain M, Altemose N, Willard HF, Kent WJ. 2014. Centromere reference models for human chromosomes X and Y satellite arrays. Genome Res 24: 697-707.
45. Miga KH, Eisenhart C, Kent WJ. 2015. Utilizing mapping targets of sequences underrepresented in the reference assembly to reduce false positive alignments. Nucleic Acids Res 43: e133.
46. Mueller JL, Skaletsky H, Brown LG, Zaghlul S, Rock S, Graves T, Auger K, Warren WC, Wilson RK, Page DC. 2013. Independent specialization of the human and mouse X chromosomes for the male germ line. Nat Genet 45: 1083-1087.
47. Nguyen N, Hickey G, Zerbino DR, Raney B, Earl D, Armstrong J, Kent WJ, Haussler D, Paten B. 2015. Building a pan-genome reference for a population. J Comput Biol 22: 387-401.
48. Novak AM, Garrison E, Paten B. 2016. A graph extension of the positional Burrows-Wheeler transform and its applications. bioRxiv doi/10.1101/051409.
49. O'Leary NA, WrightMW, Brister JR, Ciufo S, Haddad D, McVeigh R, Rajput B, Robbertse B, Smith-White B, Ako-Adjei D, et al. 2016. Reference sequence (RefSeq) database at NCBI: current status, taxonomic expansion, and functional annotation. Nucleic Acids Res 44: D733-D745.
50. Paten B, Novak A, Haussler D. 2014. Mapping to a reference genome structure. arXiv: 1404.5010.
51. Pendleton M, Sebra R, Pang AW, Ummat A, Franzen O, Rausch T, Stütz AM, Stedman W, Anantharaman T, Hastie A, et al. 2015. Assembly and diploid architecture of an individual human genome via single-molecule technologies. Nat Methods 12: 780-786.
52. Pierson E, GTEx Consortium, Koller D, Battle A, Mostafavi S, Ardlie KG, Getz G, Wright FA, Kellis M, Volpi S, et al.. 2015. Sharing and specificity of coexpression networks across 35 human tissues. PLoS Comput Biol 11: e1004220.
53. PyoCW, Guethlein LA, Vu Q, Wang R, Abi-Rached L, Norman PJ, Marsh SG, Miller JS, Parham P, Geraghty DE. 2010. Different patterns of evolution in the centromeric and telomeric regions of group A and B haplotypes of the human killer cell Ig-like receptor locus. PLoS One 5: e15115.
54. Rosenfeld JA, Mason CE, Smith TM. 2012. Limitations of the human reference genome for personalized genomics. PLoS One 7: e40294.
55. Samocha KE, Robinson EB, Sanders SJ, Stevens C, Sabo A, McGrath LM, Kosmicki JA, Rehnström K, Mallick S, Kirby A, et al. 2014. A framework for the interpretation of de novo mutation in human disease. Nat Genet 46: 944-950.
56. Schmutz J, Martin J, Terry A, Couronne O, Grimwood J, Lowry S, Gordon LA, Scott D, Xie G, Huang W, et al. 2004. The DNA sequence and comparative analysis of human chromosome 5. Nature 431: 268-274.
57. Schneider VA, Chen HC, Clausen C, Meric PA, Zhou Z, Bouk N, Husain N, Maglott DR, Church DM. 2013. Clone DB: an integrated NCBI resource for clone-associated data. Nucleic Acids Res 41: D1070-D1078.
58. Seo JS, Rhie A, Kim J, Lee S, Sohn MH, Kim CU, Hastie A, Cao H, Yun JY, Kim J, et al. 2016. De novo assembly and phasing of a Korean human genome. Nature 538: 243-247.
59. Sharp AJ, Locke DP, McGrath SD, Cheng Z, Bailey JA, Vallente RU, Pertz LM, Clark RA, Schwartz S, Segraves R, et al. 2005. Segmental duplications and copy-number variation in the human genome. Am J Hum Genet 77: 78-88.
60. Shi L, Guo Y, Dong C, Huddleston J, Yang H, Han X, Fu A, Li Q, Li N, Gong S, et al. 2016. Long-read sequencing and de novo assembly of a Chinese genome. Nat Commun 7: 12065.
61. Steinberg KM, Schneider VA, Graves-Lindsay TA, Fulton RS, Agarwala R, Huddleston J, Shiryev SA, Morgulis A, Surti U, Warren WC, et al. 2014. Single haplotype assembly of the human genome from a hydatidiform mole. Genome Res 24: 2066-2076.
62. Sudmant PH, Kitzman JO, Antonacci F, Alkan C, Malig M, Tsalenko A, Sampas N, Bruhn L, Shendure J, 1000 Genomes Project, et al.. 2010. Diversity of human copy number variation and multicopy genes. Science 330: 641-646.
63. Teague B, Waterman MS, Goldstein S, Potamousis K, Zhou S, Reslewic S, Sarkar D, Valouev A, Churas C, Kidd JM, et al. 2010. High-resolution human genome structure by single-molecule analysis. Proc Natl Acad Sci 107: 10848-10853.
64. Vezzi F, Narzisi G, Mishra B. 2012. Reevaluating assembly evaluations with feature response curves: GAGE and assemblathons. PLoS One 7: e52210.
65. Walker BJ, Abeel T, Shea T, Priest M, Abouelliel A, Sakthikumar S, Cuomo CA, Zeng Q, Wortman J, Young SK, et al. 2014. Pilon: an integrated tool for comprehensive microbial variant detection and genome assembly improvement. PLoS One 9: e112963.
66. Wang J, WangW, Li R, Li Y, Tian G, Goodman L, FanW, Zhang J, Li J, Zhang J, et al. 2008. The diploid genome sequence of an Asian individual. Nature 456: 60-65.
67. Watson CT, Steinberg KM, Huddleston J, Warren RL, Malig M, Schein J, Willsey AJ, Joy JB, Scott JK, Graves TA, et al. 2013. Complete haplotype sequence of the human immunoglobulin heavy-chain variable, diversity, and joining genes and characterization of allelic and copy-number variation. Am J Hum Genet 92: 530-546.
68. Watson CT, Steinberg KM, Graves TA, Warren RL, Malig M, Schein J, Wilson RK, Holt RA, Eichler EE, Breden F. 2015. Sequencing of the human IG light chain loci from a hydatidiform mole BAC library reveals locus-specific signatures of genetic diversity. Genes Immun 16: 24-34.
69. Xue Y, Sun D, Daly A, Yang F, Zhou X, Zhao M, Huang N, Zerjal T, Lee C, Carter NP, et al. 2008. Adaptive evolution of UGT2B17 copy-number variation. Am J Hum Genet 83: 337-346.
70. Zhao H, Sun Z, Wang J, Huang H, Kocher JP, Wang L. 2014. CrossMap: a versatile tool for coordinate conversion between genome assemblies. Bioinformatics 30: 1006-1007.
71. Zody MC, Jiang Z, Fung HC, Antonacci F, Hillier LW, Cardone MF, Graves TA, Kidd JM, Cheng Z, Abouelleil A, et al. 2008. Evolutionary toggling of the MAPT 17q21. 31 inversion region. Nat Genet 40: 1076-1083.
72. Zook JM, Chapman B, Wang J, Mittelman D, Hofmann O, HideW, Salit M. 2014. Integrating human sequence data sets provides a resource of benchmark SNP and indel genotype calls. Nat Biotechnol 32: 246-251.
73. Zook JM, Catoe D, McDaniel J, Vang L, Spies N, Sidow A, Weng Z, Liu Y, Mason CE, Alexander N, et al. 2016. Extensive sequencing of seven human genomes to characterize benchmark reference materials. Sci Data 3: 160025.