Single-molecule sequencing and chromatin conformation capture enable de novo reference assembly of the domestic goat genome

Nature Genetics

Volumn 49, Issue 4, 2017, Pages 643-650

  Bickhart, Derek M ^a   Rosen, Benjamin D ^a   Koren, Sergey ^b   Sayre, Brian L ^c   Hastie, Alex R ^d   Chan, Saki ^d   Lee, Joyce ^d   Lam, Ernest T ^d   Liachko, Ivan ^e   Sullivan, Shawn T ^f   Burton, Joshua N ^e   Huson, Heather J ^g   Nystrom, John C ^g   Kelley, Christy M ^h   Hutchison, Jana L ^a   Zhou, Yang ^a,i,l   Sun, Jiajie ^j   Crisà, Alessandra ^k   Ponce De León, F Abel ^b   Schwartz, John C ^m   Hammond, John A ^m   Waldbieser, Geoffrey C ⁿ   Schroeder, Steven G ^a   Liu, George E ^a   Dunham, Maitreya J ^e   Shendure, Jay ^e,o   Sonstegard, Tad S ^p   Phillippy, Adam M ^b   Van Tassell, Curtis P ^a   Smith, Timothy P L ^h   more..

^a AGRICULTURAL RESEARCH SERVICE   (United States)

^b NATIONAL HUMAN GENOME RESEARCH INSTITUTE   (United States)

^c VIRGINIA STATE UNIVERSITY   (United States)

^d USA   (United States)

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

^f Phase Genomics   (United States)

^g Department of Obstetrics Gynecology   (United States)

^h U S MEAT ANIMAL RESEARCH CENTER   (United States)

ⁱ NORTHWEST A F UNIVERSITY   (China)

^j SOUTH CHINA AGRICULTURAL UNIVERSITY   (China)

^k ISTITUTO NAZIONALE DELLA NUTRIZIONE   (Italy)

^l UNIVERSITY OF MINNESOTA   (United States)

^m INSTITUTE FOR ANIMAL HEALTH   (United Kingdom)

ⁿ AGRICULTURAL RESEARCH SERVICE   (United States)

^o HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^p RECOMBINETICS INC   (United States)

more..

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BENCHMARKING; BREED; CELL INTERACTION; CHROMATIN; CHROMOSOME SIZE; CONFORMATION; DOMESTIC GOAT; GENE SEQUENCE; GENETIC MARKER; GENOME; HOMOZYGOSITY; MALE; NONHUMAN; PRIORITY JOURNAL; ANIMAL; CHROMOSOME; GENETICS; GOAT; HIGH THROUGHPUT SEQUENCING; NUCLEOTIDE REPEAT; PROCEDURES;

ANIMALS; CHROMATIN; CHROMOSOMES; GENOME; GOATS; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; REPETITIVE SEQUENCES, NUCLEIC ACID;

EID: 85014528210     PISSN: 10614036     EISSN: 15461718     Source Type: Journal    
DOI: 10.1038/ng.3802     Document Type: Article

References (72)

1. Matukumalli, L.K. et al. Development and characterization of a high density SNP genotyping assay for cattle. PLoS One 4, e5350 (2009).
2. Romay, M.C. et al. Comprehensive genotyping of the USA national maize inbred seed bank. Genome Biol. 14, R55 (2013).
3. Tosser-Klopp, G. et al. Design and characterization of a 52K SNP chip for goats. PLoS One 9, e86227 (2014).
4. Lander, E.S. et al. Initial sequencing and analysis of the human genome. Nature 409, 860-921 (2001).
5. International Human Genome Sequencing Consortium. Finishing the euchromatic sequence of the human genome. Nature 431, 931-945 (2004).
6. Schatz, M.C., Delcher, A.L. & Salzberg, S.L. Assembly of large genomes using second-generation sequencing. Genome Res. 20, 1165-1173 (2010).
7. Phillippy, A.M., Schatz, M.C. & Pop, M. Genome assembly forensics: finding the elusive misassembly. Genome Biol. 9, R55 (2008).
8. Fleischmann, R.D. et al. Whole-genome random sequencing and assembly of Haemophilus influenzae Rd. Science 269, 496-512 (1995).
9. Myers, E.W. et al. A whole-genome assembly of Drosophila. Science 287, 2196-2204 (2000).
10. Pop, M., Kosack, D.S. & Salzberg, S.L. Hierarchical scaffolding with Bambus. Genome Res. 14, 149-159 (2004).
11. Boetzer, M. & Pirovano, W. SSPACE-LongRead: scaffolding bacterial draft genomes using long read sequence information. BMC Bioinformatics 15, 211 (2014).
12. McCoy, R.C. et al. Illumina TruSeq synthetic long-reads empower de novo assembly and resolve complex, highly-repetitive transposable elements. PLoS One 9, e106689 (2014).
13. Lieberman-Aiden, E. et al. Comprehensive mapping of long-range interactions reveals folding principles of the human genome. Science 326, 289-293 (2009).
14. Schwartz, D.C. et al. Ordered restriction maps of Saccharomyces cerevisiae chromosomes constructed by optical mapping. Science 262, 110-114 (1993).
15. Burton, J.N. et al. Chromosome-scale scaffolding of de novo genome assemblies based on chromatin interactions. Nat. Biotechnol. 31, 1119-1125 (2013).
16. Kaplan, N. & Dekker, J. High-throughput genome scaffolding from in vivo DNA interaction frequency. Nat. Biotechnol. 31, 1143-1147 (2013).
17. Putnam, N.H. et al. Chromosome-scale shotgun assembly using an in vitro method for long-range linkage. Genome Res. 26, 342-350 (2016).
18. Dong, Y. et al. Sequencing and automated whole-genome optical mapping of the genome of a domestic goat (Capra hircus). Nat. Biotechnol. 31, 135-141 (2013).
19. Nagarajan, N., Read, T.D. & Pop, M. Scaffolding and validation of bacterial genome assemblies using optical restriction maps. Bioinformatics 24, 1229-1235 (2008).
20. Dekker, J., Rippe, K., Dekker, M. & Kleckner, N. Capturing chromosome conformation. Science 295, 1306-1311 (2002).
21. Hastie, A.R. et al. Rapid genome mapping in nanochannel arrays for highly complete and accurate de novo sequence assembly of the complex Aegilops tauschii genome. PLoS One 8, e55864 (2013).
22. Riley, M.C., Kirkup, B.C., Johnson, J.D., Lesho, E.P. & Ockenhouse, C.F. Rapid whole genome optical mapping of Plasmodium falciparum. Malar. J. 10, 252 (2011).
23. Zhou, J., Lemos, B., Dopman, E.B. & Hartl, D.L. Copy-number variation: the balance between gene dosage and expression in Drosophila melanogaster. Genome Biol. Evol. 3, 1014-1024 (2011).
24. Zhang, G. et al. Comparative genomic data of the Avian Phylogenomics Project. Gigascience 3, 26 (2014).
25. Chaisson, M.J.P., Wilson, R.K. & Eichler, E.E. Genetic variation and the de novo assembly of human genomes. Nat. Rev. Genet. 16, 627-640 (2015).
26. Eid, J. et al. Real-time DNA sequencing from single polymerase molecules. Science 323, 133-138 (2009).
27. Gordon, D. et al. Long-read sequence assembly of the gorilla genome. Science 352, aae0344 (2016).
28. Chin, C.-S. Nonhybrid, finished microbial genome assemblies from long-read SMRT sequencing data. Nat. Methods 10, 563-569 (2013).
29. Koren, S. et al. Reducing assembly complexity of microbial genomes with single-molecule sequencing. Genome Biol. 14, R101 (2013).
30. Berlin, K. et al. Assembling large genomes with single-molecule sequencing and locality-sensitive hashing. Nat. Biotechnol. 33, 623-630 (2015).
31. Pendleton, M. et al. Assembly and diploid architecture of an individual human genome via single-molecule technologies. Nat. Methods 12, 780-786 (2015).
32. Elsik, C.G., Tellam, R.L. & Worley, K.C. The genome sequence of taurine cattle: a window to ruminant biology and evolution. Science 324, 522-528 (2009).
33. Naderi, S. et al. The goat domestication process inferred from large-scale mitochondrial DNA analysis of wild and domestic individuals. Proc. Natl. Acad. Sci. USA 105, 17659-17664 (2008).
34. Du, X.Y. et al. A whole-genome radiation hybrid panel for goat. Small Rumin. Res. 105, 114-116 (2012).
35. English, A.C. et al. Mind the gap: upgrading genomes with Pacific Biosciences RS long-read sequencing technology. PLoS One 7, e47768 (2012).
36. Walker, B.J. et al. Pilon: an integrated tool for comprehensive microbial variant detection and genome assembly improvement. PLoS One 9, e112963 (2014).
37. Garrison, E. & Marth, G. Haplotype-based variant detection from short-read sequencing. Preprint at https://arxiv.org/abs/1207.3907 (2012).
38. Iannuzzi, L. & Di Meo, G.P. Chromosomal evolution in bovids: a comparison of cattle, sheep and goat G- and R-banded chromosomes and cytogenetic divergences among cattle, goat and river buffalo sex chromosomes. Chromosome Res. 3, 291-299 (1995).
39. Schneider, V.A. et al. Evaluation of GRCh38 and de novo haploid genome assemblies demonstrates the enduring quality of the reference assembly. Preprint at bioRxiv http://dx.doi.org/10.1101/072116 (2016).
40. Ma, W. et al. Fine-scale chromatin interaction maps reveal the cis-regulatory landscape of human lincRNA genes. Nat. Methods 12, 71-78 (2015).
41. Zimin, A.V. et al. A whole-genome assembly of the domestic cow, Bos taurus. Genome Biol. 10, R42 (2009).
42. Ewing, B. & Green, P. Base-calling of automated sequencer traces using phred. II. Error probabilities. Genome Res. 8, 186-194 (1998).
43. Layer, R.M., Chiang, C., Quinlan, A.R. & Hall, I.M. LUMPY: a probabilistic framework for structural variant discovery. Genome Biol. 15, R84 (2014).
44. Vezzi, F., Narzisi, G. & Mishra, B. Reevaluating assembly evaluations with feature response curves: GAGE and Assemblathons. PLoS One 7, e52210 (2012).
45. Simao, F.A., Waterhouse, R.M., Ioannidis, P., Kriventseva, E.V. & Zdobnov, E.M. BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics 31, 3210-3212 (2015).
46. Sanderson, N.D. et al. Definition of the cattle killer cell Ig-like receptor gene family: comparison with aurochs and human counterparts. J. Immunol. 1950, 6016-6030 (2014).
47. International Sheep Genomics Consortium. The sheep genome reference sequence: a work in progress. Anim. Genet. 41, 449-453 (2010).
48. Melters, D.P. et al. Comparative analysis of tandem repeats from hundreds of species reveals unique insights into centromere evolution. Genome Biol. 14, R10 (2013).
49. Hansen, K.M. Q-band karyotype of the goat (Capra hircus) and the relation between goat and bovine Q-bands. Hereditas 75, 119-129 (1973).
50. Perez-Pardal, L. et al. Multiple paternal origins of domestic cattle revealed by Y-specific interspersed multilocus microsatellites. Heredity 105, 511-519 (2010).
51. Koren, S. et al. Hybrid error correction and de novo assembly of single-molecule sequencing reads. Nat. Biotechnol. 30, 693-700 (2012).
52. Vanneste, K., Baele, G., Maere, S. & de Peer, Y.V. Analysis of 41 plant genomes supports a wave of successful genome duplications in association with the Cretaceous-Paleogene boundary. Genome Res. 24, 1334-1347 (2014).
53. Tomaszkiewicz, M. et al. A time- and cost-effective strategy to sequence mammalian Y chromosomes: an application to the de novo assembly of gorilla Y. Genome Res. 26, 530-540 (2016).
54. Chin, C.-S. Phased diploid genome assembly with single molecule real-time sequencing. Nat Methods. 12, 1050-1054 (2016).
55. Selvaraj, S.R., Dixon, J., Bansal, V. & Ren, B. Whole-genome haplotype reconstruction using proximity-ligation and shotgun sequencing. Nat. Biotechnol. 31, 1111-1118 (2013).
56. Barriere, A. et al. Detecting heterozygosity in shotgun genome assemblies: lessons from obligately outcrossing nematodes. Genome Res. 19, 470-480 (2009).
57. Sayre, B.L. et al. Goat breeding in the tropics: development and application of genomic tools in a USAID Feed the Future program. Presented at the 50th Annual Meeting of the Brazilian Society of Animal Science (2013).
58. Burton, J.N., Liachko, I., Dunham, M.J. & Shendure, J. Species-level deconvolution of metagenome assemblies with Hi-C-based contact probability maps. G3 4, 1339-1346 (2014).
59. Li, H. & Durbin, R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25, 1754-1760 (2009).
60. Li, H. et al. The Sequence Alignment/Map format and SAMtools. Bioinformatics 25, 2078-2079 (2009).
61. Ross, M.G. et al. Characterizing and measuring bias in sequence data. Genome Biol. 14, R51 (2013).
62. Wood, D.E. & Salzberg, S.L. Kraken: ultrafast metagenomic sequence classification using exact alignments. Genome Biol. 15, R46 (2014).
63. Haas, B.J. et al. Automated eukaryotic gene structure annotation using EVidenceModeler and the Program to Assemble Spliced Alignments. Genome Biol. 9, R7 (2008).
64. Bolger, A.M., Lohse, M. & Usadel, B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30, 2114-2120 (2014).
65. Kim, D. et al. TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol. 14, R36 (2013).
66. Pertea, M. et al. StringTie enables improved reconstruction of a transcriptome from RNA-seq reads. Nat. Biotechnol. 33, 290-295 (2015).
67. Trapnell, C. et al. Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat. Biotechnol. 28, 511-515 (2010).
68. Grabherr, M.G. et al. Trinity: reconstructing a full-length transcriptome without a genome from RNA-Seq data. Nat. Biotechnol. 29, 644-652 (2011).
69. Hoff, K.J., Lange, S., Lomsadze, A., Borodovsky, M. & Stanke, M. BRAKER1: unsupervised RNA-Seq-based genome annotation with GeneMark-ET and AUGUSTUS. Bioinformatics 32, 767-769 (2016).
70. Quinlan, A.R. & Hall, I.M. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26, 841-842 (2010).
71. Kurtz, S. et al. Versatile and open software for comparing large genomes. Genome Biol. 5, R12 (2004).
72. Morgulis, A., Gertz, E.M., Schaffer, A.A. & Agarwala, R. A fast and symmetric DUST implementation to mask low-complexity DNA sequences. J. Comput. Biol. 13, 1028-1040 (2006).