Joint assembly and genetic mapping of the Atlantic horseshoe crab genome reveals ancient whole genome duplication

GigaScience

Volumn 3, Issue 1, 2014, Pages

  Nossa, Carlos W ^a,c   Havlak, Paul ^a   Yue, Jia Xing ^a   Lv, Jie ^a   Vincent, Kimberly Y ^a   Brockmann, H Jane ^b   Putnam, Nicholas H ^a  

^a RICE UNIVERSITY   (United States)

^b UNIVERSITY OF FLORIDA   (United States)

^c Gene by Gene Ltd   (United States)

Author keywords

Genetic linkage mapping; Genome evolution; Genotyping by sequencing (GBS); Limulus polyphemus

Indexed keywords

CELL NUCLEUS DNA;

AGE DISTRIBUTION; ANIMAL CELL; ARTICLE; CHROMOSOME ANALYSIS; CONTROLLED STUDY; DNA SEQUENCE; EMBRYO; GENE CLUSTER; GENE DUPLICATION; GENE MAPPING; GENETIC LINKAGE; GENETIC RECOMBINATION; GENOME; GENOMICS; GENOTYPE; LAST COMMON ANCESTOR; LIMULUS; MOLECULAR EVOLUTION; NONHUMAN; PRIORITY JOURNAL;

EID: 84905989520     PISSN: None     EISSN: 2047217X     Source Type: Journal    
DOI: 10.1186/2047-217X-3-9     Document Type: Article

References (72)

1. Ohno S. Evolution by Gene Duplication 1970, Springer-Verlag.
2. Wolfe KH, Shields DC. Molecular evidence for an ancient duplication of the entire yeast genome. Nature 1997, 387:708-713. 10.1038/42711, 9192896.
3. McLysaght A, Hokamp K, Wolfe KH. Extensive genomic duplication during early chordate evolution. Nat Genet 2002, 31:200-204. 10.1038/ng884, 12032567.
4. Simillion C, Vandepoele K, Montagu MCEV, Zabeau M, de Peer YV. The hidden duplication past of Arabidopsis thaliana. Proc Natl Acad Sci 2002, 99:13627-13632. 10.1073/pnas.212522399, 129725, 12374856.
5. Aury J-M, Jaillon O, Duret L, Noel B, Jubin C, Porcel BM, Ségurens B, Daubin V, Anthouard V, Aiach N, Arnaiz O, Billaut A, Beisson J, Blanc I, Bouhouche K, Câmara F, Duharcourt S, Guigo R, Gogendeau D, Katinka M, Keller A-M, Kissmehl R, Klotz C, Koll F, Mouël AL, Lepère G, Malinsky S, Nowacki M, Nowak JK, Plattner H, et al. Global trends of whole-genome duplications revealed by the ciliate Paramecium tetraurelia. Nature 2006, 444:171-178. 10.1038/nature05230, 17086204.
6. Putnam NH, Srivastava M, Hellsten U, Dirks B, Chapman J, Salamov A, Terry A, Shapiro H, Lindquist E, Kapitonov VV, Jurka J, Genikhovich G, Grigoriev IV, Lucas SM, Steele RE, Finnerty JR, Technau U, Martindale MQ, Rokhsar DS. Sea anemone genome reveals ancestral eumetazoan gene repertoire and genomic organization. Science 2007, 317:86-94. 10.1126/science.1139158, 17615350.
7. Putnam NH, Butts T, Ferrier DEK, Furlong RF, Hellsten U, Kawashima T, Robinson-Rechavi M, Shoguchi E, Terry A, Yu J-K, Benito-Gutierrez E, Dubchak I, Garcia-Fernandez J, Gibson-Brown JJ, Grigoriev IV, Horton AC, de Jong PJ, Jurka J, Kapitonov VV, Kohara Y, Kuroki Y, Lindquist E, Lucas S, Osoegawa K, Pennacchio LA, Salamov AA, Satou Y, Sauka-Spengler T, Schmutz J, Shin-I T, et al. The amphioxus genome and the evolution of the chordate karyotype. Nature 2008, 453:1064-1071. 10.1038/nature06967, 18563158.
8. Srivastava M, Begovic E, Chapman J, Putnam NH, Hellsten U, Kawashima T, Kuo A, Mitros T, Salamov A, Carpenter ML, Signorovitch AY, Moreno MA, Kamm K, Grimwood J, Schmutz J, Shapiro H, Grigoriev IV, Buss LW, Schierwater B, Dellaporta SL, Rokhsar DS. The Trichoplax genome and the nature of placozoans. Nature 2008, 454:955-960. 10.1038/nature07191, 18719581.
9. Srivastava M, Simakov O, Chapman J, Fahey B, Gauthier MEA, Mitros T, Richards GS, Conaco C, Dacre M, Hellsten U, Larroux C, Putnam NH, Stanke M, Adamska M, Darling A, Degnan SM, Oakley TH, Plachetzki DC, Zhai Y, Adamski M, Calcino A, Cummins SF, Goodstein DM, Harris C, Jackson DJ, Leys SP, Shu S, Woodcroft BJ, Vervoort M, Kosik KS, et al. The Amphimedon queenslandica genome and the evolution of animal complexity. Nature 2010, 466:720-726. 10.1038/nature09201, 3130542, 20686567.
10. Simakov O, Marletaz F, Cho S-J, Edsinger-Gonzales E, Havlak P, Hellsten U, Kuo D-H, Larsson T, Lv J, Arendt D, Savage R, Osoegawa K, de Jong P, Grimwood J, Chapman JA, Shapiro H, Aerts A, Otillar RP, Terry AY, Boore JL, Grigoriev IV, Lindberg DR, Seaver EC, Weisblat DA, Putnam NH, Rokhsar DS. Insights into bilaterian evolution from three spiralian genomes. Nature 2013, 493:526-531.
11. Lv J, Havlak P, Putnam N. Constraints on genes shape long-term conservation of macro-synteny in metazoan genomes. BMC Bioinformatics 2011, 12(Suppl 9):S11.
12. Earl D, Bradnam K, John JS, Darling A, Lin D, Fass J, Yu HOK, Buffalo V, Zerbino DR, Diekhans M, Nguyen N, Ariyaratne PN, Sung W-K, Ning Z, Haimel M, Simpson JT, Fonseca NA, Birol T, Docking TR, Ho IY, Rokhsar DS, Chikhi R, Lavenier D, Chapuis G, Naquin D, Maillet N, Schatz MC, Kelley DR, Phillippy AM, Koren S, et al. Assemblathon 1: A competitive assessment of de novo short read assembly methods. Genome Res 2011, 21:2224-2241. 10.1101/gr.126599.111, 3227110, 21926179.
13. Davey JW, Hohenlohe PA, Etter PD, Boone JQ, Catchen JM, Blaxter ML. Genome-wide genetic marker discovery and genotyping using next-generation sequencing. Nat Rev Genet 2011, 12:499-510. 10.1038/nrg3012, 21681211.
14. Altshuler D, Pollara VJ, Cowles CR, Van Etten WJ, Baldwin J, Linton L, Lander ES. An SNP map of the human genome generated by reduced representation shotgun sequencing. Nature 2000, 407:513-516. 10.1038/35035083, 11029002.
15. Baird NA, Etter PD, Atwood TS, Currey MC, Shiver AL, Lewis ZA, Selker EU, Cresko WA, Johnson EA. Rapid SNP discovery and genetic mapping using sequenced RAD markers. PLoS ONE 2008, 3:e3376. 10.1371/journal.pone.0003376, 2557064, 18852878.
16. Huang X, Feng Q, Qian Q, Zhao Q, Wang L, Wang A, Guan J, Fan D, Weng Q, Huang T, Dong G, Sang T, Han B. High-throughput genotyping by whole-genome resequencing. Genome Res 2009, 19:1068-1076. 10.1101/gr.089516.108, 2694477, 19420380.
17. Andolfatto P, Davison D, Erezyilmaz D, Hu TT, Mast J, Sunayama-Morita T, Stern DL. Multiplexed shotgun genotyping for rapid and efficient genetic mapping. Genome Res 2011, 21:610-617. 10.1101/gr.115402.110, 3065708, 21233398.
18. Chapman JA, Ho I, Sunkara S, Luo S, Schroth GP, Rokhsar DS. Meraculous: De novo genome assembly with short paired-end reads. PLoS ONE 2011, 6:e23501. 10.1371/journal.pone.0023501, 3158087, 21876754.
19. Butler J, MacCallum I, Kleber M, Shlyakhter IA, Belmonte MK, Lander ES, Nusbaum C, Jaffe DB. ALLPATHS: De novo assembly of whole-genome shotgun microreads. Genome Res 2008, 18:810-820. 10.1101/gr.7337908, 2336810, 18340039.
20. Gnerre S, MacCallum I, Przybylski D, Ribeiro FJ, Burton JN, Walker BJ, Sharpe T, Hall G, Shea TP, Sykes S, Berlin AM, Aird D, Costello M, Daza R, Williams L, Nicol R, Gnirke A, Nusbaum C, Lander ES, Jaffe DB. High-quality draft assemblies of mammalian genomes from massively parallel sequence data. Proc Natl Acad Sci 2011, 108:1513-1518. 10.1073/pnas.1017351108, 3029755, 21187386.
21. Rudkin DM, Young GA. Horseshoe crabs - an ancient ancestry revealed. Biol Conserv Horseshoe Crabs 2009, 25-44. New York: Springer, Tanacredi JT, Botton ML, Smith D.
22. Fisher DC. The Xiphosurida: archetypes of Bradytely?. Living Foss 1984, 196-213. New York: Springer, Eldrege N, Stanley SM.
23. Berkson J, Shuster CN. The horseshoe crab: the battle for a true multiple-use resource. Fisheries 1999, 24:6-10.
24. The American Horseshoe Crab 2003, Cambridge, MA: Harvard University Press, Shuster CN Jr, Barlow RB, Brockmann HJ.
25. Gregory TR. Animal Genome Size Database http://www.genomesize.com.
26. Pop M, Kosack DS, Salzberg SL. Hierarchical scaffolding with bambus. Genome Res 2004, 14:149-159. 314292, 14707177.
27. Van Os H, Andrzejewski S, Bakker E, Barrena I, Bryan GJ, Caromel B, Ghareeb B, Isidore E, de Jong W, van Koert P, Lefebvre V, Milbourne D, Ritter E, van der Voort JNAMR, Rousselle-Bourgeois F, van Vliet J, Waugh R, Visser RGF, Bakker J, van Eck HJ. Construction of a 10,000-marker ultradense genetic recombination map of potato: providing a framework for accelerated gene isolation and a genomewide physical map. Genetics 2006, 173:1075-1087. 10.1534/genetics.106.055871, 1526527, 16582432.
28. Sekiguchi K. Biology of Horseshoe Crabs 1988, 50-68. Tokoyo: Science House Co., Ltd..
29. Cartwright RA, Hussin J, Keebler JEM, Stone EA, Awadalla P. A family-based probabilistic method for capturing de novo mutations from high-throughput short-read sequencing data. Stat Appl Genet Mol Biol 2012, 11(2).
30. Bird AP. DNA methylation and the frequency of CpG in animal DNA. Nucleic Acids Res 1980, 8:1499-1504. 10.1093/nar/8.7.1499, 324012, 6253938.
31. Lynch M. The origins of eukaryotic gene structure. Mol Biol Evol 2006, 23:450-468.
32. Broman KW, Murray JC, Sheffield VC, White RL, Weber JL. Comprehensive human genetic maps: individual and sex-specific variation in recombination. Am J Hum Genet 1998, 63:861-869. 10.1086/302011, 1377399, 9718341.
33. Kong A, Gudbjartsson DF, Sainz J, Jonsdottir GM, Gudjonsson SA, Richardsson B, Sigurdardottir S, Barnard J, Hallbeck B, Masson G, Shlien A, Palsson ST, Frigge ML, Thorgeirsson TE, Gulcher JR, Stefansson K. A high-resolution recombination map of the human genome. Nat Genet 2002, 31:241-247.
34. Coop G, Przeworski M. An evolutionary view of human recombination. Nat Rev Genet 2007, 8:23-34.
35. Hellmann I, Ebersberger I, Ptak SE, Pääbo S, Przeworski M. A neutral explanation for the correlation of diversity with recombination rates in humans. Am J Hum Genet 2003, 72:1527-1535. 10.1086/375657, 1180312, 12740762.
36. VectorBase Ixodes scapularis annotation, IscaW1. https://www.vectorbase.org/organisms/ixodes-scapularis, VectorBase.
37. Vanneste K, Van de Peer Y, Maere S. Inference of genome duplications from age distributions revisited. Mol Biol Evol 2013, 30:177-190. 10.1093/molbev/mss214, 22936721.
38. Obst M, Faurby S, Bussarawit S, Funch P. Molecular phylogeny of extant horseshoe crabs (Xiphosura, Limulidae) indicates Paleogene diversification of Asian species. Mol Phylogenet Evol 2012, 62:21-26. 10.1016/j.ympev.2011.08.025, 21939777.
39. Begun DJ, Aquadro CF. Levels of naturally occurring DNA polymorphism correlate with recombination rates in D. melanogaster. Nature 1992, 356:519-520. 10.1038/356519a0, 1560824.
40. Cutter AD, Payseur BA. Selection at linked sites in the partial selfer caenorhabditis elegans. Mol Biol Evol 2003, 20:665-673. 10.1093/molbev/msg072, 12679551.
41. Nachman MW. Single nucleotide polymorphisms and recombination rate in humans. Trends Genet 2001, 17:481-485. 10.1016/S0168-9525(01)02409-X, 11525814.
42. Stephan W, Langley CH. DNA polymorphism in lycopersicon and crossing-over per physical length. Genetics 1998, 150:1585-1593. 1460412, 9832534.
43. Roselius K, Stephan W, Städler T. The relationship of nucleotide polymorphism, recombination rate and selection in wild tomato species. Genetics 2005, 171:753-763. 10.1534/genetics.105.043877, 1456785, 16085701.
44. Andolfatto P, Przeworski M. Regions of lower crossing over harbor more rare variants in African populations of drosophila melanogaster. Genetics 2001, 158:657-665. 1461661, 11404330.
45. Havlak P, Chen R, Durbin KJ, Egan A, Ren Y, Song X-Z, Weinstock GM, Gibbs RA. The atlas genome assembly system. Genome Res 2004, 14:721-732. 10.1101/gr.2264004, 383319, 15060016.
46. Treangen TJ, Sommer DD, Angly FE, Koren S, Pop M. Next generation sequence assembly with AMOS. Current Protocols in Bioinformatics 2011, 33:11.8.1-11.8.18.
47. The JAM-pipeline. https://github.com/putnamlab/jam-pipeline.
48. Johnson SL, Brockmann HJ. Costs of multiple mates: an experimental study in horseshoe crabs. Anim Behav 2010, 80:773-782.
49. Mullikin JC, Ning Z. The phusion assembler. Genome Res 2003, 13:81-90. 10.1101/gr.731003, 430959, 12529309.
50. Cock PJA, Fields CJ, Goto N, Heuer ML, Rice PM. The Sanger FASTQ file format for sequences with quality scores, and the Solexa/Illumina FASTQ variants. Nucleic Acids Res 2010, 38:1767-1771. 10.1093/nar/gkp1137, 2847217, 20015970.
51. Ewing B, Green P. Base-calling of automated sequencer traces usingphred. ii. error probabilities. Genome Res 1998, 8:186-194.
52. Knuth DE. Searching and Sorting, Volume 3 1973, Reading, MA: Addison-Wesley, [The Art of Computer Programming].
53. Roberts M, Hayes W, Hunt BR, Mount SM, Yorke JA. Reducing storage requirements for biological sequence comparison. Bioinformatics 2004, 20:3363-3369. 10.1093/bioinformatics/bth408, 15256412.
54. Ye C, Ma ZS, Cannon CH, Pop M, Yu DW. Exploiting sparseness in de novo genome assembly. BMC Bioinformatics 2012, 13(6):S1.
55. Ensembl. http://www.ensembl.org/index.html.
56. Chen GK, Marjoram P, Wall JD. Fast and flexible simulation of DNA sequence data. Genome Res 2009, 19:136-142. 2612967, 19029539.
57. Dehal P, Satou Y, Campbell RK, Chapman J, Degnan B, Tomaso AD, Davidson B, Gregorio AD, Gelpke M, Goodstein DM, Harafuji N, Hastings KEM, Ho I, Hotta K, Huang W, Kawashima T, Lemaire P, Martinez D, Meinertzhagen IA, Necula S, Nonaka M, Putnam N, Rash S, Saiga H, Satake M, Terry A, Yamada L, Wang H-G, Awazu S, Azumi K, et al. The draft genome of ciona intestinalis: insights into chordate and vertebrate origins. Science 2002, 298:2157-2167. 10.1126/science.1080049, 12481130.
58. Haubold B, Pfaffelhuber P, Lynch M. mlRho - a program for estimating the population mutation and recombination rates from shotgun-sequenced diploid genomes. Mol Ecol 2010, 19:277-284.
59. Small KS, Brudno M, Hill MM, Sidow A. Extreme genomic variation in a natural population. Proc Natl Acad Sci 2007, 104:5698-5703. 10.1073/pnas.0700890104, 1838466, 17372217.
60. dwgsim. https://github.com/nh13/DWGSIM/releases.
61. Lunter G, Goodson M. Stampy: a statistical algorithm for sensitive and fast mapping of Illumina sequence reads. Genome Res 2011, 21:936-939. 10.1101/gr.111120.110, 3106326, 20980556.
62. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R. The sequence alignment/Map format and SAMtools. Bioinformatics 2009, 25:2078-2079. 10.1093/bioinformatics/btp352, 2723002, 19505943.
63. Yang Z. Statistical properties of a DNA sample under the finite-sites model. Genetics 1996, 144:1941-1950. 1207741, 8978077.
64. Haldane JBS. The combination of linkage values and the calculation of distances between the loci of linked factors. J Genet 1919, 8:299-309.
65. Gordon D, Abajian C, Green P. Consed: a graphical tool for sequence finishing. Genome Res 1998, 8:195-202. 10.1101/gr.8.3.195, 9521923.
66. Slater GS, Birney E. Automated generation of heuristics for biological sequence comparison. BMC Bioinformatics 2005, 6:31. 10.1186/1471-2105-6-31, 553969, 15713233.
67. Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 2004, 32:1792-1797. 10.1093/nar/gkh340, 390337, 15034147.
68. Ronquist F, Huelsenbeck JP. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 2003, 19:1572-1574. 10.1093/bioinformatics/btg180, 12912839.
69. Yang Z, Nielsen R. Estimating synonymous and nonsynonymous substitution rates under realistic evolutionary models. Mol Biol Evol 2000, 17:32-43. 10.1093/oxfordjournals.molbev.a026236, 10666704.
70. Zhang Z, Li J, Zhao X-Q, Wang J, Wong GK-S, Yu J. KaKs calculator: calculating Ka and Ks through model selection and model averaging. Genomics Proteomics Bioinformatics 2006, 4:259-263. 10.1016/S1672-0229(07)60007-2, 17531802.
71. Benaglia T, Chauveau D, Hunter, David R, Young, Derek S. mixtools: An R package for analyzing finite mixture models. J Stat Softw 2009, 32:1-29.
72. Nossa CW, Havlak P, Yue JX, Lv J, Vincent KY, Brockmann HJ, Putnam NH. Supporting materials from " Joint assembly and genetic mapping of the Atlantic horseshoe crab genome reveals ancient whole genome duplication" . 2014, GigaScience Database. http://dx.doi.org/10.5524/100091.