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

GigaScience

Nicholas H Putnam¹  H Jane Brockmann³  Kimberly Y Vincent⁴  Jie Lv⁴  Jia-Xing Yue⁴  Paul Havlak⁴  Carlos W Nossa² 

[1] Department of Biochemistry and Cell Biology, Rice University, P.O. Box 1892, Houston, TX 77251-1892, USA;Current address: Gene by Gene, Ltd, Houston, TX 77008, USA;Department of Biology, University of Florida, P.O. Box 11-8525 Gainesville, FL 32611-8525, USA;Department of Ecology and Evolutionary Biology, Rice University, P.O. Box 1892, Houston, TX 77251-1892, USA

关键词: Limulus polyphemus;    Genome evolution;    Genetic linkage mapping;    Genotyping-by-sequencing (GBS);   

Others  :  861358
DOI  :  10.1186/2047-217X-3-9

 received in 2013-10-23, accepted in 2014-04-23,  发布年份 2014

【 摘 要 】

Background

Horseshoe crabs are marine arthropods with a fossil record extending back approximately 450 million years. They exhibit remarkable morphological stability over their long evolutionary history, retaining a number of ancestral arthropod traits, and are often cited as examples of “living fossils.” As arthropods, they belong to the Ecdysozoa, an ancient super-phylum whose sequenced genomes (including insects and nematodes) have thus far shown more divergence from the ancestral pattern of eumetazoan genome organization than cnidarians, deuterostomes and lophotrochozoans. However, much of ecdysozoan diversity remains unrepresented in comparative genomic analyses.

Results

Here we apply a new strategy of combined de novo assembly and genetic mapping to examine the chromosome-scale genome organization of the Atlantic horseshoe crab, Limulus polyphemus. We constructed a genetic linkage map of this 2.7 Gbp genome by sequencing the nuclear DNA of 34 wild-collected, full-sibling embryos and their parents at a mean redundancy of 1.1x per sample. The map includes 84,307 sequence markers grouped into 1,876 distinct genetic intervals and 5,775 candidate conserved protein coding genes.

Conclusions

Comparison with other metazoan genomes shows that the L. polyphemus genome preserves ancestral bilaterian linkage groups, and that a common ancestor of modern horseshoe crabs underwent one or more ancient whole genome duplications 300 million years ago, followed by extensive chromosome fusion. These results provide a counter-example to the often noted correlation between whole genome duplication and evolutionary radiations. The new, low-cost genetic mapping method for obtaining a chromosome-scale view of non-model organism genomes that we demonstrate here does not require laboratory culture, and is potentially applicable to a broad range of other species.

【 授权许可】

   
2014 Nossa et al.; licensee BioMed Central Ltd.

【 图 表 】

Fig. 3.

【 参考文献 】

• [1]Ohno S: Evolution by Gene Duplication. Springer-Verlag; 1970.
• [2]Wolfe KH, Shields DC: Molecular evidence for an ancient duplication of the entire yeast genome. Nature 1997, 387:708-713.
• [3]McLysaght A, Hokamp K, Wolfe KH: Extensive genomic duplication during early chordate evolution. Nat Genet 2002, 31:200-204.
• [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.
• [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.
• [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.
• [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.
• [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.
• [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]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. BioMed Central Full Text
• [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 İ, 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.
• [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.
• [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.
• [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.
• [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.
• [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.
• [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.
• [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.
• [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.
• [21]Rudkin DM, Young GA: Horseshoe crabs – an ancient ancestry revealed. In Biol Conserv Horseshoe Crabs. Edited by Tanacredi JT, Botton ML, Smith D. New York: Springer; 2009:25-44.
• [22]Fisher DC: The Xiphosurida: archetypes of Bradytely? In Living Foss. Edited by Eldrege N, Stanley SM. New York: Springer; 1984:196-213.
• [23]Berkson J, Shuster CN Jr: The horseshoe crab: the battle for a true multiple-use resource. Fisheries 1999, 24:6-10.
• [24]Shuster CN Jr, Barlow RB, Brockmann HJ (Eds): The American Horseshoe Crab. Cambridge, MA: Harvard University Press; 2003.
• [25]Gregory TR: Animal Genome Size Database. http://www.genomesize.com webcite
• [26]Pop M, Kosack DS, Salzberg SL: Hierarchical scaffolding with bambus. Genome Res 2004, 14:149-159.
• [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.
• [28]Sekiguchi K: Biology of Horseshoe Crabs. Tokoyo: Science House Co., Ltd.; 1988:50-68.
• [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.
• [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.
• [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.
• [36]VectorBase: Ixodes scapularis annotation, IscaW1. https://www.vectorbase.org/organisms/ixodes-scapularis webcite
• [37]Vanneste K, Van de Peer Y, Maere S: Inference of genome duplications from age distributions revisited. Mol Biol Evol 2013, 30:177-190.
• [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.
• [39]Begun DJ, Aquadro CF: Levels of naturally occurring DNA polymorphism correlate with recombination rates in D. melanogaster. Nature 1992, 356:519-520.
• [40]Cutter AD, Payseur BA: Selection at linked sites in the partial selfer caenorhabditis elegans. Mol Biol Evol 2003, 20:665-673.
• [41]Nachman MW: Single nucleotide polymorphisms and recombination rate in humans. Trends Genet 2001, 17:481-485.
• [42]Stephan W, Langley CH: DNA polymorphism in lycopersicon and crossing-over per physical length. Genetics 1998, 150:1585-1593.
• [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.
• [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.
• [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.
• [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 webcite
• [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.
• [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.
• [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. Reading, MA: Addison-Wesley; 1973. [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.
• [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 webcite
• [56]Chen GK, Marjoram P, Wall JD: Fast and flexible simulation of DNA sequence data. Genome Res 2009, 19:136-142.
• [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.
• [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.
• [60]dwgsim https://github.com/nh13/DWGSIM/releases webcite
• [61]Lunter G, Goodson M: Stampy: a statistical algorithm for sensitive and fast mapping of Illumina sequence reads. Genome Res 2011, 21:936-939.
• [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.
• [63]Yang Z: Statistical properties of a DNA sample under the finite-sites model. Genetics 1996, 144:1941-1950.
• [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.
• [66]Slater GS, Birney E: Automated generation of heuristics for biological sequence comparison. BMC Bioinformatics 2005, 6:31. BioMed Central Full Text
• [67]Edgar RC: MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 2004, 32:1792-1797.
• [68]Ronquist F, Huelsenbeck JP: MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 2003, 19:1572-1574.
• [69]Yang Z, Nielsen R: Estimating synonymous and nonsynonymous substitution rates under realistic evolutionary models. Mol Biol Evol 2000, 17:32-43.
• [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.
• [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 webcite