A ddRAD-based genetic map and its integration with the genome assembly of Japanese eel (Anguilla japonica) provides insights into genome evolution after the teleost-specific genome duplication

BMC Genomics

Mitsuru Ototake¹  Takanori Kobayashi²  Hideki Tanaka⁴  Jiro Nagao⁴  Koichiro Gen³  Yukinori Kazeto⁴  Akiyuki Ozaki⁴  Tetsuji Masaoka⁴  Nobuhiko Ojima¹  Motoshige Yasuike¹  Yoji Nakamura¹  Atushi Fujiwara¹  Kazuharu Nomura⁴  Wataru Kai¹ 

[1] National Research Institute of Fisheries Science, Fisheries Research Agency, Yokohama-shi, Kanagawa 236-8648, Japan;Fisheries Research Agency, Yokohama-shi, Kanagawa 220-6115, Japan;Present address: Seikai National Fisheries Research Institute, Fisheries Research Agency, Nagasaki-shi, Nagasaki 851-2213, Japan;National Research Institute of Aquaculture, Fisheries Research Agency, Minami-ise-cho, Mie 516-0193, Japan

关键词: Teleost-specific whole genome duplication;    Synteny;    Ion PGM;    ddRAD-seq;    Genetic map;    Japanese eel;   

Others  :  1217629
DOI  :  10.1186/1471-2164-15-233

 received in 2013-11-21, accepted in 2014-03-17,  发布年份 2014

【 摘 要 】

Background

Recent advancements in next-generation sequencing technology have enabled cost-effective sequencing of whole or partial genomes, permitting the discovery and characterization of molecular polymorphisms. Double-digest restriction-site associated DNA sequencing (ddRAD-seq) is a powerful and inexpensive approach to developing numerous single nucleotide polymorphism (SNP) markers and constructing a high-density genetic map. To enrich genomic resources for Japanese eel (Anguilla japonica), we constructed a ddRAD-based genetic map using an Ion Torrent Personal Genome Machine and anchored scaffolds of the current genome assembly to 19 linkage groups of the Japanese eel. Furthermore, we compared the Japanese eel genome with genomes of model fishes to infer the history of genome evolution after the teleost-specific genome duplication.

Results

We generated the ddRAD-based linkage map of the Japanese eel, where the maps for female and male spanned 1748.8 cM and 1294.5 cM, respectively, and were arranged into 19 linkage groups. A total of 2,672 SNP markers and 115 Simple Sequence Repeat markers provide anchor points to 1,252 scaffolds covering 151 Mb (13%) of the current genome assembly of the Japanese eel. Comparisons among the Japanese eel, medaka, zebrafish and spotted gar genomes showed highly conserved synteny among teleosts and revealed part of the eight major chromosomal rearrangement events that occurred soon after the teleost-specific genome duplication.

Conclusions

The ddRAD-seq approach combined with the Ion Torrent Personal Genome Machine sequencing allowed us to conduct efficient and flexible SNP genotyping. The integration of the genetic map and the assembled sequence provides a valuable resource for fine mapping and positional cloning of quantitative trait loci associated with economically important traits and for investigating comparative genomics of the Japanese eel.

【 授权许可】

   
2014 Kai et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

Figure 3.

Figure 4.

【 参考文献 】

• [1]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.
• [2]Hohenlohe PA, Bassham S, Etter PD, Stiffler N, Johnson EA, Cresko WA: Population genomics of parallel adaptation in threespine stickleback using sequenced RAD tags. PLoS Genet 2010, 6:e1000862.
• [3]Etter PD, Bassham S, Hohenlohe PA, Johnson EA, Cresko WA: SNP discovery and genotyping for evolutionary genetics using RAD sequencing. Methods Mol Biol 2011, 772:157-178.
• [4]Amores A, Catchen J, Ferrara A, Fontenot Q, Postlethwait JH: Genome evolution and meiotic maps by massively parallel DNA sequencing: spotted gar, an outgroup for the teleost genome duplication. Genetics 2011, 188:799-808.
• [5]Houston RD, Davey JW, Bishop SC, Lowe NR, Mota-Velasco JC, Hamilton A, Guy DR, Tinch AE, Thomson ML, Blaxter ML, Gharbi K, Bron JE, Taggart JB: Characterisation of QTL-linked and genome-wide restriction site-associated DNA (RAD) markers in farmed Atlantic salmon. BMC Genomics 2012, 13:244. BioMed Central Full Text
• [6]Kakioka R, Kokita T, Kumada H, Watanabe K, Okuda N: A RAD-based linkage map and comparative genomics in the gudgeons (genus Gnathopogon, Cyprinidae). BMC Genomics 2013, 14:32. BioMed Central Full Text
• [7]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.
• [8]Peterson BK, Weber JN, Kay EH, Fisher HS, Hoekstra HE: Double digest RADseq: an inexpensive method for de novo SNP discovery and genotyping in model and non-model species. PLoS One 2012, 7:e37135.
• [9]Rothberg JM, Hinz W, Rearick TM, Schultz J, Mileski W, Davey M, Leamon JH, Johnson K, Milgrew MJ, Edwards M, Hoon J, Simons JF, Marran D, Myers JW, Davidson JF, Branting A, Nobile JR, Puc BP, Light D, Clark TA, Huber M, Branciforte JT, Stoner IB, Cawley SE, Lyons M, Fu Y, Homer N, Sedova M, Miao X, Reed B, et al.: An integrated semiconductor device enabling non-optical genome sequencing. Nature 2011, 475:348-352.
• [10]Quail MA, Smith M, Coupland P, Otto TD, Harris SR, Connor TR, Bertoni A, Swerdlow HP, Gu Y: A tale of three next generation sequencing platforms: comparison of Ion Torrent, Pacific Biosciences and Illumina MiSeq sequencers. BMC Genomics 2012, 13:341. BioMed Central Full Text
• [11]Vogel U, Szczepanowski R, Claus H, Junemann S, Prior K, Harmsen D: Ion torrent personal genome machine sequencing for genomic typing of Neisseria meningitidis for rapid determination of multiple layers of typing information. J Clin Microbiol 2012, 50:1889-1894.
• [12]Yamamoto K, Yamauchi K: Sexual maturation of Japanese eel and production of eel larvae in the aquarium. Nature 1974, 251:220-222.
• [13]Yamauchi K, Nakamura M, Takahashi H, Takano K: Cultivation of larvae of Japanese eel. Nature 1976, 263:412.
• [14]Kagawa H, Tanaka H, Ohta H, Unuma T, Nomura K: The first success of glass eel production in the world: basic biology on fish reproduction advances new applied technology in aquaculture. Fish Physiol Biochem 2005, 31:193-199.
• [15]Henkel CV, Dirks RP, de Wijze DL, Minegishi Y, Aoyama J, Jansen HJ, Turner B, Knudsen B, Bundgaard M, Hvam KL, Boetzer M, Pirovano W, Weltzien FA, Dufour S, Tsukamoto K, Spaink HP, van den Thillart GE: First draft genome sequence of the Japanese eel, Anguilla japonica. Gene 2012, 511:195-201.
• [16]Nomura K, Ozaki A, Morishima K, Yoshikawa Y, Tanaka H, Unuma T, Ohta H, Arai K: A genetic linkage map of the Japanese eel (Anguilla japonica) based on AFLP and microsatellite markers. Aquaculture 2011, 310:329-342.
• [17]Grisart B, Coppieters W, Farnir F, Karim L, Ford C, Berzi P, Cambisano N, Mni M, Reid S, Simon P, Spelman R, Georges M, Snell R: Positional candidate cloning of a QTL in dairy cattle: identification of a missense mutation in the bovine DGAT1 gene with major effect on milk yield and composition. Genome Res 2002, 12:222-231.
• [18]Huang X, Qian Q, Liu Z, Sun H, He S, Luo D, Xia G, Chu C, Li J, Fu X: Natural variation at the DEP1 locus enhances grain yield in rice. Nat Genet 2009, 41:494-497.
• [19]Kasahara M, Naruse K, Sasaki S, Nakatani Y, Qu W, Ahsan B, Yamada T, Nagayasu Y, Doi K, Kasai Y, Jindo T, Kobayashi D, Shimada A, Toyoda A, Kuroki Y, Fujiyama A, Sasaki T, Shimizu A, Asakawa S, Shimizu N, Hashimoto S, Yang J, Lee Y, Matsushima K, Sugano S, Sakaizumi M, Narita T, Ohishi K, Haga S, Ohto F, et al.: The medaka draft genome and insights into vertebrate genome evolution. Nature 2007, 447:714-719.
• [20]Kai W, Kikuchi K, Tohari S, Chew AK, Tay A, Fujiwara A, Hosoya S, Suetake H, Naruse K, Brenner S, Suzuki Y, Venkatesh B: Integration of the genetic map and genome assembly of fugu facilitates insights into distinct features of genome evolution in teleosts and mammals. Genome Biol Evol 2011, 3:424-442.
• [21]Inoue JG, Miya M, Tsukamoto K, Nishida M: Basal actinopterygian relationships: a mitogenomic perspective on the phylogeny of the “ancient fish”. Mol Phylogenet Evol 2003, 26:110-120.
• [22]Nelson JS: Fishes of the world, 4th editon. New York: John Wiley and Sons, Inc; 2006.
• [23]Postlethwait JH, Yan YL, Gates MA, Horne S, Amores A, Brownlie A, Donovan A, Egan ES, Force A, Gong Z, Goutel C, Fritz A, Kelsh R, Knapik E, Liao E, Paw B, Ransom D, Singer A, Thomson M, Abduljabbar TS, Yelick P, Beier D, Joly JS, Larhammar D, Rosa F, Westerfield M, Zon LI, Johnson SL, Talbot WS, et al.: Vertebrate genome evolution and the zebrafish gene map. Nat Genet 1998, 18:345-349.
• [24]Jaillon O, Aury JM, Brunet F, Petit JL, Stange-Thomann N, Mauceli E, Bouneau L, Fischer C, Ozouf-Costaz C, Bernot A, Nicaud S, Jaffe D, Fisher S, Lutfalla G, Dossat C, Segurens B, Dasilva C, Salanoubat M, Levy M, Boudet N, Castellano S, Anthouard V, Jubin C, Castelli V, Katinka M, Vacherie B, Biémont C, Skalli Z, Cattolico L, Poulain J, et al.: Genome duplication in the teleost fish Tetraodon nigroviridis reveals the early vertebrate proto-karyotype. Nature 2004, 431:946-957.
• [25]Comai L: The advantages and disadvantages of being polyploid. Nat Rev Genet 2005, 6:836-846.
• [26]Semon M, Wolfe KH: Rearrangement rate following the whole-genome duplication in teleosts. Mol Biol Evol 2007, 24:860-867.
• [27]Satoh H, Nimura Y, Hibiya T: Sex control of the Japanese eel by an estrogen (DES-Na) in feed. Bull Japan Soc Sci Fish 1992, 58:1211-1218.
• [28]Chiba H, Iwatsuki K, Hayami K, Yamauchi K: Effects of dietary estradiol-17β on feminization, growth and body composition in the Japanese eel (Anguilla japonica). Comp Biochem Physiol 1993, 106:367-371.
• [29]Tachiki H, Nakagawa T, Tamura K, Hirose K: Effects of oral administration of estradiol-17β to young on gonadal sex and growth of Japanese eel Anguilla japonica. Suisanzoshoku 1997, 45:61-66. (in Japanese)
• [30]Ohta H, Kagawa H, Tanaka H, Okuzawa K, Hirose K: Milt production in the Japanese eel Anguilla japonica induced by repeated injections of human chorionic gonadotropin. Fish Sci 1996, 62:44-49.
• [31]Kagawa H, Tanaka H, Ohta H, Okuzawa K, Iimura N: Induced ovulation by injection of 17, 20β-dihydroxy-4-pregnen-3-one in the artificially matured Japanese eel, with special reference to ovulation time. Fish Sci 1997, 63:365-367.
• [32]Catchen JM, Amores A, Hohenlohe P, Cresko W, Postlethwait JH: Stacks: building and genotyping loci de novo from short-read sequences. G3 (Bethesda) 2011, 1:171-182.
• [33]Edgar RC: Search and clustering orders of magnitude faster than BLAST. Bioinformatics 2010, 26:2460-2461.
• [34]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.
• [35]DePristo MA, Banks E, Poplin R, Garimella KV, Maguire JR, Hartl C, Philippakis AA, del Angel G, Rivas MA, Hanna M, McKenna A, Fennell TJ, Kernytsky AM, Sivachenko AY, Cibulskis K, Gabriel SB, Altshuler D, Daly MJ: A framework for variation discovery and genotyping using next-generation DNA sequencing data. Nat Genet 2011, 43:491-498.
• [36]Nakamura N, Shigenobu Y, Sugaya T, Kurokawa T, Saitoh K: Automated screening and primer design of fish microsatellite DNA loci on pyrosequencing data. Ichthyol Res 2013, 60:184-187.
• [37]Grattapaglia D, Sederoff R: Genetic linkage maps of Eucalyptus grandis and Eucalyptus urophylla using a pseudo-testcross: mapping strategy and RAPD markers. Genetics 1994, 137:1121-1137.
• [38]Broman KW, Wu H, Sen S, Churchill GA: R/qtl: QTL mapping in experimental crosses. Bioinformatics 2003, 19:889-890.
• [39]Genetic-mapper https://code.google.com/p/genetic-mapper/ webcite
• [40]Chakravarti A, Lasher LK, Reefer JE: A maximum likelihood method for estimating genome length using genetic linkage data. Genetics 1991, 128:175-182.
• [41]ZF-Genomics http://www.zfgenomics.org webcite
• [42]UCSC Genome Bioinformatics http://genome.ucsc.edu/index.html webcite
• [43]RepeatMasker http://www.repeatmasker.org webcite
• [44]Darling AE, Mau B, Perna NT: ProgressiveMauve: multiple genome alignment with gene gain, loss and rearrangement. PLoS One 2010, 5:e11147.
• [45]Pre Ensembl http://pre.ensembl.org/index.html webcite
• [46]Park EH, Kang YS: Karyotype conservation and difference in DNA amount in anguilloid fishes. Science 1976, 193:64-66.
• [47]Nomura K, Nakajima J, Ohta H, Kagawa H, Tanaka H, Unuma T, Yamauchi K, Arai K: Induction of triploidy by heat shock in the Japanese eel Anguilla japonica. Fish Sci 2004, 70:247-255.
• [48]Lenormand T, Dutheil J: Recombination difference between sexes: a role for haploid selection. PLoS Biol 2005, 3:e63.
• [49]Lenormand T: The evolution of sex dimorphism in recombination. Genetics 2003, 163:811-822.
• [50]Sakamoto T, Danzmann RG, Gharbi K, Howard P, Ozaki A, Khoo SK, Woram RA, Okamoto N, Ferguson MM, Holm LE, Guyomard R, Hoyheim B: A microsatellite linkage map of rainbow trout (Oncorhynchus mykiss) characterized by large sex-specific differences in recombination rates. Genetics 2000, 155:1331-1345.
• [51]Singer A, Perlman H, Yan Y, Walker C, Corley-Smith G, Brandhorst B, Postlethwait J: Sex-specific recombination rates in zebrafish (Danio rerio). Genetics 2002, 160:649-657.
• [52]Fujiwara A, Nishida-Umehara C, Sakamoto T, Okamoto N, Nakayama I, Abe S: Improved fish lymphocyte culture for chromosome preparation. Genetica 2001, 111:77-89.
• [53]Minegishi Y, Henkel CV, Dirks RP, van den Thillart GE: Genomics in eels - towards aquaculture and biology. Mar Biotechnol 2012, 14:583-590.
• [54]Nakatani Y, Takeda H, Kohara Y, Morishita S: Reconstruction of the vertebrate ancestral genome reveals dynamic genome reorganization in early vertebrates. Genome Res 2007, 17:1254-1265.
• [55]Broughton RE, Betancur RR, Li C, Arratia G, Orti G: Multi-locus phylogenetic analysis reveals the pattern and tempo of bony fish evolution. PLoS Curr 2013., 5ecurrents.tol.2ca8041495ffafd0c92756e75247483e
• [56]Wolfe KH: Yesterday’s polyploids and the mystery of diploidization. Nat Rev Genet 2001, 2:333-341.
• [57]Gavranović H, Chauve C, Salse J, Tannier E: Mapping ancestral genomes with massive gene loss: a matrix sandwich problem. Bioinformatics 2011, 27:i257-265.