The channel catfish genome sequence provides insights into the evolution of scale formation in teleosts

Nature Communications

Volumn 7, Issue , 2016, Pages

  Liu, Zhanjiang ^a   Liu, Shikai ^a   Yao, Jun ^a   Bao, Lisui ^a   Zhang, Jiaren ^a   Li, Yun ^a   Jiang, Chen ^a   Sun, Luyang ^a   Wang, Ruijia ^a   Zhang, Yu ^a   Zhou, Tao ^a   Zeng, Qifan ^a   Fu, Qiang ^a   Gao, Sen ^a   Li, Ning ^a   Koren, Sergey ^b,g   Jiang, Yanliang ^a   Zimin, Aleksey ^c   Xu, Peng ^a   Phillippy, Adam M ^b,g   Geng, Xin ^a   Song, Lin ^a   Sun, Fanyue ^a   Li, Chao ^a   Wang, Xiaozhu ^a   Chen, Ailu ^a   Jin, Yulin ^a   Yuan, Zihao ^a   Yang, Yujia ^a   Tan, Suxu ^a   Peatman, Eric ^a   Lu, Jianguo ^a   Qin, Zhenkui ^a   Dunham, Rex ^a   Li, Zhaoxia ^a   Sonstegard, Tad ^d,h   Feng, Jianbin ^a   Danzmann, Roy G ^e   Schroeder, Steven ^d   Scheffler, Brian ^f   Duke, Mary V ^f   Ballard, Linda ^f   Kucuktas, Huseyin ^a   Kaltenboeck, Ludmilla ^a   Liu, Haixia ^a   Armbruster, Jonathan ^a   Xie, Yangjie ^a   Kirby, Mona L ^f   Tian, Yi ^a   Flanagan, Mary Elizabeth ^f   Mu, Weijie ^a   Waldbieser, Geoffrey C ^f   more..

^a AUBURN UNIVERSITY   (United States)

^b National Biodefense Analysis and Countermeasures Center   (United States)

^c Bldg 142   (United States)

^d AGRICULTURAL RESEARCH SERVICE   (United States)

^e UNIVERSITY OF GUELPH   (Canada)

^f AGRICULTURAL RESEARCH SERVICE   (United States)

^g NATIONAL HUMAN GENOME RESEARCH INSTITUTE   (United States)

^h RECOMBINETICS INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ECTODYSPLASIN A; FIBROBLAST GROWTH FACTOR RECEPTOR; FRESH WATER; LYMPHOID ENHANCER FACTOR 1; PHOSPHOPROTEIN; SECRETORY CALCIUM BINDING PHOSPHOPROTEIN; UNCLASSIFIED DRUG; CALCIUM BINDING PROTEIN; FISH PROTEIN;

AQUACULTURE; CALCIUM; COMPARATIVE STUDY; EXPERIMENTAL STUDY; GENETIC ANALYSIS; GENOME; PROTEIN; TELEOST;

ARTICLE; BINDING SITE; CARTILAGINOUS FISH; CHANNEL CATFISH; CONTROLLED STUDY; EXON; GENE DUPLICATION; GENE MAPPING; GENETIC LINKAGE; GENETIC RECOMBINATION; NONHUMAN; PHENOTYPE; PROMOTER REGION; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STICKLEBACK; TELEOST; ZEBRA FISH; ANATOMY AND HISTOLOGY; ANIMAL; ANIMAL SCALES; CHROMOSOMAL MAPPING; CLASSIFICATION; EVOLUTION; GENE EXPRESSION REGULATION; GENE ONTOLOGY; GENETICS; GENOME; ICTALURIDAE; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; PHYLOGENY; SEQUENCE ALIGNMENT; SINGLE NUCLEOTIDE POLYMORPHISM;

UNITED STATES;

ICTALURUS PUNCTATUS; SILURIFORMES; TELEOSTEI; VERTEBRATA;

ANIMAL SCALES; ANIMALS; BASE SEQUENCE; BIOLOGICAL EVOLUTION; CALCIUM-BINDING PROTEINS; CHROMOSOME MAPPING; FISH PROTEINS; GENE EXPRESSION REGULATION; GENE ONTOLOGY; GENOME; ICTALURIDAE; MOLECULAR SEQUENCE ANNOTATION; OPEN READING FRAMES; PHOSPHOPROTEINS; PHYLOGENY; POLYMORPHISM, SINGLE NUCLEOTIDE; SEQUENCE ALIGNMENT;

EID: 84973294639     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms11757     Document Type: Article

References (69)

1. Wilson, D. E. & Reeder, D. M. Mammal Species of the World: A Taxonomic and Geographic Reference (JHU Press, 2005).
2. Uetz, P. & Hosek, J. The Reptile Database. Available at http://www.reptiledatabase. org/(accessed 23 March 2015).
3. Gill, F. B. & Wright, M. T. Birds Of The World: Recommended English Names (Princeton Univ. Press Princeton, 2006).
4. Eschmeyer, W. & Fong, J. Catalog of fishes: Species by family/subfamily electronic version (accessed 23 March 2015). Available at http://research.calacademy.org/research/ichthyology/catalog/SpeciesByFamily.asp (2014).
5. AmphibiaWeb. AmphibiaWeb. Available at http://Amphibiaweb.org (accessed 23 March 2015).
6. Sullivan, J. P., Lundberg, J. G. & Hardman, M. A phylogenetic analysis of the major groups of catfishes (Teleostei: Siluriformes) using rag1 and rag2 nuclear gene sequences. Mol. Phylogenet. Evol. 41, 636-662 (2006).
7. Moyle, P. B. & Cech, Jr J. J. Fishes: an introduction to ichthyology 5th edn (Prentice Hall, London, England, 2004).
8. Arce, M., Reis, R. E., Geneva, A. J. & Pérez, M. H. S. Molecular phylogeny of thorny catfishes (Siluriformes: Doradidae). Mol. Phylogenet. Evol. 67, 560-577 (2013).
9. Liu, Z. Development of genomic resources in support of sequencing, assembly, and annotation of the catfish genome. Comp. Biochem. Physiol. D 6, 11-17 (2011).
10. Chen, S. et al. Whole-genome sequence of A flatfish provides insights into ZW sex chromosome evolution and adaptation to A benthic lifestyle. Nat. Genet. 46, 253-260 (2014).
11. Star, B. et al. The genome sequence of Atlantic cod reveals A unique immune system. Nature 477, 207-210 (2011).
12. Xu, P. et al. Genome sequence and genetic diversity of the common carp Cyprinus carpio. Nat. Genet. 46, 1212-1219 (2014).
13. LeGrande, W., Dunham, R. A. & Smitherman, R. O. Comparative karyology of three species of north American catfishes (siluriformes: Ictaluridae: Ictalurus) and four of their hybrid combinations. Copeia 1984, 873-878 (1984).
14. Tiersch, T. & Goudie, C. Inheritance and variation of genome size in half-sib families of hybrid catfishes. J. Hered. 84, 122-125 (1993).
15. Kasahara, M. et al. The medaka draft genome and insights into vertebrate genome evolution. Nature 447, 714-719 (2007).
16. Meyer, A. & Van de Peer, Y. From 2R to 3R: evidence for A fish-specific genome duplication (FSGD). Bioessays 27, 937-945 (2005).
17. Waldbieser, G. C., Bosworth, B. G. & Quiniou, S. M. Production of viable homozygous, doubled haploid channel catfish (Ictalurus punctatus). Mar. Biotechnol. 12, 380-385 (2010).
18. Zimin, A. V. et al. The MaSuRCA genome assembler. Bioinformatics 29, 2669-2677 (2013).
19. Koren, S. et al. Reducing assembly complexity of microbial genomes with single-molecule sequencing. Genome Biol. 14, R101 (2013).
20. Li, Y. et al. Construction of A high-density, high-resolution genetic map and its integration with BAC-based physical map in channel catfish. DNA Res. 22, 39-52 (2015).
21. Wang, S. et al. Characterization of A BAC library from channel catfish Ictalurus punctatus: indications of high levels of chromosomal reshuffling among teleost genomes. Mar. Biotechnol. 9, 701-711 (2007).
22. Sun, L. et al. Identification and analysis of genome-wide SNPs provide insight into signatures of selection and domestication in channel catfish (Ictalurus punctatus). PLoS ONE 9, e109666 (2014).
23. Howe, K. et al. The zebrafish reference genome sequence and its relationship to the human genome. Nature 496, 498-503 (2013).
24. Liu, S. et al. Efficient assembly and annotation of the transcriptome of catfish by RNA-Seq analysis of A doubled haploid homozygote. BMC Genomics 13, 595 (2012).
25. Wang, S. et al. Assembly of 500 000 inter-specific catfish expressed sequence tags and large scale gene-associated marker development for whole genome association studies. Genome Biol. 11, R8 (2010).
26. Sun, F. et al. Transcriptomic signatures of attachment, NF-kappaB suppression and IFN stimulation in the catfish gill following columnaris bacterial infection. Dev. Comp. Immunol. 38, 169-180 (2012).
27. Liu, S. et al. Generation of genome-scale gene-associated SNPs in catfish for the construction of A high-density SNP array. BMC Genomics 12, 53 (2011).
28. Li, C. et al. RNA-seq analysis of mucosal immune responses reveals signatures of intestinal barrier disruption and pathogen entry following Edwardsiella ictaluri infection in channel catfish, Ictalurus punctatus. Fish Shellfish Immunol. 32, 816-827 (2012).
29. Venkatesh, B. et al. Elephant shark genome provides unique insights into gnathostome evolution. Nature 505, 174-179 (2014).
30. Li, H. & Durbin, R. Inference of human population history from individual whole-genome sequences. Nature 475, 493-496 (2011).
31. Amores, A., Catchen, J., Ferrara, A., Fontenot, Q. & Postlethwait, J. H. Genome evolution and meiotic maps by massively parallel DNA sequencing: spotted gar, an outgroup for the teleost genome duplication. Genetics 188, 799-808 (2011).
32. Niimura, Y. & Nei, M. Evolutionary dynamics of olfactory receptor genes in fishes and tetrapods. Proc. Natl Acad. Sci. USA 102, 6039-6044 (2005).
33. Haire, R. N. et al. Genomic and functional characterization of the diverse immunoglobulin domain-containing protein (DICP) family. Genomics 99, 282-291 (2012).
34. Ryll, B., Sanchez, S., Haitina, T., Tafforeau, P. & Ahlberg, P. E. The genome of Callorhinchus and the fossil record: A new perspective on SCPP gene evolution in gnathostomes. Evol. Dev. 16, 123-124 (2014).
35. Ishimaru, Y. et al. Two families of candidate taste receptors in fishes. Mech. Dev. 122, 1310-1321 (2005).
36. Yasuoka, A., Aihara, Y., Matsumoto, I. & Abe, K. Phospholipase C-beta 2 as A mammalian taste signaling marker is expressed in the multiple gustatory tissues of medaka fish, Oryzias latipes. Mech. Dev. 121, 985-989 (2004).
37. Subramanian, S., Ross, N. W. & MacKinnon, S. L. Comparison of antimicrobial activity in the epidermal mucus extracts of fish. Comp. Biochem. Physiol. B 150, 85-92 (2008).
38. Kondo, S. et al. The medaka rs-3 locus required for scale development encodes ectodysplasin-A receptor. Curr. Biol. 11, 1202-1206 (2001).
39. Rohner, N. et al. Duplication of fgfr1 permits Fgf signaling to serve as A target for selection during domestication. Curr. Biol. 19, 1642-1647 (2009).
40. Wagner, D. O. & Aspenberg, P. Where did bone come from? An overview of its evolution. Acta Orthop. 82, 393-398 (2011).
41. Steinmetz, A. et al. Human apolipoprotein A-IV binds to apolipoprotein AI/A-II receptor sites and promotes cholesterol efflux from adipose cells. J. Biol. Chem. 265, 7859-7863 (1990).
42. Wang, Y. et al. BMP and RA signaling cooperate to regulate Apolipoprotein C1 expression during embryonic development. Gene 554, 196-204 (2015).
43. Monnot, M. J. et al. Epidermal expression of apolipoprotein E gene during fin and scale development and fin regeneration in zebrafish. Dev. Dynam. 214, 207-215 (1999).
44. Kawasaki, K., Suzuki, T. & Weiss, K. M. Genetic basis for the evolution of vertebrate mineralized tissue. Proc. Natl Acad. Sci. USA 101, 11356-11361 (2004).
45. Kawasaki, K. & Weiss, K. M. Mineralized tissue and vertebrate evolution: the secretory calcium-binding phosphoprotein gene cluster. Proc. Natl Acad. Sci. USA 100, 4060-4065 (2003).
46. Kawasaki, K. The SCPP gene repertoire in bony vertebrates and graded differences in mineralized tissues. Dev. Genes Evol. 219, 147-157 (2009).
47. Kawasaki, K. The SCPP gene family and the complexity of hard tissues in vertebrates. Cell Tissue Res. 194, 108-112 (2011).
48. Kawasaki, K. & Amemiya, C. T. SCPP genes in the coelacanth: tissue mineralization genes shared by sarcopterygians. J. Exp. Zool. B Mol. Dev. Evol. 322, 390-402 (2014).
49. Kawasaki, K., Buchanan, A. V. & Weiss, K. M. Gene duplication and the evolution of vertebrate skeletal mineralization. Cell Tissue Res. 186, 7-24 (2007).
50. Kawasaki, K. & Weiss, K. SCPP gene evolution and the dental mineralization continuum. J. Dent. Res. 87, 520-531 (2008).
51. Kawasaki, K. & Weiss, K. M. Evolutionary genetics of vertebrate tissue mineralization: the origin and evolution of the secretory calcium-binding phosphoprotein family. J. Exp. Zool. B Mol. Dev. Evol. 306, 295-316 (2006).
52. Vieira, F. A. et al. Skin healing and scale regeneration in fed and unfed sea bream, Sparus auratus. BMC Genomics 12, 490 (2011).
53. Jones, F. C. et al. The genomic basis of adaptive evolution in threespine sticklebacks. Nature 484, 55-61 (2012).
54. Miyabe, K. et al. GSP-37, A novel goldfish scale matrix protein: identification, localization and functional analysis. Faraday Discuss. 159, 463-481 (2012).
55. Koren, S. et al. Hybrid error correction and de novo assembly of single-molecule sequencing reads. Nat. Biotechnol. 30, 693-700 (2012).
56. Marçais, G. & Kingsford, C. A fast, lock-free approach for efficient parallel counting of occurrences of k-mers. Bioinformatics 27, 764-770 (2011).
57. Liu, H. et al. Comparative analysis of catfish BAC end sequences with the zebrafish genome. BMC Genomics 10, 592 (2009).
58. Xu, P. et al. A BAC-based physical map of the channel catfish genome. Genomics 90, 380-388 (2007).
59. Xue, W. et al. L-RNA-scaffolder: scaffolding genomes with transcripts. BMC Genomics 14, 604 (2013).
60. Simpson, J. T. et al. ABySS: A parallel assembler for short read sequence data. Genome Res. 19, 1117-1123 (2009).
61. Miele, V., Penel, S. & Duret, L. Ultra-fast sequence clustering from similarity networks with SiLiX. BMC Bioinformatics 12, 116 (2011).
62. Krzywinski, M. et al. Circos: an information aesthetic for comparative genomics. Genome Res. 19, 1639-1645 (2009).
63. Dobin, A. et al. STAR: ultrafast universal RNA-seq aligner. Bioinformatics 29, 15-21 (2013).
64. Spivakov, M. et al. Genomic and phenotypic characterization of A wild medaka population: towards the establishment of an isogenic population genetic resource in fish. G3 (Bethesda) 4, 433-445 (2014).
65. Zhang, Z. et al. KaKs-Calculator: calculating Ka and Ks through model selection and model averaging. Genomics Proteomics Bioinformatics 4, 259-263 (2006).
66. Ostlund, G. et al. InParanoid 7: new algorithms and tools for eukaryotic orthology analysis. Nucleic Acids Res. 38, D196-D203 (2010).
67. Tamura, K. et al. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28, 2731-2739 (2011).
68. Grabherr, M. G. et al. Full-length transcriptome assembly from RNA-Seq data without A reference genome. Nat. Biotechnol. 29, 644-652 (2011).
69. Tang, R., Dodd, A., Lai, D., McNabb, W. C. & Love, D. R. Validation of zebrafish (Danio rerio) reference genes for quantitative real-time RT-PCR normalization. Acta Biochim. Biophys. Sinica 39, 384-390 (2007).