Survey Sequencing and Comparative Analysis of the Elephant Shark (Callorhinchus milii) Genome

Owing to their phylogenetic position, cartilaginous fishes (sharks, rays, skates, and chimaeras) provide a critical reference for our understanding of vertebrate genome evolution. The relatively small genome of the elephant shark, Callorhinchus milii, a chimaera, makes it an attractive model cartilaginous fish genome for whole-genome sequencing and comparative analysis. Here, the authors describe survey sequencing (1.4× coverage) and comparative analysis of the elephant shark genome, one of the first cartilaginous fish genomes to be sequenced to this depth. Repetitive sequences, represented mainly by a novel family of short interspersed element–like and long interspersed element–like sequences, account for about 28% of the elephant shark genome. Fragments of approximately 15,000 elephant shark genes reveal specific examples of genes that have been lost differentially during the evolution of tetrapod and teleost fish lineages. Interestingly, the degree of conserved synteny and conserved sequences between the human and elephant shark genomes are higher than that between human and teleost fish genomes. Elephant shark contains putative four Hox clusters indicating that, unlike teleost fish genomes, the elephant shark genome has not experienced an additional whole-genome duplication. These findings underscore the importance of the elephant shark as a critical reference vertebrate genome for comparative analysis of the human and other vertebrate genomes. This study also demonstrates that a survey-sequencing approach can be applied productively for comparative analysis of distantly related vertebrate genomes.

[1]  E. Lander,et al.  Genomic mapping by fingerprinting random clones: a mathematical analysis. , 1988, Genomics.

[2]  P. Chambon,et al.  Characterization of a premeiotic germ cell-specific cytoplasmic protein encoded by Stra8, a novel retinoic acid-responsive gene , 1996, The Journal of cell biology.

[3]  Sonja J. Prohaska,et al.  Bichir HoxA cluster sequence reveals surprising trends in ray-finned fish genomic evolution. , 2003, Genome research.

[4]  John Postlethwait,et al.  Subfunction partitioning, the teleost radiation and the annotation of the human genome. , 2004, Trends in genetics : TIG.

[5]  F. Schwartz,et al.  Cytogenetics of the elasmobranchs: Genome evolution and phylogenetic implications , 2002 .

[6]  K. Baek,et al.  Murine Asb-17 expression during mouse testis development and spermatogenesis , 2004, Zygote (Cambridge. Print).

[7]  C. Amemiya,et al.  Evidence for a Hox14 paralog group in vertebrates , 2004, Current Biology.

[8]  D. C. Hughes,et al.  Identification of the true human orthologue of the mouse Zp1 gene: evidence for greater complexity in the mammalian zona pellucida? , 1999, Biochimica et biophysica acta.

[9]  Angel Amores,et al.  Developmental roles of pufferfish Hox clusters and genome evolution in ray-fin fish. , 2003, Genome research.

[10]  Alan Christoffels,et al.  Fugu genome analysis provides evidence for a whole-genome duplication early during the evolution of ray-finned fishes. , 2004, Molecular biology and evolution.

[11]  E. Xu,et al.  A gene family required for human germ cell development evolved from an ancient meiotic gene conserved in metazoans , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[12]  International Human Genome Sequencing Consortium Sequence and comparative analysis of the chicken genome provide unique perspectives on vertebrate evolution , 2004 .

[13]  Alan Christoffels,et al.  Hox gene clusters in the Indonesian coelacanth, Latimeria menadoensis , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[14]  V. Prince,et al.  Consequences of Hox gene duplication in the vertebrates: an investigation of the zebrafish Hox paralogue group 1 genes. , 2001, Development.

[15]  Nobuyoshi Shimizu,et al.  Genomic analysis of Hox clusters in the sea lamprey Petromyzon marinus. , 2002, The Journal of experimental zoology.

[16]  O. Jaillon,et al.  Gene loss and evolutionary rates following whole-genome duplication in teleost fishes. , 2006, Molecular biology and evolution.

[17]  Klaudia Walter,et al.  Open access, freely available online PLoS BIOLOGY Highly Conserved Non-Coding Sequences Are Associated with Vertebrate Development , 2022 .

[18]  Colin N. Dewey,et al.  Sequence and comparative analysis of the chicken genome provide unique perspectives on vertebrate evolution , 2004, Nature.

[19]  L. Du Pasquier Origin and evolution of the vertebrate immune system. , 1992, APMIS : acta pathologica, microbiologica, et immunologica Scandinavica.

[20]  J. Maetz Fish gills: mechanisms of salt transfer in fresh water and sea water , 1971 .

[21]  J. Inazawa,et al.  Identification of a novel Sry-related gene and its germ cell-specific expression. , 1999, Nucleic acids research.

[22]  M. Low,et al.  Subfunctionalization of expression and peptide domains following the ancient duplication of the proopiomelanocortin gene in teleost fishes. , 2005, Molecular biology and evolution.

[23]  A. Meyer,et al.  Asymmetric evolution in two fish-specifically duplicated receptor tyrosine kinase paralogons involved in teleost coloration. , 2006, Molecular biology and evolution.

[24]  Eugene W. Myers,et al.  A whole-genome assembly of Drosophila. , 2000, Science.

[25]  R. Poulter,et al.  A LINE element from the pufferfish (fugu) Fugu rubripes which shows similarity to the CR1 family of non-LTR retrotransposons. , 1999, Gene.

[26]  I. Wilson,et al.  Crystal Structure of a Shark Single-Domain Antibody V Region in Complex with Lysozyme , 2004, Science.

[27]  S. Brenner,et al.  Duplication, degeneration and subfunctionalization of the nested synapsin-Timp genes in Fugu. , 2003, Trends in genetics : TIG.

[28]  Wei Yan,et al.  Sequence and expression of testis-expressed gene 14 (Tex14): a gene encoding a protein kinase preferentially expressed during spermatogenesis. , 2003, Gene expression patterns : GEP.

[29]  M. Flajnik,et al.  Molecular Cloning of C4 Gene and Identification of the Class III Complement Region in the Shark MHC 1 , 2003, The Journal of Immunology.

[30]  M. Flajnik,et al.  The immune system of cartilaginous fish. , 2000, Current topics in microbiology and immunology.

[31]  M. Romero,et al.  Mechanism of acid adaptation of a fish living in a pH 3.5 lake. , 2003, American journal of physiology. Regulatory, integrative and comparative physiology.

[32]  Charles E. Chapple,et al.  Genome duplication in the teleost fish Tetraodon nigroviridis reveals the early vertebrate proto-karyotype , 2004, Nature.

[33]  N. M. Brooke,et al.  A molecular timescale for vertebrate evolution , 1998, Nature.

[34]  Christine M. Malcom,et al.  Accelerated Evolution of Nervous System Genes in the Origin of Homo sapiens , 2004, Cell.

[35]  M. Benton,et al.  Paleontological evidence to date the tree of life. , 2006, Molecular biology and evolution.

[36]  N. Nomura,et al.  Complete sequencing and characterization of 21,243 full-length human cDNAs , 2004, Nature Genetics.

[37]  D. Haussler,et al.  Ultraconserved Elements in the Human Genome , 2004, Science.

[38]  A. Sidow Gen(om)e duplications in the evolution of early vertebrates. , 1996, Current opinion in genetics & development.

[39]  Andrew P. Martin,et al.  Rates of mitochondrial DNA evolution in sharks are slow compared with mammals , 1992, Nature.

[40]  L. Schild,et al.  Epithelial sodium channel/degenerin family of ion channels: a variety of functions for a shared structure. , 2002, Physiological reviews.

[41]  Klaas Vandepoele,et al.  Major events in the genome evolution of vertebrates: paranome age and size differ considerably between ray-finned fishes and land vertebrates. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[42]  G. Barlow,et al.  Fishes of the world , 2004, Environmental Biology of Fishes.

[43]  D.Sc. Yvette W. Kunz Ph.D. Developmental Biology of Teleost Fishes , 2004, Fish & Fisheries Series.

[44]  N. Oshiro,et al.  Molecular Identification and Characterization of Xenopus Egg Uroplakin III, an Egg Raft-associated Transmembrane Protein That Is Tyrosine-phosphorylated upon Fertilization* , 2005, Journal of Biological Chemistry.

[45]  R. Krumlauf Hox genes in vertebrate development , 1994, Cell.

[46]  V. Laudet,et al.  Evolutionary rates of duplicate genes in fish and mammals. , 2001, Molecular biology and evolution.

[47]  Y L Wang,et al.  Zebrafish hox clusters and vertebrate genome evolution. , 1998, Science.

[48]  M. Nishida,et al.  Mitochondrial Molecular Clocks and the Origin of Euteleostean Biodiversity: Familial Radiation of Perciforms May Have Predated the Cretaceous/Tertiary Boundary , 2000 .

[49]  P. Holland,et al.  The amphioxus Hox cluster: deuterostome posterior flexibility and Hox14 , 2000, Evolution & development.

[50]  N. Okada,et al.  SINEs and LINEs: symbionts of eukaryotic genomes with a common tail , 2005, Cytogenetic and Genome Research.

[51]  Paramvir S. Dehal,et al.  Whole-Genome Shotgun Assembly and Analysis of the Genome of Fugu rubripes , 2002, Science.

[52]  A. Meyer,et al.  Many genes in fish have species-specific asymmetric rates of molecular evolution , 2006, BMC Genomics.

[53]  Byrappa Venkatesh,et al.  A compact cartilaginous fish model genome , 2005, Current Biology.

[54]  J. Shrager,et al.  Myosin gene mutation correlates with anatomical changes in the human lineage , 2004, Nature.

[55]  Moya M. Smith,et al.  Scales of thelodont and shark-like fishes from the Ordovician of Colorado , 1996, Nature.

[56]  D. Larhammar,et al.  Numerous groups of chromosomal regional paralogies strongly indicate two genome doublings at the root of the vertebrates , 2004, Journal of Structural and Functional Genomics.

[57]  J. Volff,et al.  Subfunctionalization of duplicate mitf genes associated with differential degeneration of alternative exons in fish. , 2002, Genetics.

[58]  Sonja J. Prohaska,et al.  Independent Hox-cluster duplications in lampreys. , 2003, Journal of experimental zoology. Part B, Molecular and developmental evolution.

[59]  I. Ovcharenko,et al.  Human-zebrafish non-coding conserved elements act in vivo to regulate transcription , 2005, Nucleic acids research.

[60]  P. Janvier Palaeontology: Modern look for ancient lamprey , 2006, Nature.

[61]  J. Stevens,et al.  Sharks and Rays of Australia , 1991 .

[62]  D. Mccormick Sequence the Human Genome , 1986, Bio/Technology.

[63]  James A. Cuff,et al.  Genome sequence, comparative analysis and haplotype structure of the domestic dog , 2005, Nature.

[64]  John H Postlethwait,et al.  The zebrafish gene map defines ancestral vertebrate chromosomes. , 2005, Genome research.

[65]  M. Flajnik,et al.  Primitive synteny of vertebrate major histocompatibility complex class I and class II genes. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[66]  Esther G. L. Koh,et al.  Highly conserved syntenic blocks at the vertebrate Hox loci and conserved regulatory elements within and outside Hox gene clusters. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[67]  Justin Johnson,et al.  Ancient Noncoding Elements Conserved in the Human Genome , 2006, Science.

[68]  M. Avella,et al.  A new analysis of ammonia and sodium transport through the gills of the freshwater rainbow trout (Salmo gairdneri) , 1989 .

[69]  F. Verbeek,et al.  Genomic annotation and transcriptome analysis of the zebrafish (Danio rerio) hox complex with description of a novel member, hoxb13a , 2005, Evolution & development.

[70]  W. Xu,et al.  The extracellular protein coat of the inner acrosomal membrane is involved in zona pellucida binding and penetration during fertilization: characterization of its most prominent polypeptide (IAM38). , 2006, Developmental biology.

[71]  J. Hughes,et al.  Identification of a human homologue of the sea urchin receptor for egg jelly: a polycystic kidney disease-like protein. , 1999, Human molecular genetics.

[72]  D. Rebouillat,et al.  The human 2',5'-oligoadenylate synthetase family: interferon-induced proteins with unique enzymatic properties. , 1999, Journal of interferon & cytokine research : the official journal of the International Society for Interferon and Cytokine Research.

[73]  Angel Amores,et al.  Hox cluster organization in the jawless vertebrate Petromyzon marinus. , 2002, The Journal of experimental zoology.

[74]  M. Flajnik,et al.  An evolutionarily mobile antigen receptor variable region gene: doubly rearranging NAR-TcR genes in sharks. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[75]  E. Kirkness,et al.  The Dog Genome: Survey Sequencing and Comparative Analysis , 2003, Science.

[76]  W Miller,et al.  Hox cluster genomics in the horn shark, Heterodontus francisci. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[77]  Thomas Hankeln,et al.  A globin gene of ancient evolutionary origin in lower vertebrates: evidence for two distinct globin families in animals. , 2005, Molecular biology and evolution.