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PMID: 24402279 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Elephant shark genome provides unique insights into gnathostome evolution.

Nature ·Vol. 505 ·No. 7482 ·2014-01-09 ·Pages 174-9

Venkatesh B, Lee AP, Ravi V, Maurya AK, Lian MM, Swann JB, Ohta Y, Flajnik MF, Sutoh Y, Kasahara M, Hoon S, Gangu V, Roy SW, Irimia M, Korzh V, Kondrychyn I, Lim ZW, Tay BH, Tohari S, Kong KW, Ho S, Lorente-Galdos B, Quilez J, Marques-Bonet T, Raney BJ, Ingham PW, Tay A, Hillier LW, Minx P, Boehm T, Wilson RK, Brenner S, Warren WC

Abstract

The emergence of jawed vertebrates (gnathostomes) from jawless vertebrates was accompanied by major morphological and physiological innovations, such as hinged jaws, paired fins and immunoglobulin-based adaptive immunity. Gnathostomes subsequently diverged into two groups, the cartilaginous fishes and the bony vertebrates. Here we report the whole-genome analysis of a cartilaginous fish, the elephant shark (Callorhinchus milii). We find that the C. milii genome is the slowest evolving of all known vertebrates, including the 'living fossil' coelacanth, and features extensive synteny conservation with tetrapod genomes, making it a good model for comparative analyses of gnathostome genomes. Our functional studies suggest that the lack of genes encoding secreted calcium-binding phosphoproteins in cartilaginous fishes explains the absence of bone in their endoskeleton. Furthermore, the adaptive immune system of cartilaginous fishes is unusual: it lacks the canonical CD4 co-receptor and most transcription factors, cytokines and cytokine receptors related to the CD4 lineage, despite the presence of polymorphic major histocompatibility complex class II molecules. It thus presents a new model for understanding the origin of adaptive immunity.

MeSH Terms
Animals Calcium/metabolism Cell Lineage/immunology Evolution, Molecular Fish Proteins/classification,genetics Gene Deletion Genome/genetics Genomics Immunity, Cellular/genetics Molecular Sequence Annotation Molecular Sequence Data Osteogenesis/genetics Phosphoproteins/genetics,metabolism Phylogeny Protein Structure, Tertiary/genetics Sharks/genetics,immunology T-Lymphocytes/cytology,immunology Time Factors Vertebrates/classification,genetics Zebrafish/genetics,growth & development
Chemicals
Fish Proteins Phosphoproteins Calcium
Authors & Affiliations
33 authors, click to expand affiliations / ORCID
Venkatesh Byrappa
1] Comparative Genomics Laboratory, Institute of Molecular and Cell Biology, A*STAR, Biopolis, Singapore 138673 [2] Department of Paediatrics, Yong Loo Lin School of Medicine, National University of Singapore, Singapore 119228.
Lee Alison P
Comparative Genomics Laboratory, Institute of Molecular and Cell Biology, A*STAR, Biopolis, Singapore 138673.
Ravi Vydianathan
Comparative Genomics Laboratory, Institute of Molecular and Cell Biology, A*STAR, Biopolis, Singapore 138673.
Maurya Ashish K
Developmental and Biomedical Genetics Laboratory, Institute of Molecular and Cell Biology, A*STAR, Biopolis, Singapore 138673.
Lian Michelle M
Comparative Genomics Laboratory, Institute of Molecular and Cell Biology, A*STAR, Biopolis, Singapore 138673.
Swann Jeremy B
Department of Developmental Immunology, Max-Planck-Institute of Immunobiology and Epigenetics, Stuebeweg 51, 79108 Freiburg, Germany.
Ohta Yuko
Department of Microbiology and Immunology, University of Maryland, Baltimore, Maryland 21201, USA.
Flajnik Martin F
Department of Microbiology and Immunology, University of Maryland, Baltimore, Maryland 21201, USA.
Sutoh Yoichi
Department of Pathology, Hokkaido University Graduate School of Medicine, Sapporo 060-8638, Japan.
Kasahara Masanori
Department of Pathology, Hokkaido University Graduate School of Medicine, Sapporo 060-8638, Japan.
Hoon Shawn
Molecular Engineering Laboratory, Biomedical Sciences Institutes, A*STAR, Biopolis, Singapore 138673.
Gangu Vamshidhar
Molecular Engineering Laboratory, Biomedical Sciences Institutes, A*STAR, Biopolis, Singapore 138673.
Roy Scott W
Department of Biology, San Francisco State University, San Francisco, California 94132, USA.
Irimia Manuel
Banting and Best Department of Medical Research and Donnelly Centre, University of Toronto, Toronto, Ontario M5S 3E1, Canada.
Korzh Vladimir
Fish Developmental Biology Laboratory, Institute of Molecular and Cell Biology, A*STAR, Biopolis, Singapore 138673.
Kondrychyn Igor
Fish Developmental Biology Laboratory, Institute of Molecular and Cell Biology, A*STAR, Biopolis, Singapore 138673.
Lim Zhi Wei
Comparative Genomics Laboratory, Institute of Molecular and Cell Biology, A*STAR, Biopolis, Singapore 138673.
Tay Boon-Hui
Comparative Genomics Laboratory, Institute of Molecular and Cell Biology, A*STAR, Biopolis, Singapore 138673.
Tohari Sumanty
Comparative Genomics Laboratory, Institute of Molecular and Cell Biology, A*STAR, Biopolis, Singapore 138673.
Kong Kiat Whye
Molecular Engineering Laboratory, Biomedical Sciences Institutes, A*STAR, Biopolis, Singapore 138673.
Ho Shufen
Molecular Engineering Laboratory, Biomedical Sciences Institutes, A*STAR, Biopolis, Singapore 138673.
Lorente-Galdos Belen
1] Institut de Biologia Evolutiva (UPF-CSIC), PRBB, 08003 Barcelona, Spain [2] Institució Catalana de Recerca i Estudis Avançats (ICREA), 08010 Barcelona, Catalonia, Spain.
Quilez Javier
1] Institut de Biologia Evolutiva (UPF-CSIC), PRBB, 08003 Barcelona, Spain [2] Institució Catalana de Recerca i Estudis Avançats (ICREA), 08010 Barcelona, Catalonia, Spain.
Marques-Bonet Tomas
1] Institut de Biologia Evolutiva (UPF-CSIC), PRBB, 08003 Barcelona, Spain [2] Institució Catalana de Recerca i Estudis Avançats (ICREA), 08010 Barcelona, Catalonia, Spain.
Raney Brian J
Center for Biomolecular Science and Engineering, School of Engineering, University of California Santa Cruz, Santa Cruz, California 95064, USA.
Ingham Philip W
Developmental and Biomedical Genetics Laboratory, Institute of Molecular and Cell Biology, A*STAR, Biopolis, Singapore 138673.
Tay Alice
Comparative Genomics Laboratory, Institute of Molecular and Cell Biology, A*STAR, Biopolis, Singapore 138673.
Hillier LaDeana W
The Genome Institute at Washington University, St Louis, Missouri 63108, USA.
Minx Patrick
The Genome Institute at Washington University, St Louis, Missouri 63108, USA.
Boehm Thomas
Department of Developmental Immunology, Max-Planck-Institute of Immunobiology and Epigenetics, Stuebeweg 51, 79108 Freiburg, Germany.
Wilson Richard K
The Genome Institute at Washington University, St Louis, Missouri 63108, USA.
Brenner Sydney
Comparative Genomics Laboratory, Institute of Molecular and Cell Biology, A*STAR, Biopolis, Singapore 138673.
Warren Wesley C
The Genome Institute at Washington University, St Louis, Missouri 63108, USA.
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Article Info
Journal
Nature
Abbr.
Nature
ISSN
1476-4687
Published
2014-01-09
Pages
174-9
Language
English
Region
England
NLM ID
0410462
PMCID
PMC3964593
Subset
IM
Grants
NIAID NIH HHS · R01 AI027877 · United States
NHGRI NIH HHS · U41 HG002371 · United States
NCRR NIH HHS · R01 RR006603 · United States
NIAID NIH HHS · AI27877 · United States
NHGRI NIH HHS · U54 HG003079 · United States
NCRR NIH HHS · RR006603 · United States
NIH HHS · R01 OD010549 · United States
Databases
GENBANK
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