The spotted gar genome illuminates vertebrate evolution and
facilitates human-to-teleost comparisons

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Abstract

To connect human biology to fish biomedical models, we sequenced the genome of spotted gar ( Lepisosteus oculatus), whose lineage diverged from teleosts before the teleost genome duplication (TGD). The slowly evolving gar genome conserved in content and size many entire chromosomes from bony vertebrate ancestors. Gar bridges teleosts to tetrapods by illuminating the evolution of immunity, mineralization, and development (e.g., Hox, ParaHox, and miRNA genes). Numerous conserved non-coding elements (CNEs, often cis-regulatory) undetectable in direct human-teleost comparisons become apparent using gar: functional studies uncovered conserved roles of such cryptic CNEs, facilitating annotation of sequences identified in human genome-wide association studies. Transcriptomic analyses revealed that the sum of expression domains and levels from duplicated teleost genes often approximate patterns and levels of gar genes, consistent with subfunctionalization. The gar genome provides a resource for understanding evolution after genome duplication, the origin of vertebrate genomes, and the function of human regulatory sequences.

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Efficient In Vivo Genome Editing Using RNA-Guided Nucleases

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Clustered regularly interspaced short palindromic repeats (CRISPR)/CRISPR-associated (Cas) systems have evolved in bacteria and archaea as a defense mechanism to silence foreign nucleic acids of viruses and plasmids. Recent work has shown that bacterial type II CRISPR systems can be adapted to create guide RNAs (gRNAs) capable of directing site-specific DNA cleavage by the Cas9 nuclease in vitro. Here we show that this system can function in vivo to induce targeted genetic modifications in zebrafish embryos with efficiencies comparable to those obtained using ZFNs and TALENs for the same genes. RNA-guided nucleases robustly enabled genome editing at 9 of 11 different sites tested, including two for which TALENs previously failed to induce alterations. These results demonstrate that programmable CRISPR/Cas systems provide a simple, rapid, and highly scalable method for altering genes in vivo, opening the door to using RNA-guided nucleases for genome editing in a wide range of organisms.

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Elephant shark genome provides unique insights into gnathostome evolution

Byrappa Venkatesh, Alison P Lee, Vydianathan Ravi … (2014)

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. Supplementary information The online version of this article (doi:10.1038/nature12826) contains supplementary material, which is available to authorized users.

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HOX genes specify cell fate in the anterior-posterior axis of animal embryos. Invertebrate chordates have one HOX cluster, but mammals have four, suggesting that cluster duplication facilitated the evolution of vertebrate body plans. This report shows that zebrafish have seven hox clusters. Phylogenetic analysis and genetic mapping suggest a chromosome doubling event, probably by whole genome duplication, after the divergence of ray-finned and lobe-finned fishes but before the teleost radiation. Thus, teleosts, the most species-rich group of vertebrates, appear to have more copies of these developmental regulatory genes than do mammals, despite less complexity in the anterior-posterior axis.

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Author and article information

Journal

Journal ID (nlm-journal-id): 9216904

Journal ID (pubmed-jr-id): 2419

Journal ID (nlm-ta): Nat Genet

Journal ID (iso-abbrev): Nat. Genet.

Title: Nature genetics

ISSN (Print): 1061-4036

ISSN (Electronic): 1546-1718

Publication date Nihms-submitted: 25 February 2016

Publication date (Electronic): 07 March 2016

Publication date (Print): April 2016

Publication date PMC-release: 01 October 2016

Volume: 48

Issue: 4

Pages: 427-437

Affiliations

[1 ]Institute of Neuroscience, University of Oregon, Eugene, Oregon, USA.

[2 ]Department of Organismal Biology and Anatomy, The University of Chicago, Chicago, Illinois, USA.

[3 ]Department of Biology, University of Kentucky, Lexington, Kentucky, USA.

[4 ]Department of Anthropology, Pennsylvania State University, University Park, Pennsylvania, USA.

[5 ]Institute of Marine Biology, Biotechnology and Aquaculture, Hellenic Centre for Marine Research, Heraklion, Greece.

[6 ]INRA, UR1037 LPGP Fish Physiology and Genomics, Campus de Beaulieu, Rennes, France.

[7 ]Department of Animal Biology, University of Illinois, Urbana-Champaign, Illinois, USA.

[8 ]Broad Institute of MIT and Harvard, Cambridge, Massachusetts, USA.

[9 ]Eccles Institute of Human Genetics, University of Utah, Salt Lake City, Utah, USA.

[10 ]Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton, Cambridge, United Kingdom.

[11 ]European Molecular Biology Laboratory, European Bioinformatics Institute, Wellcome Trust Genome Campus, Hinxton, Cambridge, United Kingdom.

[12 ]Department of Zoology, University of Oxford, Oxford, United Kingdom.

[13 ]School of Biological Sciences, Bangor University, Bangor, Gwynedd, United Kingdom.

[14 ]Comparative Genomics Laboratory, Institute of Molecular and Cell Biology, A*STAR, Biopolis, Singapore.

[15 ]Institut de Génomique Fonctionnelle de Lyon, Ecole Normale Supérieure de Lyon, Lyon, France.

[16 ]Department of Biology, University of Konstanz, Konstanz, Germany.

[17 ]Department of Molecular Biomedical Sciences, North Carolina State University, Raleigh, North Carolina, USA.

[18 ]Center for Comparative Medicine and Translational Research, North Carolina State University, Raleigh, North Carolina, USA.

[19 ]Departament de Genètica, Universitat de Barcelona, Barcelona, Spain.

[20 ]Institut de Recerca de la Biodiversitat, Universitat de Barcelona, Barcelona, Spain.

[21 ]University of Victoria, Department of Biology, Victoria, British Columbia, Canada.

[22 ]Center for Circadian Clocks, Soochow University, Suzhou, Jiangsu, China.

[23 ]School of Biology & Basic Medical Sciences, Medical College, Soochow University, Suzhou, Jiangsu, China.

[24 ]Bioinformatics Group, Department of Computer Science, Universität Leipzig, Leipzig, Germany.

[25 ]Department of Dental Hygiene, The Nippon Dental University College at Niigata, Niigata, Japan.

[26 ]Department of Pediatrics, University of South Florida Morsani College of Medicine, St. Petersburg, Florida, USA.

[27 ]Department of Microbiology, The Nippon Dental University School of Life Dentistry at Niigata, Niigata, Japan.

[28 ]Department of Evolutionary Studies of Biosystems, SOKENDAI (The Graduate University for Advanced Studies), Hayama, Japan.

[29 ]Molecular Genetics Program, Benaroya Research Institute, Seattle, Washington, USA.

[30 ]Department of Biological Sciences, Nicholls State University, Thibodaux, Louisiana, USA.

[31 ]Instituto de Ciencias Biologicas, Universidade Federal do Para, Belem, Brazil.

[32 ]International Max-Planck Research School for Organismal Biology, University of Konstanz, Konstanz, Germany.

[33 ]Science for Life Laboratory, Department of Medical Biochemistry and Microbiology, Uppsala University, Uppsala, Sweden.

Author notes

[34]

Present addresses: Department of Integrative Biology, Michigan State University, East Lansing, Michigan, USA (I.B.); Cold Spring Harbor Laboratory, Cold Spring Harbor, New York, USA (M.S.C.); Department of Animal and Plant Sciences, University of Sheffield, Sheffield, United Kingdom (K.J.M.); Department of Genetics, University of Georgia, Athens, Georgia, USA (D.C.); Department of Genetics, University of Pennsylvania, Philadelphia, Pennsylvania, USA (S.F.); Young Investigators Group Bioinformatics and Transcriptomics, Department of Proteomics, Helmholtz Centre for Environmental Research – UFZ, Leipzig, Germany (J.H.); ecSeq Bioinformatics, Leipzig, Germany (M.F.); Vertebrate and Health Genomics, The Genome Analysis Center, Norwich, United Kingdom (F.D.P.).

Correspondence should be addressed to I.B. ( braasch@ 123456msu.edu ) or J.H.P. ( jpostle@ 123456uoneuro.uoregon.edu )

Article

Manuscript ID: EMS67207

DOI: 10.1038/ng.3526

PMC ID: 4817229

PubMed ID: 26950095

SO-VID: 385d170e-a1a8-42ac-b0bf-3568ae7a6b0d

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