The amphioxus genome illuminates vertebrate origins and cephalochordate biology

  1. Linda Z. Holland1,40,
  2. Ricard Albalat2,
  3. Kaoru Azumi3,
  4. Èlia Benito-Gutiérrez2,
  5. Matthew J. Blow4,
  6. Marianne Bronner-Fraser5,
  7. Frederic Brunet6,
  8. Thomas Butts7,
  9. Simona Candiani8,
  10. Larry J. Dishaw9,10,
  11. David E.K. Ferrier7,11,
  12. Jordi Garcia-Fernàndez2,
  13. Jeremy J. Gibson-Brown12,36,
  14. Carmela Gissi13,
  15. Adam Godzik14,
  16. Finn Hallböök15,
  17. Dan Hirose16,
  18. Kazuyoshi Hosomichi17,
  19. Tetsuro Ikuta16,
  20. Hidetoshi Inoko17,
  21. Masanori Kasahara18,
  22. Jun Kasamatsu18,
  23. Takeshi Kawashima19,37,
  24. Ayuko Kimura20,
  25. Masaaki Kobayashi16,
  26. Zbynek Kozmik21,
  27. Kaoru Kubokawa22,
  28. Vincent Laudet6,
  29. Gary W. Litman9,10,23,
  30. Alice C. McHardy24,38,
  31. Daniel Meulemans5,
  32. Masaru Nonaka20,
  33. Robert P. Olinski15,
  34. Zeev Pancer25,
  35. Len A. Pennacchio4,
  36. Mario Pestarino8,
  37. Jonathan P. Rast26,
  38. Isidore Rigoutsos24,
  39. Marc Robinson-Rechavi27,
  40. Graeme Roch28,
  41. Hidetoshi Saiga16,
  42. Yasunori Sasakura29,
  43. Masanobu Satake30,
  44. Yutaka Satou31,
  45. Michael Schubert6,
  46. Nancy Sherwood28,
  47. Takashi Shiina17,
  48. Naohito Takatori16,39,
  49. Javier Tello28,
  50. Pavel Vopalensky21,
  51. Shuichi Wada32,
  52. Anlong Xu33,
  53. Yuzhen Ye14,
  54. Keita Yoshida16,
  55. Fumiko Yoshizaki34,
  56. Jr-Kai Yu5,
  57. Qing Zhang14,
  58. Christian M. Zmasek14,
  59. Pieter J. de Jong35,
  60. Kazutoyo Osoegawa35,
  61. Nicholas H. Putnam19,
  62. Daniel S. Rokhsar4,19,
  63. Noriyuki Satoh31,37,40, and
  64. Peter W.H. Holland7,40
  1. 1 Marine Biology Research Division, Scripps Institution of Oceanography, La Jolla, California 92093-0202, USA;
  2. 2 Departament of Genetics, Faculty of Biology, University of Barcelona, Barcelona E-08028, Spain;
  3. 3 Division of Innovative Research, Creative Research Initiative “Sousei”, Hokkaido University, Sapporo 001-0021, Japan;
  4. 4 U.S. Department of Energy Joint Genome Institute, Walnut Creek, California 94598, USA;
  5. 5 Division of Biology 139-74, California Institute of Technology, Pasadena, California 91125, USA;
  6. 6 Institut de Génomique Fonctionnelle de Lyon, CNRS UMR5242, UCBL, ENS, INRA 1288, IFR128 BioSciences Lyon-Gerland Ecole Normale Supérieure de Lyon, 69364 Lyon Cedex 07, France;
  7. 7 Department of Zoology, University of Oxford, South Parks Road, Oxford, OX1 3PS, UK;
  8. 8 Dipartimento di Biologia, Università di Genova, viale Benedetto XV 5, 16132 Genova, Italy;
  9. 9 H. Lee Moffitt Cancer Center and Research Institute, Tampa, Florida 33612 USA;
  10. 10 Department of Molecular Genetics, All Children’s Hospital, St. Petersburg, Florida 33701 USA;
  11. 11 The Gatty Marine Laboratory,University of St Andrews, St Andrews, Fife, KY16 8LB, Scotland;
  12. 12 Department of Biology, Washington University in St. Louis, St. Louis, Missouri 63130, USA;
  13. 13 Dipartimento di Scienze Biomolecolarie Biotecnologie, Università di Milano, Milano, Italy;
  14. 14 Burnham Institute for Medical Research, La Jolla, California 92037, USA;
  15. 15 Unit of Developmental Neuroscience, Department of Neuroscience, Uppsala University, Uppsala, Sweden;
  16. 16 Department of Biological Sciences, Graduate School of Science and Engineering, Tokyo Metropolitan University, Hachiohji, Tokyo 192-0397, Japan;
  17. 17 Department of Molecular Life Science, Tokai University School of Medicine, Bohseidai, Isehara, Kanagawa 259-1193, Japan;
  18. 18 Department of Pathology, Hokkaido University Graduate School of Medicine, Sapporo 060-8638, Japan;
  19. 19 Center for Integrative Genomics, Department of Cell and Molecular Biology, University of California at Berkeley, Berkeley, California 94720, USA;
  20. 20 Department of Biological Sciences, Graduate school of Science, The University of Tokyo, Tokyo 113-033, Japan;
  21. 21 Institute of Molecular Genetics, Academy of Sciences of the Czech Republic, Videnska 1083, 142 20 Prague 4, Czech Republic;
  22. 22 Center for Advanced Marine Research, Ocean Research Institute, University of Tokyo, Nakano, Tokyo 164-8639, Japan;
  23. 23 Department of Pediatrics, University of South Florida, St. Petersburg, Florida 33701 USA;
  24. 24 Bioinformatics and Pattern Discovery Group, IBM Thomas J. Watson Research Center, Yorktown Heights, New York 10598, USA;
  25. 25 Center of Marine Biotechnology, University of Maryland Biotechnology Institute, Baltimore, Maryland 21202 USA;
  26. 26 Sunnybrook Research Institute and Department of Medical Biophysics, University of Toronto, Toronto, Ontario M4N 3M5, Canada;
  27. 27 Department of Ecology and Evolution, Biophore, University of Lausanne, 1015 Lausanne, Switzerland;
  28. 28 Department of Biology, University of Victoria, Victoria, B.C., V8W 3N5, Canada;
  29. 29 Shimoda Marine Research Center, University of Tsukuba, 5-10-1, Shimoda, Shizuoka, 415-0025 Japan;
  30. 30 Department of Molecular Immunology, Institute of Development, Aging and Cancer, Tohoku University, Sendai 980-8575, Japan;
  31. 31 Department of Zoology, Graduate School of Science, Kyoto University, Kyoto 606-8502, Japan;
  32. 32 Department of Bioscience, Faculty of Bioscience, Nagahama Institute of Bio-Science and Technology, Nagahama, Shiga 526-0829, Japan;
  33. 33 State Key Laboratory of Biocontrol, Department of Biochemistry, College of Life Sciences, Sun Yat-Sen (Zhongshan) University, Guangzhou, People’s Republic of China;
  34. 34 Institute for Environmental and Gender-Specific Medicine, Juntendo University, Chiba 279-0021, Japan;
  35. 35 Children’s Hospital of Oakland Research Institute, Oakland, California 94609, USA

Abstract

Cephalochordates, urochordates, and vertebrates evolved from a common ancestor over 520 million years ago. To improve our understanding of chordate evolution and the origin of vertebrates, we intensively searched for particular genes, gene families, and conserved noncoding elements in the sequenced genome of the cephalochordate Branchiostoma floridae, commonly called amphioxus or lancelets. Special attention was given to homeobox genes, opsin genes, genes involved in neural crest development, nuclear receptor genes, genes encoding components of the endocrine and immune systems, and conserved cis-regulatory enhancers. The amphioxus genome contains a basic set of chordate genes involved in development and cell signaling, including a fifteenth Hox gene. This set includes many genes that were co-opted in vertebrates for new roles in neural crest development and adaptive immunity. However, where amphioxus has a single gene, vertebrates often have two, three, or four paralogs derived from two whole-genome duplication events. In addition, several transcriptional enhancers are conserved between amphioxus and vertebrates—a very wide phylogenetic distance. In contrast, urochordate genomes have lost many genes, including a diversity of homeobox families and genes involved in steroid hormone function. The amphioxus genome also exhibits derived features, including duplications of opsins and genes proposed to function in innate immunity and endocrine systems. Our results indicate that the amphioxus genome is elemental to an understanding of the biology and evolution of nonchordate deuterostomes, invertebrate chordates, and vertebrates.

Footnotes

  • ↵36 Present addresses: Institute for Evolutionary Discovery, 909 Hiawatha Drive, Mount Pleasant, MI 48858, USA;

  • ↵37 Okinawa Institute of Science and Technology (OIST), Uruma, Okinawa 904-2234, Japan;

  • ↵38 Computational Genomics and Epidemiology Group, Max-Planck Institute for Computer Science, Saarbruecken 66123, Germany;

  • ↵39 Department of Biological Sciences, Graduate School of Science, Osaka University, Toyonaka, Osaka 560-0042, Japan.

  • ↵40 Corresponding authors.

    ↵40 E-mail lzholland{at}ucsd.edu; fax (858) 534-7313.

    ↵40 E-mail satoh{at}ascidian.zool.kyoto-u.ac.jp; fax 81-75-705-1113.

    ↵40 E-mail peter.holland{at}zoo.ox.ac.uk; fax 44-1865-271184.

  • [Supplemental material is available online at www.genome.org.]

  • Article published online before print. Article and publication date are at http://www.genome.org/cgi/doi/10.1101/gr.073676.107.

    • Received October 26, 2007.
    • Accepted February 24, 2008.

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  1. Published in Advance June 18, 2008, doi: 10.1101/gr.073676.107 Genome Res. 18: 1100-1111 Copyright © 2008, Cold Spring Harbor Laboratory Press

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