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Science 314 (5801): 941-952

Copyright © 2006 by the American Association for the Advancement of Science

The Genome of the Sea Urchin Strongylocentrotus purpuratus

Sea Urchin Genome Sequencing Consortium: Erica Sodergren,1,2 George M. Weinstock,1,2* Eric H Davidson,3 R. Andrew Cameron,3 Richard A. Gibbs,1,2 Robert C. Angerer,4 Lynne M. Angerer,4 Maria Ina Arnone,5 David R. Burgess,6 Robert D. Burke,7 James A. Coffman,8 Michael Dean,9 Maurice R. Elphick,10 Charles A. Ettensohn,11 Kathy R. Foltz,12 Amro Hamdoun,13 Richard O. Hynes,14 William H. Klein,15 William Marzluff,16 David R. McClay,17 Robert L. Morris,18 Arcady Mushegian,19,20 Jonathan P. Rast,21 L. Courtney Smith,22 Michael C. Thorndyke,23 Victor D. Vacquier,24 Gary M. Wessel,25 Greg Wray,26 Lan Zhang,1,2 Christine G. Elsik,27 Olga Ermolaeva,28 Wratko Hlavina,28 Gretchen Hofmann,29 Paul Kitts,28 Melissa J. Landrum,28 Aaron J. Mackey,30{dagger} Donna Maglott,28 Georgia Panopoulou,31 Albert J. Poustka,31 Kim Pruitt,28 Victor Sapojnikov,28 Xingzhi Song,1,2 Alexandre Souvorov,28 Victor Solovyev,32 Zheng Wei,4 Charles A. Whittaker,33 Kim Worley,1,2 K. James Durbin,1,2 Yufeng Shen,1,2 Olivier Fedrigo,26 David Garfield,26 Ralph Haygood,17 Alexander Primus,26 Rahul Satija,26 Tonya Severson,26 Manuel L. Gonzalez-Garay,1,2 Andrew R. Jackson,1,2 Aleksandar Milosavljevic,1,2 Mark Tong,1,2 Christopher E. Killian,34 Brian T. Livingston,35 Fred H. Wilt,34 Nikki Adams,35 Robert Bellé,36,37 Seth Carbonneau,8 Rocky Cheung,16 Patrick Cormier,36,37 Bertrand Cosson,36,37 Jenifer Croce,17 Antonio Fernandez-Guerra,38,39 Anne-Marie Genevière,38,39 Manisha Goel,19 Hemant Kelkar,40 Julia Morales,36,37 Odile Mulner-Lorillon,36,37 Anthony J. Robertson,8 Jared V. Goldstone,41 Bryan Cole,13 David Epel,13 Bert Gold,9 Mark E. Hahn,42 Meredith Howard-Ashby,3 Mark Scally,9 John J. Stegeman,41 Erin L. Allgood,18 Jonah Cool,18 Kyle M. Judkins,18 Shawn S. McCafferty,18 Ashlan M. Musante,18 Robert A. Obar,42{ddagger} Amanda P. Rawson,18 Blair J. Rossetti,18 Ian R. Gibbons,43 Matthew P. Hoffman,6 Andrew Leone,6 Sorin Istrail,44 Stefan C. Materna,3 Manoj P. Samanta,45,46 Viktor Stolc,45 Waraporn Tongprasit,45 Qiang Tu,3 Karl-Frederik Bergeron,47 Bruce P. Brandhorst,48 James Whittle,49 Kevin Berney,3 David J. Bottjer,50 Cristina Calestani,51 Kevin Peterson,52 Elly Chow,53 Qiu Autumn Yuan,53 Eran Elhaik,54 Dan Graur,54 Justin T. Reese,27 Ian Bosdet,55 Shin Heesun,55 Marco A. Marra,55 Jacqueline Schein,55 Michele K. Anderson,56 Virginia Brockton,22 Katherine M. Buckley,22 Avis H. Cohen,57 Sebastian D. Fugmann,58 Taku Hibino,21 Mariano Loza-Coll,21 Audrey J. Majeske,22 Cynthia Messier,21 Sham V. Nair,59 Zeev Pancer,60 David P. Terwilliger,22 Cavit Agca,61 Enrique Arboleda,5 Nansheng Chen,48 Allison M. Churcher,62 F. Hallböök,63 Glen W. Humphrey,64 Mohammed M. Idris,5 Takae Kiyama,15 Shuguang Liang,15 Dan Mellott,60 Xiuqian Mu,15 Greg Murray,46 Robert P. Olinski,63 Florian Raible,65,66 Matthew Rowe,10 John S. Taylor,62 Kristin Tessmar-Raible,65 D. Wang,62 Karen H. Wilson,23 Shunsuke Yaguchi,7 Terry Gaasterland,24 Blanca E. Galindo,67 Herath J. Gunaratne,24 Celina Juliano,25 Masashi Kinukawa,24 Gary W. Moy,24 Anna T. Neill,24 Mamoru Nomura,24 Michael Raisch,12 Anna Reade,12 Michelle M. Roux,12 Jia L. Song,25 Yi-Hsien Su,3 Ian K. Townley,12 Ekaterina Voronina,25 Julian L. Wong,25 Gabriele Amore,5 Margherita Branno,5 Euan R. Brown,5 Vincenzo Cavalieri,68 Véronique Duboc,69 Louise Duloquin,69 Constantin Flytzanis,70,71 Christian Gache,69 François Lapraz,69 Thierry Lepage,69 Annamaria Locascio,5 Pedro Martinez,72,73 Giorgio Matassi,74 Valeria Matranga,75 Ryan Range,69 Francesca Rizzo,5 Eric Röttinger,69 Wendy Beane,17 Cynthia Bradham,17 Christine Byrum,17,76 Tom Glenn,17 Sofia Hussain,77 Gerard Manning,78 Esther Miranda,17 Rebecca Thomason,17,76 Katherine Walton,17 Athula Wikramanayke,76 Shu-Yu Wu,17 Ronghui Xu,76 C. Titus Brown,3 Lili Chen,3 Rachel F. Gray,3 Pei Yun Lee,3 Jongmin Nam,3 Paola Oliveri,3 Joel Smith,3 Donna Muzny,1,2 Stephanie Bell,1,2 Joseph Chacko,1,2 Andrew Cree,1,2 Stacey Curry,1,2 Clay Davis,1,2 Huyen Dinh,1,2 Shannon Dugan-Rocha,1,2 Jerry Fowler,1,2 Rachel Gill,1,2 Cerrissa Hamilton,1,2 Judith Hernandez,1,2 Sandra Hines,1,2 Jennifer Hume,1,2 LaRonda Jackson,1,2 Angela Jolivet,1,2 Christie Kovar,1,2 Sandra Lee,1,2 Lora Lewis,1,2 George Miner,1,2 Margaret Morgan,1,2 Lynne V. Nazareth,1,2 Geoffrey Okwuonu,1,2 David Parker,1,2 Ling-Ling Pu,1,2 Rachel Thorn,1,2 Rita Wright1,2

Abstract: We report the sequence and analysis of the 814-megabase genome of the sea urchin Strongylocentrotus purpuratus, a model for developmental and systems biology. The sequencing strategy combined whole-genome shotgun and bacterial artificial chromosome (BAC) sequences. This use of BAC clones, aided by a pooling strategy, overcame difficulties associated with high heterozygosity of the genome. The genome encodes about 23,300 genes, including many previously thought to be vertebrate innovations or known only outside the deuterostomes. This echinoderm genome provides an evolutionary outgroup for the chordates and yields insights into the evolution of deuterostomes.

1 Human Genome Sequencing Center, Baylor College of Medicine, One Baylor Plaza, Houston, TX 77030, USA.
2 Department of Molecular and Human Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX 77030, USA.
3 Division of Biology, California Institute of Technology, Pasadena, CA 91125, USA.
4 National Institute of Dental and Craniofacial Research, National Institutes of Health (NIH), Bethesda, MD 20892, USA.
5 Stazione Zoologica Anton Dohrn, Villa Comunale, 80121 Napoli, Italy.
6 Department of Biology, Boston College, Chestnut Hill, MA 02467, USA.
7 Department of Biology, Department of Biochemistry and Microbiology, University of Victoria, Victoria, BC, Canada, V8W 3N5.
8 Mount Desert Island Biological Laboratory, Salisbury Cove, ME 04672, USA.
9 Human Genetics Section, Laboratory of Genomic Diversity, National Cancer Institute–Frederick, Frederick, MD 21702, USA.
10 School of Biological and Chemical Sciences, Queen Mary, University of London, London E1 4NS, UK.
11 Department of Biological Sciences, Carnegie Mellon University, Pittsburgh, PA, 15213, USA.
12 Department Molecular, Cellular and Developmental Biology and the Marine Science Institute, University of California, Santa Barbara, Santa Barbara, CA 93106–9610, USA.
13 Hopkins Marine Station, Stanford University, Pacific Grove, CA 93950, USA.
14 Howard Hughes Medical Institute, Center for Cancer Research, Massachusetts Institute of Technology (MIT), Cambridge, MA 02139, USA.
15 Departments of Biochemistry and Molecular Biology, University of Texas, M.D.Anderson Cancer Center, Houston, TX, 77030, USA.
16 Molecular Biology and Biotechnology, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599, USA.
17 Department of Biology, Duke University, Durham, NC 27708, USA.
18 Department of Biology, Wheaton College, Norton, MA 02766, USA.
19 Stowers Institute for Medical Research, Kansas City, MO 64110, USA.
20 Department of Microbiology, Kansas University Medical Center, Kansas City, KS 66160, USA.
21 Sunnybrook Research Institute and Department of Medical Biophysics, University of Toronto, Toronto, Ontario, Canada, M4N 3M5.
22 Department of Biological Sciences, George Washington University, Washington, DC 20052, USA.
23 Royal Swedish Academy of Sciences, Kristineberg Marine Research Station, Fiskebackskil, 450 34, Sweden.
24 Marine Biology, Scripps Institution of Oceanography, University of California San Diego, La Jolla, CA 92093–0202, USA.
25 Department of Molecular and Cellular Biology and Biochemistry, Brown University Providence, RI 02912, USA.
26 Department of Biology and Institute for Genome Sciences and Policy, Duke University, Durham, NC 27708, USA.
27 Department of Animal Science, Texas A&M University, College Station, TX 77843, USA.
28 National Center for Biotechnology Information, National Library of Medicine, NIH, Bethesda, MD 20894, USA.
29 Department of Ecology, Evolution, and Marine Biology, University of California Santa Barbara, Santa Barbara, CA 93106, USA.
30 Penn Genomics Institute, University of Pennsylvania, Philadelphia, PA 19104, USA.
31 Evolution and Development Group, Max-Planck Institut fuer Molekulare Genetik, 14195 Berlin, Germany.
32 Royal Holloway, University of London, Egham, Surrey TW20 0EX, UK.
33 Center for Cancer Research, MIT, Cambridge, MA 02139, USA.
34 Department of Molecular and Cell Biology, University of California, Berkeley, Berkeley, CA 94720–3200, USA.
35 Biology Department, California Polytechnic State University, San Luis Obispo, CA 93407, USA.
36 Université Pierre et Marie Curie-Paris6, UMR 7150, Equipe Cycle Cellulaire et Développement, Station Biologique de Roscoff, 29682 Roscoff Cedex, France.
37 CNRS, UMR 7150, Station Biologique de Roscoff, 29682 Roscoff Cedex, France.
38 CNRS, UMR7628, Banyuls-sur-Mer, F-66650, France.
39 Université Pierre et Marie Curie-Paris 6, UMR7628, Banyuls-sur-Mer, F-66650, France.
40 Center for Bioinformatics, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599, USA.
41 Biology Department, Woods Hole Oceanographic Institution, Woods Hole, MA 02543, USA.
42 Tethys Research, LLC, 2115 Union Street, Bangor, Maine 04401, USA.
43 Department of Molecular, Cellular, and Developmental Biology, University of California, Berkeley, Berkeley, CA 94720, USA.
44 Center for Computational Molecular Biology, and Computer Science Department, Brown University, Providence, RI 02912, USA.
45 Genome Research Facility, National Aeronautics and Space Administration, Ames Research Center, Moffet Field, CA 94035, USA.
46 Systemix Institute, Cupertino, CA 95014, USA.
47 Department of Molecular Biology and Biochemistry, Simon Fraser University, Burnaby, British Columbia, Canada, V5A 1S6.
48 Department of Molecular Biology and Biochemistry, Simon Fraser University, Burnaby, BC, Canada, V5A 1S6.
49 Department of Biology, Center for Cancer Research, MIT, Cambridge, MA 02139, USA.
50 Department of Earth Sciences, University of Southern California, Los Angeles, CA 90089–0740, USA.
51 Department of Biology, University of Central Florida, Orlando, FL 32816–2368, USA.
52 Department of Biological Sciences, Dartmouth College, Hanover, NH 03755, USA.
53 Center for Computational Regulatory Genomics, Beckman Institute, California Institute of Technology, Pasadena, CA 91125, USA.
54 Department of Biology and Biochemistry, University of Houston, Houston, TX 77204, USA.
55 Genome Sciences Centre, British Columbia Cancer Agency, Vancouver, BC, Canada, V5Z 4E6.
56 Department of Immunology, University of Toronto, Toronto, Ontario, Canada, M4N 3M5.
57 Department of Biology and the Institute of Systems Research, University of Maryland, College Park, MD 20742, USA.
58 Laboratory of Cellular and Molecular Biology, National Institute on Aging, NIH, Baltimore, MD 21224, USA.
59 Department of Biological Sciences, Macquarie University, Sydney NSW 2109, Australia.
60 Center of Marine Biotechnology, UMBI, Columbus Center, Baltimore, MD 21202, USA.
61 Department of Cell Biology and Anatomy, Louisiana State University Health Sciences Center, New Orleans, LA 70112, USA.
62 Department of Biology, University of Victoria, Victoria, BC, Canada, V8W 2Y2.
63 Department of Neuroscience, Uppsala University, Uppsala, Sweden.
64 Laboratory of Cellular and Molecular Biophysics, National Institute of Child Health and Development, NIH, Bethesda, MD 20895, USA.
65 Developmental Unit, EMBL, 69117 Heidelberg, Germany.
66 Computational Unit, EMBL, 69117 Heidelberg, Germany.
67 Biotechnology Institute, Universidad Nacional Autónoma de Mexico (UNAM), Cuernavaca, Morelos, Mexico 62250.
68 Department of Cellular and Developmental Biology "Alberto Monroy," University of Palermo, 90146 Palermo, Italy.
69 Laboratoire de Biologie du Développement (UMR 7009), CNRS and Université Pierre et Marie Curie (Paris 6), Observatoire Océanologique, 06230 Villefranche-sur-Mer, France.
70 Department of Biology, University of Patras, Patras, Greece.
71 Department of Molecular and Cellular Biology, Baylor College of Medicine, One Baylor Plaza, Houston, TX 77030, USA.
72 Departament de Genetica, Universitat de Barcelona, 08028–Barcelona, Spain.
73 Institució Catalana de Recerca i Estudis Avancats (ICREA), Barcelona, Spain.
74 Institut Jacques Monod, CNR-UMR 7592, 75005 Paris, France.
75 Consiglio Nazionale delle Ricerche, Istituto di Biomedicina e Immunologia Molecolare "Alberto Monroy," 90146 Palermo, Italy.
76 Department of Zoology, University of Hawaii at Manoa, Honolulu, HI 96822, USA.
77 Department of Biology, University of South Florida, Tampa, FL 33618, USA.
78 Razavi-Newman Center for Bioinformatics, Salk Institute for Biological Studies, La Jolla, CA 92186, USA.

{dagger} Present address: GlaxoSmithKline, 1250 South Collegeville Road, Collegeville, PA 19426, USA.

{ddagger} Present address: Massachusetts General Hospital Cancer Center, Charlestown, MA 02129, USA.

* To whom correspondence should be addressed. E-mail: gwstock{at}bcm.tmc.edu

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   Abstract »    Full Text »    PDF »
Whole-Genome Positive Selection and Habitat-Driven Evolution in a Shallow and a Deep-Sea Urchin.
T. A. Oliver, D. A. Garfield, M. K. Manier, R. Haygood, G. A. Wray, and S. R. Palumbi (2010)
Genome Biol Evol 2, 800-814
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Characterizing the Embryonic Transcriptome of the Snail Ilyanassa.
J. D. Lambert, X. Y. Chan, B. Spiecker, and H. C. Sweet (2010)
Integr. Comp. Biol. 50, 768-777
   Abstract »    Full Text »    PDF »
High Level of Structural Polymorphism Driven by Mobile Elements in the Hox Genomic Region of the Chaetognath Spadella cephaloptera.
F. Marletaz, G. Gyapay, and Y. Le Parco (2010)
Genome Biol Evol 2, 665-667
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The Evolution of Thrombospondins and Their Ligand-Binding Activities.
A. A. Bentley and J. C. Adams (2010)
Mol. Biol. Evol. 27, 2187-2197
   Abstract »    Full Text »    PDF »
Membrane wounding triggers ATP release and dysferlin-mediated intercellular calcium signaling.
J. F. Covian-Nares, S. V. Koushik, H. L. Puhl III, and S. S. Vogel (2010)
J. Cell Sci. 123, 1884-1893
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Diversification of innate immune genes: lessons from the purple sea urchin.
L. C. Smith (2010)
Dis. Model. Mech. 3, 274-279
   Abstract »    Full Text »    PDF »
Functional cis-regulatory genomics for systems biology.
J. Nam, P. Dong, R. Tarpine, S. Istrail, and E. H. Davidson (2010)
PNAS 107, 3930-3935
   Abstract »    Full Text »    PDF »
Genome 10K: A Proposal to Obtain Whole-Genome Sequence for 10 000 Vertebrate Species.
Genome 10K Community of Scientists (2009)
J. Hered.
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MGEScan-non-LTR: computational identification and classification of autonomous non-LTR retrotransposons in eukaryotic genomes.
M. Rho and H. Tang (2009)
Nucleic Acids Res. 37, e143
   Abstract »    Full Text »    PDF »
Dynamic Evolution of Immune System Regulators: The History of the Interferon Regulatory Factor Family.
J. Nehyba, R. Hrdlickova, and H. R. Bose (2009)
Mol. Biol. Evol. 26, 2539-2550
   Abstract »    Full Text »    PDF »
Regulative recovery in the sea urchin embryo and the stabilizing role of fail-safe gene network wiring.
J. Smith and E. H. Davidson (2009)
PNAS 106, 18291-18296
   Abstract »    Full Text »    PDF »
The emerging role of pharmacology in understanding consumer-prey interactions in marine and freshwater systems.
E. E. Sotka, J. Forbey, M. Horn, A. G. B. Poore, D. Raubenheimer, and K. E. Whalen (2009)
Integr. Comp. Biol. 49, 291-313
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Evolution of Vault RNAs.
P. F. Stadler, J. J.-L. Chen, J. Hackermuller, S. Hoffmann, F. Horn, P. Khaitovich, A. K. Kretzschmar, A. Mosig, S. J. Prohaska, X. Qi, et al. (2009)
Mol. Biol. Evol. 26, 1975-1991
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Transcriptomic response of sea urchin larvae Strongylocentrotus purpuratus to CO2-driven seawater acidification.
A. E. Todgham and G. E. Hofmann (2009)
J. Exp. Biol. 212, 2579-2594
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Alternative oxidase in animals: unique characteristics and taxonomic distribution.
A. E. McDonald, G. C. Vanlerberghe, and J. F. Staples (2009)
J. Exp. Biol. 212, 2627-2634
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Nutrient Uptake by Marine Invertebrates: Cloning and Functional Analysis of Amino Acid Transporter Genes in Developing Sea Urchins (Strongylocentrotus purpuratus).
E. Meyer and D. T. Manahan (2009)
Biol. Bull. 217, 6-24
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Domain shuffling and the evolution of vertebrates.
T. Kawashima, S. Kawashima, C. Tanaka, M. Murai, M. Yoneda, N. H. Putnam, D. S. Rokhsar, M. Kanehisa, N. Satoh, and H. Wada (2009)
Genome Res. 19, 1393-1403
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Extracellular matrix modifications at fertilization: regulation of dityrosine crosslinking by transamidation.
J. L. Wong and G. M. Wessel (2009)
Development 136, 1835-1847
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Blood Brothers or Just Neighbours: Modelling the Functional Psychoses.
G. Parker (2009)
Australian and New Zealand Journal of Psychiatry 43, 486-489
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NGFFFamide and echinotocin: structurally unrelated myoactive neuropeptides derived from neurophysin-containing precursors in sea urchins.
M. R. Elphick and M. L. Rowe (2009)
J. Exp. Biol. 212, 1067-1077
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Detecting heterozygosity in shotgun genome assemblies: Lessons from obligately outcrossing nematodes.
A. Barriere, S.-P. Yang, E. Pekarek, C. G. Thomas, E. S. Haag, and I. Ruvinsky (2009)
Genome Res. 19, 470-480
   Abstract »    Full Text »    PDF »
Highly Variable Immune-Response Proteins (185/333) from the Sea Urchin, Strongylocentrotus purpuratus: Proteomic Analysis Identifies Diversity within and between Individuals.
N. M. Dheilly, S. V. Nair, L. C. Smith, and D. A. Raftos (2009)
J. Immunol. 182, 2203-2212
   Abstract »    Full Text »    PDF »
The Talpid3 gene (KIAA0586) encodes a centrosomal protein that is essential for primary cilia formation.
Y. Yin, F. Bangs, I. R. Paton, A. Prescott, J. James, M. G. Davey, P. Whitley, G. Genikhovich, U. Technau, D. W. Burt, et al. (2009)
Development 136, 655-664
   Abstract »    Full Text »    PDF »
Two ParaHox genes, SpLox and SpCdx, interact to partition the posterior endoderm in the formation of a functional gut.
A. G. Cole, F. Rizzo, P. Martinez, M. Fernandez-Serra, and M. I. Arnone (2009)
Development 136, 541-549
   Abstract »    Full Text »    PDF »
On the Origin and Evolution of Vertebrate Olfactory Receptor Genes: Comparative Genome Analysis Among 23 Chordate Species.
Y. Niimura (2009)
Genome Biol Evol 1, 34-44
   Abstract »    Full Text »    PDF »
Lessons from a gene regulatory network: echinoderm skeletogenesis provides insights into evolution, plasticity and morphogenesis.
C. A. Ettensohn (2009)
Development 136, 11-21
   Abstract »    Full Text »    PDF »
SpBase: the sea urchin genome database and web site.
R. A. Cameron, M. Samanta, A. Yuan, D. He, and E. Davidson (2009)
Nucleic Acids Res. 37, D750-D754
   Abstract »    Full Text »    PDF »
Gene regulatory network subcircuit controlling a dynamic spatial pattern of signaling in the sea urchin embryo.
J. Smith and E. H. Davidson (2008)
PNAS 105, 20089-20094
   Abstract »    Full Text »    PDF »
Sequence Variations in 185/333 Messages from the Purple Sea Urchin Suggest Posttranscriptional Modifications to Increase Immune Diversity.
K. M. Buckley, D. P. Terwilliger, and L. C. Smith (2008)
J. Immunol. 181, 8585-8594
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