The Genome of the Sea Urchin Strongylocentrotus purpuratus

Sea Urchin Genome Sequencing Consortium Overall project leadership: Erica Sodergren,¹,² George M. Weinstock,^1,2 Eric H. Davidson,³ R. Andrew Cameron³Principal investigators: Richard A. Gibbs,^1,2 George M. Weinstock^1,2

Annotation section leaders: Robert C. Angerer,⁴ Lynne M. Angerer,⁴ Maria Ina Arnone,⁵ David R. Burgess,⁶ Robert D. Burke,⁷ R. Andrew Cameron,³ James A. Coffman,⁸ Eric H. Davidson,³ 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 Erica Sodergren,^1,2 L. Courtney Smith,²³ Michael C. Thorndyke,²⁴ Victor D. Vacquier,²⁴ George M. Weinstock,^1,2 Gary M. Wessel,²⁶ Greg Wray,²⁷ Lan Zhang^1,2

Annotation: Gene list: Erica Sodergren^1,2 (leader), George M. Weinstock^1,2 (leader), Robert C. Angerer,⁴ Lynne M. Angerer,⁴ R. Andrew Cameron,³ Eric H. Davidson,³ Christine G. Elsik,²⁷ Olga Ermolaeva,²⁹ Wratko Hlavina,²⁹ Gretchen Hofmann,³⁰ Paul Kitts,²⁸ Melissa J. Landrum,²⁸ Aaron J. Mackey,³² Donna Maglott,²⁸ Georgia Panopoulou,³³ Albert J. Poustka,³³ Kim Pruitt,²⁸ Victor Sapojnikov,²⁹ Xingzhi Song,^1,2 Alexandre Souvorov,²⁸ Victor Solovyev,³⁴ Zheng Wei,⁴ Charles A. Whittaker,³⁵ Kim Worley,^1,2 Lan Zhang^1,2

Assembly of genome: Erica Sodergren^1,2 (leader), George M. Weinstock^1,2 (leader), K. James Durbin,^1,2 Richard A. Gibbs,^1,2 Yufeng Shen^1,2 (v 2.1), Xingzhi Song^1,2 (v 0.5), Kim Worley,^1,2 Lan Zhang^1,2

Basal transcription apparatus proteins and polymerases chromatin proteins: Greg Wray²⁷ (leader), Olivier Fedrigo,²⁶ David Garfield,²⁷ Ralph Haygood,¹⁷ Alexander Primus,²⁶ Rahul Satija,²⁶ Tonya Severson²⁷

BCM-HGSC annotation database and Genboree: Lan Zhang^1,2(leader), Erica Sodergren^1,2 (leader), George M. Weinstock^1,2 (leader), Manuel L. Gonzalez-Garay,^1,2 Andrew R. Jackson,^1,2 Aleksandar Milosavljevic,^1,2 Xingzhi Song,^1,2 Mark Tong,^1,2 Kim Worley^1,2

Biomineralization: Charles A. Ettensohn¹¹ (leader), R. Andrew Cameron,³ Christopher E. Killian,³⁶ Melissa J. Landrum,³¹ Brian T. Livingston,³⁷ Fred H. Wilt³⁶

Cell physiology: James A. Coffman⁸ (leader), William Marzluff¹⁶ (leader), Arcady Mushegian^19,20 (leader), Nikki Adams,³⁷ Robert Bellé,^38,39 Seth Carbonneau,⁸ Rocky Cheung,¹⁶ Patrick Cormier,^38,39 Bertrand Cosson,^38,39 Jenifer Croce,¹⁷ Antonio Fernandez-Guerra,^40,41 Anne-Marie GenevieÌ€re,^40,41 Manisha Goel,¹⁹ Hemant Kelkar,⁴² Julia Morales,^38,39 Odile Mulner-Lorillon,^39,40 Anthony J. Robertson⁸

Cellular defense: Amro Hamdoun¹³ (leader), Jared V. Goldstone⁴² (leader), Nikki Adams,³⁶ Bryan Cole,¹³ Michael Dean,⁹ David Epel,¹³ Bert Gold,⁹ Mark E. Hahn,⁴³ Meredith Howard-Ashby,³ Mark Scally,⁹ John J. Stegeman⁴³

Ciliogenesis and ciliary compounds: Robert L. Morris¹⁸ (leader), Erin L. Allgood,¹⁸ Jonah Cool,¹⁸ Kyle M. Judkins,¹⁸ Shawn S. McCafferty,¹⁸ Ashlan M. Musante,¹⁸ Robert A. Obar,⁴⁴ Amanda P. Rawson,¹⁸ Blair J. Rossetti¹⁸

Cytoskeletal and organelle genes: David R. Burgess⁶ (leader), Erin L. Allgood,¹⁸ Jonah Cool,¹⁸ Ian R. Gibbons,⁴⁵ Matthew P. Hoffman,⁶ Kyle M. Judkins,¹⁸ Andrew Leone,⁶ Shawn S. McCafferty,¹⁸ Robert L. Morris,¹⁸ Ashlan M. Musante,¹⁸ Robert A. Obar,⁴⁴ Amanda P. Rawson,¹⁸ Blair J. Rossetti,¹⁸ Gary M. Wessel²⁶Embryonic transcriptome: Eric H. Davidson³ (leader), R. Andrew Cameron,³ Sorin Istrail,⁴⁶ Stefan C. Materna,³ Manoj P. Samanta,^47,48 Viktor Stolc,⁴⁷ Waraporn Tongprasit,⁴⁷ Qiang Tu³

Embryonic temporal expression pattern list: Robert C. Angerer⁴ (leader), Lynne M. Angerer⁴ (leader), Zheng Wei⁴

Echinoderm adhesome: Richard O. Hynes¹⁴ (leader), Karl-Frederik Bergeron,⁴⁹ Bruce P. Brandhorst,⁵⁰ Robert D. Burke,⁷ Charles A. Whittaker,³⁵ James Whittle⁵¹

Echinoderm evolution: R. Andrew Cameron³ (leader), Kevin Berney,³ David J. Bottjer,⁵¹ Cristina Calestani,⁵³ Eric H. Davidson,³ Kevin Peterson,⁵⁴ Elly Chow,⁵⁵ Qiu Autumn Yuan⁵⁵

Genome analysis [GC content]: Eran Elhaik,⁵⁶ Christine G. Elsik,²⁸ Dan Graur,⁵⁶ Justin T. Reese²⁸

Genome FPC map: Ian Bosdet,⁵⁷ Shin Heesun,⁵⁷ Marco A. Marra,⁵⁷ Jacqueline Schein⁵⁷

Human genetic disease orthologs: Michael Dean⁹ (leader), Amro Hamdoun¹³ (leader), The Sea Urchin Genome Sequencing Consortium

Immunity: Jonathan P. Rast²¹ (leader), L. Courtney Smith²³ (leader), Michele K. Anderson,²² Kevin Berney,³ Virginia Brockton,²³ Katherine M. Buckley,²³ R. Andrew Cameron,³ Avis H. Cohen,⁵⁸ Sebastian D. Fugmann,⁵⁹ Taku Hibino,²¹ Mariano Loza-Coll,²¹ Audrey J. Majeske,²³ Cynthia Messier,²¹ Sham V. Nair,⁶⁰ Zeev Pancer,⁶¹ David P. Terwilliger²²

Neurobiology and sensory systems: Robert D. Burke⁷ (leader), Maurice R. Elphick¹⁰ (leader), William H. Klein¹⁵ (leader), Michael C. Thorndyke²⁴ (leader), Cavit Agca,⁶² Lynne M. Angerer,⁴ Enrique Arboleda,⁵ Maria Ina Arnone,⁵ Bruce P. Brandhorst,⁵⁰ Nansheng Chen,⁵⁰ Allison M. Churcher,⁶³ F. Hallböök,⁶⁴ Glen W. Humphrey,⁶⁵ Richard O. Hynes,¹⁴ Mohammed M. Idris,⁵ Takae Kiyama,¹⁵ Shuguang Liang,¹⁵ Dan Mellott,⁶⁰ Xiuqian Mu,¹⁵ Greg Murray,⁴⁸ Robert P. Olinski,⁶⁴ Florian Raible,^66,67 Matthew Rowe,¹⁰ John S. Taylor,⁶³ Kristin Tessmar-Raible,⁶⁶ D. Wang,⁶³ Karen H. Wilson,²⁴ Shunsuke Yaguchi⁷

Reproduction: Kathy R. Foltz¹² (leader), Victor D. Vacquier²⁵ (leader), Gary M. Wessel²⁶ (leader), Terry Gaasterland,²⁵ Blanca E. Galindo,⁶⁷ Herath J. Gunaratne,²⁵ Meredith Howard-Ashby,³ Glen W. Humphrey,⁶⁵ Celina Juliano,²⁶ Masashi Kinukawa,²⁵ Gary W. Moy,²⁵ Anna T. Neill,²⁵ Mamoru Nomura,²⁵ Michael Raisch,¹² Anna Reade,¹² Michelle M. Roux,¹² Jia L. Song,²⁵ Yi-Hsien Su,³ Ian K. Townley,¹² Ekaterina Voronina,²⁶ Julian L. Wong²⁶

Sea Urchin Genome Annotation Workshop in Naples: Maria Ina Arnone⁵ (leader), Michael C. Thorndyke²⁴ (leader), Gabriele Amore,⁵ Lynne M. Angerer,⁴ Enrique Arboleda,⁵ Margherita Branno,⁵ Euan R. Brown,⁵ Vincenzo Cavalieri,⁶⁹ Véronique Duboc,⁷⁰ Louise Duloquin,⁷⁰ Maurice R. Elphick,¹⁰ Constantin Flytzanis,^70,71 Christian Gache,⁷⁰ Anne-Marie GenevieÌ€re,^40,41 Mohammed M. Idris,⁵ François Lapraz,⁷⁰ Thierry Lepage,⁷⁰ Annamaria Locascio,⁵ Pedro Martinez,^73,74 Giorgio Matassi,⁷⁵ Valeria Matranga,⁷⁶ David R. McClay,¹⁷ Julia Morales,^38,39 Albert J. Poustka,³³ Florian Raible,^66,67 Ryan Range,⁷⁰ Francesca Rizzo,⁵ Eric Röttinger,⁷⁰ Matthew Rowe,¹⁰ Kristin Tessmar-Raible,⁶⁶ Erica Sodergren,^1,2 George M. Weinstock,^1,2 Karen Wilson²⁴

Signal transduction: David R. McClay¹⁷ (leader), Lynne M. Angerer,⁴ Maria Ina Arnone,⁵ Wendy Beane,¹⁷ Cynthia Bradham,¹⁷ Christine Byrum,^17,78 Jenifer Croce,¹⁷ Veronique Duboc,⁷⁰ Louise Duloquin,⁷⁰ Christian Gache,⁷⁰ Anne-Marie GenevieÌ€re,^40,41 Tom Glenn,¹⁷ Taku Hibino,²² Sofia Hussain,³⁷ François Lapraz,⁷⁰ Thierry Lepage,⁷⁰ Brian T. Livingston,³⁷ Mariano Loza,²¹ Gerard Manning,⁷⁶ Esther Miranda,¹⁷ Ryan Range,⁷⁰ Francesca Rizzo,⁵ Eric Röttinger,⁷⁰ Rebecca Thomason,^17,78 Katherine Walton,¹⁷ Zheng Wei,⁴ Gary M. Wessel,²⁶ Athula Wikramanayke,⁷⁷ Karen H. Wilson,²³ Charles Whittaker,³⁵ Shu-Yu Wu,¹⁷ Ronghui Xu⁷⁸

Transcription regulatory factors: Eric H. Davidson³ (leader), Maria Ina Arnone,⁵ Margherita Branno,⁵ C. Titus Brown,³ R. Andrew Cameron,³ Lili Chen,³ Rachel F. Gray,³ Meredith Howard-Ashby,³ Sorin Istrail,⁴⁶ Pei Yun Lee,³ Annamaria Locascio,⁵ Pedro Martinez,^73,74 Stefan C. Materna,³ Jongmin Nam,³ Paola Oliveri,³ Francesca Rizzo,⁵ Joel Smith³

DNA sequencing: Donna Muzny^1,2 (leader), Erica Sodergren^1,2 (leader), Richard A. Gibbs^1,2 (leader), George M. Weinstock^1,2 (leader), 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 Yufeng Shen,^1,2 Rachel Thorn,^1,2 Rita Wright^1,2

¹Human Genome Sequencing Center, Baylor College of Medicine, One Baylor Plaza, Houston, TX 77030, USA. ²Department of Molecular and Human Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX 77030, USA. ³Division of Biology, California Institute of Technology, Pasadena, CA 91125, USA. ⁴National Institute of Dental and Craniofacial Research, NIH, Bethesda, MD20892, USA. ⁵Stazione Zoologica Anton Dohrn, Villa Comunale, 80121 Napoli, Italy. ⁶Department of Biology, Boston College, Chestnut Hill, MA 02467, USA. ⁷Department of Biology, Department of Biochemistry and Microbiology, University of Victoria, Victoria, BC, Canada, V8W 3N5. ⁸Mount Desert Island Biological Laboratory, Salisbury Cove, ME 04672, USA. ⁹Human Genetics Section, Laboratory of Genomic Diversity, National Cancer Institute–Frederick, Frederick, MD 21702, USA. ¹⁰School of Biological and Chemical Sciences, Queen Mary, University of London, London E1 4NS, UK. ¹¹Department of Biological Sciences, Carnegie Mellon University, Pittsburgh, PA, 15213, USA. ¹²Department Molecular, Cellular and Developmental Biology and the Marine Science Institute, University of California, Santa Barbara, Santa Barbara, CA 93106–9610, USA. ¹³Hopkins Marine Station, Stanford University, Pacific Grove, CA 93950, USA. ¹⁴Howard Hughes Medical Institute, Center for Cancer Research, Massachusetts Institute of Technology (MIT), Cambridge, MA 02139, USA. ¹⁵Departments of Biochemistry and Molecular Biology, University of Texas, M. D. Anderson Cancer Center, Houston, TX, 77030, USA. ¹⁶Molecular Biology and Biotechnology, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599, USA. ¹⁷Department of Biology, Duke University, Durham, NC 27708, USA. ¹⁸Department of Biology, Wheaton College, Norton, MA 02766, USA. ¹⁹Stowers Institute for Medical Research, Kansas City, MO 64110, USA. ²⁰Department of Microbiology, Kansas University Medical Center, Kansas City, KS 66160, USA. ²¹Sunnybrook Research Institute and Department of Medical Biophysics, University of Toronto, Toronto, Ontario, Canada M4N 3M5. ²²Department of Immunology, University of Toronto, Toronto, Ontario, Canada, M4N 3M5. ²³Department of Biological Sciences, George Washington University, Washington, DC 20052, USA. ²⁴Royal Swedish Academy of Sciences, Kristineberg Marine Research Station, Fiskebackskil, 450 34, Sweden. ²⁵Marine Biology, Scripps Institution of Oceanography, University of California San Diego, La Jolla, CA 92093–0202, USA. ²⁶Department of Molecular and Cellular Biology and Biochemistry, Brown University Providence, RI 02912, USA. ²⁷Department of Biology and Institute for Genome Sciences and Policy, Duke University, Durham, NC 27708, USA. ²⁸Department of Animal Science, Texas A&M University, College Station, TX 77843, USA. ²⁹National Center for Biotechnology Information, National Library of Medicine, NIH, Bethesda, MD 20894, USA. ³⁰Department of Ecology, Evolution, and Marine Biology, University of California Santa Barbara, Santa Barbara, CA 93106, USA. ³¹National Center for Biotechnology Information, NIH, Bethesda, MD 20892, USA. ³²Penn Genomics Institute, University of Pennsylvania, Philadelphia, PA 19104, USA. ³³Evolution and Development Group, Max-Planck Institut für Molekulare Genetik, 14195 Berlin, Germany. ³⁴Royal Holloway, University of London, Egham, Surrey TW20 0EX, UK. ³⁵Center for Cancer Research, MIT, Cambridge, MA 02139, USA. ³⁶Department of Molecular and Cell Biology, University of California, Berkeley, Berkeley, CA 94720–3200, USA. ³⁷Department of Biology, University of South Florida, Tampa, FL 33618, USA. ³⁸Université Pierre et Marie Curie (Paris 6), UMR 7150, Equipe Cycle Cellulaire et Développement, Station Biologique de Roscoff, 29682 Roscoff Cedex, France. ³⁹CNRS, UMR 7150, Station Biologique de Roscoff, 29682 Roscoff Cedex, France. ⁴⁰CNRS, UMR7628, Banyuls-sur-Mer, F-66650, France. ⁴¹Université Pierre et Marie Curie (Paris 6), UMR7628, Banyuls-sur-Mer, F-66650, France. ⁴²Center for Bioinformatics, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599, USA. ⁴³Biology Department, Woods Hole Oceanographic Institution, Woods Hole, MA 02543, USA. ⁴⁴Tethys Research, LLC, 2115 Union Street, Bangor, Maine 04401, USA. ⁴⁵Department of Molecular, Cellular, and Developmental Biology, University of California, Berkeley, Berkeley, CA 94720, USA. ⁴⁶Center for Computational Molecular Biology, and Computer Science Department, Brown University, Providence, RI 02912, USA. ⁴⁷Genome Research Facility, National Aeronautics and Space Administration, Ames Research Center, Moffet Field, CA 94035, USA. ⁴⁸Systemix Institute, Cupertino, CA 95014, USA. ⁴⁹Department of Molecular Biology and Biochemistry, Simon Fraser University, Burnaby, British Columbia, Canada, V5A 1S6. ⁵⁰Department of Molecular Biology and Biochemistry, Simon Fraser University, Burnaby, BC, Canada, V5A 1S6. ⁵¹Department of Biology, Center for Cancer Research, MIT, Cambridge, MA 02139, USA. ⁵²Department of Earth Sciences, University of Southern California, Los Angeles, CA 90089–0740, USA. ⁵³Department of Biology, University of Central Florida, Orlando, FL 32816–2368, USA. ⁵⁴Department of Biological Sciences, Dartmouth College, Hanover, NH 03755, USA. ⁵⁵Center for Computational Regulatory Genomics, Beckman Institute, California Institute of Technology, Pasadena, CA 91125, USA. ⁵⁶Department of Biology and Biochemistry, University of Houston, Houston, TX 77204, USA. ⁵⁷Genome Sciences Centre, British Columbia Cancer Agency, Vancouver, BC, Canada, V5Z 4E6. ⁵⁸Department of Biology and the Institute of Systems Research, University of Maryland, College Park, MD 20742, USA. ⁵⁹Laboratory of Cellular and Molecular Biology, National Institute on Aging, NIH, Baltimore, MD 21224, USA. ⁶⁰Department of Biological Sciences, Macquarie University, Sydney NSW 2109, Australia. ⁶¹Center of Marine Biotechnology, UMBI, Columbus Center, Baltimore, MD 21202, USA. ⁶²Department of Cell Biology and Anatomy, Louisiana State University Health Sciences Center, New Orleans, LA 70112, USA. ⁶³Department of Biology, University of Victoria, Victoria, BC, Canada, V8W 2Y2. ⁶⁴Department of Neuroscience, Uppsala University, Uppsala, Sweden. ⁶⁵Laboratory of Cellular and Molecular Biophysics, National Institute of Child Health and Development, NIH, Bethesda, MD 20895, USA. ⁶⁶Developmental Unit, EMBL, 69117 Heidelberg, Germany. ⁶⁷Computational Unit, EMBL, 69117 Heidelberg, Germany. ⁶⁸Biotechnology Institute, Universidad Nacional Autónoma de Mexico (UNAM), Cuernavaca, Morelos, Mexico 62250. ⁶⁹Department of Cellular and Developmental Biology “Alberto Monroy,” University of Palermo, 90146 Palermo, Italy. ⁷⁰Laboratoire de Biologie du Développement (UMR 7009), CNRS and Université Pierre et Marie Curie (Paris 6), Observatoire Océanologique, 06230 Villefranche-sur-Mer, France. ⁷¹Department of Biology, University of Patras, Patras, Greece. ⁷²Department of Molecular and Cellular Biology, Baylor College of Medicine, One Baylor Plaza, Houston, TX 77030, USA. ⁷³Departament de Genetica, Universitat de Barcelona, 08028–Barcelona, Spain. ⁷⁴Institució Catalana de Recerca i Estudis Avancats (ICREA), Barcelona, Spain. ⁷⁵Institut Jacques Monod, CNR-UMR 7592, 75005 Paris, France. ⁷⁶Consiglio Nazionale delle Ricerche, Istituto di Biomedicina e Immunologia Molecolare “Alberto Monroy,” 90146 Palermo, Italy. ⁷⁷Razavi-Newman Center for Bioinformatics, Salk Institute for Biological Studies, La Jolla, CA 92186, USA. ⁷⁸Department of Zoology, University of Hawaii at Manoa, Honolulu, HI 96822, USA.

Supporting Online Material

www.sciencemag.org/cgi/content/full/314/5801/941/DC1

Materials and Methods

SOM Text

Figs. S1 to S6

Tables S1 to S8

Reference