, 941 (2006); 314 Science et al. Erica Sodergren Strongylocentrotus purpuratus The Genome of the Sea Urchin This copy is for your personal, non-commercial use only. clicking here. colleagues, clients, or customers by , you can order high-quality copies for your If you wish to distribute this article to others here. following the guidelines can be obtained by Permission to republish or repurpose articles or portions of articles ): November 5, 2014 www.sciencemag.org (this information is current as of The following resources related to this article are available online at http://www.sciencemag.org/content/315/5813/766.2.full.html A correction has been published for this article at: http://www.sciencemag.org/content/314/5801/941.full.html version of this article at: including high-resolution figures, can be found in the online Updated information and services, http://www.sciencemag.org/content/suppl/2006/11/07/314.5801.941.DC1.html can be found at: Supporting Online Material http://www.sciencemag.org/content/314/5801/941.full.html#related found at: can be related to this article A list of selected additional articles on the Science Web sites http://www.sciencemag.org/content/314/5801/941.full.html#ref-list-1 , 15 of which can be accessed free: cites 42 articles This article http://www.sciencemag.org/content/314/5801/941.full.html#related-urls 100 articles hosted by HighWire Press; see: cited by This article has been http://www.sciencemag.org/cgi/collection/genetics Genetics subject collections: This article appears in the following

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. The genome of the sea urchin was sequenced primarily because of the remarkable usefulness of the echinoderm embryo as a research model system for modern molecular, evolutionary, and cell biology. The sea urchin is the first animal with a sequenced genome that (i) is a free-living, motile marine invertebrate; (ii) has a bilaterally organized embryo but a radial adult body plan; (iii) has the endoskeleton and water vascular system found only in echinoderms; and (iv) has a nonadaptive immune system that is unique in the enormous complexity of its receptor repertoire. Sea urchins are remarkably long-lived with life spans of Strongylocentrotid species extending to over a century [see supporting online material (SOM)] and highly fecund, producing millions of gametes each year; and Strongylocentrotus purpuratus is a pivotal component of subtidal marine ecology and an important fishery catch in several areas of the world, including the United States. Although a research model in developmental biology for a century and a half, for most of that time, few were aware of one of the most important characteristics of sea urchins, a character that directly enhances its significance for genomic analysis: Echinoderms (and their sister phylum, the hemichordates) are the closest known relatives of the chordates (Fig. 1 and SOM). A description of the echinoderm body plan, as well as aspects of the life-style, longevity, polymorphic gene pool, and characteristics that make the sea urchin so valuable as a research organism, are presented in the SOM. The last common ancestors of the deuterostomal groups at the branch points shown in Fig. 1 are of Precambrian antiquity [>540 million years ago (Ma)], according to protein molecular phylogeny. Stem group echinoderms appear in the Lower Cambrian fossil assemblages dating to 520 Ma. Cambrian echinoderms came in many distinct forms, but from their first appearance, the fossil record illustrates certain distinctive features that are still present: their water vascular system, including rows of tube feet protruding through holes in the ambulacral grooves and their calcite endoskeleton (mainly, a certain form of CaCO3), which displays the specific three-dimensional structure known as “stereom.” The species sequenced, Strongylocentrotus purpuratus, commonly known as the “California purple sea urchin” is a representative of the thin-spined “modern” group of regularly developing sea urchins (euechinoids). These evolved to become the dominant echinoid form after the great Permian-Triassic extinction 250 million years ago. NIH Public Access Author Manuscript Science. Author manuscript; available in PMC 2011 August 22. Published in final edited form as: Science. 2006 November 10; 314(5801): 941–952. doi:10.1126/science.1133609. N IH PA Athor M anscript N IH PA Athor M anscript N IH PA Athor M anscript We present here a description of the S. purpuratus genome and gene products. The genome Copyright 2006 by the American Association for the Advancement of Science; all rights reserved. *Correspondence should be addressed to gwstock@bcm.tmc.edu . †All authors with their contributions and affiliations appear at the end of this paper. 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 Sea Urchin Genome Sequencing Consortium Overall project leadership: Erica Sodergren,1,2 George M. Weinstock,1,2 Eric H. Davidson,3 R. Andrew Cameron3 Principal investigators: Richard A. Gibbs,1,2 George M. Weinstock1,2 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 Zhang1,2 Annotation: Gene list: Erica Sodergren1,2 (leader), George M. Weinstock1,2 (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 Zhang1,2 Assembly of genome: Erica Sodergren1,2 (leader), George M. Weinstock1,2 (leader), K. James Durbin,1,2 Richard A. Gibbs,1,2 Yufeng Shen1,2 (v 2.1), Xingzhi Song1,2 (v 0.5), Kim Worley,1,2 Lan Zhang1,2 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 Zhang1,2 (leader), Erica Sodergren1,2 (leader), George M. Weinstock1,2 (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 Worley1,2 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 Mushegian19,20 (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 Genevière,40,41 Manisha Goel,19 Hemant Kelkar,42 Julia Morales,38,39 Odile MulnerLorillon,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. Wessel26 Embryonic 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 Genevière,40,41 Mohammed M. Idris,5 François Lapraz,70 Thierry Lepage,70 Annamari

To understand the biology and evolution of ruminants, the cattle genome was sequenced to about sevenfold coverage. The cattle genome contains a minimum of 22,000 genes, with a core set of 14,345 orthologs shared among seven mammalian species of which 1217 are absent or undetected in noneutherian (marsupial or monotreme) genomes. Cattle-specific evolutionary breakpoint regions in chromosomes have a higher density of segmental duplications, enrichment of repetitive elements, and species-specific variations in genes associated with lactation and immune responsiveness. Genes involved in metabolism are generally highly conserved, although five metabolic genes are deleted or extensively diverged from their human orthologs. The cattle genome sequence thus provides a resource for understanding mammalian evolution and accelerating livestock genetic improvement for milk and meat production.

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