The Draft Genome of Ciona intestinalis: Insights into Chordate and Vertebrate Origins

The first chordates appear in the fossil record at the time of the Cambrian explosion, nearly 550 million years ago. The modern ascidian tadpole represents a plausible approximation to these ancestral chordates. To illuminate the origins of chordate and vertebrates, we generated a draft of the protein-coding portion of the genome of the most studied ascidian, Ciona intestinalis. TheCiona genome contains ∼16,000 protein-coding genes, similar to the number in other invertebrates, but only half that found in vertebrates. Vertebrate gene families are typically found in simplified form in Ciona, suggesting that ascidians contain the basic ancestral complement of genes involved in cell signaling and development. The ascidian genome has also acquired a number of lineage-specific innovations, including a group of genes engaged in cellulose metabolism that are related to those in bacteria and fungi.

Paul Richardson | David N. Keys | Fumiko Ohta | Ian A. Meinertzhagen | Takeshi Kawashima | Yuji Kohara | Kazuhiro W. Makabe | Kenji Kobayashi | Olivier Tassy | Monica Medina | Paramvir S. Dehal | Shuichi Wada | Jarrod Chapman | Sachiko Miura | David M. Goodstein | Michael Levine | Kazuo Inaba | Daniel S. Rokhsar | Frank Larimer | Tomomi Morishita | Kohji Hotta | Yutaka Satou | Lixy Yamada | Yasunori Sasakura | Norman Doggett | Kaoru Azumi | Paramvir Dehal | Masanobu Satake | Isaac Y. Ho | Tijana Glavina | Isaac Ho | Satoko Awazu | Isidore Rigoutsos | Sam Rash | Astrid Terry | Akie Nakayama | Naohito Takatori | Shinobu Haga | Hisayo Nomoto | Nori Satoh | M. Levine | I. Meinertzhagen | B. Degnan | J. Chapman | Y. Kohara | N. Doggett | I. Rigoutsos | T. Hawkins | P. Richardson | S. Lucas | N. Putnam | Sam Rash | M. Gelpke | C. Detter | D. Rokhsar | R. Campbell | K. Hotta | D. Stainier | J. Boore | P. Lemaire | D. Keys | Olivier Tassy | C. Manohar | G. Matassi | D. Goodstein | N. Satoh | E. Shoguchi | F. Larimer | A. Terry | M. Medina | N. Takatori | H. Saiga | Kazuko Oishi | T. Shin-I | Diego Martínez | T. Glavina | S. Wada | K. Inaba | Wayne Huang | Miho M. Suzuki | Anna Di Gregorio | M. Nonaka | K. Yagi | K. Azumi | Y. Satou | M. Branno | T. Kawashima | Y. Sasakura | K. Makabe | K. Hastings | S. Doyle | Fumiko Yoshizaki | M. Satake | Akane Sasaki | Susan Lucas | Giorgio Matassi | Diego Martinez | L. Yamada | Chris Detter | Eiichi Shoguchi | Brad Davidson | A. De Tomaso | B. Davidson | N. Harafuji | Simona Necula | Hong-gang Wang | S. Awazu | S. Chin-bow | R. Desantis | P. Francino | S. Haga | H. Hayashi | K. Hino | K. Imai | S. Kano | Kenji Kobayashi | Mari Kobayashi | Byung-in Lee | Y. Mochizuki | S. Mount | T. Morishita | Sachiko Miura | A. Nakayama | Satoko Nishizaka | H. Nomoto | Fumiko Ohta | Masako Sano | Antoinetta Spagnuolo | M. Tokuoka | Cindy Zhang | P. D. Hyatt | Anna Di Gregorio | Kazuko Oishi | Kyosuke Hino | Kasumi Yagi | Patrick Lemaire | Wayne Huang | Didier Stainier | Miki Tokuoka | Masaru Nonaka | Tadasu Shin-i | Masako Sano | Hiroko Hayashi | Satoko Nishizaka | Jeffrey Boore | Hong-Gang Wang | Yasuaki Mochizuki | Akane Sasaki | Naoe Harafuji | Hidetoshi Saiga | Nik Putnam | Robert K. Campbell | Bernard Degnan | Anthony De Tomaso | Maarten Gelpke | Kenneth E. M. Hastings | Simona Necula | Margherita Branno | Stephen Chin-bow | Rosaria DeSantis | Sharon Doyle | Pilar Francino | Kaoru S. Imai | Shungo Kano | Mari Kobayashi | Byung-In Lee | Chitra Manohar | Steve Mount | Antoinetta Spagnuolo | Fumiko Yoshizaki | Cindy Zhang | P. Douglas Hyatt | Trevor Hawkins | Satoko Awazu | A. D. De Tomaso | Hong-Gang Wang | Tijana Glavina | Naohito Takatori | Akie Nakayama | Lixy Yamada | Pilar Francino | Yasuaki Mochizuki | Jarrod Chapman

[1]  N. Satoh,et al.  An essential role of a FoxD gene in notochord induction in Ciona embryos. , 2002, Development.

[2]  A. Romer The vertebrate body , 1971 .

[3]  Takeshi Kawashima,et al.  A cDNA resource from the basal chordate Ciona intestinalis , 2002, Genesis.

[4]  Anthony V. Boccabella,et al.  Thyroid , 1908, The Journal of Laryngology, Rhinology, and Otology.

[5]  K. Hotta,et al.  Brachyury downstream notochord differentiation in the ascidian embryo. , 1999, Genes & development.

[6]  C. Heisenberg,et al.  A mutational approach to the study of development of the protochordate Ciona intestinalis (Tunicata, Chordata) , 2000 .

[7]  N. Saitou,et al.  Phylogenetic relationship of muscle tissues deduced from superimposition of gene trees. , 1999, Molecular biology and evolution.

[8]  Juliette Gardner Genesis , 1985 .

[9]  W. J. Kent,et al.  BLAT--the BLAST-like alignment tool. , 2002, Genome research.

[10]  G. Krishnan Nature of tunicin & its interaction with other chemical components of the tunic of the ascidian, Polyclinum madrasensis Sebastian. , 1975, Indian journal of experimental biology.

[11]  W. Smith,et al.  Mutations affecting tail and notochord development in the ascidian Ciona savignyi. , 1999, Development.

[12]  Stephen M. Mount,et al.  The genome sequence of Drosophila melanogaster. , 2000, Science.

[13]  N. Satoh,et al.  Developmental Biology of Ascidians , 1995 .

[14]  A. Mccarthy Development , 1996, Current Opinion in Neurobiology.

[15]  J. Gerhart,et al.  Formation and function of Spemann's organizer. , 1997, Annual review of cell and developmental biology.

[16]  N. Chua,et al.  KORRIGAN, an Arabidopsis Endo-1,4-β-Glucanase, Localizes to the Cell Plate by Polarized Targeting and Is Essential for Cytokinesis , 2000, Plant Cell.

[17]  P. Holland,et al.  The amphioxus Hox cluster: deuterostome posterior flexibility and Hox14 , 2000, Evolution & development.

[18]  M. Levine,et al.  Characterization of a notochord-specific enhancer from the Brachyury promoter region of the ascidian, Ciona intestinalis. , 1997, Development.

[19]  H. Ulrich Natural substrates of the proteasome and their recognition by the ubiquitin system. , 2002, Current topics in microbiology and immunology.

[20]  H. Gee Heads and Tails. (Book Reviews: Before the Backbone. Views on the Origin of the Vertebrates.) , 1996 .

[21]  Michael Levine,et al.  The Ascidian as a Model Organism in Developmental and Evolutionary Biology , 2001, Cell.

[22]  M. Flajnik,et al.  Comparative genomics of the MHC: glimpses into the evolution of the adaptive immune system. , 2001, Immunity.

[23]  R. Cripps,et al.  Control of cardiac development by an evolutionarily conserved transcriptional network. , 2002, Developmental biology.

[24]  H. Lehrach,et al.  Miniature genome in the marine chordate Oikopleura dioica. , 2001, Science.

[25]  Jordi Garcia-Fernàndez,et al.  Archetypal organization of the amphioxus Hox gene cluster , 1994, Nature.

[26]  H Decker,et al.  Hemocyanins and Invertebrate Evolution* , 2001, The Journal of Biological Chemistry.

[27]  AC Tose Cell , 1993, Cell.

[28]  G. Salvesen,et al.  Caspases: Intracellular Signaling by Proteolysis , 1997, Cell.

[29]  J. Graves The descent of man , 2004, Nature.

[30]  K. Brennan,et al.  Notching up another pathway. , 2002, BioEssays : news and reviews in molecular, cellular and developmental biology.

[31]  H. Nishida,et al.  Cell lineage analysis in ascidian embryos by intracellular injection of a tracer enzyme. III. Up to the tissue restricted stage. , 1987, Developmental biology.

[32]  M W Simmen,et al.  Gene number in an invertebrate chordate, Ciona intestinalis. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[33]  E. Davidson,et al.  Organization of an echinoderm Hox gene cluster. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[34]  L. Stryer,et al.  Cyclic GMP cascade of vision. , 1986, Annual review of neuroscience.

[35]  C. Weichert Elements of Chordate Anatomy , 1967 .

[36]  I. Ruvinsky,et al.  Genetic and developmental bases of serial homology in vertebrate limb evolution. , 2000, Development.

[37]  A. Poustka,et al.  Cloning of the T gene required in mesoderm formation in the mouse , 1990, Nature.

[38]  Y. Kohara,et al.  Gene expression profiles in Ciona intestinalis tailbud embryos. , 2001, Development.

[39]  Shoichiro Tsukita,et al.  Multifunctional strands in tight junctions , 2001, Nature Reviews Molecular Cell Biology.

[40]  G. Mahairas,et al.  A sea urchin genome project: sequence scan, virtual map, and additional resources. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[41]  Timothy B. Stockwell,et al.  The Sequence of the Human Genome , 2001, Science.

[42]  김삼묘,et al.  “Bioinformatics” 특집을 내면서 , 2000 .

[43]  Alex Bateman,et al.  InterPro: An Integrated Documentation Resource for Protein Families, Domains and Functional Sites , 2002, Briefings Bioinform..

[44]  J. Bonner,et al.  Differentiation , 1968, Nature.

[45]  A. D. Dunn,et al.  Update on intrathyroidal iodine metabolism. , 2001, Thyroid : official journal of the American Thyroid Association.

[46]  N. Satoh,et al.  The simple tail of chordates: Phylogenetic significance of appendicularians , 2001, Genesis.

[47]  R. di Lauro,et al.  Cihox5, a new Ciona intestinalisHox-related gene, is involved in regionalization of the spinal cord , 1998, Development Genes and Evolution.

[48]  E Pennisi,et al.  Ideas Fly at Gene-Finding Jamboree , 2000, Science.

[49]  S. Filetti,et al.  Expression of nicotinamide adenine dinucleotide phosphate oxidase flavoprotein DUOX genes and proteins in human papillary and follicular thyroid carcinomas. , 2001, Thyroid : official journal of the American Thyroid Association.

[50]  I. Meinertzhagen,et al.  The larval ascidian nervous system: the chordate brain from its small beginnings , 2001, Trends in Neurosciences.

[51]  H. Noda,et al.  Evidence from multiple gene sequences indicates that termites evolved from wood-feeding cockroaches , 2000, Current Biology.

[52]  A. Capponi Regulation of cholesterol supply for mineralocorticoid biosynthesis , 2002, Trends in Endocrinology & Metabolism.

[53]  Response to Comment on "Otolith δ18O Record of Mid-Holocene Sea Surface Temperatures in Peru" , 2003, Science.

[54]  R. Hardison,et al.  A brief history of hemoglobins: plant, animal, protist, and bacteria. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[55]  W. Jeffery Determinants of cell and positional fate in ascidian embryos. , 2001, International review of cytology.

[56]  D. Wilkinson,et al.  Molecular control of neural crest formation, migration and differentiation. , 2000, Current opinion in cell biology.

[57]  N. Satoh,et al.  Fgf genes in the basal chordate Ciona intestinalis , 2002, Development Genes and Evolution.

[58]  F C Kafatos,et al.  Phylogenetic perspectives in innate immunity. , 1999, Science.

[59]  Michael Levine,et al.  Genome-wide identification of tissue-specific enhancers in the Ciona tadpole , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[60]  C. Freund,et al.  Guidebook to the Homeobox Genes , 1995 .

[61]  J. Sellers,et al.  Myosins: a diverse superfamily. , 2000, Biochimica et biophysica acta.

[62]  W. Jeffery,et al.  Evolution of the chordate muscle actin gene , 1993, Journal of Molecular Evolution.

[63]  A. Spagnuolo,et al.  Cloning of ascidian homeobox genes provides evidence for a primordial chordate cluster. , 1995, Gene.

[64]  J. Vandekerckhove,et al.  Chordate muscle actins differ distinctly from invertebrate muscle actins. The evolution of the different vertebrate muscle actins. , 1984, Journal of molecular biology.

[65]  V. Papaioannou T-box genes in development: from hydra to humans. , 2001, International review of cytology.

[66]  O. Hobert,et al.  Functions of LIM-homeobox genes. , 2000, Trends in genetics : TIG.

[67]  C. Zuker,et al.  The biology of vision of Drosophila. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[68]  S. Read,et al.  Prime Time for Cellulose , 2002, Science.

[69]  D. Kirsten The Thyroid Gland: Physiology and Pathophysiology , 2000, Neonatal Network.

[70]  R. Durbin,et al.  Using GeneWise in the Drosophila annotation experiment. , 2000, Genome research.

[71]  V. Cryns,et al.  Proteases to die for. , 1998, Genes & development.

[72]  T. H. Meedel,et al.  Lineage segregation and developmental autonomy in expression of functional muscle acetylcholinesterase mRNA in the ascidian embryo. , 1984, Developmental biology.

[73]  M. Levine,et al.  Analyzing gene regulation in ascidian embryos: new tools for new perspectives. , 2002, Differentiation; research in biological diversity.

[74]  V. Laudet,et al.  Evolution of the nuclear receptor superfamily: early diversification from an ancestral orphan receptor. , 1997, Journal of molecular endocrinology.

[75]  N. Lartillot,et al.  The new animal phylogeny: reliability and implications. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[76]  S. Tomarev Pax-6, eyes absent, and Prox 1 in eye development. , 1997, The International journal of developmental biology.

[77]  N. Satoh,et al.  Ascidian embryos as a model system to analyze expression and function of developmental genes. , 2001, Differentiation; research in biological diversity.

[78]  Y. Kohara,et al.  Gene expression profiles in tadpole larvae of Ciona intestinalis. , 2002, Developmental biology.

[79]  J. V. Moran,et al.  Initial sequencing and analysis of the human genome. , 2001, Nature.

[80]  Rolf Apweiler,et al.  InterProScan - an integration platform for the signature-recognition methods in InterPro , 2001, Bioinform..