The Draft Genome of Ciona

intestinalis: Insights into

Chordate and Vertebrate Origins

Paramvir Dehal,1

* Yutaka Satou,2

* Robert K. Campbell,3,4

Jarrod Chapman,1 Bernard Degnan,5 Anthony De Tomaso,6

Brad Davidson,7 Anna Di Gregorio,7 Maarten Gelpke,1

David M. Goodstein,1 Naoe Harafuji,7 Kenneth E. M. Hastings,8

Isaac Ho,1 Kohji Hotta,9 Wayne Huang,1 Takeshi Kawashima,10

Patrick Lemaire,11 Diego Martinez,1 Ian A. Meinertzhagen,12

Simona Necula,1 Masaru Nonaka,13 Nik Putnam,1 Sam Rash,1

Hidetoshi Saiga,14 Masanobu Satake,15 Astrid Terry,1

Lixy Yamada,2 Hong-Gang Wang,16 Satoko Awazu,2

Kaoru Azumi,17 Jeffrey Boore,1 Margherita Branno,18

Stephen Chin-bow,19 Rosaria DeSantis,18 Sharon Doyle,1

Pilar Francino,1 David N. Keys,1,7 Shinobu Haga,9

Hiroko Hayashi,9 Kyosuke Hino,2 Kaoru S. Imai,2 Kazuo Inaba,20

Shungo Kano,2,18 Kenji Kobayashi,2 Mari Kobayashi,2

Byung-In Lee,1 Kazuhiro W. Makabe,2 Chitra Manohar,1

Giorgio Matassi,18 Monica Medina,1 Yasuaki Mochizuki,2

Steve Mount,21 Tomomi Morishita,9 Sachiko Miura,9

Akie Nakayama,2 Satoko Nishizaka,9 Hisayo Nomoto,9

Fumiko Ohta,9 Kazuko Oishi,9 Isidore Rigoutsos,19 Masako Sano,9

Akane Sasaki,2 Yasunori Sasakura,2 Eiichi Shoguchi,2

Tadasu Shin-i,9 Antoinetta Spagnuolo,18 Didier Stainier,22

Miho M. Suzuki,23 Olivier Tassy,11 Naohito Takatori,2

Miki Tokuoka,2 Kasumi Yagi,2 Fumiko Yoshizaki,13

Shuichi Wada,2 Cindy Zhang,1 P. Douglas Hyatt,24

Frank Larimer,24 Chris Detter,1 Norman Doggett,25

Tijana Glavina,1 Trevor Hawkins,1 Paul Richardson,1

Susan Lucas,1 Yuji Kohara,9

† Michael Levine,7,26† Nori Satoh,2

†

Daniel S. Rokhsar1,7,26†

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. The Ciona

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.

Introduction

There has been considerable debate regarding

the evolutionary origins of the chordates and,

within them, of vertebrates, and the relationships between the first chordates and invertebrate deuterostomes (1–3). There is a

consensus that the three major deuterostome phyla (echinoderms, hemichordates,

and chordates) arose from a common ancestor more than 550 million years ago.

The chordates subsequently diverged into

three subphyla: urochordates (also known

as tunicates), cephalochordates, and vertebrates (Fig. 1). It is generally believed that

cephalochordates and vertebrates are sister

groups, with the urochordate lineage most

basal among the chordates.

The most prevalent modern urochordates

are the ascidians, known familiarly as sea

squirts. The analysis of ascidians offers the

simultaneous prospects of providing insights into two compelling problems in

evolutionary biology: the origins of the

chordates from an ancestral deuterostome,

and the origins of the vertebrates from a

simple chordate.

Ascidians, or sea squirts, are sessile, hermaphroditic marine invertebrates that live in

shallow ocean waters around the world. The

adults are simple filter feeders encased in a

fibrous tunic supporting incurrent and outcurrent siphons, and were classified by Aristotle

as related to mollusks (Fig. 2A). The close

kinship of ascidians with vertebrates was discovered over 130 years ago by Kowalevsky

(4), who recognized that the ascidian larva

has the general appearance of a vertebrate

tadpole (Fig. 2L). Most notably, the tail of the

ascidian tadpole contains a prominent notochord and a dorsal tubular nerve cord. These

findings elevated ascidians to the ranks of the

1

U.S. Department of Energy Joint Genome Institute,

2800 Mitchell Drive, Walnut Creek, CA 94598, USA.

2

Department of Zoology, Graduate School of Science,

Kyoto University, Kyoto 606-8502, Japan. 3

Marine

Biological Laboratories, Woods Hole, MA 02543, USA.

4

Serono Reproductive Biology Institute, One Technology Place, Rockland, MA 02370, USA. 5

Department of

Zoology and Entomology, University of Queensland,

Brisbane, Qld 4072, Australia. 6

Department of Pathology, Stanford University School of Medicine, Stanford,

CA 93950, USA. 7

Department of Molecular and Cellular Biology, Division of Genetics, 401 Barker Hall,

University of California, Berkeley, CA 94720, USA.

8

Montreal Neurological Institute, McGill University,

Montreal, H3A 2T5, Canada. 9

National Institute of

Genetics, Mishima 411-8540, Japan. 10Bioinformatics

Center, Institute for Chemical Research, Kyoto Univeristy, Uji, Kyoto 611-0011, Japan. 11LGPD, IBDM,

Case 907, Campus de Luminy, F-13288 Marseille Cedex 09, France. 12Life Sciences Centre, Dalhousie University, Halifax, Nova Scotia, B3H 4J1, Canada. 13Department of Biological Sciences, Graduate School of

Science, University of Tokyo, Tokyo 113-0033, Japan.

14Department of Biological Sciences, Graduate School

of Science, Tokyo Metropolitan University, Hachiohji,

Tokyo 192-0397, Japan. 15Department of Molecular

Immunology, Institute of Development, Aging and

Cancer, Tohoku University, Seiryo-machi, Aoba-ku,

Sendai 980-8575, Japan. 16Drug Discovery Program,

Moffitt Cancer Center, 12902 Magnolia Drive, Tampa,

FL 33612, USA. 17Department of Biochemistry, Graduate School of Pharmaceutical Sciences, Hokkaido

University, Sapporo 060-0812, Japan. 18Stazione Zoologica “Anton Dohrn,” Villa Comunale, 80121 Napoli,

Italy. 19IBM Watson Research Center, Post Office Box

218, Yorktown Heights, NY 10598, USA. 20Asamushi

Marine Biological Station, Graduate School of Science,

Tohoku University, Asamushi, Aomori 039-3501, Japan. 21University of Maryland, College Park, MD

20742, USA. 22Department of Biochemistry and Biophysics, Programs in Developmental Biology, Genetics, and Human Genetics, University of California, San

Francisco, CA 94143, USA. 23Wellcome Trust Centre

for Cell Biology, Institute of Cell and Molecular Biology, University of Edinburgh, Edinburgh EH9 3JR, UK.

24Oak Ridge National Laboratory, Post Office Box

2008, Oak Ridge, TN 37831, USA. 25Los Alamos National Laboratory, Los Alamos, NM 87545, USA.

26Center for Integrative Genomics, University of California, Berkeley 94720, USA.

*These authors contributed equally to this work.

†To whom correspondence should be addressed. Email: ykohara@lab.nig.ac.jp (Y.K.), mlevine@uclink4.

berkeley.edu (M.L.), satoh@ascidian.zool.kyoto-u.ac.jp

(N.S.), dsrokhsar@lbl.gov(D.R.)