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The Draft Genome of Ciona intestinalis : Insights into Chordate and Vertebrate Origins
Open accessAbstract
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.
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“The difference is consistent with the lower gene number and reduced genome size in the urochordates (4).”
From The Genome of the Sea Urchin Strongylocentrotus purpuratus (2006) · cites this paper as [4]
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BackgroundMethodAscidians as models for studying invasion success
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BackgroundAn unappreciated role for RNA surveillance
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“Five long sequences of defective transposons present in a few copies each were assembled from the C. intestinalis draft genome sequence (Dehal et al. 2002), together with an apparently domesticated sequence (CinPBD1).”
BackgroundEvolutionary Diversity of Vertebrate Small Heat Shock Proteins
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“Also, the finding of only six sHsp genes in the C. intestinalis genome may agree with the fact that vertebrate gene families are typically found in simplified form in C. intestinalis, reflecting the ancestral complement of such genes (Dehal et al. 2002).”
BackgroundApoptosis in molluscan immune defense
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“2% heterozygosity), assembly contiguity and completeness is significantly lower than would have been expected in the absence of heterozygosity, although factors such as repeat content, segmental duplications, and library quality could also affect assembly quality (Aparicio et al. 2002; Dehal et al. 2002).”
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“The complete genome sequence of the ascidian Ciona intestinalis revealed the essential toolkit of vertebrate genes in a small and compact genome that had not undergone the round of vertebrate-specific genome duplication events [2,3].”
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Imai, K. S., Stolfi, A., Levine, M., & Satou, Y. (2008) · Development · doi:10.1242/dev.026419 · Cited by 166
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Miranda‐Saavedra, D., & Barton, G. J. (2007) · Proteins Structure Function and Bioinformatics · doi:10.1002/prot.21444 · Cited by 176
Evolution of steroid receptors from an estrogen-sensitive ancestral receptor
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Precraniate origin of cranial motoneurons
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“Although vertebrates contain about twice the number of genes as invertebrates, this increase in number is primarily due to the duplication of ‘old’ genes rather than the invention of new ones (e.g. Dehal et al., 2002).”
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Amphioxus and tunicates as evolutionary model systems
Schubert, M., Escrivá, H., Xavier‐Neto, J., & Laudet, V. (2006) · Trends in Ecology & Evolution · doi:10.1016/j.tree.2006.01.009 · Cited by 161
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“In the present analysis, we identified 83 homeobox genes in the completely sequenced Ciona intestinalis genome (Dehal et al. 2002) and in a cDNA/EST database (Satou et al. 2002), and they are classified according to the previously proposed classification schemes for vertebrate homeobox genes.”
MethodSelf-citationThe UHRF family: Oncogenes that are drugable targets for cancer therapy in the near future?
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Self-citationHox cluster duplications and the opportunity for evolutionary novelties
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“It is the first eukaryotic marine species whose genome was completely sequenced (Dehal et al. 2002) after Takifugu rubripes (Aparicio et al. 2002).”
BackgroundMolecular phylogeny of the protochordates: chordate evolution
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“More elaborate explanations for the term Appendicularia can be found in Fenaux (1993, 1998) and Kott (1998). There are 3 families of Appendicularia with about 15 genera, which are classified mainly according to the structures of the digestive tract (Fenaux 1993, 1998).”
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Self-citationCross-kingdom patterns of alternative splicing and splice recognition
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“However, the large effective population size (Dehal et al. 2002), broadcast-spawning nature and the relatively long free larval phase of 1–5 days compared with other tunicates (Carver et al. 2003) indicate that Ciona might have a high potential for natural dispersal.”
BackgroundA novel docking site on Mediator is critical for activation by VP16 in mammalian cells
Mittler, G., Stühler, T., Santolin, L., Uhlmann, T., Kremmer, E., Lottspeich, F., Berti, L., & Meisterernst, M. (2003) · The EMBO Journal · doi:10.1093/emboj/cdg619 · Cited by 154
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“Recent genome analyses of primitive eukaryotes, such as the sea squirt (Ciona intestinalis) [8] and single-celled parasitic diplomonads [9], implicate HGT events in early eukaryotic evolution.”
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The chordate amphioxus: an emerging model organism for developmental biology
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“Thus, most Ciona developmental regulatory factors are represented by a single ortholog, while in vertebrates there are often multiple paralogs with partially redundant functions (Dehal et al. 2002).”
BackgroundSelf-citationUrochordate βγ-Crystallin and the Evolutionary Origin of the Vertebrate Eye Lens
Shimeld, S. M., Purkiss, A. G., Dirks, R. P., Bateman, O. A., Slingsby, C., & Lubsen, N. H. (2005) · Current Biology · doi:10.1016/j.cub.2005.08.046 · Cited by 147
“A search of the genome [ 8 ]o fC. intestinalis for βγ-crystallin-like sequences identified one gene coding for a single domain protein with homology to vertebrate βγ-crystallins (for full details of methods, please see the Supplemental Data available with this article online).”
A functional cellulose synthase from ascidian epidermis
Matthysse, A. G., Deschet, K., Williams, M. L., Marry, M., White, A. R., & Smith, W. C. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0303623101 · Cited by 146
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“Although most studies have focused on larval structures, the development of the adult form is also very interesting in relation to tissues and organs of vertebrate body.”
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“Furthermore, a large set of genomic data was gathered in recent years, including assembled sequences of two small and compact annotated Ciona genomes [7, 8], more than 700,000 ESTs, and expression patterns for around 20% of predicted protein-coding genes [9, 10].”
Self-citationAlternative oxidase in animals: unique characteristics and taxonomic distribution
McDonald, A. E., Vanlerberghe, G. C., & Staples, J. F. (2009) · Journal of Experimental Biology · doi:10.1242/jeb.032151 · Cited by 143
Rothbächer, U., Bertrand, V., Lamy, C., & Lemaire, P. (2007) · Development · doi:10.1242/dev.010850 · Cited by 140
“Second, studies on the ascidian Ciona intestinalis have progressed at an impressive pace since the release of the draft sequence of its genome (Dehal et al., 2002), culminating recently in the first whole embryo draft zygotic gene regulatory network in a metazoan (Imai et al., 2006).”
BackgroundInfluentialSelf-citationSchlosser, G. (2005) · Journal of Experimental Zoology Part B Molecular and Developmental Evolution · doi:10.1002/jez.b.21055 · Cited by 140
Reschly, E. J., & Krasowski, M. D. (2006) · Current Drug Metabolism · doi:10.2174/138920006776873526 · Cited by 142
Ciona intestinalis: Chordate development made simple
Passamaneck, Y. J., & Gregorio, A. D. (2005) · Developmental Dynamics · doi:10.1002/dvdy.20300 · Cited by 140
“However, the C. intestinalis genome carries several genes involved in innate immunity, including Toll-like receptors, which have homologs in vertebrates, as well as in protostomes such as Drosophila (Dehal et al., 2002; Azumi et al., 2003).”
BackgroundInfluentialKasahara, M., Suzuki, T., & Pasquier, L. D. (2003) · Trends in Immunology · doi:10.1016/j.it.2003.11.005 · Cited by 139
Reconstruction of the ancestral metazoan genome reveals an increase in genomic novelty
Paps, J., & Holland, P. W. H. (2018) · Nature Communications · doi:10.1038/s41467-018-04136-5 · Cited by 140
Evolution of the Class 2 cytokines and receptors, and discovery of new friends and relatives
Krause, C. D., & Pestka, S. (2005) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2004.12.002 · Cited by 143
Ben‐Shlomo, I., Hsu, S. Y., Rauch, R., Kowalski, H. W., & Hsueh, A. J. W. (2003) · Science Signaling · doi:10.1126/stke.2003.187.re9 · Cited by 139
Diversity as opportunity: Insights from 600 million years of AHR evolution
Hahn, M. E., Karchner, S. I., & Merson, R. R. (2017) · Current Opinion in Toxicology · doi:10.1016/j.cotox.2017.02.003 · Cited by 134
“Predicted AHR homologs are found in genomes of the echinoderm Strongylocentrotus (sea urchin) [55,56], hemichordate Saccoglossus (acorn worm) [57], and invertebrate chordates such as the cephalochordate Branchiostoma (amphioxus) [58,59] and urochordate Ciona (sea squirt) [60].”
Alpha-kinases: analysis of the family and comparison with conventional protein kinases
Drennan, D., & Ryazanov, A. G. (2003) · Progress in Biophysics and Molecular Biology · doi:10.1016/s0079-6107(03)00060-9 · Cited by 134
New insights into the evolution of the relaxin–LGR signaling system
Hsu, S. Y. (2003) · Trends in Endocrinology and Metabolism · doi:10.1016/s1043-2760(03)00106-1 · Cited by 134
Presnell, J. S., Schnitzler, C. E., & Browne, W. E. (2015) · Genome Biology and Evolution · doi:10.1093/gbe/evv141 · Cited by 119
“org/Ciona_intestinalis/Info/Index Dehal et al. (2002)”
A genetic regulatory network for Xenopus mesendoderm formation
Loose, M., & Patient, R. K. (2004) · Developmental Biology · doi:10.1016/j.ydbio.2004.04.014 · Cited by 132
Prostaglandins in non-insectan invertebrates: recent insights and unsolved problems
Rowley, A. F., Vogan, C. L., Taylor, G. W., & Clare, A. S. (2004) · Journal of Experimental Biology · doi:10.1242/jeb.01275 · Cited by 133
Cole, A. G., & Meinertzhagen, I. A. (2004) · Developmental Biology · doi:10.1016/j.ydbio.2004.04.001 · Cited by 131
Self-citationKeay, J., & Thornton, J. W. (2008) · Endocrinology · doi:10.1210/en.2008-1338 · Cited by 130
The evolutionary origin of cardiac chambers
Simões-Costa, M., Vasconcelos, M., Sampaio, A. C., Cravo, R. M., Linhares, V. L., Hochgreb, T., Yan, C. Y. I., Davidson, B., & Xavier‐Neto, J. (2004) · Developmental Biology · doi:10.1016/j.ydbio.2004.09.026 · Cited by 129
“Thus, the urochordate pump, the vessels of amphioxus and the hearts of vertebrates are united in a lineage sharing genetic and morphogenetic mechanisms (Davidson and Levine, 2003; Dehal et al., 2002; Hirakow, 1985; Holland et al., 2003; Rahr, 1981).”
BackgroundSelf-citationAscidians and the Plasticity of the Chordate Developmental Program
Lemaire, P., Smith, W. C., & Nishida, H. (2008) · Current Biology · doi:10.1016/j.cub.2008.05.039 · Cited by 130
“In contrast to vertebrates, their genome is not duplicated and is remarkably compact, with an intergenic distance of only 5 kb on average [ 106 ].”
Self-citationMini-review: Impact and dynamics of surface fouling by solitary and compound ascidians
Aldred, N., & Clare, A. S. (2014) · Biofouling · doi:10.1080/08927014.2013.866653 · Cited by 128
“It also became one of the first higher organisms to have its genome fully sequenced (Dehal et al. 2002) and there now exists a considerable bioinformatics resource.”
Hamada, M., Shoguchi, E., Shinzato, C., Kawashima, T., Miller, D. J., & Satoh, N. (2012) · Molecular Biology and Evolution · doi:10.1093/molbev/mss213 · Cited by 128
“2000), the sea urchin Strongylocentrotus pupuratus (Sea Urchin Genome Sequencing Consortium 2006), the ascidian Ciona intestinalis (Dehal et al. 2002), the amphioxus Branchiostoma floridae (Putnam et al.”
BackgroundSelf-citationTassy, O., Dauga, D., Daian, F., Sobral, D., Robin, F., Khoueiry, P., Salgado, D., Fox, V., Caillol, D., Schiappa, R., et al. (2010) · Genome Research · doi:10.1101/gr.108175.110 · Cited by 128
“ANISEED defines a set of 20,631 Ciona intestinalis gene models obtained by clustering transcripts models predicted from JGI (Dehal et al. 2002), Ensembl (Hubbard et al.”
BackgroundMethodInfluentialSelf-citationEvolution of the Insect Yellow Gene Family
Ferguson, L. C., Green, J. E., Surridge, A. K., & Jiggins, C. D. (2010) · Molecular Biology and Evolution · doi:10.1093/molbev/msq192 · Cited by 131
“Blast searches were carried out against the predicted protein sets and genomes of Nematostella vectensis (Putnam et al. 2007), Ciona intestinalis (Dehal et al. 2002), Caenorhabditis briggsae (Stein et al. 2003), Schmidtea mediterranea (Robb et al. 2008), Lottia gigantean (JGI), and Capitella…”
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Self-citationOn the origins of the extracellular matrix in vertebrates
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“Within-species variation data in a genome-wide scale are required to disentangle these many influences, through the comparison of nonsynonymous (selected) versus synonymous (neutral) patterns of polymorphism and divergence, according to the McDonald and Kreitman (1991) approach (Keightley and…”
BackgroundAlbuixech-Crespo, B., López-Blanch, L., Burguera, D., Maeso, I., Sánchez‐Arrones, L., Moreno‐Bravo, J. A., Somorjai, I., Pascual‐Anaya, J., Puelles, E., Bovolenta, P., et al. (2017) · PLoS Biology · doi:10.1371/journal.pbio.2001573 · Cited by 124
Neurons of the ascidian larval nervous system in Ciona intestinalis: II. Peripheral nervous system
Imai, J. H., & Meinertzhagen, I. A. (2007) · The Journal of Comparative Neurology · doi:10.1002/cne.21247 · Cited by 124
Self-citationPrimitive complement system?recognition and activation
Fujita, T., Endo, Y., & Nonaka, M. (2004) · Molecular Immunology · doi:10.1016/j.molimm.2004.03.026 · Cited by 124
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Metadata
- Authors
- Dehal, P., Satou, Y., Campbell, R. K., Chapman, J., Degnan, B., De Tomaso, A., Davidson, B., Di Gregorio, A., Gelpke, M., Goodstein, D. M., Harafuji, N., Hastings, K. E. M., Ho, I., Hotta, K., Huang, W., Kawashima, T., Lemaire, P., Martinez, D., Meinertzhagen, I. A., Necula, S., Nonaka, M., Putnam, N., Rash, S., Saiga, H., Satake, M., Terry, A., Yamada, L., Wang, H.-G., Awazu, S., Azumi, K., Boore, J., Branno, M., Chin-bow, S., DeSantis, R., Doyle, S., Francino, P., Keys, D. N., Haga, S., Hayashi, H., Hino, K., Imai, K. S., Inaba, K., Kano, S., Kobayashi, K., Kobayashi, M., Lee, B.-I., Makabe, K. W., Manohar, C., Matassi, G., Medina, M., Mochizuki, Y., Mount, S., Morishita, T., Miura, S., Nakayama, A., Nishizaka, S., Nomoto, H., Ohta, F., Oishi, K., Rigoutsos, I., Sano, M., Sasaki, A., Sasakura, Y., Shoguchi, E., Shin-i, T., Spagnuolo, A., Stainier, D., Suzuki, M. M., Tassy, O., Takatori, N., Tokuoka, M., Yagi, K., Yoshizaki, F., Wada, S., Zhang, C., Hyatt, P. D., Larimer, F., Detter, C., Doggett, N., Glavina, T., Hawkins, T., Richardson, P., Lucas, S., Kohara, Y., Levine, M., Satoh, N., & Rokhsar, D. S.
- Affiliations
- Joint Genome Institute (US)
- Kyoto University (JP)
- Marine Biological Laboratory (US)
- The University of Queensland (AU)
- Department of Pathology, Stanford University School of Medicine, Stanford, CA 93950, USA.
- University of California, Berkeley (US)
- Department of Molecular and Cellular Biology, Division of Genetics, 401 Barker Hall, University of California, Berkeley, CA 94720, USA.
- McGill University (CA)
- National Institute of Genetics (JP)
- Institut de Biologie du Développement Marseille (FR)
- Dalhousie University (CA)
- The University of Tokyo (JP)
- U.S. Department of Energy Joint Genome Institute, 2800 Mitchell Drive, Walnut Creek, CA 94598, USA.
- Tokyo Metropolitan University (JP)
- Tohoku University (JP)
- Moffitt Cancer Center (US)
- Hokkaido University (JP)
- Stazione Zoologica Anton Dohrn (IT)
- IBM (United States) (US)
- University of Maryland, College Park, MD 20742, USA.
- National Institute of Genetics, Mishima 411-8540, Japan.
- Stazione Zoologica “Anton Dohrn,” Villa Comunale, 80121 Napoli, Italy.
- University of California, San Francisco (US)
- Wellcome Centre for Cell Biology (GB)
- Oak Ridge National Laboratory, Post Office Box 2008, Oak Ridge, TN 37831, USA.
- Oak Ridge National Laboratory (US)
- Los Alamos National Laboratory (US)
- Corresponding author
- Dehal, Paramvir
- Satou, Yutaka
- Kohara, Yuji
- Levine, Michael
- Satoh, Nori
- Rokhsar, Daniel S.
- ORCID
- Dehal, Paramvir
- Satou, Yutaka
- Degnan, Bernard
- Davidson, Brad
- Goodstein, David M.
- Harafuji, Naoe
- Hotta, Kohji
- Kawashima, Takeshi
- Lemaire, Patrick
- Martinez, Diego
- Meinertzhagen, Ian A.
- Saiga, Hidetoshi
- Terry, Astrid
- Wang, Hong-Gang
- Boore, Jeffrey
- Hino, Kyosuke
- Imai, Kaoru S.
- Inaba, Kazuo
- Kobayashi, Kenji
- Lee, Byung-In
- Manohar, Chitra
- Matassi, Giorgio
- Rigoutsos, Isidore
- Sasakura, Yasunori
- Shoguchi, Eiichi
- Stainier, Didier
- Suzuki, Miho M.
- Tassy, Olivier
- Tokuoka, Miki
- Doggett, Norman
- Kohara, Yuji
- Levine, Michael
- Rokhsar, Daniel S.
- Venue
- Science
- Published
- 2002-12-13
- Volume
- 298
- Issue
- 5601
- Pages
- 2157-2167
- ISSN
- 0036-8075 (ISSN-L)
- 1095-9203
- OpenAlex
- W2170258388
- Cited by
- 1,641
- References
- 81
- Citations by year
- 2026: 20 · 2025: 15 · 2024: 41 · 2023: 26 · 2022: 27 · 2021: 36 · 2020: 41 · 2019: 29 · 2018: 51 · 2017: 49 · 2016: 43 · 2015: 46 · 2014: 62 · 2013: 62 · 2012: 74
- FWCI
- 49.61
- Type
- journal article
- Language
- en
- Open access
- green
- hal.science
- Licence
- cc-by-nc
- Locations
- Science (publishedVersion)
- PubMed (publishedVersion)
- HAL AMU (submittedVersion, cc-by-nc)
- Tokyo Tech Research Repository (Tokyo Institute of Technology) (submittedVersion)
- Funders
- National Institutes of Health (5p01hd037105-20)
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (HD37105)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Phylogenetic Studies
- Life Sciences › Agricultural and Biological Sciences › Animal Science and Zoology › Marine Invertebrate Physiology and Ecology
- Keywords
- Ciona intestinalis, chordate evolution, vertebrate origin, gene family evolution, protein-coding genes, gene loss, developmental genes, Cambrian explosion
- MeSH terms
- Alleles, Animals, Base Sequence, Cellulose, Central Nervous System, Ciona intestinalis, Endocrine System, Genes, Genes, Homeobox, Multigene Family, Heart, Immunity, Molecular Sequence Data, Muscle Proteins, Phylogeny, Polymorphism, Genetic, Proteins, Sequence Homology, Nucleic Acid, Species Specificity, Thyroid Gland, Urochordata, Vertebrates, Genome, Apoptosis, Sequence Analysis, DNA, Gene Dosage, Computational Biology, Gene Duplication, Organizers, Embryonic
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