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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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“While EGF signalling might play a similar role in Ciona metamorphosis (Nakayama et al., 2001), the gene encoding the putative EGF protein, Ci-meta1, does not appear to be a homologue of Hemps (Dehal et al., 2002).”
InfluentialSelf-citationGriggio, F., Voskoboynik, A., Iannelli, F., Justy, F., Tilak, M., Turón, X., Pesole, G., Douzery, E., Mastrototaro, F., & Gissi, C. (2014) · Genome Biology and Evolution · doi:10.1093/gbe/evu041 · Cited by 51
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“This change resulted in the establishment of several genome-sequencing projects, expanding the activities that were mainly focused on reference model species for marine biology, such as Ciona robusta or Strongylocentrotus purpuratus [78,79], to other species, with the release of many draft genomes obtained from the se…”
BackgroundAncient Origin of the Complement System: Emerging Invertebrate Models
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Community annotation: Procedures, protocols, and supporting tools: Table 1.Preprint
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“html) (Dehal et al., 2002) showed that the XPA16474 sequence straddles two closely neighboring gene models, ci0100137797 and ci0100137819, on chromosome 9q (Shoguchi et al.”
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Kusakabe, T. G., Yoshida, R., Ikeda, Y., & Tsuda, M. (2004) · Developmental Biology · doi:10.1016/j.ydbio.2004.09.037 · Cited by 49
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“(2004) 46 , 163–180 Tracing cell fate in brain formation during embryogenesis of the ascidian Halocynthia roretzi”
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Self-citationParalogous Vitamin D Receptors in Teleosts: Transition of Nuclear Receptor Function
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“the ascidian, Ciona intestinalis (33), revealed that this protochor-”
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Acquisition of Retinoic Acid Signaling Pathway and Innovation of the Chordate Body Plan
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Self-citationMetaphylogeny of 82 gene families sheds a new light on chordate evolution
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“intestinalis was published in 2002 by the international genome sequencing project (6).”
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“In contrast to the homogeneous distribution of GC-content with sharp peaks in non-amniotic species, such as the tiger pufferfish (Fugu rubripes) and the tunicate (Ciona intestinalis) (Aparicio et al. 2002; Dehal et al. 2002), amniotes, such as human and chicken, show intra-genome GC heterogeneity; however, GC-content…”
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“The Ciona intestinalis genome is extremely small at ∼160 Mb and it diverged before the major genome duplications in the vertebrates (Dehal et al., 2002; Satoh, 2013).”
BackgroundThe regulation of oocyte maturation and ovulation in the closest sister group of vertebrates
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“This is also consistent with the complete absence of major steroidogenesis genes in the Ciona genome (Dehal et al., 2002).”
ResultChopra, S. S., Watanabe, H., Zhong, T. P., & Roden, D. M. (2007) · BMC Evolutionary Biology · doi:10.1186/1471-2148-7-113 · Cited by 49
Hypervariable and Highly Divergent Intron?Exon Organizations in the Chordate Oikopleura dioica
Edvardsen, R. B., Lerat, E., Maeland, A. D., Fl�t, M., Tewari, R., Jensen, M. F., Lehrach, H. R., Reinhardt, R., Seo, H., & Chourrout, D. M. (2004) · Journal of Molecular Evolution · doi:10.1007/s00239-004-2636-5 · Cited by 45
Cell type and function of neurons in the ascidian nervous system
Horie, T., Nakagawa, M., Sasakura, Y., & Kusakabe, T. G. (2009) · Development Growth & Differentiation · doi:10.1111/j.1440-169x.2009.01105.x · Cited by 44
Self-citationLi, G., Shu, Z., & Wang, Y. (2013) · PLoS ONE · doi:10.1371/journal.pone.0075461 · Cited by 44
Peitsaro, N., Polianskyte-Prause, Z., Tuimala, J., Pörn-Ares, I., Liobikas, J., Speer, O., Lindholm, D., Thompson, J. S., & Eriksson, O. (2008) · BMC Evolutionary Biology · doi:10.1186/1471-2148-8-26 · Cited by 43
“Ciona intestinalis ENSCING00000006798 Ensembl LACTB [50]”
How much does the amphioxus genome represent the ancestor of chordates?
Louis, A., Crollius, H. R., & Robinson‐Rechavi, M. (2012) · Briefings in Functional Genomics · doi:10.1093/bfgp/els003 · Cited by 45
“potentially useful to reconstruct the chordate ancestor: Ciona [10, 11], sea urchin [12] and Oikopleura”
BackgroundHamilton, B. A. (2003) · Genomics · doi:10.1016/j.ygeno.2003.09.016 · Cited by 44
Scheibye-Alsing, K., Hoffmann, S., Frankel, A., Jensen, P., Stadler, P. F., Mang, Y., Tommerup, N., Gilchrist, M. J., Nygård, A.-B., Cirera, S., et al. (2008) · Computational Biology and Chemistry · doi:10.1016/j.compbiolchem.2008.11.003 · Cited by 46
“…part of AMOS) [45] [46] and GigAssembler [39], both applied to human genome data sets; the JAZZ-assembler, which was applied to both the genome of Takifugu rubripes (the pufferfish) [47] and Ciona intestinalis [48]; and the ARACHNE [49] and Phusion [50] assemblers, both applied to the mouse genome.”
MethodToxicity of nanoplastics during the embryogenesis of the ascidian Ciona robusta (Phylum Chordata)
Eliso, M. C., Bergami, E., Manfra, L., Spagnuolo, A., & Corsi, I. (2020) · Nanotoxicology · doi:10.1080/17435390.2020.1838650 · Cited by 44
Self-citationNew Insights into Alternative Mechanisms of Immune Receptor Diversification
Litman, G. W., Cannon, J. P., & Rast, J. P. (2005) · Advances in immunology · doi:10.1016/s0065-2776(05)87006-3 · Cited by 44
Culture of Adult Ascidians and Ascidian Genetics
Hendrickson, C., Christiaen, L., Deschet, K., Jiang, D., Joly, J., Legendre, L., Nakatani, Y., Tresser, J., & Smith, W. C. (2004) · Methods in cell biology · doi:10.1016/s0091-679x(04)74007-8 · Cited by 44
Nodal regulates neural tube formation in the Ciona intestinalis embryo
Mita, K., & Fujiwara, S. (2007) · Development Genes and Evolution · doi:10.1007/s00427-007-0168-x · Cited by 44
Exclusion of repetitive DNA elements from gnathostome Hox clusters
Claudia Fried, A., Prohaska, S. J., & Stadler, P. F. (2004) · Journal of Experimental Zoology Part B Molecular and Developmental Evolution · doi:10.1002/jez.b.20007 · Cited by 44
Evolution and divergence of the genes for cytoplasmic, mitochondrial, and flagellar creatine kinases
Suzuki, T., Mizuta, C., Uda, K., Ishida, K., Mizuta, K., Sona, S., Compaan, D. M., & Ellington, W. R. (2004) · Journal of Molecular Evolution · doi:10.1007/s00239-004-2615-x · Cited by 43
“Analysis of Ciona intestinalis Genomic Data Very recently, a complete genomic sequence has been reported for the tunicate Ciona intestinalis (Dehal et al. 2002) and EST analyses have also become available at a Web site (http://ghost.zool.kyotou.ac.jp/indexr1.html).”
BackgroundCellulose synthesizing terminal complexes in the ascidians
Kimura, S., & Itoh, T. (2004) · Cellulose · doi:10.1023/b:cell.0000046414.72903.33 · Cited by 43
Proteomic profiles of embryonic development in the ascidian Ciona intestinalis
Nomura, M., Nakajima, A., & Inaba, K. (2008) · Developmental Biology · doi:10.1016/j.ydbio.2008.10.038 · Cited by 43
Self-citationPu, C., & Zhan, A. (2017) · Biological Invasions · doi:10.1007/s10530-017-1409-1 · Cited by 43
Blanchoud, S., Rutherford, K., Zondag, L., Gemmell, N. J., & Wilson, M. J. (2018) · Scientific Reports · doi:10.1038/s41598-018-23749-w · Cited by 42
Vertebrate Cranial Placodes as Evolutionary Innovations—The Ancestor's Tale
Schlosser, G. (2015) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/bs.ctdb.2014.11.008 · Cited by 45
Bassham, S., Cañestro, C., & Postlethwait, J. H. (2008) · BMC Biology · doi:10.1186/1741-7007-6-35 · Cited by 44
“As gene duplication is pervasive [31,32], non-vertebrate chordates sometimes have genes that duplicated independently in the cephalochordate [33-35] or urochordate lineages [35-41].”
Hung, C., & Li, C. (2004) · Gene · doi:10.1016/j.gene.2004.07.039 · Cited by 43
LRRCE: a leucine-rich repeat cysteine capping motif unique to the chordate lineage
Park, H., Huxley‐Jones, J., Boot-Handford, R., Bishop, P. N., Attwood, T. K., & Bella, J. (2008) · BMC Genomics · doi:10.1186/1471-2164-9-599 · Cited by 42
“The short model was part of the first draft for the Ciona intestinalis genome [55] (JGI assembly version 1.”
MethodHozumi, A., Kawai, N., Yoshida, R., Ogura, Y., Ohta, N., Satake, H., Satoh, N., & Sasakura, Y. (2010) · Developmental Dynamics · doi:10.1002/dvdy.22254 · Cited by 42
Self-citationDeyts, C., Casañe, D., Vernier, P., Bourrat, F., & Joly, J. (2006) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2006.05073.x · Cited by 42
“The entire genomes of two ascidian species (Ciona intestinalis and Ciona savignyi) have recently been sequenced (Dehal et al., 2002; Vinson et al., 2005).”
BackgroundMethodInfluentialHow do spermatozoa activate oocytes?
Dale, B., Wilding, M., Coppola, G., & Tosti, E. (2010) · Reproductive BioMedicine Online · doi:10.1016/j.rbmo.2010.02.015 · Cited by 42
“The recent sequencing of the genome in the sea urchin and ascidian (see Davidson (2006), Dehal et al. (2002)) means that these invertebrate oocytes, long-time protagonists of cell physiology, may now be used for a range of molecular biology experiments.”
BackgroundCastellano, I., Ercolesi, E., & Palumbo, A. (2014) · PLoS ONE · doi:10.1371/journal.pone.0102907 · Cited by 42
“the ascidian tadpole, the rapid rate of development, the availability of genome sequence [6] and the extensive in situ gene expression”
BackgroundBiological Functions of the Novel Collectins CL-L1, CL-K1, and CL-P1
Ohtani, K., Suzuki, Y., & Wakamiya, N. (2012) · BioMed Research International · doi:10.1155/2012/493945 · Cited by 42
“Very recently, the entire genomes of amphioxus and urochordates have revealed that amphioxus have 66 collectin model genes and urochordates have 9 genes, whereas humans retain only 6 [42, 43].”
BackgroundGermline transgenesis and insertional mutagenesis in the ascidian Ciona intestinalis
Sasakura, Y. (2007) · Developmental Dynamics · doi:10.1002/dvdy.21111 · Cited by 42
Self-citationBonchuk, A. N., Kamalyan, S., Mariasina, S. S., Boyko, K. M., Popov, V. O., Maksimenko, O. G., & Georgiev, P. G. (2020) · Scientific Reports · doi:10.1038/s41598-020-59459-5 · Cited by 42
Time course for tail regression during metamorphosis of the ascidian Ciona intestinalis
Matsunobu, S., & Sasakura, Y. (2015) · Developmental Biology · doi:10.1016/j.ydbio.2015.06.016 · Cited by 42
Self-citationMaternal factor-mediated epigenetic gene silencing in the ascidian Ciona intestinalis
Sasakura, Y., Suzuki, M. M., Hozumi, A., Inaba, K., & Satoh, N. (2009) · Molecular Genetics and Genomics · doi:10.1007/s00438-009-0500-4 · Cited by 42
Self-citation
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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