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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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“At the top is a depiction of a gene model predicted in the previous study (Dehal et al. 2002) in terms of intron (dashed lines) and exon (black boxes) structures.”
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“…Voluminous data including hundreds of thousands of ESTs and the whole genome sequences were published, which are free for use in academic research (Dehal et al., 2002; Satoh et al., 2003); (2) The body of C. intestinalis is transparent regardless of its size and the embryos develop quickly; the…”
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The Lancelet and Ammocoete Mouths
Yasui, K., & Kaji, T. (2008) · ZOOLOGICAL SCIENCE · doi:10.2108/zsj.25.1012 · Cited by 21
“As to why ascidian phylogeny changes radically among analyses, we may consider the genomic compaction and rapid modification of the mitochondrial and nuclear genomes in urochordates (Seo et al., 2001; Dehal et al., 2002; Winchell et al., 2002).”
An introgression breakthrough left by an anthropogenic contact between two ascidians
Moan, A. L., Roby, C., Fraïssé, C., Daguin‐Thiébaut, C., Bierne, N., & Viard, F. (2021) · Molecular Ecology · doi:10.1111/mec.16189 · Cited by 23
Gibbons, T., Mount, S. M., Cooper, E. D., & Delwiche, C. F. (2015) · BMC Bioinformatics · doi:10.1186/s12859-015-0625-x · Cited by 21
“The addition of sequences from four other eukaryotes (Anopheles gambiae [23], Ciona intestinalis [24], Chlamydomonas reinhardtii [25], and Toxoplasma gondii [26]), for which the CEGMA developers have provided annotations, led to a test data set we refer to as the Expanded CEGMA KOGs (ECK) database.”
MethodSelf-citationRichter, I., & Fidler, A. E. (2014) · Toxicon · doi:10.1016/j.toxicon.2014.12.011 · Cited by 21
Tissue-Specific Profile of DNA Replication in the Swimming Larvae of Ciona intestinalis
Nakayama, A., Satoh, N., & Sasakura, Y. (2005) · ZOOLOGICAL SCIENCE · doi:10.2108/zsj.22.301 · Cited by 21
“In Ciona intestinalis , the draft genome sequences have been determined (Dehal et al ., 2002), a large EST/cDNA database is available (Satou et al ., 2002), and many genes including genes regulating the cell cycle are annotated (e. g. Kawashima et al ., 2003; Sasakura et al ., 2003c, d; Satou and…”
BackgroundSelf-citationHahn, M. E., Merson, R. R., & Karchner, S. I. (2005) · Biochemistry and molecular biology of fishes · doi:10.1016/s1873-0140(05)80010-4 · Cited by 21
Nitta, K. R., Vincentelli, R., Jacox, E. H., Cimino, A., Ohtsuka, Y., Sobral, D., Satou, Y., Cambillau, C., & Lemaire, P. (2019) · Methods in molecular biology · doi:10.1007/978-1-4939-9624-7_23 · Cited by 21
Self-citationBlock, W. D., & Lees‐Miller, S. P. (2005) · DNA repair · doi:10.1016/j.dnarep.2005.06.008 · Cited by 20
Sea squirts and immune tolerance
Tomaso, A. W. D. (2009) · Disease Models & Mechanisms · doi:10.1242/dmm.001156 · Cited by 22
A word-oriented approach to alignment validation
Beiko, R. G., Chan, C. X., & Ragan, M. A. (2005) · Computer applications in the biosciences · doi:10.1093/bioinformatics/bti335 · Cited by 21
A genomic overview of short genetic variations in a basal chordate, Ciona intestinalis
Satou, Y., Shin‐I, T., Kohara, Y., Satoh, N., & Chiba, S. (2012) · BMC Genomics · doi:10.1186/1471-2164-13-208 · Cited by 21
“Of these ESTs, 73% are derived from animals sampled from Onagawa, Miyagi, Japan, where we sampled the animals for generating the JP dataset.”
BackgroundMethodInfluentialSelf-citationFrom so simple a beginning – what amphioxus can teach us about placode evolution
Schlosser, G. (2017) · The International Journal of Developmental Biology · doi:10.1387/ijdb.170127gs · Cited by 20
“…none of the neuropeptides produced by the vertebrate adenohypophysis (MSH, ACTH) was found in either the amphioxus, ascidian or any other invertebrate genomes suggesting that these are vertebrate innovations (Campbell et al., 2004, Dehal et al., 2002, Holland et al., 2008, Putnam et al., 2008).”
BackgroundEcological Review of the Ciona Species Complex
Wilson, E. R., Murphy, K. J., & Wyeth, R. C. (2022) · Biological Bulletin · doi:10.1086/719476 · Cited by 20
“…the sequencing and manipulation of the genome of each Ciona spp. have shed light on the genetics behind the development and adaptations of the species and other chordates (Simmen and Bird, 2000; Dehal et al., 2002; Satoh, 2003; Nydam and Harrison, 2007; Silva and Smith, 2008; Ni et al., 2018).”
BackgroundCiliary photoreceptors in sea urchin larvae indicate pan-deuterostome cell type conservation
Valencia, J. E., Feuda, R., Mellott, D. O., Burke, R. D., & Peter, I. S. (2021) · BMC Biology · doi:10.1186/s12915-021-01194-y · Cited by 21
Mechanisms of Sperm–Egg Interactions: What Ascidian Fertilization Research Has Taught Us
Sawada, H., & Saitô, T. (2022) · Cells · doi:10.3390/cells11132096 · Cited by 20
“On the other hand, the N-terminal sequence of the 25-kDa CUB1-interacting protein was found at the upstream region of the cDNA of the CT and was identified as a penultimate C-terminal fragment of vitellogenin (Figure 4), referred to as the von Willebrand factor D (vWF-D) region [13].”
BackgroundEliso, M. C., Bergami, E., Bonciani, L., Riccio, R., Belli, G., Belli, M., Corsi, I., & Spagnuolo, A. (2022) · Environmental Pollution · doi:10.1016/j.envpol.2022.120892 · Cited by 20
Self-citationNatural Variation of Model Mutant Phenotypes in Ciona intestinalis
Sordino, P., Andreakis, N., Brown, E. R., Leccia, N. I., Squarzoni, P., Tarallo, R., Alfano, C., Caputi, L., D’Ambrosio, P., Daniele, P., et al. (2008) · PLoS ONE · doi:10.1371/journal.pone.0002344 · Cited by 20
Self-citationOren, M., Douek, J., Fishelson, Z., & Rinkevich, B. (2007) · Developmental & Comparative Immunology · doi:10.1016/j.dci.2006.12.009 · Cited by 20
“This is further supported by the availability of improved research tools, such as the publication of the draft genome from the solitary ascidian Ciona intestinalis [4].”
BackgroundCha, I. S., del Castillo, C. S., Nho, S. W., Hikima, J.-I., Aoki, T., & Jung, T. S. (2011) · Developmental & Comparative Immunology · doi:10.1016/j.dci.2011.01.011 · Cited by 20
Bauermeister, A., Branco, P. C., Furtado, L. C., Jimenez, P. C., Costa-Lotufo, L. V., & Lotufo, T. M. D. C. (2018) · Drug Discovery Today Disease Models · doi:10.1016/j.ddmod.2019.08.008 · Cited by 20
Rosental, B., Raveh, T., Voskoboynik, A., & Weissman, I. L. (2020) · Current Opinion in Immunology · doi:10.1016/j.coi.2019.12.006 · Cited by 19
Mita, K., Kawai, N., Rueckert, S., & Sasakura, Y. (2012) · Diseases of Aquatic Organisms · doi:10.3354/dao02534 · Cited by 20
“In 2002, the draft genome of this species was determined with about 160 mega base pairs (Mbp) per haploid, encoding 15 852 protein-coding genes (Dehal et al. 2002).”
BackgroundSelf-citationStudy of Cis-regulatory Elements in the Ascidian Ciona intestinalis
Irvine, S. Q. (2013) · Current Genomics · doi:10.2174/138920213804999192 · Cited by 19
“The high allelic variation makes genome assembly a difficult task [4, 15].”
BackgroundBartl, S., Miracle, A. L., Rumfelt, L. L., Kepler, T. B., Mochon, E., Litman, G. W., & Flajnik, M. F. (2003) · Immunogenetics · doi:10.1007/s00251-003-0608-3 · Cited by 21
“The combined activities of the RAG proteins and TdT in lymphocyte development result in such high diversity of receptors that only rarely do two B or T cells with Nregion addition have the same receptor on their surfaces (Alt et al. 1992; Chen and Alt 1993; Davis 1990; Lieber et al. 1994; Matis 1988).”
Background
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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