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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).”
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“intestinalis [24], a urochordate and one of the closest invertebrate relatives of vertebrates, provides a unique opportunity to gain insight into the complete set of sep-”
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“However, no homologue of the protein family was detected within the Plasmodium falciparum (Gardner et al. 2002) and Caenorhabditis elegans (Rachael et al. 1998) or within the whole genome shotgun data of Ciona intestinalis (Dehal et al. 2002).”
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Self-citationThe vertebrate connexin family
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O-GlcNAc modifications regulate cell survival and epiboly during zebrafish development
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MethodHaploMerger: Reconstructing allelic relationships for polymorphic diploid genome assembliesPreprint
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“intestinalis is identical to the value published in two earlier studies (Dehal et al. 2002; Kim et al. 2007).”
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“Ciona has a compact genome size of about 160 million base pairs and contains approximately 16,000 proteincoding genes [4].”
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Khalturin, K., Anton‐Erxleben, F., Sassmann, S., Wittlieb, J., Hemmrich, G., & Bosch, T. C. G. (2008) · PLoS Biology · doi:10.1371/journal.pbio.0060278 · Cited by 109
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Meinertzhagen, I. A., Lemaire, P., & Okamura, Y. (2004) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.27.070203.144255 · Cited by 106
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Sela, N., Kim, E., & Ast, G. (2010) · Genome biology · doi:10.1186/gb-2010-11-6-r59 · Cited by 104
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A genomewide survey of developmentally relevant genes in Ciona intestinalis
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“In the present study, we have examined the different kinds of cell junctions in an ascidian from a molecular perspective, using the completely determined genome sequence (Dehal et al. 2002) and a cDNA/EST database (Satou et al.”
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Identification of All-trans-Retinol:All-trans-13,14-dihydroretinol Saturase
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“The identification of a TRBP homolog in tunicates, the closest living invertebrate relative of vertebrates (32), and the presence of both TRBP and a related protein, PACT, in bony fishes suggests that the separation between TRBP and PACT occurred between invertebrates and vertebrates (Fig.”
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“elegans, Anopheles gambiae, Ciona intestinalis, Fugu rubripes, Mus musculus, and Rattus norvegicus were obtained from NCBI, ENSEMBL and species specific databases (Additional file 1) [53-58].”
Methodfester, a Candidate Allorecognition Receptor from a Primitive Chordate
Nyholm, S. V., Passegue, E. A., Ludington, W. B., Voskoboynik, A., Mitchel, K., Weissman, I. L., & Tomaso, A. W. D. (2006) · Immunity · doi:10.1016/j.immuni.2006.04.011 · Cited by 101
Similar Ratios of Introns to Intergenic Sequence across Animal Genomes
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“91 92 Genomic scaffolds and annotations for Ciona intestinalis [22], Branchiostoma floridae [23], Trichoplax ad93 herens [24], Capitella teleta [25], Lottia gigantea [25], Helobdella robusta [25], Saccoglossus kowalevskii [26], 94 Monosiga brevicollis [27], Emiliania huxleyi [28], and Volvox carteri [29] were download…”
MethodCo-evolution of steroidogenic and steroid-inactivating enzymes and adrenal and sex steroid receptors
Baker, M. E. (2004) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2003.11.007 · Cited by 97
The neuropeptide transcriptome of a model echinoderm, the sea urchin Strongylocentrotus purpuratus
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“Previous reports revealed that the numbers of Sox genes greatly varied in animals, namely five in the nematode (Caenorhabditis elegans) [26], seven in the calcareous sponge (Sycon ciliatum) [1], seven in the sea lamprey (Petromyzon marinus) [4], seven in the sea squirt (Ciona intestinalis) [27,28], eight in the fruit…”
BackgroundFunctional evolution of ADAMTS genes: Evidence from analyses of phylogeny and gene organization
Nicholson, A. C., Malik, S.-B., Logsdon, J. M., Jr., & Meir, E. G. V. (2005) · BMC Evolutionary Biology · doi:10.1186/1471-2148-5-11 · Cited by 103
“Sequences of ADAMTS homolog sequences presented here were identified from 2001 to 2004 using genomic sequences cataloged in the NCBI, JGI (Fugu and Ciona [52,70]) and Celera genome databases using BLASTp, BLASTn, BLASTx, tBLASTn and tBLASTx searches [71].”
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Chapter 7 Establishment of Hox Vertebral Identities in the Embryonic Spine Precursors
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“In contrast, flies or ascidians, in which the Hox cluster is broken into several pieces, do not show temporal colinearity and form their axis and segments in a highly derived fashion (Dehal et al., 2002; Duboule, 2007; Seo et al., 2004).”
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“intestinalis (14) made it possible to perform a genome-wide search for the possible complement component genes in silico.”
BackgroundSelf-citationKinomer v. 1.0: a database of systematically classified eukaryotic protein kinases
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BackgroundComparative genomics and evolution of eukaryotic phospholipid biosynthesis
Lykidis, A. (2007) · Progress in Lipid Research · doi:10.1016/j.plipres.2007.03.003 · Cited by 103
Barbosa‐Morais, N. L., Carmo‐Fonseca, M., & Aparicio, S. A. J. R. (2005) · Genome Research · doi:10.1101/gr.3936206 · Cited by 100
“…sequencing and annotation of the genomes of the Japanese puffer fish, Fugu rubripes (Aparicio et al. 2002), and the sea squirt, Ciona intestinalis (Dehal et al. 2002), allows us now to fill that gap with fiducial branches of distant vertebrates and chordates, respectively, providing an…”
BackgroundIkuta, T., & Saiga, H. (2007) · Developmental Biology · doi:10.1016/j.ydbio.2007.10.005 · Cited by 97
Self-citationZhang, S., & Loker, E. S. (2004) · Gene · doi:10.1016/j.gene.2004.07.003 · Cited by 97
Hudson, C., Lotito, S., & Yasuo, H. (2007) · Development · doi:10.1242/dev.002352 · Cited by 97
“The recent surge in interest in the Ciona model has resulted in the availability of the draft genome (Dehal et al., 2002), extensive EST collections (Satou et al.”
BackgroundDomain shuffling and the evolution of vertebratesPreprint
Kawashima, T., Kawashima, S., Tanaka, C., Murai, M., Yoneda, M., Putnam, N. H., Rokhsar, D. S., Kanehisa, M., Satoh, N., & Wada, H. (2009) · Genome Research · doi:10.1101/gr.087072.108 · Cited by 102
“The complete amphioxus genome sequence provides sufficient deuterostome genomic sequences (Dehal et al. 2002; Sea Urchin Genome Sequencing Consortium 2006; Putnam et al. 2008) to map the domain shuffling events accurately.”
BackgroundSelf-citationA genomewide survey of developmentally relevant genes in Ciona intestinalis
Hino, K., Satou, Y., Yagi, K., & Satoh, N. (2003) · Development Genes and Evolution · doi:10.1007/s00427-003-0318-8 · Cited by 96
“Since the Ciona intestinalis genome contains a basic set of genes to make a chordate body plan with less redundancy (Dehal et al. 2002), it will provide an ideal system for studying the molecular mechanisms of these signaling pathways.”
BackgroundSelf-citationLischer, H. E. L., Excoffier, L., & Heckel, G. (2013) · Molecular Biology and Evolution · doi:10.1093/molbev/mst271 · Cited by 93
“However, the number of heterozygous positions can be large as in M. arvalis here and in other taxa (Griffiths et al. 2000; Dehal et al. 2002; Sota and Vogler 2003; Kelleher et al. 2007; Fink et al. 2010).”
BackgroundOkamura, Y., Nishino, A., Murata, Y., Nakajo, K., Iwasaki, H., Ohtsuka, Y., Tanaka‐Kunishima, M., Takahashi, N., Hara, Y., Yoshida, T., et al. (2005) · Physiological Genomics · doi:10.1152/physiolgenomics.00229.2004 · Cited by 102
“Ciona moreover lacks the gene for Nav -subunits, which induce clustering of Nav channels at the initial segment and node of Ranvier of myelinated neurons, consistent with the fact that myelination does not occur in the ascidian nervous system (30) and that there is no myelinrelated gene in the Ciona genome (11).”
BackgroundResultInfluentialSelf-citationGenealogical relationships within and among shallow-water Ciona species (Ascidiacea)
Nydam, M. L., & Harrison, R. G. (2007) · Marine Biology · doi:10.1007/s00227-007-0617-0 · Cited by 94
“Recently, the genome sequences of C. intestinalis and C. savignyi have become available (Dehal et al. 2002; Vinson et al. 2005), providing tools for comparative genomics and insights into vertebrate evolution (BoVelli et al. 2004; Johnson et al. 2004; Missal et al. 2005).”
BackgroundEvidence for the presence of a cellulase gene in the last common ancestor of bilaterian animals
Lo, N. C., Watanabe, H., & Sugimura, M. (2003) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rsbl.2003.0016 · Cited by 96
“The nature of this organism is the subject of continuing debate (reviewed in Erwin & Davidson 2002), though one possibility is that it was some kind of marine filter feeder.”
BackgroundThe Ciona intestinalis genome: When the constraints are off
Holland, L. Z., & Gibson‐Brown, J. J. (2003) · BioEssays · doi:10.1002/bies.10302 · Cited by 94
Kimura, T., Jindo, T., Narita, T., Naruse, K., Kobayashi, D., Shin‐I, T., Kitagawa, T., Sakaguchi, T. F., Mitani, H., Shima, A., et al. (2004) · Mechanisms of Development · doi:10.1016/j.mod.2004.03.033 · Cited by 94
Self-citationIsolation and primary structure of a cellulase from the Japanese sea urchin Strongylocentrotus nudus
Nishida, Y., Suzuki, K., Kumagai, Y., Tanaka, H., Inoue, A., & Ojima, T. (2007) · Biochimie · doi:10.1016/j.biochi.2007.03.015 · Cited by 93
Polymorphism and divergence within the ascidian genus Ciona
Nydam, M. L., & Harrison, R. G. (2010) · Molecular Phylogenetics and Evolution · doi:10.1016/j.ympev.2010.03.042 · Cited by 92
Evolution of the complement system
Nonaka, M. I. (2003) · Molecular Immunology · doi:10.1016/j.molimm.2003.10.009 · Cited by 92
Self-citationGenome-scale evidence of the nematode-arthropod clade
Dopazo, H., & Dopazo, J. (2005) · Genome biology · doi:10.1186/gb-2005-6-5-r41 · Cited by 94
“Materials and methods Dataset collection Complete genome sequences from Plasmodium falciparum [41], Arabidopsis thaliana [42], Oryza sativa [43], Saccharomyces cerevisae [44], Caenorhabditis elegans [45], Anopheles gambiae [46], Drosophila melanogaster [47], Ciona intestinalis [48], Fugu rubripes [49], Mus musculus [5…”
Evidence for a Diverse Cys-Loop Ligand-Gated Ion Channel Superfamily in Early Bilateria
Dent, J. A. (2006) · Journal of Molecular Evolution · doi:10.1007/s00239-005-0018-2 · Cited by 93
“intestinalis (Dehal et al. 2002), the nematode C.”
BackgroundPhylogenetic Analysis of the Plant Endo-�-1,4-Glucanase Gene Family
Libertini, E., Li, Y., & McQueen‐Mason, S. J. (2004) · Journal of Molecular Evolution · doi:10.1007/s00239-003-2571-x · Cited by 92
“Because ascidians are the only animals known to make cellulose, Dehal et al. (2002) suggested that the genes involved in the metabolism of cellulose in Ciona might be a lineage-specific innovation.”
BackgroundLeafing through the genomes of our major crop plants: strategies for capturing unique information
Paterson, A. H. (2006) · Nature Reviews Genetics · doi:10.1038/nrg1806 · Cited by 93
Chambon, J., Nakayama, A., Takamura, K., McDougall, A., & Satoh, N. (2007) · Development · doi:10.1242/dev.002220 · Cited by 91
“The gene features were searched against the C. intestinalis draft genome sequence (Dehal et al., 2002) to obtain information about corresponding genes.”
BackgroundMethodInfluentialSelf-citationHas the yo‐yo stopped? An assessment of human protein‐coding gene number
Southan, C. (2004) · PROTEOMICS · doi:10.1002/pmic.200300700 · Cited by 90
The history of a developmental stage: Metamorphosis in chordates
Paris, M., & Laudet, V. (2008) · genesis · doi:10.1002/dvg.20443 · Cited by 90
“Facultative neoteny has been attributed especially to low levels of circulating THs due to weak activation of the thyroid axis by the pituitary gland, when the rest of TH signaling pathway is ‘‘normally’’ functional (Boorse and Denver, 2002; Safi et al., 2004).”
Integrin evolution: Insights from ascidian and teleost fish genomes
Huhtala, M. T., Heino, J., Casciari, D., de Luise, A., & Johnson, M. S. (2005) · Matrix Biology · doi:10.1016/j.matbio.2005.01.003 · Cited by 85
Isolation and expression pattern of three mouse homologues of chick Rgm
Schmidtmer, J., & Engelkamp, D. (2003) · Gene Expression Patterns · doi:10.1016/s1567-133x(03)00144-3 · Cited by 89
Presence of Sex Steroids and Cytochrome P450 Genes in Amphioxus
Mizuta, T., & Kubokawa, K. (2007) · Endocrinology · doi:10.1210/en.2007-0109 · Cited by 88
Early Evolution of Conserved Regulatory Sequences Associated with Development in Vertebrates
McEwen, G. K., Goode, D. K., Parker, H. J., Woolfe, A., Callaway, H., & Elgar, G. (2009) · PLoS Genetics · doi:10.1371/journal.pgen.1000762 · Cited by 86
“However, analyses suggest that urochordates are evolving very rapidly [6,8,9] which may have resulted in loss of CNE-like sequences in this lineage.”
BackgroundAlverson, A. J., & Kolnick, L. (2005) · Journal of Phycology · doi:10.1111/j.1529-8817.2005.00136.x · Cited by 88
“This value is comparable with allelic polymorphism levels inferred from wholegenome sequencing projects of a teleost fish (0.4%, Aparicio et al. 2002), a sea squirt (1.2%, Dehal et al. 2002), and the closely related diatom Thalassiosira pseudonana Hasle & Heimdal (0.75%, Armbrust et al. 2004).”
BackgroundInfluentialGlutamatergic networks in the Ciona intestinalis larva
Horie, T., Kusakabe, T. G., & Tsuda, M. (2008) · The Journal of Comparative Neurology · doi:10.1002/cne.21678 · Cited by 87
“Isolation and characterization of Ci-vGLUT cDNA The gene encoding vesicular glutamate transporter (Ci-VGLUT) was found in the C. intestinalis genome database (Dehal et al., 2002) by TBLASTN searches using amino acid sequences of mammalian vesicular glutamate transporter as queries.”
BackgroundMethodInfluentialCFGP: a web-based, comparative fungal genomics platform
Park, J., Park, J., Jung, K., Jang, S., Yu, K., Choi, J., Kong, S., Park, J., Kim, S., Kim, H.-Y., et al. (2007) · Nucleic Acids Research · doi:10.1093/nar/gkm758 · Cited by 88
Independent Hox‐cluster duplications in lampreys
Claudia Fried, A., Prohaska, S. J., & Stadler, P. F. (2003) · Journal of Experimental Zoology Part B Molecular and Developmental Evolution · doi:10.1002/jez.b.37 · Cited by 88
Lai, A. G., & Aboobaker, A. A. (2017) · Developmental Biology · doi:10.1016/j.ydbio.2017.10.010 · Cited by 84
“With the availability of a complete draft genome (Dehal et al. 2002), transgenesis techniques (Awazu et al.”
BackgroundHox genes are not always Colinear
Monteiro, A. S., & Ferrier, D. E. K. (2006) · International Journal of Biological Sciences · doi:10.7150/ijbs.2.95 · Cited by 86
“between them that contain many non-Hox genes [48, 50].”
BackgroundWhole body regeneration in a colonial ascidian, Botrylloides violaceus
Brown, F. D., Keeling, E. L., Le, A. D., & Swalla, B. J. (2009) · Journal of Experimental Zoology Part B Molecular and Developmental Evolution · doi:10.1002/jez.b.21303 · Cited by 87
Paris, M., Pettersson, K., Schubert, M., Bertrand, S., Pongratz, I., Escrivá, H., & Laudet, V. (2008) · BMC Evolutionary Biology · doi:10.1186/1471-2148-8-219 · Cited by 87
“There is no ER in the sequenced genome of Ciona intestinalis [33] or in the sea urchin [34], one ER was previously cloned in lamprey [8], only one ER was found in the amphioxus genome [35].”
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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