Abstract
ABSTRACT The notochord and dorsal ectoderm induce dorsoventral compartmentalization of the vertebrate neural tube through the differential regulation of genes such as HNF-3 β, Pax3, Pax6 and snail. Here we analyze the expression of HNF-3 β and snail homologues in the ascidian, Ciona intestinalis, a member of the subphylum Urochordata, the earliest branch in the chordate phylum. A combination of in situ hybridization and promoter fusion analyses was used to demonstrate that the Ciona HNF-3 β homologue is expressed in the ventralmost ependymal cells of the neural tube, while the Ciona snail homologue is expressed at the junction between the invaginating neuroepithelium and dorsal ectoderm, similar to the patterns seen in vertebrates. These findings provide evidence that dorsoventral compartmentalization of the chordate neural tube is not an innovation of the vertebrates. We propose that precursors of the floor plate and neural crest were present in a common ancestor of both vertebrates and ascidians.
References
63
Referenced
167
10.1242/dev.111.4.983
/ Development / The snail gene required for mesoderm formation in Drosophila is expressed dynamically in derivatives of all three germ layers by Alberga (1991)10.1016/0092-8674(94)90522-3
/ Cell / HNF-3 β is essential for node and notochord formation in mouse development by Ang (1994)10.1016/S0074-7696(08)60383-6
/ Int. Rev. Cytol / Genetics, development, and malignancy of melanocytes by Bennett (1993){'volume-title': 'The Origin of the Vertebrates', 'year': '1955', 'author': 'Berrill', 'key': '2025021403420347100_DEVELOP_124_12_2335C4'}
/ The Origin of the Vertebrates by Berrill (1955)10.1038/330395a0
/ Nature / The Drosophila developmental gene snail encodes a protein with nucleic acid binding fingers by Boulay (1987)10.1016/0092-8674(78)90044-2
/ Cell / The single copy DNA sequence polymorphism of the sea urchin Strongylocentrotus purpuratus by Britten (1978){'key': '2025021403420347100_DEVELOP_124_12_2335C7', 'first-page': '111', 'article-title': 'Development of the ascidian notochord', 'volume': '7', 'author': 'Cloney', 'year': '1964', 'journal-title': 'Acta Embryol. Morphol. Exp'}
/ Acta Embryol. Morphol. Exp / Development of the ascidian notochord by Cloney (1964){'key': '2025021403420347100_DEVELOP_124_12_2335C8', 'first-page': '391', 'article-title': 'Urochordata-Ascidiacea', 'volume-title': 'In Reproductive Biology of Invertebrates', 'author': 'Cloney', 'year': '1990'}
/ In Reproductive Biology of Invertebrates / Urochordata-Ascidiacea by Cloney (1990)10.1146/annurev.ne.18.030195.002433
/ Ann. Rev. Neurosci / The role of the floor plate in axon guidance by Colamarino (1995)10.1242/dev.124.3.589
/ Development / Characterization of a notochord-specific enhancer from the Brachyury promoter region of the ascidian, Ciona intestinalis by Corbo (1997)10.1002/neu.480230307
/ J. Neurobiol / Structure of the caudal neural tube in an ascidian larva: vestiges of its possible evolutionary origin from a ciliated band by Crowther (1992){'volume-title': 'The Descent of Man, and Selection in Relation to Sex', 'year': '1871', 'author': 'Darwin', 'key': '2025021403420347100_DEVELOP_124_12_2335C12'}
/ The Descent of Man, and Selection in Relation to Sex by Darwin (1871)10.1242/dev.121.7.2099
/ Development / Dorsalization of the neural tube by the non-neural ectoderm by Dickinson (1995)10.1016/0092-8674(91)90071-6
/ Cell / Splotch (Sp2H), a mutation affecting development of the mouse neural tube, shows a deletion within the paired domain of Pax-3 by Epstein (1991){'key': '2025021403420347100_DEVELOP_124_12_2335C15', 'first-page': '51', 'article-title': 'The morphology of the tunicata, and its bearing on the phylogeny of the chordata', 'volume': '72', 'author': 'Garstrang', 'year': '1928', 'journal-title': 'Q. J. Microsc. Sci'}
/ Q. J. Microsc. Sci / The morphology of the tunicata, and its bearing on the phylogeny of the chordata by Garstrang (1928)10.1242/dev.124.4.817
/ Development / Conservation of Pax-6 in a lower chordate, the ascidian, Phallusia mammillata by Glardon (1997)10.1242/dev.117.3.1001
/ Development / Signals from the notochord and floor plate regulate the region-specific expression of two Pax genes in the developing spinal cord by Goulding (1993)10.1242/dev.119.4.1107
/ Development / The expression of a zebrafish gene homologous to Drosophila snail suggests a conserved function in invertebrate and vertebrate gastrulation by Hammerschmidt (1993)10.1016/0896-6273(92)90027-B
/ Neuron / Role of the floor plate in axonal patterning in the zebrafish CNS by Hatta (1992)10.1016/S1044-5781(06)80001-0
/ Sem. in Dev. Biol / Introduction: the Brachyury gene by Herrmann (1995)10.1111/j.1463-6395.1973.tb00445.x
/ Acta Zool / The origin of the chordates by Jollie (1973)10.1006/geno.1994.1191
/ Genomics / The HNF-3 gene family of transcription factors in mice: gene structure, cDNA sequence, and mRNA distribution by Kaestner (1994)10.1016/S0022-2836(95)80047-6
/ J. Mol. Biol / DNA recognition site analysis of Xenopus winged-helix proteins by Kaufmann (1995)10.1126/science.1925551
/ Science / Establishment of the mesoderm-neuroectoderm boundary in the Drosophila embryo by Kosman (1991){'key': '2025021403420347100_DEVELOP_124_12_2335C25', 'first-page': '1', 'article-title': 'Entwicklungsgeschichte der einfachen Ascidien', 'volume': '10', 'author': 'Kowalevsky', 'year': '1866', 'journal-title': 'Mem. l’Acad. St. Petersbourg. Ser. 7'}
/ Mem. l’Acad. St. Petersbourg. Ser. 7 / Entwicklungsgeschichte der einfachen Ascidien by Kowalevsky (1866)10.1006/dbio.1995.1161
/ Dev. Biol / Coexpression and promoter function in two muscle actin gene complexes of different structural organization in the ascidian Halocynthia roretzi by Kusakabe (1995)10.1101/gad.5.9.1568
/ Genes Dev / twist and snail as positive and negative regulators during Drosophila mesoderm development by Leptin (1991)10.1016/0092-8674(95)90276-7
/ Cell / Dorsal differentiation of neural plate cells induced by BMP-mediated signals from epidermal ectoderm by Liem (1995){'key': '2025021403420347100_DEVELOP_124_12_2335C29', 'first-page': '207', 'article-title': 'Aspetti ultrastrutturali della corda delle larve di Ciona intestinalis durante l’allungamento della coda', 'volume': '2', 'author': 'Mancuso', 'year': '1977', 'journal-title': 'Acta Embryol. Exp'}
/ Acta Embryol. Exp / Aspetti ultrastrutturali della corda delle larve di Ciona intestinalis durante l’allungamento della coda by Mancuso (1977)10.1242/dev.122.3.831
/ Development / Dysgenesis of cephalic neural crest derivatives in Pax7−/− mutant mice by Mansouri (1996)10.1242/dev.121.3.767
/ Development / Induction of the prospective neural crest of Xenopus by Mayor (1995)10.1016/0925-4773(96)00545-X
/ Mech. Dev / An ascidian homologue of vertebrate BMPs5-8 is expressed in the midline of the anterior neuroectoderm and in the midline of the ventral epidermis of the embryo by Miya (1996)10.1002/cne.903090402
/ J. Comp. Neurol / Cell counts and maps in the larval central nervous system of the ascidian Ciona intestinalis (L by Nicol (1991)10.1016/0012-1606(88)90363-6
/ Dev. Biol / Development of the central nervous system of the larva of the ascidian, Ciona intestinalis. I. The early lineages of the neural plate by Nicol (1988)10.1016/0012-1606(88)90364-8
/ Dev. Biol / Development of the central nervous system of the larva of the ascidian, Ciona intestinalis. II. Neural plate morphogenesis and cell lineages during neurulation by Nicol (1988)10.1242/dev.116.1.227
/ Development / Cloning and developmental expression of Sna, a murine homologue of the Drosophila snail gene by Nieto (1992)10.1126/science.7513443
/ Science / Control of cell behavior during vertebrate development by Slug, a zinc finger gene by Nieto (1994)10.1016/0012-1606(87)90188-6
/ Dev. Biol / Cell lineage analysis in ascidian embryos by intracellular injection of a tracer enzyme. III. Up to the tissue restricted stage by Nishida (1987)10.1016/0012-1606(83)90288-9
/ Dev. Biol / Cell lineage analysis in ascidian embryos by intracellular injection of a tracer enzyme. I. Up to the eight-cell stage by Nishida (1983)10.1016/0012-1606(85)90102-2
/ Dev. Biol / Cell lineage analysis in ascidian embryos by intracellular injection of a tracer enzyme. II. The 16- and 32-cell stages by Nishida (1985)10.1016/0012-1606(89)90232-7
/ Dev. Biol / Determination and regulation in the pigment cell lineage of the ascidian embryo by Nishida (1989)10.1242/dev.117.1.205
/ Development / Induction of floor plate differentiation by contact-dependent, homeogenetic signals by Placzek (1993)10.1016/0092-8674(94)90514-2
/ Cell / Floor plate and motor neuron induction by vhh-1, a vertebrate homolog of hedgehog expressed by the notochord by Roelink (1994)10.1016/0092-8674(95)90397-6
/ Cell / Floor plate and motor neuron induction by different concentrations of the amino-terminal cleavage product of Sonic hedgehog autoproteolysis by Roelink (1995)10.1242/dev.116.1.81
/ Development / Pintallavis, a gene expressed in the organizer and midline cells of frog embryos: involvement in the development of the neural axis by Ruiz i Altaba (1992)10.1006/dbio.1995.1216
/ Dev. Biol / Early stages of notochord and floor plate development in the chick embryo defined by normal and induced expression of HNF-3 β by Ruiz i Altaba (1995)10.1006/mcne.1995.1011
/ Mol. Cell. Neurosci / Restrictions to floor plate induction by hedgehog and winged-helix genes in the neural tube of frog embryos by Ruiz i Altaba (1995){'volume-title': 'Molecular Cloning: a Laboratory Manual', 'year': '1989', 'author': 'Sambrook', 'key': '2025021403420347100_DEVELOP_124_12_2335C48'}
/ Molecular Cloning: a Laboratory Manual by Sambrook (1989)10.1242/dev.109.4.967
/ Development / Identification in Xenopus of a structural homologue of the Drosophila gene snail by Sargent (1990)10.1016/0092-8674(94)90176-7
/ Cell / HNF-3 β as a regulator of floor plate development by Sasaki (1994){'volume-title': 'Developmental Biology of Ascidians', 'year': '1994', 'author': 'Satoh', 'key': '2025021403420347100_DEVELOP_124_12_2335C51'}
/ Developmental Biology of Ascidians by Satoh (1994){'key': '2025021403420347100_DEVELOP_124_12_2335C52', 'first-page': '175', 'article-title': 'Deuterostome monophyly and phylogeny', 'volume': '21', 'author': 'Schaeffer', 'year': '1987', 'journal-title': 'Evol. Biol'}
/ Evol. Biol / Deuterostome monophyly and phylogeny by Schaeffer (1987)10.1101/gad.7.7b.1436
/ Genes Dev / Axial, a zebrafish gene expressed along the developing body axis, shows altered expression in cyclops mutant embryos by Strahle (1993)10.1126/science.274.5290.1115
/ Science / Diversity and pattern in the development spinal cord by Tanabe (1996)10.1006/dbio.1995.0007
/ Dev. Biol / Expression of snail2, a second member of the zebrafish snail family, in cephalic mesendoderm and presumptive neural crest of wild-type and spadetail mutant embryos by Thisse (1995){'key': '2025021403420347100_DEVELOP_124_12_2335C56', 'first-page': '648', 'article-title': 'Deuterostome phylogeny and the sister group of the chordates: evidence from molecules and morphology', 'volume': '11', 'author': 'Turbeville', 'year': '1994', 'journal-title': 'Mol. Biol. Evol'}
/ Mol. Biol. Evol / Deuterostome phylogeny and the sister group of the chordates: evidence from molecules and morphology by Turbeville (1994)10.1073/pnas.91.5.1801
/ Proc. Natl. Acad. Sci. USA / Details of the evolutionary history from invertebrates to vertebrates, as deduced from the sequences of 18S rDNA by Wada (1994)10.1038/384123a0
/ Nature / Origin of patterning in neural tubes by Wada (1996)10.1016/0092-8674(89)90133-5
/ Cell / The homeotic gene fork head encodes a nuclear protein and is expressed in the terminal regions of the Drosophila embryo by Weigel (1989)10.1016/0092-8674(94)90523-1
/ Cell / The winged-helix transcription factor HNF-3 β is required for notochord development in the mouse embryo by Weinstein (1994){'volume-title': 'Zoological results based on material from New Britain, New Guinea, Loyalty Islands and elsewhere, collected during the years 1895, 1896, and 1897, by Arthur Willey', 'year': '1899', 'author': 'Willey', 'key': '2025021403420347100_DEVELOP_124_12_2335C61'}
/ Zoological results based on material from New Britain, New Guinea, Loyalty Islands and elsewhere, collected during the years 1895, 1896, and 1897, by Arthur Willey by Willey (1899)10.1002/aja.1002030308
/ Dev. Dyn / Expression of a type II collagen gene in the zebrafish embryonic axis by Yan (1995)10.1111/j.1440-169X.1994.00009.x
/ Dev. Growth Differ / An ascidian homolog of the mouse Brachyury (T) gene is expressed exclusively in notochord cells at the fate restricted stage by Yasuo (1994)
Dates
Type | When |
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Created | 4 years, 4 months ago (April 23, 2021, 3:12 p.m.) |
Deposited | 6 months, 2 weeks ago (Feb. 13, 2025, 10:42 p.m.) |
Indexed | 6 months, 2 weeks ago (Feb. 13, 2025, 11:10 p.m.) |
Issued | 28 years, 2 months ago (June 15, 1997) |
Published | 28 years, 2 months ago (June 15, 1997) |
Published Online | 28 years, 2 months ago (June 15, 1997) |
Published Print | 28 years, 2 months ago (June 15, 1997) |
@article{Corbo_1997, title={Dorsoventral patterning of the vertebrate neural tube is conserved in a protochordate}, volume={124}, ISSN={1477-9129}, url={http://dx.doi.org/10.1242/dev.124.12.2335}, DOI={10.1242/dev.124.12.2335}, number={12}, journal={Development}, publisher={The Company of Biologists}, author={Corbo, Joseph C. and Erives, Albert and Gregorio, Anna Di and Chang, Audrey and Levine, Michael}, year={1997}, month=jun, pages={2335–2344} }