Crossref
journal-article
The Company of Biologists
Development (237)
Abstract
ABSTRACT We identified 6 genes that are essential for specifying ventral regions of the early zebrafish embryo. Mutations in these genes cause an expansion of structures normally derived from dorsal-lateral regions of the blastula at the expense of ventrally derived structures. A series of phenotypes of varied strengths is observed with different alleles of these mutants. The weakest phenotype is a reduction in the ventral tail fin, observed as a dominant phenotype of swirl, piggytail, and somitabun and a recessive phenotype of mini fin, lost-a-fin and some piggytail alleles. With increasing phenotypic strength, the blood and pronephric anlagen are also reduced or absent, while the paraxial mesoderm and anterior neuroectoderm is progressively expanded. In the strong phenotypes, displayed by homozygous embryos of snailhouse, swirl and somitabun, the somites circle around the embryo and the midbrain region is expanded laterally. Several mutations in this group of genes are semidominant as well as recessive indicating a strong dosage sensitivity of the processes involved. Mutations in the piggytail gene display an unusual dominance that depends on both a maternal and zygotic heterozygous genotype, while somitabun is a fully penetrant dominant maternal-effect mutation. The similar and overlapping phenotypes of mutants of the 6 genes identified suggest that they function in a common pathway, which begins in oogenesis, but also depends on factors provided after the onset of zygotic transcription, presumably during blastula stages. This pathway provides ventral positional information, counteracting the dorsalizing instructions of the organizer, which is localized in the dorsal shield.
Bibliography
Mullins, M. C., Hammerschmidt, M., Kane, D. A., Odenthal, J., Brand, M., Eeden, F. J. M. van, Furutani-Seiki, M., Granato, M., Haffter, P., Heisenberg, C.-P., Jiang, Y.-J., Kelsh, R. N., & Nüsslein-Volhard, C. (1996). Genes establishing dorsoventral pattern formation in the zebrafish embryo: the ventral specifying genes. Development, 123(1), 81â93.
Authors
13
- Mary C. Mullins (first)
- Matthias Hammerschmidt (additional)
- Donald A. Kane (additional)
- Jörg Odenthal (additional)
- Michael Brand (additional)
- Fredericus J. M. van Eeden (additional)
- Makoto Furutani-Seiki (additional)
- Michael Granato (additional)
- Pascal Haffter (additional)
- Carl-Philipp Heisenberg (additional)
- Yun-Jin Jiang (additional)
- Robert N. Kelsh (additional)
- Christiane Nüsslein-Volhard (additional)
References
82
Referenced
369
10.1016/0092-8674(94)90522-3/ Cell / HNF-3 beta is essential for node and notochord formation in mouse development by Ang (1994){'key': '2023072810040486000_DEVELOP_123_1_81C2', 'first-page': '157', 'article-title': 'Brachyury – a gene affecting mouse gastrulation and early organogenesis', 'volume-title': 'Development', 'author': 'Beddington', 'year': '1992'}/ Development / Brachyury – a gene affecting mouse gastrulation and early organogenesis by Beddington (1992)10.1101/gad.7.1.13/ Genes Dev / Interactions between Xwnt-8 and Spemann organizer signaling pathways generate dorsoventral pattern in the embryonic mesoderm of Xenopus by Christian (1993)10.1242/dev.120.7.1919/ Development / A primary requirement for nodal in the formation and maintenance of the primitive streak in the mouse by Conlon (1994)10.1242/dev.121.7.2177/ Development / Xwnt-8b: a maternally expressed Xenopus Wnt gene with a potential role in establishing the dorsoventral axis by Cui (1995)10.1242/dev.115.2.573/ Development / Bone morphogenetic protein 4: a ventralising factor in Xenopus development by Dale (1992)10.1242/dev.99.4.527/ Development / Fate map for the 32-cell stage of Xenopus laevis by Dale (1987)10.1101/gad.8.24.3045/ Genes Dev / Murine FGFR-1 is required for early postimplantation growth and axial organization by Deng (1994)10.1038/380037a0/ Nature / A common plan for dorsoventral patterning in Bilateria by De Robertis (1996)10.1073/pnas.92.23.10713/ Proc. Nat. Acad. Sci. USA / Intraembryonic hematopoietic cell migration during vertebrate development by Detrich (1995){'key': '2023072810040486000_DEVELOP_123_1_81C11', 'first-page': '304', 'article-title': 'Coordination des forces épiboliques dans la gastrulation de Salmo', 'volume': '77', 'author': 'Devillers', 'year': '1952', 'journal-title': 'Bull. Soc. Zool. Fr'}/ Bull. Soc. Zool. Fr / Coordination des forces épiboliques dans la gastrulation de Salmo by Devillers (1952)10.1002/j.1460-2075.1994.tb06830.x/ EMBO J / On the function of BMP-4 in patterning the marginal zone of the Xenopus embryo by Fainsod (1994)10.1016/0012-1606(91)90314-S/ Dev. Biol / The fub-1 Mutation Blocks Initial Myofibril Formation in Zebrafish Muscle Pioneer Cells by Felsenfeld (1991)10.1016/0092-8674(92)90514-D/ Cell / Decapentaplegic acts as a morphogen to organize dorsal-ventral pattern in the Drosophila embryo by Ferguson (1992)10.1016/0092-8674(95)90446-8/ Cell / Xenopus chordin and Drosophila short gastulation genes encode homologous proteins functioning in dorsal-ventral axis formation by François (1995)10.1101/gad.8.21.2602/ Genes Dev / Dorsal-ventral pattening of the Drosophila embryo depends on a putative negative growth factor encoded by the short gastrulation gene by François (1994)10.1016/0092-8674(94)90409-X/ Cell / Studies with a Xenopus BMP receptor suggest that ventral mesoderm-inducing signals override dorsal signals in vivo by Graff (1994)10.1242/dev.123.1.1/ Development / The identification of genes with unique and essential functions in the development of the zebrafish, Danio rerio by Haffter (1996)10.1242/dev.123.1.95/ Development / dino and mercedes, two genes regulating dorsal development in the zebrafish embryo by Hammerschmidt (1996)10.1073/pnas.91.22.10243/ Proc. Natl. Acad. Sci. USA / The transforming growth factor beta family and induction of the vertebrate mesoderm: Bone morphogenetic proteins are ventral inducers by Harland (1994)10.1101/gad.9.23.2923/ Genes Dev / Disruption of BMP signals in embryonic Xenopus ectoderm leads to direct neural induction by Hawley (1995)10.1038/374617a0/ Nature / Glycogen synthase kinase-3 and dorsoventral patterning in Xenopus embryos by He (1995)10.1016/0092-8674(94)90320-4/ Cell / Follistatin, an antagonist of activin, is expressed in the Spemann organizer and displays direct neuralizing activity by Hemmati-Brivanlou (1994)10.1002/dvg.1020170109/ Dev. Genet / Ventral mesodermal patterning in Xenopus embryos: Expression Patterns and activities of BMP-2 and BMP-4 by Hemmati-Brivanlou (1995)10.1016/0168-9525(90)90011-T/ Trends Genet / The T genes in embryogenesis by Herrmann (1994){'key': '2023072810040486000_DEVELOP_123_1_81C26', 'first-page': '53', 'article-title': 'Axis formation in the embryo of the zebrafish, Brachydanio rerio', 'volume': '3', 'author': 'Ho', 'year': '1992', 'journal-title': 'Semin. Dev. Biol'}/ Semin. Dev. Biol / Axis formation in the embryo of the zebrafish, Brachydanio rerio by Ho (1992){'key': '2023072810040486000_DEVELOP_123_1_81C27', 'first-page': '53', 'article-title': 'Growth factos in development: the role of TGF-ß related polypeptide signalling molecules in embryogenesis', 'volume-title': 'Development', 'author': 'Hogan', 'year': '1994'}/ Development / Growth factos in development: the role of TGF-ß related polypeptide signalling molecules in embryogenesis by Hogan (1994)10.1038/376210a0/ Nature / Upside-down ideas vindicated by Hogan (1995)10.1038/376249a0/ Nature / A conserved system for dorsal-ventral patterning in insects and vertebrates involving sog and chordin by Holley (1995)10.1101/gad.1.8.868/ Genes Dev / The decapentaplegic gene is required for dorsal-ventral patterning of the Drosophila embryo by Irish (1987)10.1002/jez.1402260311/ J. Exp. Zool / Erythropoiesis in the developing rainbow trout, salmo gairdneri deus: histochemical and immunological detection of erythropoietic organs by Iuchi (1993)10.1242/dev.119.4.1261/ Development / The ventral and posterior expression of the zebrafish homeobox gene eve1 is perturbed in dorsalized and mutant embryos by Joly (1993)10.1242/dev.115.2.639/ Development / DVR-4 (Bone morphogenetic protein-4) as a posterior-ventralizing factor in Xenopus mesoderm induction by Jones (1992)10.1242/dev.123.1.47/ Development / The zebrafish epiboly mutants by Kane (1996)10.1242/dev.121.6.1787/ Development / Zebrafish wnt8 and wnt8b share a common activity but are involved in distinct developmental pathways by Kelly (1995)10.1242/dev.121.7.2155/ Development / Induction of dorsal mesoderm by soluble, mature VG1 protein by Kessler (1995)10.1126/science.7939714/ Science / Vertebrate embryonic induction: mesodermal and neural patterning by Kessler (1994)10.1002/aja.1002030302/ Dev. Dyn / Stages of embryonic development of the zebrafish by Kimmel (1995)10.1242/dev.108.4.581/ Development / Origin and organization of the zebrafish fate map by Kimmel (1990)10.1242/dev.116.1.1/ Development / Synergistic principles of development: overlapping patterning systems in Xenopus mesoderm induction by Kimelman (1992)10.1016/0925-4773(91)90027-4/ Mech. Dev / Bone morphogenetic protein 4 (BMP-4), a member of the TGF-beta family, in early embryos of Xenopus laevis: analysis of mesoderm inducing activity by Köster (1991){'key': '2023072810040486000_DEVELOP_123_1_81C42', 'first-page': '407', 'article-title': 'The differentiation capactiy of isolated loach (Misgurnis fossilis L. ) blastoderm', 'volume': '22', 'author': 'Kostomarova', 'year': '1969', 'journal-title': 'J. Embryol. Exp. Morphol'}/ J. Embryol. Exp. Morphol / The differentiation capactiy of isolated loach (Misgurnis fossilis L. ) blastoderm by Kostomarova (1969)10.1242/dev.113.4.1193/ Development / Expression of the zebrafish paired box gene pax(zf-b) during early neurogenesis by Krauss (1991)10.1038/353267a0/ Nature / Expression pattern of zebrafish pax genes suggests a role in early brain regionalization by Krauss (1991)10.1242/dev.119.4.1161/ Development / Xwnt-11: a maternally expressed Xenopus wnt gene by Ku (1993)10.1126/science.8235591/ Science / Neural induction by the secreted polypeptide noggin by Lamb (1993)10.1242/dev.120.12.3361/ Development / Cardiovascular development in the zebrafish. II. Endocardial progenitors are sequestered within the heart field by Lee (1994)10.1073/pnas.89.10.4519/ Proc. Natl. Acad. Sci. USA / Production of germ-line chimeras in zebrafish by cell transplants from genetically pigmented to albino embryos by Lin (1992)10.1073/pnas.91.22.10260/ Proc. Natl. Acad. Sci. USA / A truncated bone morphogenetic protein receptor alters the fate of ventral mesoderm to dorsal mesoderm: roles of animal pole tissue in the development of the ventral mesoderm by Maeno (1994)10.1101/gad.9.24.3027/ Genes Dev / Bmpr encodes a type I bone morphogenetic protein receptor that is essential for gastrulation during mouse embryogenesis by Mishina (1995)10.1016/S0960-9822(00)00048-8/ Curr. Biol / Large-scale mutagenesis in the zebrafish: in search of genes controlling development in a vertebrate by Mullins (1994)10.1007/BF00188683/ Roux Arch. Dev. Biol / Is ventral in insects dorsal in vertebrates? by Nübler-Jung (1994)10.3181/00379727-34-8659C/ Proc. Soc. Exp. Biol. Med / Structures developed in amphibians by implantation of living fish organizer by Oppenheimer (1936)10.1038/325081a0/ Nature / A transcript from a Drosophila pattern gene predicts a protein homologous to the transforming growth factor-β family by Padgett (1987)10.1073/pnas.90.7.2905/ Proc. Natl. Acad. Sci. USA / Human BMP sequences can confer normal dorsal-ventral patterning in the Drosophila embryo by Padgett (1993)10.1242/dev.121.3.755/ Development / Regulation of Spemann organizer formation by the intracellular kinase Xgsk-3 by Pierce (1995)10.1126/science.8171321/ Science / A genetic linkage map for the zebrafish by Postlethwait (1994)10.1038/376333a0/ Nature / Regulation of neural induction by the Chd and BMP-4 antagonistic patterning signals in Xenopus by Sasai (1995)10.1016/0092-8674(94)90068-X/ Cell / Xenopus chordin: a novel dorsalizing factor activated by organizer-specific homeobox genes by Sasai (1994)10.1006/dbio.1995.1124/ Dev. Biol / Localized BMP-4 mediates dorsal/ventral patterning in the early Xenopus embryo by Schmidt (1995)10.1242/dev.121.12.4319/ Development / Drosophila short gastrualation induces an ectopic axis in Xenopus: evidence for conserved mechanisms of dorsal-ventral patterning by Schmidt (1995)10.1007/BF00188685/ Roux Arch. Dev. Biol / Dorso-ventral polarity of the zebrafish embryo is distinguishable prior to the onset of gastrulation by Schmitz (1994)10.1242/dev.120.4.843/ Development / Expression of zebrafish goosecoid and no tail products in wild type and mutant no tail embryos by Schulte-Merker (1994)10.1242/dev.116.4.1021/ Development / The protein product of the zebrafish homologue of the mouse T-gene is expressed in nuclei of the germ ring and the notochord of the early embryo by Schulte-Merker (1992)10.1038/374425a0/ Nature / Requirement for Lim1 in head-organizer function by Shawlot (1995)10.1242/dev.121.9.2755/ Development / Distribution of tissue progenitors within the shield region of the zebrafish gastrula by Shih (1995)10.1101/gad.7.1.1/ Genes Dev / The frog prince-ss: A molecular formula for dorsoventral patterning in Xenopus by Sive (1993)10.1016/S0960-9822(94)00027-8/ Curr. Biol / Inducing factors in Xenopus early embryos by Slack (1994)10.1016/0092-8674(91)90070-F/ Cell / Injected Xwnt-8 RNA acts early in Xenopus embryos to promote formation of a vegetal dorsalizing center by Smith (1991)10.1038/361547a0/ Nature / Secreted noggin protein mimics the Spemann organizer in dorsalizing Xenopus mesoderm by Smith (1993)10.1242/dev.117.4.1261/ Development / Lithium perturbation and goosecoid expression identify a dorsal specification pathway in the pregastrula zebrafish by Stachel (1993)10.1242/dev.119.1.31/ Development / Cardiovascular development in the zebrafish. 1. Myocardial fate map and heart tube formation by Stainier (1993)10.1002/j.1460-2075.1995.tb00208.x/ EMBO J / The role of gsc and BMP-4 in dorsal-ventral patterning of the marginal zone in Xenopus: a loss-of-function study using antisense RNA by Steinbeisser (1995)10.1073/pnas.91.22.10255/ Proc. Natl. Acad. Sci. USA / A truncated bone morphogenetic protein receptor affects dorsal-ventral patterning in the early Xenopus embryo by Suzuki (1994)10.1242/dev.119.4.1203/ Development / Structure of the Zebrafish snail1 gene and its expression in wild-type, spadetail and no-tail mutant embryos by Thisse (1993)10.1242/dev.108.4.569/ Development / Cell movements during epiboly and gastrulation in zebrafish by Warga (1990)10.1242/dev.122.1.271/ Development / Developmental regulation of zebrafish MyoD in wild-type, no tail and spadetail embryos by Weinberg (1996)10.1016/0092-8674(94)90523-1/ Cell / The winged-helix transcription factor HNF-3 beta is required for notochord development in the mouse embryo by Weinstein (1994)10.1242/dev.117.2.807/ Development / An activity gradient of decapentaplegic is necessary for the specification of dorsal pattern elements in the Drosophila embryo by Wharton (1993)10.1038/376331a0/ Nature / Induction of epidermis and inhibition of neural fate by BMP-4 by Wilson (1995)10.1101/gad.9.17.2105/ Genes Dev / Bone morphogenetic protein-4 is required for mesoderm formation and patterning in the mouse by Winnier (1995)10.1101/gad.8.24.3032/ Genes Dev / fgfr-1 is required for embryonic growth and mesodermal patterning during mouse gastrulation by Yamaguchi (1994)
Dates
| Type | When |
|---|---|
| Created | 4 years, 4 months ago (April 25, 2021, 10:50 p.m.) |
| Deposited | 2 years, 1 month ago (July 28, 2023, 6:08 a.m.) |
| Indexed | 1 month ago (July 25, 2025, 6:36 a.m.) |
| Issued | 28 years, 9 months ago (Dec. 1, 1996) |
| Published | 28 years, 9 months ago (Dec. 1, 1996) |
| Published Online | 28 years, 9 months ago (Dec. 1, 1996) |
| Published Print | 28 years, 9 months ago (Dec. 1, 1996) |
@article{Mullins_1996, title={Genes establishing dorsoventral pattern formation in the zebrafish embryo: the ventral specifying genes}, volume={123}, ISSN={1477-9129}, url={http://dx.doi.org/10.1242/dev.123.1.81}, DOI={10.1242/dev.123.1.81}, number={1}, journal={Development}, publisher={The Company of Biologists}, author={Mullins, Mary C. and Hammerschmidt, Matthias and Kane, Donald A. and Odenthal, Jörg and Brand, Michael and Eeden, Fredericus J. M. van and Furutani-Seiki, Makoto and Granato, Michael and Haffter, Pascal and Heisenberg, Carl-Philipp and Jiang, Yun-Jin and Kelsh, Robert N. and Nüsslein-Volhard, Christiane}, year={1996}, month=dec, pages={81–93} }