DOI: 10.1242/dev.121.12.4319. <i>Drosophila short gastrulation</i> induces an ectopic axis in <i>Xenopus</i>: evidence for conserved mechanisms of dorsal-ventral patterning

Drosophila short gastrulation induces an ectopic axis in Xenopus: evidence for conserved mechanisms of dorsal-ventral patterning

10.1242/dev.121.12.4319

Crossref journal-article

The Company of Biologists

Development (237)

Abstract

ABSTRACT The Spemann organizer has long been recognized as a major source of patterning signals during the gastrula stage of amphibian embryogenesis. More recent evidence has suggested that the ventral side of the embryo also plays an important role in dorsal-ventral patterning during gastrulation through the action of signaling factors such as BMP-4. Bmp-4 is closely related to the Drosophila decapen-taplegic (dpp) gene, and like Bmp-4, dpp is excluded from the neurogenic region. Recently we showed that Bmp-4 functions in an analogous role to that of dpp in Drosophila, suggesting that the mechanism of dorsal-ventral patterning in Xenopus and Drosophila embryos may be conserved. To further test this hypothesis, RNA of the Drosophila short gastrulation (sog) gene was injected into Xenopus embryos, since sog has been shown genetically to be an antagonist of dpp function. Overexpression of sog RNA in Xenopus dorsalizes the embryo by expanding neurogenic and dorsal paraxial tissue. When ectopically expressed on the ventral side of the embryo, sog induces a partial secondary axis. In addition, sog partially rescues embryos ventralized by ultraviolet irradiation. Since sog induces many similar changes in gene expression to that caused by truncated BMP receptors, we suggest that sog functions in part by opposing BMP-4 signaling. The recent identification of a possible Xenopus sog homolog, chordin, in conjunction with these results supports the hypothesis that dorsalventral patterning mechanisms are conserved between these two species.

Bibliography

Schmidt, J., Francois, V., Bier, E., & Kimelman, D. (1995). Drosophila short gastrulation induces an ectopic axis in Xenopus: evidence for conserved mechanisms of dorsal-ventral patterning. Development, 121(12), 4319â4328.

Authors 4

Jennifer Schmidt (first)
Vincent Francois (additional)
Ethan Bier (additional)
David Kimelman (additional)

References 59 Referenced 72

10.1038/371026a0 / Nature / Inversion of dorsoventral axis? by Arendt (1994)
10.1101/gad.8.21.2588 / Genes Dev / The screw gene encodes a ubiquitously expressed member of the TGF-β family required for specification of dorsal cell fates in the Drosophila embryo by Arora (1994)
10.1242/dev.114.4.1003 / Development / Altered mitotic domains reveal fate map changes in Drosophila embryos mutant for zygotic dorsoventral patterning genes by Arora (1992)
10.1016/0925-4773(93)90089-G / Mech. Dev / The structure and expression of the Xenopus Krox-20 gene: conserved and divergent patterns of expression in rhombomeres and neural crest by Bradley (1992)
10.1016/0092-8674(89)90242-0 / Cell / The role of easter, an apparent serine protease, in organizing the dorsal-ventral pattern of the Drosophila embryo by Chasen (1989)
10.1016/0092-8674(91)90288-A / Cell / Molecular nature of Spemann’s organizer: the role of the Xenopus homeobox gene goosecoid by Cho (1991)
10.1242/dev.111.4.1045 / Development / Xwnt-8, a Xenopus Wnt-1/int-1-related gene responsive to mesoderm inducing factors, may play a role in ventral mesodermal patterning during embryogenesis by Christian (1991)
10.1242/dev.115.2.573 / Development / Bone morphogenetic protein 4: a ventralizing factor in early Xenopus development by Dale (1992)
10.1242/dev.100.2.279 / Development / Regional specification within the mesoderm of early embryos of Xenopus laevis by Dale (1987)
{'key': '2025011515284448000_DEVELOP_121_12_4319C10', 'first-page': '289', 'article-title': 'Mesoderm induction in Xenopus laevis: a quantitative study using a cell lineage label and tissue- specific antibodies', 'volume': '89', 'author': 'Dale', 'year': '1985', 'journal-title': 'J. Embryol. Exp. Morphol'} / J. Embryol. Exp. Morphol / Mesoderm induction in Xenopus laevis: a quantitative study using a cell lineage label and tissue- specific antibodies by Dale (1985)
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)
10.1242/dev.114.3.583 / Development / Localized enhancement and repression of the activity of the TGF-β family member, decapentaplegic, is necessary for dorsal-ventral pattern formation in the Drosophila embryo by Ferguson (1992)
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 gastrulation genes encode homologous proteins functioning in dorsal- ventral axis formation by Francois (1995)
10.1101/gad.8.21.2602 / Genes Dev / Dorsal-ventral patterning of the Drosophila embryo depends on a putative negative growth factor encoded by the short gastrulation gene by Francois (1994)
10.1242/dev.113.4.1387 / Development / Transient expression of XMyoD in non- somite mesoderm of Xenopus gastrulae by Frank (1991)
{'key': '2025011515284448000_DEVELOP_121_12_4319C17', 'first-page': '89', 'article-title': 'Considerations generales sur la vertebre', 'volume': '9', 'author': 'Geoffroy St. Hillaire', 'year': '1822', 'journal-title': 'Mem. Mus. Hist. Nat'} / Mem. Mus. Hist. Nat / Considerations generales sur la vertebre by Geoffroy St. Hillaire (1822)
10.1242/dev.107.Supplement.37 / Development / Cortical rotation of the Xenopus egg: consequences for the anteroposterior pattern of embryonic dorsal development by Gerhart (1989)
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)
{'key': '2025011515284448000_DEVELOP_121_12_4319C20', 'article-title': 'In situ hybridization: an improved whole mount method for Xenopus embryos', 'volume-title': 'Methods in Cell Biology', 'author': 'Harland', 'year': '1991'} / Methods in Cell Biology / In situ hybridization: an improved whole mount method for Xenopus embryos by Harland (1991)
10.1073/pnas.91.22.10243 / Proc. Natl. Acad. Sci. USA / The transforming growth factor β family and induction of the vertebrate mesoderm: Bone morphogenetic proteins are ventral inducers by Harland (1994)
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)
10.1038/376249a0 / Nature / A conserved system for dorsal-ventral patterning in insects and vertebrates involving sog and chordin by Holley (1995)
10.1038/374022a0 / Nature / Dorsoventral axis inversion? by Jefferies (1995)
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)
10.1016/0012-1606(88)90189-3 / Dev. Biol / The entire mesodermal mantle behaves as Spemann’s organizer in dorsoanterior enhanced Xenopus laevis embryos by Kao (1988)
10.1242/dev.116.Supplement.81 / Development supplement, 81-91 / The patterning and functioning of protrusive activity during convergence and extension of the Xenopus organiser by Keller (1992)
10.1016/S0091-679X(08)60289-7 / Xenopus laevis: Practical Uses in Cell and Molecular Biology / Histological preparations of Xenopus laevis oocytes and embryos by Kelly (1991)
10.1126/science.7939714 / Science / Vertebrate embryonic induction: mesodermal and neural patterning by Kessler (1994)
10.1242/dev.116.1.1 / Development / Synergistic principles of development: overlapping patterning systems in Xenopus mesoderm induction by Kimelman (1992)
10.1038/373110c0 / Nature / Dorsoventral axis inversion by Lacalli (1995)
10.1073/pnas.91.22.10260 / Proc. Natl. Acad. Sci. USA / A truncated bone morphogenetic protein 4 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)
10.1016/0012-1606(77)90152-X / Dev. Biol / Destruction of components of the neural induction system of the amphibian egg with ultraviolet irradiation by Malacinski (1977)
{'key': '2025011515284448000_DEVELOP_121_12_4319C34', 'first-page': '76', 'article-title': 'Microinjection and expression of synthetic mRNAs in Xenopus embryos', 'volume': '1', 'author': 'Moon', 'year': '1989', 'journal-title': 'Technique'} / Technique / Microinjection and expression of synthetic mRNAs in Xenopus embryos by Moon (1989)
10.1016/0092-8674(92)90545-N / Cell / Competence modifiers synergize with growth factors during mesoderm induction and patterning in Xenopus by Moon (1992)
10.1016/0092-8674(82)90272-0 / Cell / A major developmental transition in early Xenopus embryos. I. Characterization and timing of cellular changes at the midblastula stage by Newport (1982)
{'volume-title': 'Normal Tables of Xenopus laevis', 'year': '1967', 'author': 'Nieuwkoop', 'key': '2025011515284448000_DEVELOP_121_12_4319C37'} / Normal Tables of Xenopus laevis by Nieuwkoop (1967)
10.1038/325081a0 / Nature / A transcript from 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)
10.1038/373111a0 / Nature / Dorsoventral axis inversion by Peterson (1995)
10.1242/dev.113.1.35 / Development / The control of cell fate along the dorsal-ventral axis of the Drosophila embryo by Ray (1991)
10.1073/pnas.90.13.6004 / Proc. Natl. Acad. Sci. USA / Drosophila transforming growth factor beta superfamily proteins induce endochondrial bone formation in mammals by Sampath (1993)
10.1016/0092-8674(94)90068-X / Cell 779-790 / Xenopus chordin: a novel dorsalizing factor activated by organizer-specific homeobox genes by Sasai (1994)
10.1016/0012-1606(80)90082-2 / Dev. Biol / Determination of the dorsal-ventral axis in eggs of Xenopus laevis: complete rescue of uv-impaired eggs by oblique orientation before first cleavage by Scharf (1980)
10.1006/dbio.1995.1124 / Dev. Biol / Localized BMP-4 mediates dorsal-ventral patterning in the early Xenopus embryo by Schmidt (1995)
10.1101/gad.7.1.1 / Genes Dev / The frog prince-cess: A molecular formula for dorsoventral patterning in Xenopus by Sive (1993)
{'key': '2025011515284448000_DEVELOP_121_12_4319C47', 'first-page': '317', 'article-title': 'Cell lineage of labels and region-specific markers in the analysis of inductive interactions', 'volume': '89', 'author': 'Smith', 'year': '1985', 'journal-title': 'J. Embryol. Exp. Morphol'} / J. Embryol. Exp. Morphol / Cell lineage of labels and region-specific markers in the analysis of inductive interactions by Smith (1985)
10.1038/368548a0 / Nature / Ventralising signal determined by protease activation in Drosophila embryogenesis by Smith (1994)
10.1016/0092-8674(91)90573-H / Cell / Expression of a Xenopus homolog of brachyury (T) is an immediate-early response to mesoderm induction by Smith (1991)
{'key': '2025011515284448000_DEVELOP_121_12_4319C50', 'first-page': '299', 'article-title': 'Dorsalization and neural induction: properties of the organizer in Xenopus laevis', 'volume': '78', 'author': 'Smith', 'year': '1983', 'journal-title': 'J. Embryol. Exp. Morphol'} / J. Embryol. Exp. Morphol / Dorsalization and neural induction: properties of the organizer in Xenopus laevis by Smith (1983)
10.1016/0092-8674(91)90070-F / Cell / Injected Xwnt-8 acts early in Xenopus embryos to promote formation of a vegetal dorsalizing center by Smith (1991)
10.1016/0092-8674(92)90316-5 / Cell / Expression cloning of noggin, a new dorsalizing factor localized in the Spemann organizer in Xenopus embryos by Smith (1992)
10.1002/j.1460-2075.1987.tb02574.x / EMBO / decapentaplegic transcripts are localized along the dorsal-ventral axis of the Drosophila embryo by St. Johnston (1987)
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)
{'key': '2025011515284448000_DEVELOP_121_12_4319C55', 'first-page': '497', 'article-title': 'Peptides derived from two separate domains of the matrix protein thrombospondin-1 have anti-angiogenic activity', 'volume-title': 'J. CellBiol', 'author': 'Jolsma', 'year': '1993'} / J. CellBiol / Peptides derived from two separate domains of the matrix protein thrombospondin-1 have anti-angiogenic activity by Jolsma (1993)
10.1101/gad.8.12.1434 / Genes Dev / Expression of achaete-scute homolog 3 in Xenopus embryos converts ectodermal cells to a neural fate by Turner (1994)
10.1101/gad.7.3.355 / Genes Dev / Induction of the Xenopus organizer: expression and regulation of Xnot, a novel FGF and activin-regulated homeobox gene by von Dassow (1993)
10.1242/dev.117.2.807 / Development / The activity gradient of decapentaplegic is necessary for the specification of dorsal pattern elements in the Drosophila embryo by Wharton (1993)
10.1016/0012-1606(88)90389-2 / Dev. Biol / Short gastrulation, a mutation causing delays in stage specific cell shape changes during gastrulation in Drosophila melanogaster by Zusman (1988)

Dates

Type	When
Created	4 years, 4 months ago (April 25, 2021, 10:18 p.m.)
Deposited	7 months, 1 week ago (Jan. 15, 2025, 10:29 a.m.)
Indexed	7 months, 1 week ago (Jan. 15, 2025, 11:10 a.m.)
Issued	29 years, 8 months ago (Dec. 1, 1995)
Published	29 years, 8 months ago (Dec. 1, 1995)
Published Online	29 years, 8 months ago (Dec. 1, 1995)
Published Print	29 years, 8 months ago (Dec. 1, 1995)

Funders 0

None

JSON

{
  "indexed": {
    "date-parts": [
      [
        2025,
        1,
        15
      ]
    ],
    "date-time": "2025-01-15T16:10:18Z",
    "timestamp": 1736957418506,
    "version": "3.33.0"
  },
  "reference-count": 59,
  "publisher": "The Company of Biologists",
  "issue": "12",
  "content-domain": {
    "domain": [],
    "crossmark-restriction": false
  },
  "published-print": {
    "date-parts": [
      [
        1995,
        12,
        1
      ]
    ]
  },
  "abstract": "<jats:title>ABSTRACT</jats:title>\n               <jats:p>The Spemann organizer has long been recognized as a major source of patterning signals during the gastrula stage of amphibian embryogenesis. More recent evidence has suggested that the ventral side of the embryo also plays an important role in dorsal-ventral patterning during gastrulation through the action of signaling factors such as BMP-4. Bmp-4 is closely related to the Drosophila decapen-taplegic (dpp) gene, and like Bmp-4, dpp is excluded from the neurogenic region. Recently we showed that Bmp-4 functions in an analogous role to that of dpp in Drosophila, suggesting that the mechanism of dorsal-ventral patterning in Xenopus and Drosophila embryos may be conserved. To further test this hypothesis, RNA of the Drosophila short gastrulation (sog) gene was injected into Xenopus embryos, since sog has been shown genetically to be an antagonist of dpp function. Overexpression of sog RNA in Xenopus dorsalizes the embryo by expanding neurogenic and dorsal paraxial tissue. When ectopically expressed on the ventral side of the embryo, sog induces a partial secondary axis. In addition, sog partially rescues embryos ventralized by ultraviolet irradiation. Since sog induces many similar changes in gene expression to that caused by truncated BMP receptors, we suggest that sog functions in part by opposing BMP-4 signaling. The recent identification of a possible Xenopus sog homolog, chordin, in conjunction with these results supports the hypothesis that dorsalventral patterning mechanisms are conserved between these two species.</jats:p>",
  "DOI": "10.1242/dev.121.12.4319",
  "type": "journal-article",
  "created": {
    "date-parts": [
      [
        2021,
        4,
        26
      ]
    ],
    "date-time": "2021-04-26T02:18:15Z",
    "timestamp": 1619403495000
  },
  "page": "4319-4328",
  "source": "Crossref",
  "is-referenced-by-count": 72,
  "title": "<i>Drosophila short gastrulation</i> induces an ectopic axis in <i>Xenopus</i>: evidence for conserved mechanisms of dorsal-ventral patterning",
  "prefix": "10.1242",
  "volume": "121",
  "author": [
    {
      "given": "Jennifer",
      "family": "Schmidt",
      "sequence": "first",
      "affiliation": [
        {
          "name": "Department of Biochemistry Box 357350 1 , University of Washington, Seattle, Washington 98195-7350, USA"
        }
      ]
    },
    {
      "given": "Vincent",
      "family": "Francois",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Department of Biology and Center for Molecular Genetics 2 , University of California San Diego, La Jolla, California 92093, USA"
        }
      ]
    },
    {
      "given": "Ethan",
      "family": "Bier",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Department of Biology and Center for Molecular Genetics 2 , University of California San Diego, La Jolla, California 92093, USA"
        }
      ]
    },
    {
      "given": "David",
      "family": "Kimelman",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Department of Biochemistry Box 357350 1 , University of Washington, Seattle, Washington 98195-7350, USA"
        }
      ]
    }
  ],
  "member": "237",
  "published-online": {
    "date-parts": [
      [
        1995,
        12,
        1
      ]
    ]
  },
  "reference": [
    {
      "key": "2025011515284448000_DEVELOP_121_12_4319C1",
      "doi-asserted-by": "publisher",
      "first-page": "26",
      "DOI": "10.1038/371026a0",
      "article-title": "Inversion of dorsoventral axis?",
      "volume": "371",
      "author": "Arendt",
      "year": "1994",
      "journal-title": "Nature"
    },
    {
      "key": "2025011515284448000_DEVELOP_121_12_4319C2",
      "doi-asserted-by": "publisher",
      "first-page": "2588",
      "DOI": "10.1101/gad.8.21.2588",
      "article-title": "The screw gene encodes a ubiquitously expressed member of the TGF-\u03b2 family required for specification of dorsal cell fates in the Drosophila embryo",
      "volume": "8",
      "author": "Arora",
      "year": "1994",
      "journal-title": "Genes Dev"
    },
    {
      "key": "2025011515284448000_DEVELOP_121_12_4319C3",
      "doi-asserted-by": "publisher",
      "first-page": "1003",
      "DOI": "10.1242/dev.114.4.1003",
      "article-title": "Altered mitotic domains reveal fate map changes in Drosophila embryos mutant for zygotic dorsoventral patterning genes",
      "volume": "114",
      "author": "Arora",
      "year": "1992",
      "journal-title": "Development"
    },
    {
      "key": "2025011515284448000_DEVELOP_121_12_4319C4",
      "doi-asserted-by": "publisher",
      "first-page": "73",
      "DOI": "10.1016/0925-4773(93)90089-G",
      "article-title": "The structure and expression of the Xenopus Krox-20 gene: conserved and divergent patterns of expression in rhombomeres and neural crest",
      "volume": "40",
      "author": "Bradley",
      "year": "1992",
      "journal-title": "Mech. Dev"
    },
    {
      "key": "2025011515284448000_DEVELOP_121_12_4319C5",
      "doi-asserted-by": "publisher",
      "first-page": "391",
      "DOI": "10.1016/0092-8674(89)90242-0",
      "article-title": "The role of easter, an apparent serine protease, in organizing the dorsal-ventral pattern of the Drosophila embryo",
      "volume": "56",
      "author": "Chasen",
      "year": "1989",
      "journal-title": "Cell"
    },
    {
      "key": "2025011515284448000_DEVELOP_121_12_4319C6",
      "doi-asserted-by": "publisher",
      "first-page": "1111",
      "DOI": "10.1016/0092-8674(91)90288-A",
      "article-title": "Molecular nature of Spemann\u2019s organizer: the role of the Xenopus homeobox gene goosecoid",
      "volume": "67",
      "author": "Cho",
      "year": "1991",
      "journal-title": "Cell"
    },
    {
      "key": "2025011515284448000_DEVELOP_121_12_4319C7",
      "doi-asserted-by": "publisher",
      "first-page": "1045",
      "DOI": "10.1242/dev.111.4.1045",
      "article-title": "Xwnt-8, a Xenopus Wnt-1/int-1-related gene responsive to mesoderm inducing factors, may play a role in ventral mesodermal patterning during embryogenesis",
      "volume": "111",
      "author": "Christian",
      "year": "1991",
      "journal-title": "Development"
    },
    {
      "key": "2025011515284448000_DEVELOP_121_12_4319C8",
      "doi-asserted-by": "publisher",
      "first-page": "573",
      "DOI": "10.1242/dev.115.2.573",
      "article-title": "Bone morphogenetic protein 4: a ventralizing factor in early Xenopus development",
      "volume": "115",
      "author": "Dale",
      "year": "1992",
      "journal-title": "Development"
    },
    {
      "key": "2025011515284448000_DEVELOP_121_12_4319C9",
      "doi-asserted-by": "publisher",
      "first-page": "279",
      "DOI": "10.1242/dev.100.2.279",
      "article-title": "Regional specification within the mesoderm of early embryos of Xenopus laevis",
      "volume": "100",
      "author": "Dale",
      "year": "1987",
      "journal-title": "Development"
    },
    {
      "key": "2025011515284448000_DEVELOP_121_12_4319C10",
      "first-page": "289",
      "article-title": "Mesoderm induction in Xenopus laevis: a quantitative study using a cell lineage label and tissue- specific antibodies",
      "volume": "89",
      "author": "Dale",
      "year": "1985",
      "journal-title": "J. Embryol. Exp. Morphol"
    },
    {
      "key": "2025011515284448000_DEVELOP_121_12_4319C11",
      "doi-asserted-by": "publisher",
      "first-page": "5015",
      "DOI": "10.1002/j.1460-2075.1994.tb06830.x",
      "article-title": "On the function of BMP-4 in patterning the marginal zone of the Xenopus embryo",
      "volume": "13",
      "author": "Fainsod",
      "year": "1994",
      "journal-title": "EMBO J"
    },
    {
      "key": "2025011515284448000_DEVELOP_121_12_4319C12",
      "doi-asserted-by": "publisher",
      "first-page": "583",
      "DOI": "10.1242/dev.114.3.583",
      "article-title": "Localized enhancement and repression of the activity of the TGF-\u03b2 family member, decapentaplegic, is necessary for dorsal-ventral pattern formation in the Drosophila embryo",
      "volume": "114",
      "author": "Ferguson",
      "year": "1992",
      "journal-title": "Development"
    },
    {
      "key": "2025011515284448000_DEVELOP_121_12_4319C13",
      "doi-asserted-by": "publisher",
      "first-page": "451",
      "DOI": "10.1016/0092-8674(92)90514-D",
      "article-title": "decapentaplegic acts as a morphogen to organize dorsal-ventral pattern in the Drosophila embryo",
      "volume": "71",
      "author": "Ferguson",
      "year": "1992",
      "journal-title": "Cell"
    },
    {
      "key": "2025011515284448000_DEVELOP_121_12_4319C14",
      "doi-asserted-by": "publisher",
      "first-page": "19",
      "DOI": "10.1016/0092-8674(95)90446-8",
      "article-title": "Xenopus chordin and Drosophila short gastrulation genes encode homologous proteins functioning in dorsal- ventral axis formation",
      "volume": "80",
      "author": "Francois",
      "year": "1995",
      "journal-title": "Cell"
    },
    {
      "key": "2025011515284448000_DEVELOP_121_12_4319C15",
      "doi-asserted-by": "publisher",
      "first-page": "2602",
      "DOI": "10.1101/gad.8.21.2602",
      "article-title": "Dorsal-ventral patterning of the Drosophila embryo depends on a putative negative growth factor encoded by the short gastrulation gene",
      "volume": "8",
      "author": "Francois",
      "year": "1994",
      "journal-title": "Genes Dev"
    },
    {
      "key": "2025011515284448000_DEVELOP_121_12_4319C16",
      "doi-asserted-by": "publisher",
      "first-page": "1387",
      "DOI": "10.1242/dev.113.4.1387",
      "article-title": "Transient expression of XMyoD in non- somite mesoderm of Xenopus gastrulae",
      "volume": "113",
      "author": "Frank",
      "year": "1991",
      "journal-title": "Development"
    },
    {
      "key": "2025011515284448000_DEVELOP_121_12_4319C17",
      "first-page": "89",
      "article-title": "Considerations generales sur la vertebre",
      "volume": "9",
      "author": "Geoffroy St. Hillaire",
      "year": "1822",
      "journal-title": "Mem. Mus. Hist. Nat"
    },
    {
      "issue": "Supplement",
      "key": "2025011515284448000_DEVELOP_121_12_4319C18",
      "doi-asserted-by": "publisher",
      "first-page": "37",
      "DOI": "10.1242/dev.107.Supplement.37",
      "article-title": "Cortical rotation of the Xenopus egg: consequences for the anteroposterior pattern of embryonic dorsal development",
      "volume": "107",
      "author": "Gerhart",
      "year": "1989",
      "journal-title": "Development"
    },
    {
      "key": "2025011515284448000_DEVELOP_121_12_4319C19",
      "doi-asserted-by": "publisher",
      "first-page": "169",
      "DOI": "10.1016/0092-8674(94)90409-X",
      "article-title": "Studies with a Xenopus BMP receptor suggest that ventral mesoderm- inducing signals override dorsal signals in vivo",
      "volume": "79",
      "author": "Graff",
      "year": "1994",
      "journal-title": "Cell"
    },
    {
      "key": "2025011515284448000_DEVELOP_121_12_4319C20",
      "article-title": "In situ hybridization: an improved whole mount method for Xenopus embryos",
      "volume-title": "Methods in Cell Biology",
      "author": "Harland",
      "year": "1991"
    },
    {
      "key": "2025011515284448000_DEVELOP_121_12_4319C21",
      "doi-asserted-by": "publisher",
      "first-page": "10243",
      "DOI": "10.1073/pnas.91.22.10243",
      "article-title": "The transforming growth factor \u03b2 family and induction of the vertebrate mesoderm: Bone morphogenetic proteins are ventral inducers",
      "volume": "91",
      "author": "Harland",
      "year": "1994",
      "journal-title": "Proc. Natl. Acad. Sci. USA"
    },
    {
      "key": "2025011515284448000_DEVELOP_121_12_4319C22",
      "doi-asserted-by": "publisher",
      "first-page": "283",
      "DOI": "10.1016/0092-8674(94)90320-4",
      "article-title": "Follistatin, an antagonist of activin, is expressed in the Spemann organizer and displays direct neuralizing activity",
      "volume": "77",
      "author": "Hemmati-Brivanlou",
      "year": "1994",
      "journal-title": "Cell"
    },
    {
      "key": "2025011515284448000_DEVELOP_121_12_4319C23",
      "doi-asserted-by": "publisher",
      "first-page": "249",
      "DOI": "10.1038/376249a0",
      "article-title": "A conserved system for dorsal-ventral patterning in insects and vertebrates involving sog and chordin",
      "volume": "376",
      "author": "Holley",
      "year": "1995",
      "journal-title": "Nature"
    },
    {
      "key": "2025011515284448000_DEVELOP_121_12_4319C24",
      "doi-asserted-by": "publisher",
      "first-page": "22",
      "DOI": "10.1038/374022a0",
      "article-title": "Dorsoventral axis inversion?",
      "volume": "374",
      "author": "Jefferies",
      "year": "1995",
      "journal-title": "Nature"
    },
    {
      "key": "2025011515284448000_DEVELOP_121_12_4319C25",
      "doi-asserted-by": "publisher",
      "first-page": "639",
      "DOI": "10.1242/dev.115.2.639",
      "article-title": "DVR-4 (bone morphogenetic protein-4) as a posterior ventralizing factor in Xenopus mesoderm induction",
      "volume": "115",
      "author": "Jones",
      "year": "1992",
      "journal-title": "Development"
    },
    {
      "key": "2025011515284448000_DEVELOP_121_12_4319C26",
      "doi-asserted-by": "publisher",
      "first-page": "64",
      "DOI": "10.1016/0012-1606(88)90189-3",
      "article-title": "The entire mesodermal mantle behaves as Spemann\u2019s organizer in dorsoanterior enhanced Xenopus laevis embryos",
      "volume": "127",
      "author": "Kao",
      "year": "1988",
      "journal-title": "Dev. Biol"
    },
    {
      "key": "2025011515284448000_DEVELOP_121_12_4319C27",
      "doi-asserted-by": "crossref",
      "DOI": "10.1242/dev.116.Supplement.81",
      "article-title": "The patterning and functioning of protrusive activity during convergence and extension of the Xenopus organiser",
      "volume-title": "Development supplement, 81-91",
      "author": "Keller",
      "year": "1992"
    },
    {
      "key": "2025011515284448000_DEVELOP_121_12_4319C28",
      "doi-asserted-by": "crossref",
      "DOI": "10.1016/S0091-679X(08)60289-7",
      "article-title": "Histological preparations of Xenopus laevis oocytes and embryos",
      "volume-title": "Xenopus laevis: Practical Uses in Cell and Molecular Biology",
      "author": "Kelly",
      "year": "1991"
    },
    {
      "key": "2025011515284448000_DEVELOP_121_12_4319C29",
      "doi-asserted-by": "publisher",
      "first-page": "596",
      "DOI": "10.1126/science.7939714",
      "article-title": "Vertebrate embryonic induction: mesodermal and neural patterning",
      "volume": "266",
      "author": "Kessler",
      "year": "1994",
      "journal-title": "Science"
    },
    {
      "key": "2025011515284448000_DEVELOP_121_12_4319C30",
      "doi-asserted-by": "publisher",
      "first-page": "1",
      "DOI": "10.1242/dev.116.1.1",
      "article-title": "Synergistic principles of development: overlapping patterning systems in Xenopus mesoderm induction",
      "volume": "116",
      "author": "Kimelman",
      "year": "1992",
      "journal-title": "Development"
    },
    {
      "key": "2025011515284448000_DEVELOP_121_12_4319C31",
      "doi-asserted-by": "publisher",
      "first-page": "110",
      "DOI": "10.1038/373110c0",
      "article-title": "Dorsoventral axis inversion",
      "volume": "373",
      "author": "Lacalli",
      "year": "1995",
      "journal-title": "Nature"
    },
    {
      "key": "2025011515284448000_DEVELOP_121_12_4319C32",
      "doi-asserted-by": "publisher",
      "first-page": "10260",
      "DOI": "10.1073/pnas.91.22.10260",
      "article-title": "A truncated bone morphogenetic protein 4 receptor alters the fate of ventral mesoderm to dorsal mesoderm: Roles of animal pole tissue in the development of the ventral mesoderm",
      "volume": "91",
      "author": "Maeno",
      "year": "1994",
      "journal-title": "Proc. Natl. Acad. Sci. USA"
    },
    {
      "key": "2025011515284448000_DEVELOP_121_12_4319C33",
      "doi-asserted-by": "publisher",
      "first-page": "24",
      "DOI": "10.1016/0012-1606(77)90152-X",
      "article-title": "Destruction of components of the neural induction system of the amphibian egg with ultraviolet irradiation",
      "volume": "56",
      "author": "Malacinski",
      "year": "1977",
      "journal-title": "Dev. Biol"
    },
    {
      "key": "2025011515284448000_DEVELOP_121_12_4319C34",
      "first-page": "76",
      "article-title": "Microinjection and expression of synthetic mRNAs in Xenopus embryos",
      "volume": "1",
      "author": "Moon",
      "year": "1989",
      "journal-title": "Technique"
    },
    {
      "key": "2025011515284448000_DEVELOP_121_12_4319C35",
      "doi-asserted-by": "publisher",
      "first-page": "709",
      "DOI": "10.1016/0092-8674(92)90545-N",
      "article-title": "Competence modifiers synergize with growth factors during mesoderm induction and patterning in Xenopus",
      "volume": "71",
      "author": "Moon",
      "year": "1992",
      "journal-title": "Cell"
    },
    {
      "key": "2025011515284448000_DEVELOP_121_12_4319C36",
      "doi-asserted-by": "publisher",
      "first-page": "675",
      "DOI": "10.1016/0092-8674(82)90272-0",
      "article-title": "A major developmental transition in early Xenopus embryos. I. Characterization and timing of cellular changes at the midblastula stage",
      "volume": "30",
      "author": "Newport",
      "year": "1982",
      "journal-title": "Cell"
    },
    {
      "volume-title": "Normal Tables of Xenopus laevis",
      "year": "1967",
      "author": "Nieuwkoop",
      "key": "2025011515284448000_DEVELOP_121_12_4319C37"
    },
    {
      "key": "2025011515284448000_DEVELOP_121_12_4319C38",
      "doi-asserted-by": "publisher",
      "first-page": "81",
      "DOI": "10.1038/325081a0",
      "article-title": "A transcript from Drosophila pattern gene predicts a protein homologous to the transforming growth factor-\u03b2 family",
      "volume": "325",
      "author": "Padgett",
      "year": "1987",
      "journal-title": "Nature"
    },
    {
      "key": "2025011515284448000_DEVELOP_121_12_4319C39",
      "doi-asserted-by": "publisher",
      "first-page": "2905",
      "DOI": "10.1073/pnas.90.7.2905",
      "article-title": "Human BMP sequences can confer normal dorsal-ventral patterning in the Drosophila embryo",
      "volume": "90",
      "author": "Padgett",
      "year": "1993",
      "journal-title": "Proc. Natl. Acad. Sci. USA"
    },
    {
      "key": "2025011515284448000_DEVELOP_121_12_4319C40",
      "doi-asserted-by": "publisher",
      "first-page": "111",
      "DOI": "10.1038/373111a0",
      "article-title": "Dorsoventral axis inversion",
      "volume": "373",
      "author": "Peterson",
      "year": "1995",
      "journal-title": "Nature"
    },
    {
      "key": "2025011515284448000_DEVELOP_121_12_4319C41",
      "doi-asserted-by": "publisher",
      "first-page": "35",
      "DOI": "10.1242/dev.113.1.35",
      "article-title": "The control of cell fate along the dorsal-ventral axis of the Drosophila embryo",
      "volume": "113",
      "author": "Ray",
      "year": "1991",
      "journal-title": "Development"
    },
    {
      "key": "2025011515284448000_DEVELOP_121_12_4319C42",
      "doi-asserted-by": "publisher",
      "first-page": "6004",
      "DOI": "10.1073/pnas.90.13.6004",
      "article-title": "Drosophila transforming growth factor beta superfamily proteins induce endochondrial bone formation in mammals",
      "volume": "90",
      "author": "Sampath",
      "year": "1993",
      "journal-title": "Proc. Natl. Acad. Sci. USA"
    },
    {
      "key": "2025011515284448000_DEVELOP_121_12_4319C43",
      "doi-asserted-by": "crossref",
      "DOI": "10.1016/0092-8674(94)90068-X",
      "article-title": "Xenopus chordin: a novel dorsalizing factor activated by organizer-specific homeobox genes",
      "volume-title": "Cell 779-790",
      "author": "Sasai",
      "year": "1994"
    },
    {
      "key": "2025011515284448000_DEVELOP_121_12_4319C44",
      "doi-asserted-by": "publisher",
      "first-page": "181",
      "DOI": "10.1016/0012-1606(80)90082-2",
      "article-title": "Determination of the dorsal-ventral axis in eggs of Xenopus laevis: complete rescue of uv-impaired eggs by oblique orientation before first cleavage",
      "volume": "79",
      "author": "Scharf",
      "year": "1980",
      "journal-title": "Dev. Biol"
    },
    {
      "key": "2025011515284448000_DEVELOP_121_12_4319C45",
      "doi-asserted-by": "publisher",
      "first-page": "37",
      "DOI": "10.1006/dbio.1995.1124",
      "article-title": "Localized BMP-4 mediates dorsal-ventral patterning in the early Xenopus embryo",
      "volume": "169",
      "author": "Schmidt",
      "year": "1995",
      "journal-title": "Dev. Biol"
    },
    {
      "key": "2025011515284448000_DEVELOP_121_12_4319C46",
      "doi-asserted-by": "publisher",
      "first-page": "1",
      "DOI": "10.1101/gad.7.1.1",
      "article-title": "The frog prince-cess: A molecular formula for dorsoventral patterning in Xenopus",
      "volume": "7",
      "author": "Sive",
      "year": "1993",
      "journal-title": "Genes Dev"
    },
    {
      "key": "2025011515284448000_DEVELOP_121_12_4319C47",
      "first-page": "317",
      "article-title": "Cell lineage of labels and region-specific markers in the analysis of inductive interactions",
      "volume": "89",
      "author": "Smith",
      "year": "1985",
      "journal-title": "J. Embryol. Exp. Morphol"
    },
    {
      "key": "2025011515284448000_DEVELOP_121_12_4319C48",
      "doi-asserted-by": "publisher",
      "first-page": "548",
      "DOI": "10.1038/368548a0",
      "article-title": "Ventralising signal determined by protease activation in Drosophila embryogenesis",
      "volume": "368",
      "author": "Smith",
      "year": "1994",
      "journal-title": "Nature"
    },
    {
      "key": "2025011515284448000_DEVELOP_121_12_4319C49",
      "doi-asserted-by": "publisher",
      "first-page": "79",
      "DOI": "10.1016/0092-8674(91)90573-H",
      "article-title": "Expression of a Xenopus homolog of brachyury (T) is an immediate-early response to mesoderm induction",
      "volume": "67",
      "author": "Smith",
      "year": "1991",
      "journal-title": "Cell"
    },
    {
      "key": "2025011515284448000_DEVELOP_121_12_4319C50",
      "first-page": "299",
      "article-title": "Dorsalization and neural induction: properties of the organizer in Xenopus laevis",
      "volume": "78",
      "author": "Smith",
      "year": "1983",
      "journal-title": "J. Embryol. Exp. Morphol"
    },
    {
      "key": "2025011515284448000_DEVELOP_121_12_4319C51",
      "doi-asserted-by": "publisher",
      "first-page": "753",
      "DOI": "10.1016/0092-8674(91)90070-F",
      "article-title": "Injected Xwnt-8 acts early in Xenopus embryos to promote formation of a vegetal dorsalizing center",
      "volume": "67",
      "author": "Smith",
      "year": "1991",
      "journal-title": "Cell"
    },
    {
      "key": "2025011515284448000_DEVELOP_121_12_4319C52",
      "doi-asserted-by": "publisher",
      "first-page": "829",
      "DOI": "10.1016/0092-8674(92)90316-5",
      "article-title": "Expression cloning of noggin, a new dorsalizing factor localized in the Spemann organizer in Xenopus embryos",
      "volume": "70",
      "author": "Smith",
      "year": "1992",
      "journal-title": "Cell"
    },
    {
      "key": "2025011515284448000_DEVELOP_121_12_4319C53",
      "doi-asserted-by": "publisher",
      "first-page": "2785",
      "DOI": "10.1002/j.1460-2075.1987.tb02574.x",
      "article-title": "decapentaplegic transcripts are localized along the dorsal-ventral axis of the Drosophila embryo",
      "volume": "6",
      "author": "St. Johnston",
      "year": "1987",
      "journal-title": "EMBO"
    },
    {
      "key": "2025011515284448000_DEVELOP_121_12_4319C54",
      "doi-asserted-by": "publisher",
      "first-page": "10255",
      "DOI": "10.1073/pnas.91.22.10255",
      "article-title": "A truncated bone morphogenetic protein receptor affects dorsal-ventral patterning in the early Xenopus embryo",
      "volume": "91",
      "author": "Suzuki",
      "year": "1994",
      "journal-title": "Proc. Natl. Acad. Sci. USA"
    },
    {
      "key": "2025011515284448000_DEVELOP_121_12_4319C55",
      "first-page": "497",
      "article-title": "Peptides derived from two separate domains of the matrix protein thrombospondin-1 have anti-angiogenic activity",
      "volume-title": "J. CellBiol",
      "author": "Jolsma",
      "year": "1993"
    },
    {
      "key": "2025011515284448000_DEVELOP_121_12_4319C56",
      "doi-asserted-by": "publisher",
      "first-page": "1434",
      "DOI": "10.1101/gad.8.12.1434",
      "article-title": "Expression of achaete-scute homolog 3 in Xenopus embryos converts ectodermal cells to a neural fate",
      "volume": "8",
      "author": "Turner",
      "year": "1994",
      "journal-title": "Genes Dev"
    },
    {
      "key": "2025011515284448000_DEVELOP_121_12_4319C57",
      "doi-asserted-by": "publisher",
      "first-page": "355",
      "DOI": "10.1101/gad.7.3.355",
      "article-title": "Induction of the Xenopus organizer: expression and regulation of Xnot, a novel FGF and activin-regulated homeobox gene",
      "volume": "7",
      "author": "von Dassow",
      "year": "1993",
      "journal-title": "Genes Dev"
    },
    {
      "key": "2025011515284448000_DEVELOP_121_12_4319C58",
      "doi-asserted-by": "publisher",
      "first-page": "807",
      "DOI": "10.1242/dev.117.2.807",
      "article-title": "The activity gradient of decapentaplegic is necessary for the specification of dorsal pattern elements in the Drosophila embryo",
      "volume": "117",
      "author": "Wharton",
      "year": "1993",
      "journal-title": "Development"
    },
    {
      "key": "2025011515284448000_DEVELOP_121_12_4319C59",
      "doi-asserted-by": "publisher",
      "first-page": "417",
      "DOI": "10.1016/0012-1606(88)90389-2",
      "article-title": "Short gastrulation, a mutation causing delays in stage specific cell shape changes during gastrulation in Drosophila melanogaster",
      "volume": "129",
      "author": "Zusman",
      "year": "1988",
      "journal-title": "Dev. Biol"
    }
  ],
  "container-title": "Development",
  "original-title": [],
  "language": "en",
  "link": [
    {
      "URL": "https://journals.biologists.com/dev/article-pdf/121/12/4319/3120263/develop_121_12_4319.pdf",
      "content-type": "application/pdf",
      "content-version": "vor",
      "intended-application": "syndication"
    },
    {
      "URL": "https://journals.biologists.com/dev/article-pdf/121/12/4319/3120263/develop_121_12_4319.pdf",
      "content-type": "unspecified",
      "content-version": "vor",
      "intended-application": "similarity-checking"
    }
  ],
  "deposited": {
    "date-parts": [
      [
        2025,
        1,
        15
      ]
    ],
    "date-time": "2025-01-15T15:29:31Z",
    "timestamp": 1736954971000
  },
  "score": 1,
  "resource": {
    "primary": {
      "URL": "https://journals.biologists.com/dev/article/121/12/4319/38665/Drosophila-short-gastrulation-induces-an-ectopic"
    }
  },
  "subtitle": [],
  "short-title": [],
  "issued": {
    "date-parts": [
      [
        1995,
        12,
        1
      ]
    ]
  },
  "references-count": 59,
  "journal-issue": {
    "issue": "12",
    "published-print": {
      "date-parts": [
        [
          1995,
          12,
          1
        ]
      ]
    }
  },
  "URL": "http://dx.doi.org/10.1242/dev.121.12.4319",
  "relation": {},
  "ISSN": [
    "0950-1991",
    "1477-9129"
  ],
  "subject": [],
  "published": {
    "date-parts": [
      [
        1995,
        12,
        1
      ]
    ]
  }
}