DOI: 10.1101/gad.6.9.1728. The dorsal gradient morphogen regulates stripes of rhomboid expression in the presumptive neuroectoderm of the Drosophila embryo.

The dorsal gradient morphogen regulates stripes of rhomboid expression in the presumptive neuroectoderm of the Drosophila embryo.

10.1101/gad.6.9.1728

Crossref journal-article

Cold Spring Harbor Laboratory

Genes & Development (246)

Abstract

rhomboid (rho) encodes a putative transmembrane receptor that is required for the differentiation of the ventral epidermis. It is initially expressed before the completion of cellularization in lateral stripes within the presumptive neuroectoderm. Here, we present evidence that the maternal morphogen dorsal (dl) acts in concert with basic helix-loop-helix (b-HLH) proteins, possibly including twist (twi), to activate rho in both lateral and ventral regions. Expression is blocked in ventral regions (the presumptive mesoderm) by snail (sna), which is also a direct target of the dl morphogen. A 300-bp region of the rho promoter (the NEE), which is sufficient for neuroectoderm expression, contains a cluster of dl and b-HLH activator sites that are closely linked to sna repressor sites. Mutations in these binding sites cause genetically predicted changes in the levels and limits of rho expression. In particular, the disruption of sna-binding sites causes a derepression of the pattern throughout ventral regions, providing evidence that sna is directly responsible for establishing the mesoderm/neuroectoderm boundary before gastrulation. The tight linkage of activator and repressor sites in the rho NEE is similar to the arrangement of binding sites observed in the even-skipped stripe 2 element, which is regulated by bicoid (bcd). This suggests that the dl and bcd morphogens use a similar mechanism to make stripes in the Drosophila embryo.

Authors 5

Y T Ip (first)
R E Park (additional)
D Kosman (additional)
E Bier (additional)
M Levine (additional)

References 54 Referenced 265

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. (1991)
10.1016/0168-9525(87)90191-0
10.1016/0092-8674(85)90274-0
10.1016/0092-8674(85)90275-2
10.1101/gad.4.2.190
10.1038/330395a0
10.1101/gad.3.10.1518
10.1038/340363a0
10.1126/science.1900130
10.1016/0092-8674(90)90276-K
{'key': '2021111320242785000_6.9.1728.11', 'first-page': '119', 'article-title': 'Dorsoventral pattern formation in Drosophila.', 'volume': '7', 'year': '1991', 'journal-title': 'Trends Genet.'} / Trends Genet. / Dorsoventral pattern formation in Drosophila. (1991)
{'key': '2021111320242785000_6.9.1728.12', 'first-page': '4598', 'article-title': 'DNA-binding activities of the Drosophila melanogaster even-skipped protein are mediated by its homeo domain and influenced by protein context.', 'volume': '8', 'year': '1988', 'journal-title': 'Mol. Cell. Biol.'} / Mol. Cell. Biol. / DNA-binding activities of the Drosophila melanogaster even-skipped protein are mediated by its homeo domain and influenced by protein context. (1988)
{'key': '2021111320242785000_6.9.1728.13', 'first-page': '15', 'article-title': 'The role of the dorsal morphogen gradient in Drosophila embryogenesis.', 'volume': '3', 'year': '1992', 'journal-title': 'Sem. Dev. Biol.'} / Sem. Dev. Biol. / The role of the dorsal morphogen gradient in Drosophila embryogenesis. (1992)
10.1016/0092-8674(91)90651-E
10.1101/gad.6.8.1518
10.1101/gad.1.8.868
10.1101/gad.5.10.1881
10.1002/j.1460-2075.1992.tb05387.x / EMBO J. / Individual dorsal binding sites mediate activation and repression in the Drosophila embryo. (1992)
10.1073/pnas.89.8.3414
{'key': '2021111320242785000_6.9.1728.20', 'first-page': '5228', 'article-title': 'Yeast repressor a2 binds to its operator cooperatively with yeast protein MCM1.', 'volume': '9', 'year': '1989', 'journal-title': 'Mol. Cell. Biol.'} / Mol. Cell. Biol. / Yeast repressor a2 binds to its operator cooperatively with yeast protein MCM1. (1989)
10.1101/gad.5.5.868
10.1016/0092-8674(90)90275-J
10.1126/science.1925551
10.1126/science.3109035
10.1101/gad.5.9.1568
10.1016/0092-8674(88)90418-7
10.1016/0092-8674(89)90024-X
10.1101/gad.2.11.1496
10.1016/0092-8674(89)90682-X
10.1101/gad.5.10.1892
10.1016/0092-8674(90)90414-A
10.1101/gad.5.9.1577
10.1242/dev.113.1.35 / Development / The control of cell fate along the dorsal-ventral axis of the Drosophila embryo. (1991)
10.1002/j.1460-2075.1987.tb02474.x / EMBO J. / The achaete-scute complex is expressed in the neurogenic regions of Drosophila embryos. (1987)
10.1016/0092-8674(89)90774-5
{'key': '2021111320242785000_6.9.1728.36', 'first-page': '173', 'article-title': 'Dorsal-ventral polarity and pattern formation in Drosophila. Pattern formation in Drosophila.', 'volume': '1', 'year': '1990', 'journal-title': 'Sem. Cell Biol.'} / Sem. Cell Biol. / Dorsal-ventral polarity and pattern formation in Drosophila. Pattern formation in Drosophila. (1990)
10.1038/330583a0
10.1016/0092-8674(89)90772-1
10.1002/j.1460-2075.1987.tb02574.x / EMBO J. / decapentaplegic transcripts are localized along the dorsal-ventral axis of the Drosophila embryo. (1987)
10.1016/0092-8674(86)90346-6
10.1093/genetics/105.3.615 / Genetics / Matemal-zygotic gene interactions during formation of the dorsoventral pattern in Drosophila embryos. (1983)
10.1101/gad.5.5.827
Small, S., Blair, A. and Levine. M. 1992. Regulation of even-skipped stripe 2 in the Drosophila embryo. EMBO J. in press. (10.1002/j.1460-2075.1992.tb05498.x)
10.1016/0378-1119(88)90005-4
10.1038/341331a0
10.1126/science.1683715
10.1016/0092-8674(91)90381-8
10.1126/science.3118464
10.1016/0092-8674(89)90773-3
10.1016/0092-8674(89)90062-7
10.1007/BF00291041
10.1101/gad.1.7.709
10.1016/0092-8674(91)90014-P
10.1016/0378-1119(88)90177-1

Dates

Type	When
Created	18 years, 2 months ago (June 5, 2007, 5:15 p.m.)
Deposited	3 years, 9 months ago (Nov. 13, 2021, 11:27 p.m.)
Indexed	3 months, 2 weeks ago (May 10, 2025, 11:44 a.m.)
Issued	32 years, 11 months ago (Sept. 1, 1992)
Published	32 years, 11 months ago (Sept. 1, 1992)
Published Online	32 years, 11 months ago (Sept. 1, 1992)
Published Print	32 years, 11 months ago (Sept. 1, 1992)

Funders 0

None

BibTeX

@article{Ip_1992, title={The dorsal gradient morphogen regulates stripes of rhomboid expression in the presumptive neuroectoderm of the Drosophila embryo.}, volume={6}, ISSN={1549-5477}, url={http://dx.doi.org/10.1101/gad.6.9.1728}, DOI={10.1101/gad.6.9.1728}, number={9}, journal={Genes & Development}, publisher={Cold Spring Harbor Laboratory}, author={Ip, Y T and Park, R E and Kosman, D and Bier, E and Levine, M}, year={1992}, month=sep, pages={1728–1739} }

JSON

{
  "indexed": {
    "date-parts": [
      [
        2025,
        5,
        10
      ]
    ],
    "date-time": "2025-05-10T15:44:26Z",
    "timestamp": 1746891866927
  },
  "reference-count": 54,
  "publisher": "Cold Spring Harbor Laboratory",
  "issue": "9",
  "content-domain": {
    "domain": [],
    "crossmark-restriction": false
  },
  "published-print": {
    "date-parts": [
      [
        1992,
        9
      ]
    ]
  },
  "abstract": "<jats:p>rhomboid (rho) encodes a putative transmembrane receptor that is required for the differentiation of the ventral epidermis. It is initially expressed before the completion of cellularization in lateral stripes within the presumptive neuroectoderm. Here, we present evidence that the maternal morphogen dorsal (dl) acts in concert with basic helix-loop-helix (b-HLH) proteins, possibly including twist (twi), to activate rho in both lateral and ventral regions. Expression is blocked in ventral regions (the presumptive mesoderm) by snail (sna), which is also a direct target of the dl morphogen. A 300-bp region of the rho promoter (the NEE), which is sufficient for neuroectoderm expression, contains a cluster of dl and b-HLH activator sites that are closely linked to sna repressor sites. Mutations in these binding sites cause genetically predicted changes in the levels and limits of rho expression. In particular, the disruption of sna-binding sites causes a derepression of the pattern throughout ventral regions, providing evidence that sna is directly responsible for establishing the mesoderm/neuroectoderm boundary before gastrulation. The tight linkage of activator and repressor sites in the rho NEE is similar to the arrangement of binding sites observed in the even-skipped stripe 2 element, which is regulated by bicoid (bcd). This suggests that the dl and bcd morphogens use a similar mechanism to make stripes in the Drosophila embryo.</jats:p>",
  "DOI": "10.1101/gad.6.9.1728",
  "type": "journal-article",
  "created": {
    "date-parts": [
      [
        2007,
        6,
        5
      ]
    ],
    "date-time": "2007-06-05T21:15:46Z",
    "timestamp": 1181078146000
  },
  "page": "1728-1739",
  "source": "Crossref",
  "is-referenced-by-count": 265,
  "title": "The dorsal gradient morphogen regulates stripes of rhomboid expression in the presumptive neuroectoderm of the Drosophila embryo.",
  "prefix": "10.1101",
  "volume": "6",
  "author": [
    {
      "given": "Y T",
      "family": "Ip",
      "sequence": "first",
      "affiliation": []
    },
    {
      "given": "R E",
      "family": "Park",
      "sequence": "additional",
      "affiliation": []
    },
    {
      "given": "D",
      "family": "Kosman",
      "sequence": "additional",
      "affiliation": []
    },
    {
      "given": "E",
      "family": "Bier",
      "sequence": "additional",
      "affiliation": []
    },
    {
      "given": "M",
      "family": "Levine",
      "sequence": "additional",
      "affiliation": []
    }
  ],
  "member": "246",
  "published-online": {
    "date-parts": [
      [
        1992,
        9,
        1
      ]
    ]
  },
  "reference": [
    {
      "key": "2021111320242785000_6.9.1728.1",
      "doi-asserted-by": "crossref",
      "first-page": "983",
      "DOI": "10.1242/dev.111.4.983",
      "article-title": "The snail gene required for mesoderm formation in Drosophila is expressed dynamically in derivatives of all three germ layers.",
      "volume": "111",
      "year": "1991",
      "journal-title": "Development"
    },
    {
      "key": "2021111320242785000_6.9.1728.2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0168-9525(87)90191-0"
    },
    {
      "key": "2021111320242785000_6.9.1728.3",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0092-8674(85)90274-0"
    },
    {
      "key": "2021111320242785000_6.9.1728.4",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0092-8674(85)90275-2"
    },
    {
      "key": "2021111320242785000_6.9.1728.5",
      "doi-asserted-by": "publisher",
      "DOI": "10.1101/gad.4.2.190"
    },
    {
      "key": "2021111320242785000_6.9.1728.6",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/330395a0"
    },
    {
      "key": "2021111320242785000_6.9.1728.7",
      "doi-asserted-by": "publisher",
      "DOI": "10.1101/gad.3.10.1518"
    },
    {
      "key": "2021111320242785000_6.9.1728.8",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/340363a0"
    },
    {
      "key": "2021111320242785000_6.9.1728.9",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.1900130"
    },
    {
      "key": "2021111320242785000_6.9.1728.10",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0092-8674(90)90276-K"
    },
    {
      "key": "2021111320242785000_6.9.1728.11",
      "first-page": "119",
      "article-title": "Dorsoventral pattern formation in Drosophila.",
      "volume": "7",
      "year": "1991",
      "journal-title": "Trends Genet."
    },
    {
      "key": "2021111320242785000_6.9.1728.12",
      "first-page": "4598",
      "article-title": "DNA-binding activities of the Drosophila melanogaster even-skipped protein are mediated by its homeo domain and influenced by protein context.",
      "volume": "8",
      "year": "1988",
      "journal-title": "Mol. Cell. Biol."
    },
    {
      "key": "2021111320242785000_6.9.1728.13",
      "first-page": "15",
      "article-title": "The role of the dorsal morphogen gradient in Drosophila embryogenesis.",
      "volume": "3",
      "year": "1992",
      "journal-title": "Sem. Dev. Biol."
    },
    {
      "key": "2021111320242785000_6.9.1728.14",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0092-8674(91)90651-E"
    },
    {
      "key": "2021111320242785000_6.9.1728.15",
      "doi-asserted-by": "publisher",
      "DOI": "10.1101/gad.6.8.1518"
    },
    {
      "key": "2021111320242785000_6.9.1728.16",
      "doi-asserted-by": "publisher",
      "DOI": "10.1101/gad.1.8.868"
    },
    {
      "key": "2021111320242785000_6.9.1728.17",
      "doi-asserted-by": "publisher",
      "DOI": "10.1101/gad.5.10.1881"
    },
    {
      "key": "2021111320242785000_6.9.1728.18",
      "doi-asserted-by": "crossref",
      "first-page": "3147",
      "DOI": "10.1002/j.1460-2075.1992.tb05387.x",
      "article-title": "Individual dorsal binding sites mediate activation and repression in the Drosophila embryo.",
      "volume": "11",
      "year": "1992",
      "journal-title": "EMBO J."
    },
    {
      "key": "2021111320242785000_6.9.1728.19",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.89.8.3414"
    },
    {
      "key": "2021111320242785000_6.9.1728.20",
      "first-page": "5228",
      "article-title": "Yeast repressor a2 binds to its operator cooperatively with yeast protein MCM1.",
      "volume": "9",
      "year": "1989",
      "journal-title": "Mol. Cell. Biol."
    },
    {
      "key": "2021111320242785000_6.9.1728.21",
      "doi-asserted-by": "publisher",
      "DOI": "10.1101/gad.5.5.868"
    },
    {
      "key": "2021111320242785000_6.9.1728.22",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0092-8674(90)90275-J"
    },
    {
      "key": "2021111320242785000_6.9.1728.23",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.1925551"
    },
    {
      "key": "2021111320242785000_6.9.1728.24",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.3109035"
    },
    {
      "key": "2021111320242785000_6.9.1728.25",
      "doi-asserted-by": "publisher",
      "DOI": "10.1101/gad.5.9.1568"
    },
    {
      "key": "2021111320242785000_6.9.1728.26",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0092-8674(88)90418-7"
    },
    {
      "key": "2021111320242785000_6.9.1728.27",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0092-8674(89)90024-X"
    },
    {
      "key": "2021111320242785000_6.9.1728.28",
      "doi-asserted-by": "publisher",
      "DOI": "10.1101/gad.2.11.1496"
    },
    {
      "key": "2021111320242785000_6.9.1728.29",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0092-8674(89)90682-X"
    },
    {
      "key": "2021111320242785000_6.9.1728.30",
      "doi-asserted-by": "publisher",
      "DOI": "10.1101/gad.5.10.1892"
    },
    {
      "key": "2021111320242785000_6.9.1728.31",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0092-8674(90)90414-A"
    },
    {
      "key": "2021111320242785000_6.9.1728.32",
      "doi-asserted-by": "publisher",
      "DOI": "10.1101/gad.5.9.1577"
    },
    {
      "key": "2021111320242785000_6.9.1728.33",
      "doi-asserted-by": "crossref",
      "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",
      "year": "1991",
      "journal-title": "Development"
    },
    {
      "key": "2021111320242785000_6.9.1728.34",
      "doi-asserted-by": "crossref",
      "first-page": "2085",
      "DOI": "10.1002/j.1460-2075.1987.tb02474.x",
      "article-title": "The achaete-scute complex is expressed in the neurogenic regions of Drosophila embryos.",
      "volume": "6",
      "year": "1987",
      "journal-title": "EMBO J."
    },
    {
      "key": "2021111320242785000_6.9.1728.35",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0092-8674(89)90774-5"
    },
    {
      "key": "2021111320242785000_6.9.1728.36",
      "first-page": "173",
      "article-title": "Dorsal-ventral polarity and pattern formation in Drosophila. Pattern formation in Drosophila.",
      "volume": "1",
      "year": "1990",
      "journal-title": "Sem. Cell Biol."
    },
    {
      "key": "2021111320242785000_6.9.1728.37",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/330583a0"
    },
    {
      "key": "2021111320242785000_6.9.1728.38",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0092-8674(89)90772-1"
    },
    {
      "key": "2021111320242785000_6.9.1728.39",
      "doi-asserted-by": "crossref",
      "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",
      "year": "1987",
      "journal-title": "EMBO J."
    },
    {
      "key": "2021111320242785000_6.9.1728.40",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0092-8674(86)90346-6"
    },
    {
      "key": "2021111320242785000_6.9.1728.41",
      "doi-asserted-by": "crossref",
      "first-page": "615",
      "DOI": "10.1093/genetics/105.3.615",
      "article-title": "Matemal-zygotic gene interactions during formation of the dorsoventral pattern in Drosophila embryos.",
      "volume": "105",
      "year": "1983",
      "journal-title": "Genetics"
    },
    {
      "key": "2021111320242785000_6.9.1728.42",
      "doi-asserted-by": "publisher",
      "DOI": "10.1101/gad.5.5.827"
    },
    {
      "key": "2021111320242785000_6.9.1728.43",
      "doi-asserted-by": "crossref",
      "unstructured": "Small, S., Blair, A. and Levine. M. 1992. Regulation of even-skipped stripe 2 in the Drosophila embryo. EMBO J. in press.",
      "DOI": "10.1002/j.1460-2075.1992.tb05498.x"
    },
    {
      "key": "2021111320242785000_6.9.1728.44",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0378-1119(88)90005-4"
    },
    {
      "key": "2021111320242785000_6.9.1728.45",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/341331a0"
    },
    {
      "key": "2021111320242785000_6.9.1728.46",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.1683715"
    },
    {
      "key": "2021111320242785000_6.9.1728.47",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0092-8674(91)90381-8"
    },
    {
      "key": "2021111320242785000_6.9.1728.48",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.3118464"
    },
    {
      "key": "2021111320242785000_6.9.1728.49",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0092-8674(89)90773-3"
    },
    {
      "key": "2021111320242785000_6.9.1728.50",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0092-8674(89)90062-7"
    },
    {
      "key": "2021111320242785000_6.9.1728.51",
      "doi-asserted-by": "publisher",
      "DOI": "10.1007/BF00291041"
    },
    {
      "key": "2021111320242785000_6.9.1728.52",
      "doi-asserted-by": "publisher",
      "DOI": "10.1101/gad.1.7.709"
    },
    {
      "key": "2021111320242785000_6.9.1728.53",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0092-8674(91)90014-P"
    },
    {
      "key": "2021111320242785000_6.9.1728.54",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0378-1119(88)90177-1"
    }
  ],
  "container-title": "Genes &amp; Development",
  "original-title": [],
  "language": "en",
  "link": [
    {
      "URL": "https://syndication.highwire.org/content/doi/10.1101/gad.6.9.1728",
      "content-type": "unspecified",
      "content-version": "vor",
      "intended-application": "similarity-checking"
    }
  ],
  "deposited": {
    "date-parts": [
      [
        2021,
        11,
        14
      ]
    ],
    "date-time": "2021-11-14T04:27:59Z",
    "timestamp": 1636864079000
  },
  "score": 1,
  "resource": {
    "primary": {
      "URL": "http://genesdev.cshlp.org/lookup/doi/10.1101/gad.6.9.1728"
    }
  },
  "subtitle": [],
  "short-title": [],
  "issued": {
    "date-parts": [
      [
        1992,
        9
      ]
    ]
  },
  "references-count": 54,
  "journal-issue": {
    "issue": "9",
    "published-print": {
      "date-parts": [
        [
          1992,
          9
        ]
      ]
    }
  },
  "alternative-id": [
    "10.1101/gad.6.9.1728"
  ],
  "URL": "http://dx.doi.org/10.1101/gad.6.9.1728",
  "relation": {},
  "ISSN": [
    "0890-9369",
    "1549-5477"
  ],
  "subject": [],
  "container-title-short": "Genes Dev.",
  "published": {
    "date-parts": [
      [
        1992,
        9
      ]
    ]
  }
}