Advertisement
JOURNAL ARTICLES
Creating a Drosophila wing de novo, the role of engrailed, and the compartment border hypothesis
T. Tabata, C. Schwartz, E. Gustavson, Z. Ali, T.B. Kornberg
Development 1995 121: 3359-3369;

Summary

Anterior/posterior compartment borders bisect every Drosophila imaginal disc, and the engrailed gene is essential for their function. We analyzed the role of the engrailed and invected genes in wing discs by eliminating or increasing their activity. Removing engrailed/invected from posterior wing cells created two new compartments: an anterior compartment consisting of mutant cells and a posterior compartment that grew from neighboring cells. In some cases, these compartments formed a complete new wing. Increasing engrailed activity also affected patterning. These findings demonstrate that engrailed both directs the posterior compartment pathway and creates the compartment border. These findings also establish the compartment border as the pre-eminent organizational feature of disc growth and patterning.

Reference

    1. Basler C.,
    2. Struhl G.
    (1994) Compartment boundaries and the control of Drosophila limb pattern by the hedgehog protein. Nature 368, 208–215
    OpenUrlCrossRefPubMedWeb of Science
    1. Blair S.
    (1993) Mechanisms of compartment formation: evidence that non-proliferating cells do not play a critical role in defining the D/V lineage restriction in the developing wing of Drosophila. Development 119, 339–51
    OpenUrlAbstract
    1. Blair S. S.
    (1992) Engrailed expression in the anterior lineage compartment of the developing wing blade of Drosophila. Development 115, 21–33
    OpenUrlAbstract
    1. Brand A. H.,
    2. Perrimon N.
    (1993) Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118, 401–415
    OpenUrlAbstract
    1. Campbell G.,
    2. Weaver T.,
    3. Tomlinson A.
    (1993) Axis specification in the developing Drosophila appendage: the role of wingless, decapentaplegic, and the homeobox gene aristaless. Cell 74, 1113–1123
    OpenUrlCrossRefPubMedWeb of Science
    1. Capdevila J.,
    2. Guerrero I.
    (1994) Targeted expression of the signaling molecule decapentaplegic induces pattern duplications and growth alterations in Drosophila wings. EMBO J 13, 4459–68
    OpenUrlPubMedWeb of Science
    1. Coleman K. G.,
    2. Poole S. J.,
    3. Weir M. P.,
    4. Soeller W. C.,
    5. Kornberg T. B.
    (1987) The invected gene of Drosophila: sequence analysis and expression studies reveal a close kinship to the engrailed gene. Genes Dev 1, 19–28
    OpenUrlAbstract/FREE Full Text
    1. Diaz-Benjumea F. a. C. S.
    (1993) Interaction between dorsal and ventral cells in the imaginal disc direct wing development in Drosophila. Cell 75, 741–752
    OpenUrlCrossRefPubMedWeb of Science
    1. Eaton S.,
    2. Kornberg T.B.
    (1990) Repression of ci-D in posterior compartments of Drosophila by engrailed. Genes Dev 4, 1068–1077
    OpenUrlAbstract/FREE Full Text
    1. Garcia-Bellido A.,
    2. Ripoll P.,
    3. Morata G.
    (1973) Developmental compartmentalization of the wing disc of Drosophila. Nature New Biol 245, 251–253
    OpenUrlCrossRefPubMedWeb of Science
    1. Garcia-Bellido A.,
    2. Santamaria P.
    (1972) Developmental analysis of the wing disc in the mutant engrailed of Drosophila melanogaster. Genetics 72, 87–104
    OpenUrlAbstract/FREE Full Text
    1. Golic K.
    (1991) Site-specific recombination between homologous chromosomes in Drosophila segmentation and pattern formation. Science 252, 958–961
    OpenUrlAbstract/FREE Full Text
    1. Hama C.,
    2. Ali Z.,
    3. Kornberg T. B.
    (1990) Region-specific recombination and expression are directed by portions of the Drosophila engrailed promoter. Genes Dev 4, 1079–1093
    OpenUrlAbstract/FREE Full Text
    1. Hidalgo A.
    (1995) Three distinct roles for the engrailed gene in Drosophila wing development. Current Biology 4, 1087–1098
    OpenUrl
    1. Jiang J.,
    2. Struhl G.
    (1995) Protein kinase A and hedgehog signaling in Drosophila limb development. Cell 80, 563–572
    OpenUrlCrossRefPubMedWeb of Science
    1. Kojima T.,
    2. Michiue T.,
    3. Orihara M.,
    4. Saigo K.
    (1994) Induction of a mirror-image duplication of anterior wing structures by localized hedgehog expression in the anterior compartment of Drosophila melanogaster wing imaginal discs. Gene 148, 211–217
    OpenUrlCrossRefPubMed
    1. Kornberg T.
    (1981) Compartments in the abdomen of Drosophila and the role of the engrailed locus. Dev. Biol 86, 363–381
    OpenUrlCrossRefPubMedWeb of Science
    1. Kornberg T.
    (1981) engrailed: A gene controlling compartment and segment formation in Drosophila. Proc. Nat. Acad. Sci. USA 78, 1095–1099
    OpenUrlAbstract/FREE Full Text
    1. Kornberg T.,
    2. Siden I.,
    3. O'Farrell P.,
    4. Simon M.
    (1985) The engrailed locus of Drosophila: in situ localization of transcripts reveals compartment-specific expression. Cell 40, 45–53
    OpenUrlCrossRefPubMedWeb of Science
    1. Lawrence P.,
    2. Morata G.
    (1976) Compartments in the wing of Drosophila: A study of the engrailed gene. Dev. Biol 50, 321–337
    OpenUrlCrossRefPubMedWeb of Science
    1. Lawrence P.,
    2. Morata G.
    (1994) Homeobox genes: their function in Drosophila segmentation and pattern formation. Cell 78, 181–190
    OpenUrlCrossRefPubMedWeb of Science
    1. Lawrence P.,
    2. Struhl G.
    (1982) Further studies on the engrailed phenotype in Drosophila. EMBO J 1, 827–833
    OpenUrlPubMedWeb of Science
    1. Lawrence P. A.
    (1973) A clonal analysis of segment development in Oncopeltus (Hemiptera). J. Embryol. exp. Morph 30, 681–699
    OpenUrlPubMedWeb of Science
    1. Morata G.,
    2. Lawrence P. A.
    (1975) Control of compartment development by the engrailed gene of Drosophila. Nature 255, 614–618
    OpenUrlCrossRefPubMed
    1. Mortin M.,
    2. Lefevre G.
    (1981) An RNA polymerase II mutation in Drosophila melanogaster that mimics Ultrabithorax. Chromosoma 82, 237–247
    OpenUrlCrossRefPubMed
    1. Padgett R. W.,
    2. St. Johnston D.,
    3. Gelbart W. M.
    (1987) A transcript from a Drosophila pattern gene predicts a protein homologous to the transforming growth factor-family. Nature 325, 81–84
    OpenUrlCrossRefPubMed
    1. Patel N. H.,
    2. Martin-Blanco E.,
    3. Coleman K.,
    4. Poole S.,
    5. Ellis M. C.,
    6. Kornberg T. B.,
    7. Goodman C. S.
    (1989) Expression of engrailed proteins in arthropods, annelids, and chordates. Cell 58, 955–968
    OpenUrlCrossRefPubMedWeb of Science
    1. Perrimon N.
    (1995) Hedgehog and beyond. Cell 80, 517–20
    OpenUrlCrossRefPubMedWeb of Science
    1. Phillips R. G.,
    2. Roberts I. J. H.,
    3. Ingham P. W.,
    4. Whittle R. S.
    (1990) The Drosophila segment polarity gene patched is involved in a position-signalling mechanism in imaginal discs. Development 110, 105–114
    OpenUrlAbstract
    1. Raftery L. A.,
    2. Sanicola M.,
    3. Blackman R. K.,
    4. Gelbart W. M.
    (1991) The relationship of decapentaplegic and engrailed expression in Drosophila imaginal disks: do these genes mark the anterior-posterior compartment boundary?. Development 113, 27–33
    OpenUrlAbstract
    1. Sanicola M.,
    2. Sekelsky J.,
    3. Elson S.,
    4. Gelbart W. M.
    (1995) Drawing a stripe in Drosophila imaginal disks: negative regulation of decapentaplegic and patched expression by engrailed. Genetics 139, 754–756
    OpenUrl
    1. Schwartz C.,
    2. Locke J.,
    3. Nishida C.,
    4. Kornberg T. B.
    (1995) Analysis of cubitus interruptus regulation in Drosophila embryos and imaginal disks. Development 121, 1626–35
    OpenUrl
    1. Slusarski D. C.,
    2. Motzny C. K.,
    3. Holmgren R.
    (1995) Mutations that alter the timing and pattern of cubitus interruptus gene expression in Drosophila melanogaster. Genetics 139, 229–240
    OpenUrlAbstract/FREE Full Text
    1. Spencer F. A.,
    2. Hoffmann F. M.,
    3. Gelbart W. M.
    (1982) Decapentaplegic: A gene complex affecting morphogenesis in Drosophila melanogaster. Cell 28, 451–461
    OpenUrlCrossRefPubMedWeb of Science
    1. Tabata T.,
    2. Eaton S. E.,
    3. Kornberg T. B.
    (1992) The Drosophila hedgehog gene is expressed specifically in posterior compartment cells and is a target of engrailed regulation. Genes Dev 6, 2635–2645
    OpenUrlAbstract/FREE Full Text
    1. Tabata T.,
    2. Kornberg T. B.
    (1994) Hedgehog is a signaling protein with a key role in patterning Drosophila imaginal discs. Cell 76, 89–102
    OpenUrlCrossRefPubMedWeb of Science
    1. Williams J. A.,
    2. Paddock S. W.,
    3. Carroll S. B.
    (1993) Pattern formation in a secondary field: a hierarchy of regulatory genes subdivides the developing Drosophila wing disc into discrete subregions. Development 117, 571–84
    OpenUrlAbstract
    1. Williams J. A.,
    2. Scott I. M.,
    3. Atkin A. L.,
    4. Brook W. J.,
    5. Russell M. A.,
    6. Bell J. B.
    (1990) Genetic and molecular analysis of vgU and vgW: two dominant vg alleles associated with gene fusions in Drosophila. Genetics 125, 833–844
    OpenUrlAbstract/FREE Full Text
    1. Xu T.,
    2. Rubin G. M.
    (1993) Analysis of genetic mosaics in developing and adult Drosophila tissues. Development 117, 1223–1237
    OpenUrlAbstract
Back to top

 Download PDF

Email
JOURNAL ARTICLES
Creating a Drosophila wing de novo, the role of engrailed, and the compartment border hypothesis
T. Tabata, C. Schwartz, E. Gustavson, Z. Ali, T.B. Kornberg
Development 1995 121: 3359-3369;
del.icio.us logo Digg logo Reddit logo Twitter logo CiteULike logo Facebook logo Google logo Mendeley logo
Citation Tools
Alerts

Article navigation

Other journals from The Company of Biologists

Advertisement

The people behind the papers – George Britton and Aryeh Warmflash

George and Aryeh

First author George Britton and his supervisor Aryeh Warmflash discuss their new Development paper in which they apply advanced in vitro culturing techniques to investigate embryonic ectoderm patterning.

Travelling Fellowship – New imaging approach unveils a bigger picture

Highlights from Travelling Fellowship trips

Find out how Pamela Imperadore’s Travelling Fellowship grant from The Company of Biologists took her to Germany, where she used new imaging techniques to investigate the cellular machinery underlying octopus arm regeneration. Don’t miss the next application deadline for 2020 travel, coming up on 29 November. Where will your research take you?

Protein function can be controlled by light using optogenetic techniques. In their new Primer, Stefano De Renzis and his colleagues in Heidelberg provide an overview of the most commonly used optogenetic tools and their application in developmental biology.

preLights – Self-organised symmetry breaking in zebrafish reveals feedback from morphogenesis to pattern formation

Sundar Naganathan

preLighter Sundar Naganathan explains his selected preprint by Vikas Trivedi, Benjamin Steventon and their co-workers on pescoids, a new in vitro model system to study early zebrafish embryogenesis.

Spotlight – Can laboratory model systems instruct human limb regeneration?

An extract from a schematic demonstrating the possible pipeline for how discovery in lab model systems can influence applications for regenerative therapies.

One of the most challenging objectives of tissue regeneration research is regrowth of a lost or amputated limb. Here, Ben Cox, Maximina Yun and Kenneth Poss outline the research avenues yet to be explored to move closer to this capstone achievement.

Articles of interest in our sister journals

Tox4 modulates cell fate reprogramming

Lotte Vanheer, Juan Song, Natalie De Geest, Adrian Janiszewski, Irene Talon, Caterina Provenzano, Taeho Oh, Joel Chappell, Vincent Pasque
Journal of Cell Science

Drosophila melanogaster: a simple system for understanding complexity

Stephanie E. Mohr, Norbert Perrimon
Disease Models & Mechanisms