Home LiteratureArticle Details
PMID: 9303541 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

The homeobox gene Distal-less induces ventral appendage development in Drosophila.

Genes & development ·Vol. 11 ·No. 17 ·1997-09-01 ·Pages 2259-71

Gorfinkiel N, Morata G, Guerrero I

Abstract

This study investigates the role of the homeobox gene Distal-less (Dll) in the development of the legs, antennae, and wings of Drosophila. Lack of Dll function causes a change in the identity of ventral appendage cells (legs and antennae) that often results in the loss of the appendage. Ectopic Dll expression in the proximal region of ventral appendages induces nonautonomous duplication of legs and antennae by the activation of wingless and decapentaplegic. Ectopic Dll expression in dorsal appendages produces transformation into corresponding ventral appendages; wings and halteres develop ectopic legs and the head-eye region develops ectopic antennae. In the wing, the exogenous Dll product induces this transformation by activating the endogenous Dll gene and repressing the wing determinant gene vestigial. It is proposed that Dll induces the development of ventral appendages and also participates in a genetic address that specifies the identity of ventral appendages and discriminates the dorsal versus the ventral appendages in the adult. However, unlike other homeotic genes, Dll expression and function is not defined by a cell lineage border. Dll also performs a secondary and late function required for the normal patterning of the wing.

MeSH Terms
Animals Animals, Genetically Modified Drosophila/genetics,growth & development Extremities/growth & development Female Gene Expression Regulation, Developmental Genes, Homeobox Genes, Insect Genes, Reporter Male Phenotype Sense Organs/growth & development Wings, Animal/growth & development
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Gorfinkiel N
Centro de Biología Molecular Severo Ochoa (CSIC-UAM), Universidad Autónoma de Madrid, Cantoblanco, Spain.
Morata G
Guerrero I
References (71)
71 references, click to expand
  1. A gene complex controlling segmentation in Drosophila.
    Nature. 1978 Dec 7;276(5688):565-70 PMID: 103000
  2. Control of compartment development by the engrailed gene in Drosophila.
    Nature. 1975 Jun 19;255(5510):614-7 PMID: 1134551
  3. apterous, a gene required for imaginal disc development in Drosophila encodes a member of the LIM family of developmental regulatory proteins.
    Genes Dev. 1992 May;6(5):715-29 PMID: 1349545
  4. Homeotic genes of the Bithorax complex repress limb development in the abdomen of the Drosophila embryo through the target gene Distal-less.
    Cell. 1992 Oct 30;71(3):437-50 PMID: 1358457
  5. Localization of the Antennapedia protein in Drosophila embryos and imaginal discs.
    EMBO J. 1986 Dec 1;5(12):3327-34 PMID: 16453732
  6. Proximal-distal pattern formation in Drosophila: cell autonomous requirement for Distal-less gene activity in limb development.
    EMBO J. 1989 Jul;8(7):2045-55 PMID: 16453891
  7. Control of Drosophila wing and haltere development by the nuclear vestigial gene product.
    Genes Dev. 1991 Dec;5(12B):2481-95 PMID: 1752439
  8. The segment polarity gene armadillo interacts with the wingless signaling pathway in both embryonic and adult pattern formation.
    Development. 1991 Apr;111(4):1029-43 PMID: 1879348
  9. An extensive 3' cis-regulatory region directs the imaginal disk expression of decapentaplegic, a member of the TGF-beta family in Drosophila.
    Development. 1991 Mar;111(3):657-66 PMID: 1908769
  10. Site-specific recombination between homologous chromosomes in Drosophila.
    Science. 1991 May 17;252(5008):958-61 PMID: 2035025
  11. Spatial and temporal control elements of the Drosophila engrailed gene.
    Genes Dev. 1990 Mar;4(3):433-43 PMID: 2110923
  12. Genetic mosaic analysis of decapentaplegic and wingless gene function in the Drosophila leg.
    Dev Genes Evol. 1996 Nov;206(3):180-94 PMID: 24173520
  13. Distal-less encodes a homoeodomain protein required for limb development in Drosophila.
    Nature. 1989 Mar 30;338(6214):432-4 PMID: 2564639
  14. Expression of engrailed proteins in arthropods, annelids, and chordates.
    Cell. 1989 Sep 8;58(5):955-68 PMID: 2570637
  15. Developmental analysis of some mutants of the bithorax system ofDrosophila.
    Wilehm Roux Arch Dev Biol. 1976 Jun;179(2):125-143 PMID: 28304753
  16. Establishment of compartments in the developing leg imaginal discs ofDrosophila melanogaster.
    Wilehm Roux Arch Dev Biol. 1976 Mar;180(1):9-30 PMID: 28304893
  17. Brista: a gene involved in the specification and differentiation of distal cephalic and thoracic structures in Drosophila melanogaster.
    Roux Arch Dev Biol. 1987 Feb;196(2):124-132 PMID: 28305467
  18. Proximal-distal pattern formation inDrosophila: graded requirement forDistal-less gene activity during limb development.
    Roux Arch Dev Biol. 1989 Oct;198(3):157-169 PMID: 28305718
  19. Interactions of decapentaplegic, wingless, and Distal-less in the Drosophila leg.
    Roux Arch Dev Biol. 1994 May;203(6):310-319 PMID: 28305824
  20. Spatial and temporal expression of an Antennapedia/lac Z gene construct integrated into the endogenous Antennapedia gene of Drosophila melanogaster.
    Roux Arch Dev Biol. 1992 Apr;201(2):65-80 PMID: 28305895
  21. Initiation of the proximodistal axis in insect legs
    Development. 1995 Mar 01;121(3):619-28 PMID: 29708314
  22. Redesigning the body plan of Drosophila by ectopic expression of the homoeotic gene Antennapedia.
    Nature. 1987 Feb 26-Mar 4;325(6107):816-8 PMID: 3821869
  23. Genetic organization of Drosophila bithorax complex.
    Nature. 1985 Jan 10-18;313(5998):108-13 PMID: 3917555
  24. Recessive lethal mutations within the bithorax-complex in Drosophila.
    Mol Gen Genet. 1985;200(2):335-42 PMID: 3929021
  25. Pattern formation and determination in the antenna of the homoeotic mutant Antennapedia of Drosophila melanogaster.
    Dev Biol. 1971 Aug;25(4):606-40 PMID: 5001609
  26. [Formation of a complete mid leg with sternopleura in the antennae region by the mutant Nasobemia (Ns) of Drosophila melanogaster].
    Arch Julius Klaus Stift Vererbungsforsch Sozialanthropol Rassenhyg. 1967;41(2-4):44-54 PMID: 5631505
  27. [The imaginal cells of the clypeolabrum and the formation of labial disks in Drosophila melanogaster].
    Rev Suisse Zool. 1967 Dec;74(3):589-96 PMID: 6081341
  28. Genes controlling segmental specification in the Drosophila thorax.
    Proc Natl Acad Sci U S A. 1982 Dec;79(23):7380-4 PMID: 6961417
  29. A homoeotic mutation transforming leg to antenna in Drosophila.
    Nature. 1981 Aug 13;292(5824):635-8 PMID: 7254358
  30. Gene disruptions using P transposable elements: an integral component of the Drosophila genome project.
    Proc Natl Acad Sci U S A. 1995 Nov 21;92(24):10824-30 PMID: 7479892
  31. How the Hox gene Ultrabithorax specifies two different segments: the significance of spatial and temporal regulation within metameres.
    Development. 1995 Sep;121(9):2973-82 PMID: 7555723
  32. Creating a Drosophila wing de novo, the role of engrailed, and the compartment border hypothesis.
    Development. 1995 Oct;121(10):3359-69 PMID: 7588069
  33. The function of engrailed and the specification of Drosophila wing pattern.
    Development. 1995 Oct;121(10):3447-56 PMID: 7588077
  34. Control of Drosophila adult pattern by extradenticle.
    Development. 1995 Jul;121(7):2117-25 PMID: 7635057
  35. Axes, boundaries and coordinates: the ABCs of fly leg development.
    Bioessays. 1995 Aug;17(8):721-32 PMID: 7661853
  36. Dual functions of wingless in the Drosophila leg imaginal disc.
    Development. 1995 Feb;121(2):477-88 PMID: 7768188
  37. dachshund encodes a nuclear protein required for normal eye and leg development in Drosophila.
    Development. 1994 Dec;120(12):3473-86 PMID: 7821215
  38. Induction of ectopic eyes by targeted expression of the eyeless gene in Drosophila.
    Science. 1995 Mar 24;267(5205):1788-92 PMID: 7892602
  39. 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. 1993 Oct;119(2):339-51 PMID: 7904556
  40. Pattern formation in the limbs of Drosophila: bric à brac is expressed in both a gradient and a wave-like pattern and is required for specification and proper segmentation of the tarsus.
    Development. 1993 Nov;119(3):799-812 PMID: 7910551
  41. Homeobox genes: their function in Drosophila segmentation and pattern formation.
    Cell. 1994 Jul 29;78(2):181-9 PMID: 7913879
  42. Targeted expression of the signaling molecule decapentaplegic induces pattern duplications and growth alterations in Drosophila wings.
    EMBO J. 1994 Oct 3;13(19):4459-68 PMID: 7925288
  43. Cell interaction between compartments establishes the proximal-distal axis of Drosophila legs.
    Nature. 1994 Nov 10;372(6502):175-9 PMID: 7969450
  44. wingless acts through the shaggy/zeste-white 3 kinase to direct dorsal-ventral axis formation in the Drosophila leg.
    Development. 1994 Jun;120(6):1661-70 PMID: 8050372
  45. Compartment boundaries and the control of Drosophila limb pattern by hedgehog protein.
    Nature. 1994 Mar 17;368(6468):208-14 PMID: 8145818
  46. The wingless signalling pathway and the patterning of the wing margin in Drosophila.
    Development. 1994 Mar;120(3):621-36 PMID: 8162860
  47. Targeted gene expression as a means of altering cell fates and generating dominant phenotypes.
    Development. 1993 Jun;118(2):401-15 PMID: 8223268
  48. wingless expression mediates determination of peripheral nervous system elements in late stages of Drosophila wing disc development.
    Development. 1993 Jun;118(2):427-38 PMID: 8223270
  49. Interaction between dorsal and ventral cells in the imaginal disc directs wing development in Drosophila.
    Cell. 1993 Nov 19;75(4):741-52 PMID: 8242746
  50. The basic-helix-loop-helix domain of Drosophila lethal of scute protein is sufficient for proneural function and activates neurogenic genes.
    Cell. 1994 Jan 14;76(1):77-87 PMID: 8287481
  51. Allocation of the thoracic imaginal primordia in the Drosophila embryo.
    Development. 1993 Feb;117(2):597-608 PMID: 8330530
  52. Analysis of genetic mosaics in developing and adult Drosophila tissues.
    Development. 1993 Apr;117(4):1223-37 PMID: 8404527
  53. A wingless-dependent polar coordinate system in Drosophila imaginal discs.
    Science. 1993 Jan 22;259(5094):484-9 PMID: 8424170
  54. Organizing activity of wingless protein in Drosophila.
    Cell. 1993 Feb 26;72(4):527-40 PMID: 8440019
  55. Serrate signals through Notch to establish a Wingless-dependent organizer at the dorsal/ventral compartment boundary of the Drosophila wing.
    Development. 1995 Dec;121(12):4215-25 PMID: 8575321
  56. decapentaplegic overexpression affects Drosophila wing and leg imaginal disc development and wingless expression.
    Dev Biol. 1996 Jul 10;177(1):136-51 PMID: 8660883
  57. Dpp receptors are autonomously required for cell proliferation in the entire developing Drosophila wing.
    Development. 1996 Jul;122(7):2261-9 PMID: 8681806
  58. Integration of positional signals and regulation of wing formation and identity by Drosophila vestigial gene.
    Nature. 1996 Jul 11;382(6587):133-8 PMID: 8700202
  59. Decapentaplegic restricts the domain of wingless during Drosophila limb patterning.
    Nature. 1996 Jul 11;382(6587):162-4 PMID: 8700205
  60. Antagonistic interactions between wingless and decapentaplegic responsible for dorsal-ventral pattern in the Drosophila Leg.
    Science. 1996 Sep 6;273(5280):1373-7 PMID: 8703069
  61. Complementary and mutually exclusive activities of decapentaplegic and wingless organize axial patterning during Drosophila leg development.
    Cell. 1996 Aug 9;86(3):401-9 PMID: 8756722
  62. Visualization of gene expression in living adult Drosophila.
    Science. 1996 Oct 11;274(5285):252-5 PMID: 8824191
  63. The fu gene discriminates between pathways to control dpp expression in Drosophila imaginal discs.
    Mech Dev. 1996 Apr;55(2):159-70 PMID: 8861096
  64. Dual roles for patched in sequestering and transducing Hedgehog.
    Cell. 1996 Nov 1;87(3):553-63 PMID: 8898207
  65. Direct and long-range action of a wingless morphogen gradient.
    Cell. 1996 Nov 29;87(5):833-44 PMID: 8945511
  66. Ectopic expression of wingless in imaginal discs interferes with decapentaplegic expression and alters cell determination.
    Development. 1996 Nov;122(11):3519-29 PMID: 8951067
  67. Genetic evidence for the subdivision of the arthropod limb into coxopodite and telopodite.
    Development. 1996 Dec;122(12):3921-8 PMID: 9012512
  68. Developmental territories created by mutual antagonism between Wingless and Decapentaplegic.
    Development. 1996 Dec;122(12):3939-48 PMID: 9012514
  69. Induction of Drosophila eye development by decapentaplegic.
    Development. 1997 Jan;124(2):271-8 PMID: 9053304
  70. Expression and function of decapentaplegic and thick veins during the differentiation of the veins in the Drosophila wing.
    Development. 1997 Mar;124(5):1007-18 PMID: 9056776
  71. Shaggy and dishevelled exert opposite effects on Wingless and Decapentaplegic expression and on positional identity in imaginal discs.
    Development. 1997 Mar;124(5):1069-78 PMID: 9056781
Article Info
Journal
Genes & development
Abbr.
Genes Dev
ISSN
0890-9369
DOI
10.1101/gad.11.17.2259
Published
1997-09-01
Pages
2259-71
Language
English
Region
United States
NLM ID
8711660
PMCID
PMC275395
Subset
IM
External Links
PubMed source DOI: 10.1101/gad.11.17.2259 PMC Full Text View journal details
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2