Three distinct roles for the engrailed gene in Drosophila wing development

Curr Biol. 1994 Dec 1;4(12):1087-98. doi: 10.1016/s0960-9822(00)00247-5.

Abstract

Background: The development of Drosophila includes stages at which the future component parts of the adult seem to be divided into distinct anterior and posterior compartments, with clones of cells restricted by their lineage to only one of the two compartments. The engrailed gene is thought to be a 'selector' gene that controls the expression of other genes to confer a 'posterior identity' on groups of cells that are related to each other by lineage. Consistent with this notion, engrailed encodes a homeo-domain-containing transcription factor that is expressed in all posterior developmental compartments of the fly. In this paper, the processes that are regulated by engrailed during morphogenesis of the fly wing are analyzed.

Results: The effects of a total lack of engrailed function in the wing have been analyzed for the first time. This has revealed three different requirements for engrailed during wing development. It has a late role in patterning the wing margin, which includes cells within the anterior compartment. In addition, it is involved in the cell-cell interactions that maintain the expression of the decapentaplegic gene along the antero-posterior compartment boundary; decapentaplegic, in turn, controls growth through a mechanism that depends on the activity of the gene hedgehog, and the maintenance of the compartment boundary depends on these cell-cell interactions. Finally, there is a global requirement for engrailed in the control of growth through a hedgehog-independent mechanism. In fact, cell proliferation is induced after removal of the functions provided by both engrailed and a second gene, patched.

Conclusions: The multiple roles of engrailed and the temporal specificity for each function of the gene suggest that engrailed does not act simply by assigning an identity to cells, as had been supposed previously, but rather that is has more complex roles. Establishment and maintenance of the antero-posterior compartment boundary does not depend exclusively on the engrailed gene product. In addition, engrailed plays a major role in the control of growth by a pathway independent of putative inducing signals.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cell Communication
  • Cell Division
  • Drosophila / embryology*
  • Drosophila / genetics
  • Drosophila / physiology
  • Drosophila Proteins*
  • Gene Expression
  • Gene Expression Regulation, Developmental / genetics
  • Gene Expression Regulation, Developmental / physiology
  • Hedgehog Proteins
  • Homeodomain Proteins*
  • Insect Hormones / genetics*
  • Insect Hormones / physiology*
  • Male
  • Membrane Proteins / genetics
  • Membrane Proteins / physiology
  • Mutation
  • Proteins / genetics
  • Proteins / physiology
  • Receptors, Cell Surface
  • Transcription Factors / genetics*
  • Transcription Factors / physiology*
  • Wings, Animal / embryology*

Substances

  • Drosophila Proteins
  • En protein, Drosophila
  • Hedgehog Proteins
  • Homeodomain Proteins
  • Insect Hormones
  • Membrane Proteins
  • Proteins
  • Receptors, Cell Surface
  • Transcription Factors
  • dpp protein, Drosophila
  • inv protein, Drosophila
  • ptc protein, Drosophila
  • hh protein, Drosophila