Abstract

BackgroundThe organization of the different tissues of an animal requires mechanisms that regulate cell-cell adhesion to promote and maintain the physical separation of adjacent cell populations. In the Drosophila imaginal wing disc the iroquois homeobox genes are expressed in the notum anlage and contribute to the specification of notum identity. These genes are not expressed in the adjacent wing hinge territory. These territories are separated by an approximately straight boundary that in the mature disc is associated with an epithelial fold. The mechanism by which these two cell populations are kept separate is unclear.ResultsHere we show that the Iro-C genes participate in keeping the notum and wing cell populations separate. Indeed, within the notum anlage, cells not expressing Iro-C tend to join together and sort out from their Iro-C expressing neighbours. We also show that apposition of Iro-C expressing and non-expressing cells induces invagination and apico-basal shortening of the Iro-C- cells. This effect probably underlies formation of the fold that separates the notum and wing hinge territories. In addition, cells overexpressing a member of the Iro-C contact one another and become organized in a network of thin strings that surrounds and isolates large groups of non-overexpressing cells. The strings appear to exert a pulling force along their longitudinal axis.ConclusionApposition of cells expressing and non-expressing the Iro-C, as it occurs in the notum-wing hinge border of the Drosophila wing disc, influences cell behaviour. It leads to cell sorting, and cellular invagination and apical-basal shortening. These effects probably account for keeping the prospective notum and wing hinge cell populations separate and underlie epithelial fold formation. Cells that overexpress a member of the Iro-C and that confront non-expressing cells establish contacts between themselves and become organized in a network of thin strings. This is a complex and unique phenotype that might be important for the generation of a straight notum-wing hinge border.

Highlights

  • The organization of the different tissues of an animal requires mechanisms that regulate cell-cell adhesion to promote and maintain the physical separation of adjacent cell populations

  • We have shown that cell sorting behaviour occurs in the intact wing disc: Iro-Ccells located within the notum, which will develop as wing hinge cells, have a tendency to join together and minimize contacts with wild-type cells

  • This behaviour seems to be induced by the different levels of Iro-C homeoproteins that occur in the apposing cells, rather than by the transformation of notum cells to hinge cells, since homozygous Iro-C+ cells tend to join together when located in an heterozygous Iro-C+/- background of non-transformed cells

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Summary

Introduction

The organization of the different tissues of an animal requires mechanisms that regulate cell-cell adhesion to promote and maintain the physical separation of adjacent cell populations. Development of an organism requires that adjacent cell populations acquire different cell fates and give rise to different tissues This is accomplished by the activation of specific sets of genes in each of the cell populations. In Drosophila, developmental boundaries were discovered in the wings, by means of genetically marked recombination clones, as straight lines that proliferating cells did not trespass [1] (reviewed by [2,3,4,5]). One of these boundaries corresponded to an invisible line that subdivided the wing into anterior (A) and posterior (P) compartments. The short-range signalling gave rise to longrange signalling that organized the growth and patterning of the entire wing

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