Patterned Anchorage to the Apical Extracellular Matrix Defines Tissue Shape in the Developing Appendages of Drosophila

Summary

How tissues acquire their characteristic shape is a fundamental unresolved question in biology. While genes have been characterized that control local mechanical forces to elongate epithelial tissues, genes controlling global forces in epithelia have yet to be identified. Here, we describe a genetic pathway that shapes appendages in Drosophila by defining the pattern of global tensile forces in the tissue. In the appendages, shape arises from tension generated by cell constriction and localized anchorage of the epithelium to the cuticle via the apical extracellular-matrix protein Dumpy (Dp). Altering Dp expression in the developing wing results in predictable changes in wing shape that can be simulated by a computational model that incorporates only tissue contraction and localized anchorage. Three other wing shape genes, narrow, tapered, and lanceolate, encode components of a pathway that modulates Dp distribution in the wing to refine the global force pattern and thus wing shape.

Graphical Abstract

Highlights

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  The apical extracellular matrix protein Dumpy (Dp) is required for appendage shape

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  Dp anchors the epidermis to the cuticle, generating tension during tissue contraction

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  Alteration of the pattern of Dp gives rise to predictable changes in appendage shape

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  Narrow (Nw), Tapered (Ta), and Lanceolate (Ll) affect shape by modulating Dp

Abstract

Regulation of global tensile forces in epithelia is one mechanism of determining tissue shape. Ray and Matamoro-Vidal et al. show that tissue contraction, in combination with localized anchorage to the cuticle by the apical extracellular matrix protein Dumpy, gives rise to anisotropic tensions that shape the appendages in the Drosophila pupa.