Wnt/Wingless signaling in Drosophila

Abstract

The Wingless (Wg) pathway represents one of the best-characterized intercellular signaling networks. Studies performed in Drosophila over the last 30 years have contributed to our understanding of the role of Wg signaling in the regulation of tissue growth, polarity, and patterning. These studies have revealed mechanisms conserved in the vertebrate Wnt pathways and illustrate the elegance of using the Drosophila model to understand evolutionarily conserved modes of gene regulation. In this article, we describe the function of Wg signaling in patterning the Drosophila embryonic epidermis and wing imaginal disc. As well, we present an overview of the establishment of the Wg morphogen gradient and discuss the differential modes of Wg-regulated gene expression.

Figure 1.

Wingless-regulated patterning of the Drosophila embryonic epidermis. The interplay between the Wg and Hh signaling pathways initially establishes the parasegment boundaries and subsequently directs the intrasegmental pattern to establish the stereotypical arrangement of denticles and naked cuticle at the end of embryogenesis (see text for details). The embryo is positioned with its anterior end to the left. (Top panel courtesy of L.R. Braid.)

Figure 2.

wingless mutant phenotypes of the Drosophila embryonic epidermis. (A) In a wild type (wt) embryo, wg expression in segmental stripes generates regions of naked cuticle that are intercalated by regions of denticles. (B) A wg^CX4 mutant embryo results in an excess specification of denticles, whereas (C) the overexpression of wg (69B-Gal4>UAS-wg) results in the excess specification of naked cuticle.

Figure 3.

wingless expression in the wing imaginal disc. wg is expressed at the dorsal/ventral boundary, in two concentric rings and in a broad stripe in the dorsal region of a third instar wing disc. The expression of wg in the disc regulates the patterning of the wing margin, blade, hinge, and notum of the adult fly.

Figure 4.

Morphogen gradient of Wingless. In the third instar wing disc, Wg is secreted from cells at the dorsal/ventral boundary and forms a concentration gradient on either side to regulate the expression of its target genes, senseless (Sens, blue, high threshold), distalless (Dll, red, medium threshold), and vestigial (Vg, green, low threshold). The expression of distalless is graded throughout its domain, whereas vestigial expression is graded only at its edges. senseless, like achaete (discussed in the text), requires high levels of Wg signaling and is expressed only in cells abutting the dorsal/ventral boundary.