The molecular mechanisms controlling cell-fate determination and movement of the morphogenetic furrow in the eye

The adult epidermis in higher dipteran insects such as Drosophila is derived from specialized structures in larvae known as imaginal discs. Set aside during mid-embryogenesis as small groups of 10 to 70 cells each, imaginal disc primordia grow and differentiate during larval development as epithelial monolayers. Metamorphosis of imaginal discs during early pupal life generates the adult cuticle and appendages, including the eyes, legs and wings (reviewed in Cohen, 1993). While a morphological description of these events has been well-documented, the genetic and molecular mechanisms controlling pattern formation and morphogenesis of imaginal discs are just now being unraveled. Eye imaginal disc development creates a highly ordered array of differentiated cells from a pool of equivalent, undetermined cells (Ready et al., 1976; Lawrence and Green, 1979). This process generates the adult eye, which consists of about 800 unit eyes or ommatidia. Each ommatidium comprises eight photoreceptors, termed R1-R8, as well as a dozen accessory cells, including lens-secreting cone cells, pigment cells and a mechanosensory bristle. During late larval and early pupal development, photoreceptor cell determination and differentiation sweep across the eye imaginal disc following an indentation in the epithelial monolayer termed the morphogenetic furrow (Ready et al., 1976). The morphogenetic furrow is characterized by an apical-basal shortening of cells, synchronization of the cell cycle, coordinated gene expression and initiation of neural differentiation (Wolff and Ready, 1991; Heberlein et al., 1993; Ma et al., 1993). The furrow begins at the posterior margin of the eye disc and proceeds anteriorly as a linear front, traversing the disc during a period of about 2 days. Immediately posterior to the furrow, the first presumptive photoreceptor cells become apparent by both morphological and molecular criteria (Tomlinson and Ready, 1987a; Wolff and Ready, 1991). As the furrow progresses across the eye disc, photoreceptor cells are recruited in a stepwise fashion such that all stages of ommatidial assembly can be viewed in a single disc preparation (reviewed in Wolff and Ready, 1993). The molecular mechanisms controlling cell-fate determination and movement of the morphogenetic furrow in the eye imaginal disc are the subjects of this report. Two genes that are involved in progression of the morphogenetic furrow, decapentaplegic (dpp) and hedgehog (hh), are also key determinants of pattern formation in other imaginal discs as well as in the Drosophila embryo. Both dpp and hh encode phylogenetically conserved, secreted proteins that act as concentration-dependent morphogens responsible for organizing tissue polarity throughout development. dpp specifies dorsal-ventral pattern formation in the embryo (Ferguson and 3473 Development 120, 3473-3486 (1994) Printed in Great Britain © The Company of Biologists Limited 1994