Notch signaling controls formation of joints at leg segment borders and growth of the developing Drosophila leg. Here, we identify the odd-skipped gene family as a key group of genes that function downstream of the Notch receptor to promote morphological changes associated with joint formation during leg development. odd, sob, drm, and bowl are expressed in a segmental pattern in the developing leg, and their expression is regulated by Notch signaling. Ectopic expression of odd, sob, or drm can induce invaginations in the leg disc epithelium and morphological changes in the adult leg that are characteristic of endogenous invaginating joint cells. These effects are not due to an alteration in the expression of other genes of the developing joint. While odd or drm mutant clones do not affect leg segmentation, and thus appear to act redundantly, bowl mutant clones do perturb leg development. Specifically, bowl mutant clones result in a failure of joint formation from the distal tibia to tarsal segment 5, while more proximal clones cause melanotic protrusions from the leg cuticle. Together, these results indicate that the odd-skipped family of genes mediates Notch function during leg development by promoting a specific aspect of joint formation, an epithelial invagination. As the odd-skipped family genes are involved in regulating cellular morphogenesis during both embryonic segmentation and hindgut development, we suggest that they may be required in multiple developmental contexts to induce epithelial cellular changes.
Hedgehog and Wingless signaling in theSpecialized groups of cells known as organizers establish the pattern of cell differentiation and morphogenesis across fields of progenitor cells. Although many organizer signals and their signal transducers have been identified, the pathways that link organizer signaling activity with subsequent cellular patterning and morphogenesis remain to be elucidated (Hatini and DiNardo 2001b). The embryonic epidermis in Drosophila has been contributing general insights into the mechanism of organizer function (Hatini and DiNardo 2001; Sanson 2001b). The pattern of cell differentiation across this epidermis is organized by two conserved signals, Hedgehog and Wingless, produced from adjacent sources that flank the boundary between parasegments (PS) (Baker 1987;Lee et al. 1992;Mohler and Vani 1992). Following the establishment of the sources of Hedgehog and Wingless production (DiNardo et al. 1988;Martinez Arias et al. 1988;Bejsovec and Martinez-Arias 1991;Heemskerk et al. 1991), each signal inhibits cellular responses elicited by the other signal. Wingless inhibits Hedgehog activity by repressing Hedgehog target gene expression anterior to the source of Hedgehog production. Hedgehog, however, inhibits Wingless activity posterior to the source of Wingless production by several distinct mechanisms (Sanson et al. 1999;Pfeiffer et al. 2000;Piepenburg et al. 2000;Dubois et al. 2001;Hatini and DiNardo 2001a
The elucidation of pathways linking patterning to morphogenesis is a problem of great interest. We show here that, in addition to their roles in patterning and morphogenesis of the hindgut, the Drosophila genes drumstick (drm) and bowl are required in the foregut for spatially localized gene expression and the morphogenetic processes that form the proventriculus. drm and bowl belong to a family of genes encoding C(2)H(2) zinc finger proteins; the other two members of this family are odd-skipped (odd) and sob. In both the fore- and hindgut, drm acts upstream of lines (lin), which encodes a putative transcriptional regulator, and relieves its repressive function. In spite of its phenotypic similarities with drm, bowl was found in both foregut and hindgut to act downstream, rather than upstream, of lin. These results support a hierarchy in which Drm relieves the repressive effect of Lin on Bowl, and Bowl then acts to promote spatially localized expression of genes (particularly the JAK/STAT pathway ligand encoded by upd) that control fore- and hindgut morphogenesis. Since the odd-family and lin are conserved in mosquito, mouse, and humans, we propose that the odd-family genes and lin may also interact to control patterning and morphogenesis in other insects and in vertebrates.
scite is a Brooklyn-based organization that helps researchers better discover and understand research articles through Smart Citations–citations that display the context of the citation and describe whether the article provides supporting or contrasting evidence. scite is used by students and researchers from around the world and is funded in part by the National Science Foundation and the National Institute on Drug Abuse of the National Institutes of Health.