The role of morphogenetic cell death during Drosophila embryonic head development.

This article addresses the role of programmed cell death (apoptosis) during embryonic head development of Drosophila. Previous studies showed that reaper (rpr) is expressed in and required by cells undergoing apoptosis. We have analyzed the correlation between the pattern of expression of rpr and morphogenetic movements affecting head development. Furthermore, we have investigated the defects in head development resulting from the absence of apoptosis in embryos deficient for rpr. Our results show that, in the head, domains of high incidence of cell death as marked by expression of rpr correlate with regions where most morphogenetic movements occur; these regions are involved in formation of mouth structures, the internalization of neural progenitors, and head involution. Cellular events driving these movements are delamination, invagination, and intercalation as well as disruption and reformation of contacts among epithelial cells. The analysis of rpr-deficient embryos demonstrates that, despite of the widespread occurrence of apoptosis during normal head morphogenesis, many aspects of this process proceed in an apparently unperturbed manner even when cell death is blocked. In particular, movements that happen early during embryonic development and that are evolutionarily more ancient (e.g., formation of the dorsal ridge and the pharynx) take place almost normally in rpr-deficient embryos. Later events which are mostly associated with head involution (e.g., retraction of the clypeolabrum, formation of the dorsal pouch, fusion of lateral gnathal lobes) are evolutionarily more recent and fail to occur normally in rpr-deficient embryos.