Extensive regulatory capabilities of a Drosophila imaginal disk blastema

Abstract

Every organism develops body patterns that are accurately repeated among individuals of the same species. To understand how cells interact to form these patterns, many investigators have studied the re-establishment of patterns following genetic and/or physical perturbations. In regulating systems, missing structures may be replaced by cell proliferation (epimorphosis) or by respecification without growth (morphallaxis)¹. Epimorphosis involves the formation and growth of a blastema², defined for vertebrate regeneration as a zone of proliferating cells, localized near the wound surface³, which becomes capable of regenerating even when isolated from the rest of the limb⁴. Clonal analysis of Drosophila imaginal disk fragments indicates that during pattern regulation most dividing cells are located near the wound surface⁵. Furthermore, mitotic figures (L. C. Abbott, personal communication) and cells incorporating ³H-thymidine⁶ are clustered near the wound surface of regulating fragments. Here we describe experiments involving cultures of this zone of proliferating cells, and report that it can regulate in isolation. These observations provide evidence that regulation of disk fragments is accomplished by growth of a blastema. Surprisingly, the isolated blastema regenerated more pattern elements than predicted by the polar coordinate model⁷. We resolve this paradox by proposing that regulation is initiated at free cut edges, where a blastema is formed that adds new positional values in a sequence. On completion of wound healing, blastema growth continues until remaining positional disparities are eliminated by intercalation, as presented in the polar coordinate model.