Cellular Basis of the Dynamic Behavior of the Imaginal Thoracic Discs during Drosophila Metamorphosis

Abstract

The eversion, migration, spreading, and fusion of the thoracic imaginal discs during metamorphosis of Drosophila are described using timed whole-mount preparations and several molecular markers. The leading edge of the migrating disc epithelia consists of two groups of cells, stalk cells (S cells) and specialized imaginal cells (I cells), that both express the gene puckered. With this and other markers, opening of the stalk, eversion of the discs, migration of the leading edges, and fusion of the imaginal epithelia can be visualized in detail. Fusion is initiated by S cells that migrate over the larval epithelium and constitute a bridge between two imaginal epithelia. S cells are subsequently lost and imaginal fusion is mediated by the I cells that remain at the site of fusion. The possible cellular basis of this process is discussed. Fusion along the dorsal midline of the notum from the mesothoracic wing discs occurs earlier than that of the prothoracic and metathoracic discs, which remain in a lateral position. For a relatively long period (30 h) the mesothoracic epithelium becomes attached to the head and abdomen, causing a temporary local discontinuity of the order of segments. Later the pro- and metathoracic discs intercalate between head and mesothorax and between abdomen and mesothorax, respectively, to reestablish the normal order.

Drosophila AP-1: lessons from an invertebrate

“…At this stage, a puparium is formed and the larval tissue becomes histolysed and replaced by the imaginal epithelia. The notum of the adult¯y is derived from the two wing imaginal discs (Usui and Simpson, 2000). These discs are comprised of epithelial sacs that had been set aside early in embryonic development.…”

“…These discs are comprised of epithelial sacs that had been set aside early in embryonic development. Imaginal discs are divided into three structures: the imaginal disc proper (which consists of columnar cells), the peripodial membrane (a squamous epithelium) and the peripodial stalk (which attaches the disc to the larval epidermis), (Usui and Simpson, 2000). During larval stages, wing imaginal sacs proliferate and become patterned to form the anlagen of the wing and thorax (Blair, 1995;Brook et al, 1996).…”

“…In the process of thorax closure, the proximal parts of the two contralateral wing imaginal discs approach each other and join to form the continuous notum of the adult¯y. Thorax closure proceeds in four steps (Figure 7): Eversion of the imaginal disc epithelia through the peripodial stalk, dorsal migration of disc epithelia over larval tissue, cell shape changes towards the future dorsal midline and, ®nally, the fusion of the two heminota (Usui and Simpson, 2000).…”

“…On the other hand, DC is driven largely by cell shape changes in the epidermis and amnioserosa, whereas thorax closure relies on cell migration over larval tissue and cell stretching of a few rows of cells at the ®nal stages only (Martin-Blanco et al, 2000; Usui and Simpson, 2000;Zeitlinger and Bohmann, 1999). The leading edge in dorsal closure consists of a wellde®ned single row of epidermal cells, resembling a sharp boundary between the lateral epidermis and the squamous cells of the amnioserosa.…”

“…In the wild-type situation, the two heminota of the wing imaginal discs have fused to form a continuous structure with no visible midline. In the kay 2 homozygote, the thorax closure process cannot proceed normally and leaves a cleft in the dorsal midline Drosophila AP-1: lessons from an invertebrate L Kockel et al leading edge of wing imaginal discs in thorax closure contains columnar epithelial cells of the disc proper as well as squamous cells of the former peripodial membrane, and is several rows of cells wide (Usui and Simpson, 2000). Defective thorax closure manifests itself late during development.…”