Determining the role of patterned cell proliferation in the shape and size of the Drosophila wing

Abstract

In multicellular organisms morphogenesis highly depends on cell proliferation. Morphogenesis relates to the genetic mechanisms that determine specific sizes and shapes. Morphogenetic analyses need a detailed description of growth in terms of cell lineages. Cell lineage studies reveal spatial and numerical parameters of ordered cell proliferation, an indication of genetic control of cell behavior. The wing disk of Drosophila melanogaster possibly is, in this sense, the best-studied growing anlage. The imaginal wing disk is a monolayer of cells that give rise to the adult epidermis of the dorsal mesothorax, including notum and wing. Cell lineage analyses of the disk have been carried out with mitotic recombination clones labeled with mutant but gratuitous cell markers (1, 2). These clonal analyses have revealed clonal restrictions that separate so-called ''compartments,'' subdividing the early anlage in four major compartments, anterior͞posterior (A͞P) and dorsal͞ventral (D͞V). A subsequent subdivision separates notum and pleura from the wing proper (3, 4). New clonal restrictions, less stringent than in compartment boundaries, later symmetrically subdivide the dorsal and ventral wing compartments into sectors delimited by the veins (5, 6). Cell proliferation within these compartments and wing sectors is more undetermined with clone borders overlapping in the same regions of different wings. The shape of these clones is, however, region characteristic, symmetrical in both dorsal and ventral surfaces and near symmetrical in both anterior and posterior compartments (1, 2); see ref. 7 for review.In the wing disk and the presumptive wing blade in particular, cell proliferation increases the number of cells in an exponential mode, with an average cycle time of 8.5 h (8). The wing disk primordium in the embryo contains about 20 cells and the proliferation period ends with about 50,000, the equivalent to 10-11 rounds of cell division (8). Direct observation of growing imaginal discs has shown that clusters of neighboring cells, not clonally related, enter both the S phase of the cell cycle and mitosis in synchrony (9). Anaphases in a cluster are randomly oriented in the planar axis, but subsequently the two daughter cells allocate along either the A͞P axis (y axis) or the proximodistal axis (x axis) (9). Moreover, the shape of the clones in the growing disk corresponds with that of the clones seen in the adult wing, indicating that there are no major changes in the relative position of neighboring cells during the eversion of the disk at metamorphosis (9). During the larval and pupal periods cell death in the disk affects a very low number of cells in the hinge. There are therefore no major morphogenetic changes associated with cell death in late larval or pupal stages (10).But how do these morphogenetic parameters relate to the final constant wing shape and size? It has been proposed that compartment boundaries work as ''organizers'' of compartment growth and patterning. Along the growing A͞P boundary, the selector gene...

Control of growth and positional information by the graded vestigial expression pattern in the wing of Drosophila melanogaster

“…3E). These findings suggest that the homogenous rate of clone size throughout the wing blade (28,29) requires local cell interactions between neighboring cells, and it is not cell autonomously determined by the amount of vg expression in cells. These observations clearly indicate that the autonomous expression of Vg-Sd complex does not stimulate cell proliferation per se.…”

Origin and proliferation of blastema cells during regeneration of Drosophila wing imaginal discs

“…Indeed, our clonal analysis shows that the largest clones are elongated and peripherally oriented in the PL. However, as in the regenerating 3/4A fragment, clones in the developing wing grow along the proximodistal axis when fall in the WP and along the periphery when fall in the PL (Baena-López et al, 2005, Garcia-Bellido and Merriam, 1971, Resino et al, 2002. It has been proposed that during wing development, preferential orientations of cell division along axes of growth and lineage boundaries are linked to positional disparities and, hence, to final organ and tissue shape (Baena-López et al, 2005).…”

The cellular and genetic bases of organ size and shape in Drosophila

“…Analysis of twin clones allows us to ascertain the topological location of the mother cell in the interface between the two twin clones and thus define their growth directions (Resino et al, 2002). Mother cells can be anywhere in the disc.…”