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Organ shape depends on the coordination between cell proliferation and the spatial arrangement of cells during development. Much is known about the mechanisms that regulate cell proliferation, but the processes by which the cells are orderly distributed remain unknown. This can be accomplished either by random division of cells that later migrate locally to new positions (cell allocation) or through polarized cell division (oriented cell division; OCD). Recent data suggest that the OCD is involved in some morphogenetic processes such as vertebrate gastrulation, neural tube closure, and growth of shoot apex in plants; however, little is known about the contribution of OCD during organogenesis. We have analyzed the orientation patterns of cell division throughout the development of wild-type and mutant imaginal discs of Drosophila. Our results show a causal relationship between the orientation of cell divisions in the imaginal disc and the adult morphology of the corresponding organs, indicating a key role of OCD in organ-shape definition. In addition, we find that a subset of planar cell polarity genes is required for the proper orientation of cell division during organ development.

The pattern of cell proliferation in the Drosophila imaginal wing primordium is spatially and temporally heterogeneous. Direct visualization of cells in S, G2, and mitosis phases of the cell cycle reveals several features invariant throughout development. The fraction of cells in the disc in the different cell cycle stages is constant, the majority remaining in G1. Cells in the different phases of the cell cycle mainly appear in small synchronic clusters that are nonclonally derived but result from changing local cell-cell interactions. Cluster synchronization occurs before S and in the G2/M phases. Rates of cell division are neither constant nor clonal features. Cell cycle progression is linear rather than concentric. Clusters appear throughout the disc but with symmetries related to presumptive wing patterns, compartment boundaries, and vein clonal restrictions.Morphogenesis in multicellular organisms is associated with patterned cell proliferation. As a rule, the size of an organ and its shape are species specific. Specific forms then result from local cell behavior reflecting the active genome of the proliferating cells.

Apoptotic cell death in wing imaginal discs takes place in single cells or small clusters of neighboring cells. These cells are distributed throughout the anlage at early stages and in recognizable territories at late larval and pupal stages. Apoptotic cells remain in the epithelium 2-4 h, prior to being engulfed in place by hemolymph cells. Experimentally induced apoptosis in single cells or territories is accompanied by nonautonomous death of adjacent cells and of cells further away in adjacent territories. These effects are followed by changes in cell proliferation in both territories. Apogenetic mosaics in mutant discs show cell death throughout the anlage. Apoptosis provides a mechanism, in addition to cell proliferation control, for matching territories with different positional values or different genetic specifications.