Fruit Flies Reveal the Interplay Between Development and the Cell Cycle

The development of complex tissues often requires specific modifications to the cell cycle. Understanding the interplay between development and cell division is thus crucial if we want to understand how complex organisms are built. Drosophila melanogaster has established itself as the premier model system for studying the interplay between development and the cell cycle. Not only does the development of this organism involve several highly unusual cell cycles, but the powerful genetic techniques that can be applied to fruit flies facilitated the discovery of genes involved in the developmental control of the cell cycle.

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The first 13 nuclear divisions of the fertilized Drosophila embryo are rapid cycles of DNA replication and mitosis (with no gap phases), fueled by key cell cycle regulators that were stockpiled in the egg cytoplasm as it matured. These divisions, which all occur in a common cytoplasm, are called the syncytial divisions and occur in unison (Figure 19-6). As maternal stockpiles run out, gap phases are introduced, first G2, followed by G1. Most cells in the embryo cease to divide at this point, form plasma membranes, and undergo a specialized cell cycle known as the endocycle. In the endocycle, cells replicate their DNA but do not undergo mitosis. This replication leads to an increase in gene dosage and fuels increased macromolecule biosynthesis, which allows individual cells to grow in size. Thus the embryo, which has now developed into a crawling larva, grows simply by an increase in cell size and not through cell multiplication. A select number of cells do not share this fate. These cells are in the imaginal disks, the organs that will give rise to the adult fly tissues during metamorphosis. Metamorphosis occurs during the pupa stage and transforms larvae into adult flies. The divisions that give rise to the adult fly are canonical cell cycles leading to a diploid organism.

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FIGURE 19-6 Cell division patterns during the life cycle of Drosophila melanogaster. After fertilization, nuclei in the embryo undergo 13 rapid S phase–M phase cycles. These cycles are followed by three divisions that include a G2 phase. All these nuclear divisions occur within a common cytoplasm and are therefore called the syncytial divisions. During late stages of embryogenesis and throughout larval development (with the exception of the nervous system), cells undergo endocycles. These cycles lead to an increase in cellular ploidy and size and hence larval growth. In the pupa, during a process called metamorphosis, imaginal disks, the tissues that give rise to the adult organs, undergo mitotic divisions and then differentiate to form adult structures. Several types of divisions are seen in the adult fly. Stem cells undergo mitotic divisions, meiosis gives rise to sperm and eggs, and endocycles create polyploid cells in the ovary. See L. A. Lee and T. L. Orr-Weaver, 2003, Ann. Rev. Genet. 37:545–578.