Cytoplasmic organization, nuclear migration, and nuclear division in the early syncytial Drosophila embryo

The generation of order and asymmetry at the cytoplasmic level is fundamental to many basic cellular functions including mitosis, directed cell movement, and developmental processes such as axis specification. All of these events are largely dependent on the cytoskeleton, which is responsible for organizing the cytoplasm of eukaryotic cells. The problem of cytoplasmic organization is particularly acute during early embryogenesis in Drosophila: the initial divisions are syncytial and many of the nuclei undergo a precise program of movements leading to the formation of a highly regular blastoderm embryo. The initial nuclear divisions of early Drosophila embryogenesis have been thoroughly studied (Rabinowitz, 1941; Sonnenblick, 1950; Turner and Mahowald, 1977; Zalokar and Erk, 1976; Foe and Alberts, 1983; Stafstrom and Staehelin, 1984; Minden et al., 1989). The Drosophila embryo undergoes 13 rapid (8-21 minutes) synchronous nuclear divisions without accompanying cytokinesis. The first eight nuclear divisions occur in the interior of the embryo. After these divisions, the nuclei embark along one of three different division programs. The majority of the nuclei migrate to the cortex during nuclear cycles 8, 9, and 10. By the end of nuclear cycle 10, these nuclei are positioned at the surface of the embryo just beneath the plasma membrane, where they undergo four synchronous divisions as a regularly spaced cortical monolayer. Cellularization occurs during interphase of nuclear cycle 14. A second nuclear division pathway involves a few nuclei that migrate ahead of the main body of nuclei and reach the posterior cortex during nuclear cycle 9. During cycle 10, these nuclei are surrounded by plasma membranes to form the pole cells, the precursors of the germ line. A third nuclear division program is exhibited by a group of nuclei that fail to migrate outward toward the cortex during nuclear cycle 8. These nuclei, known as the yolk nuclei, remain in the interior of the embryo and become polyploid. The cortical cytoskeleton of the Drosophila embryo has been characterized through immunofluorescence analysis of fixed material (Warn et al., 1984; Warn et al., 1985; Karr and Alberts, 1986; Warn and Warn, 1986; Warn et al., 1987). In addition, the dynamics of the cortical cytoskeleton has been followed in living embryos by microinjecting fluorescently labeled actin and tubulin (Kellogg et al., 1988). The injection of fluorescently labeled histones provides a means of following chromosome behavior (Minden et al., 1989). During interphase, the cortical actin becomes organized in a cap between the plasma membrane and the nucleus. At this stage, microtubule networks, which originate from a centrosome pair located between the nucleus and the actin cap, radiate inwards to encompass each 1245 Development 118, 1245-1254 (1993) Printed in Great Britain © The Company of Biologists Limited 1993