Delays in anaphase initiation occur in individual nuclei of the syncytial Drosophila embryo.

Abstract

The syncytial divisions of the Drosophila melanogaster embryo lack some of the well established cell-cycle checkpoints. It has been suggested that without these checkpoints the divisions would display a reduced fidelity. To test this idea, we examined division error frequencies in individuals bearing an abnormally long and rearranged second chromosome, designated C(2)EN. Relative to a normal chromosome, this chromosome imposes additional structural demands on the mitotic apparatus in both the early syncytial embryonic divisions and the later somatic divisions. We demonstrate that the C(2)EN chromosome does not increase the error frequency of the late larva neuroblast divisions. However, in the syncytial embryonic nuclear divisions, the C(2)EN chromosome produces a 10-fold increase in division errors relative to embryos with a normal karyotype. During late anaphase of the neuroblast divisions, the sister C(2)EN chromosomes cleanly separate from one another. In contrast, during late anaphase of the syncytial divisions in C(2)EN-bearing nuclei, large amounts of chromatin often lag on the metaphase plate. Live analysis of C(2)EN-bearing embryos demonstrates that individual nuclei in the syncytial population of dividing nuclei often delay in their initiation of anaphase. These delays frequently lead to division errors. Eventually the products of the nuclei delayed in anaphase sink inward and are removed from the dividing population of syncytial nuclei. These results suggest that the Drosophila embryo may be equipped with mechanisms that monitor the fidelity of the syncytial nuclear divisions. Unlike checkpoints that rely on cell cycle delays to identify and correct division errors, these embryonic mechanisms rely on cell cycle delays to identify and discard the products of division errors.

A Mutation indVps28Reveals a Link between a Subunit of the Endosomal Sorting Complex Required for Transport-I Complex and the Actin Cytoskeleton inDrosophila

“…Such nuclei seem to be displaced toward the interior of the embryos ( Figure 7F and 6, C and D). This is similar to other mutants in which nuclear divisions fail with the resulting oversized nuclei either remaining at or retreating to the interior of the embryo (Sullivan et al, 1993). Importantly, such a failure of nuclear divisions is not a prerequisite for the actin gaps that also were found in the presence of normal-looking interphase ( Figure 7C) or metaphase nuclei ( Figure 7B).…”

Risk and the Evolution of Cell-Cycle Durations of Embryos

“…As an example, cells with checkpoints are delayed in their cell cycles to ensure completion of DNA replication or events in mitosis before moving to the next stage (Hartwell and Weinert 1989;Paulovich et al 1997;Epel et al 1999). Embryos without checkpoints in early cell cycles may lose cells because of uncorrected errors from uncompleted events in DNA replication and mitosis (Sullivan et al 1993;Anderson et al 1997), whereas those that do have checkpoints may be afflicted with abnormal asynchronies among cell lineages when some cell cycles are delayed. Slower development could reduce the frequency of either of these potential errors in development.…”

Genomic imprinting proposed as a surveillance mechanism for chromosome loss.

“…Such a mechanism would be most effective in detecting large-scale loss of heterozygosity, since such events would tend to affect more imprinted genes. Though it is unlikely to be based on an imprinting mechanism, an interesting precedent for chromosome segregation surveillance has been demonstrated: when a chromosome rearrangement causes abnormal mitosis in the early Drosophila melanogaster embryo, the resulting nuclei are selectively eliminated from the dividing population of nuclei that will form the embryo (16).…”