Topoisomerase II is required for the proper separation of heterochromatic regions during Drosophila melanogaster female meiosis

Heterochromatic homology ensures the segregation of achiasmate chromosomes during meiosis I in Drosophila melanogaster females, perhaps as a consequence of the heterochromatic threads that connect achiasmate homologs during prometaphase I. Here, we ask how these threads, and other possible heterochr...

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Bibliographic Details
Published in:PLoS genetics 2014-10, Vol.10 (10), p.e1004650
Main Authors: Hughes, Stacie E, Hawley, R Scott
Format: Article
Language:English
Subjects:
Animals
Biology and life sciences
Cell Cycle - genetics
Chromatin
Chromosome Segregation - genetics
Chromosomes
DNA topoisomerase II
DNA Topoisomerases, Type II - genetics
Drosophila
Drosophila melanogaster
Eukaryotes
Female
Genetic aspects
Genetic research
Genomics
Heterochromatin
Heterochromatin - genetics
Meiosis
Meiosis - genetics
Metaphase - genetics
Nondisjunction, Genetic
Oocytes - cytology
X Chromosome - genetics
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Summary:Heterochromatic homology ensures the segregation of achiasmate chromosomes during meiosis I in Drosophila melanogaster females, perhaps as a consequence of the heterochromatic threads that connect achiasmate homologs during prometaphase I. Here, we ask how these threads, and other possible heterochromatic entanglements, are resolved prior to anaphase I. We show that the knockdown of Topoisomerase II (Top2) by RNAi in the later stages of meiosis results in a specific defect in the separation of heterochromatic regions after spindle assembly. In Top2 RNAi-expressing oocytes, heterochromatic regions of both achiasmate and chiasmate chromosomes often failed to separate during prometaphase I and metaphase I. Heterochromatic regions were stretched into long, abnormal projections with centromeres localizing near the tips of the projections in some oocytes. Despite these anomalies, we observed bipolar spindles in most Top2 RNAi-expressing oocytes, although the obligately achiasmate 4th chromosomes exhibited a near complete failure to move toward the spindle poles during prometaphase I. Both achiasmate and chiasmate chromosomes displayed defects in biorientation. Given that euchromatic regions separate much earlier in prophase, no defects were expected or observed in the ability of euchromatic regions to separate during late prophase upon knockdown of Top2 at mid-prophase. Finally, embryos from Top2 RNAi-expressing females frequently failed to initiate mitotic divisions. These data suggest both that Topoisomerase II is involved in the resolution of heterochromatic DNA entanglements during meiosis I and that these entanglements must be resolved in order to complete meiosis.
ISSN:1553-7404
1553-7390
1553-7404
DOI:10.1371/journal.pgen.1004650