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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Main Authors: Stacie E Hughes, R Scott Hawley
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2014-10-01
Series:PLoS Genetics
Online Access:http://europepmc.org/articles/PMC4207608?pdf=render
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spelling doaj-7579508782cc4eefa407dff94a502d412020-11-25T02:36:32ZengPublic Library of Science (PLoS)PLoS Genetics1553-73901553-74042014-10-011010e100465010.1371/journal.pgen.1004650Topoisomerase II is required for the proper separation of heterochromatic regions during Drosophila melanogaster female meiosis.Stacie E HughesR Scott HawleyHeterochromatic 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.http://europepmc.org/articles/PMC4207608?pdf=render
collection DOAJ
language English
format Article
sources DOAJ
author Stacie E Hughes
R Scott Hawley
spellingShingle Stacie E Hughes
R Scott Hawley
Topoisomerase II is required for the proper separation of heterochromatic regions during Drosophila melanogaster female meiosis.
PLoS Genetics
author_facet Stacie E Hughes
R Scott Hawley
author_sort Stacie E Hughes
title Topoisomerase II is required for the proper separation of heterochromatic regions during Drosophila melanogaster female meiosis.
title_short Topoisomerase II is required for the proper separation of heterochromatic regions during Drosophila melanogaster female meiosis.
title_full Topoisomerase II is required for the proper separation of heterochromatic regions during Drosophila melanogaster female meiosis.
title_fullStr Topoisomerase II is required for the proper separation of heterochromatic regions during Drosophila melanogaster female meiosis.
title_full_unstemmed Topoisomerase II is required for the proper separation of heterochromatic regions during Drosophila melanogaster female meiosis.
title_sort topoisomerase ii is required for the proper separation of heterochromatic regions during drosophila melanogaster female meiosis.
publisher Public Library of Science (PLoS)
series PLoS Genetics
issn 1553-7390
1553-7404
publishDate 2014-10-01
description 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.
url http://europepmc.org/articles/PMC4207608?pdf=render
work_keys_str_mv AT stacieehughes topoisomeraseiiisrequiredfortheproperseparationofheterochromaticregionsduringdrosophilamelanogasterfemalemeiosis
AT rscotthawley topoisomeraseiiisrequiredfortheproperseparationofheterochromaticregionsduringdrosophilamelanogasterfemalemeiosis
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