Chromosome separation during Drosophila male meiosis I requires separase-mediated cleavage of the homolog conjunction protein UNO.

Regular chromosome segregation during the first meiotic division requires prior pairing of homologous chromosomes into bivalents. During canonical meiosis, linkage between homologous chromosomes is maintained until late metaphase I by chiasmata resulting from meiotic recombination in combination wit...

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Main Authors: Joe Weber, Zeynep Kabakci, Soumya Chaurasia, Erich Brunner, Christian F Lehner
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2020-10-01
Series:PLoS Genetics
Online Access:https://doi.org/10.1371/journal.pgen.1008928
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author Joe Weber
Zeynep Kabakci
Soumya Chaurasia
Erich Brunner
Christian F Lehner
author_facet Joe Weber
Zeynep Kabakci
Soumya Chaurasia
Erich Brunner
Christian F Lehner
author_sort Joe Weber
collection DOAJ
description Regular chromosome segregation during the first meiotic division requires prior pairing of homologous chromosomes into bivalents. During canonical meiosis, linkage between homologous chromosomes is maintained until late metaphase I by chiasmata resulting from meiotic recombination in combination with distal sister chromatid cohesion. Separase-mediated elimination of cohesin from chromosome arms at the end of metaphase I permits terminalization of chiasmata and homolog segregation to opposite spindle poles during anaphase I. Interestingly, separase is also required for bivalent splitting during meiosis I in Drosophila males, where homologs are conjoined by an alternative mechanism independent of meiotic recombination and cohesin. Here we report the identification of a novel alternative homolog conjunction protein encoded by the previously uncharacterized gene univalents only (uno). The univalents that are present in uno null mutants at the start of meiosis I, instead of normal bivalents, are segregated randomly. In wild type, UNO protein is detected in dots associated with bivalent chromosomes and most abundantly at the localized pairing site of the sex chromosomes. UNO is cleaved by separase. Expression of a mutant UNO version with a non-functional separase cleavage site restores homolog conjunction in a uno null background. However, separation of bivalents during meiosis I is completely abrogated by this non-cleavable UNO version. Therefore, we propose that homolog separation during Drosophila male meiosis I is triggered by separase-mediated cleavage of UNO.
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spelling doaj.art-be01854c664e434c9e127a2cc0effae62022-12-21T22:36:13ZengPublic Library of Science (PLoS)PLoS Genetics1553-73901553-74042020-10-011610e100892810.1371/journal.pgen.1008928Chromosome separation during Drosophila male meiosis I requires separase-mediated cleavage of the homolog conjunction protein UNO.Joe WeberZeynep KabakciSoumya ChaurasiaErich BrunnerChristian F LehnerRegular chromosome segregation during the first meiotic division requires prior pairing of homologous chromosomes into bivalents. During canonical meiosis, linkage between homologous chromosomes is maintained until late metaphase I by chiasmata resulting from meiotic recombination in combination with distal sister chromatid cohesion. Separase-mediated elimination of cohesin from chromosome arms at the end of metaphase I permits terminalization of chiasmata and homolog segregation to opposite spindle poles during anaphase I. Interestingly, separase is also required for bivalent splitting during meiosis I in Drosophila males, where homologs are conjoined by an alternative mechanism independent of meiotic recombination and cohesin. Here we report the identification of a novel alternative homolog conjunction protein encoded by the previously uncharacterized gene univalents only (uno). The univalents that are present in uno null mutants at the start of meiosis I, instead of normal bivalents, are segregated randomly. In wild type, UNO protein is detected in dots associated with bivalent chromosomes and most abundantly at the localized pairing site of the sex chromosomes. UNO is cleaved by separase. Expression of a mutant UNO version with a non-functional separase cleavage site restores homolog conjunction in a uno null background. However, separation of bivalents during meiosis I is completely abrogated by this non-cleavable UNO version. Therefore, we propose that homolog separation during Drosophila male meiosis I is triggered by separase-mediated cleavage of UNO.https://doi.org/10.1371/journal.pgen.1008928
spellingShingle Joe Weber
Zeynep Kabakci
Soumya Chaurasia
Erich Brunner
Christian F Lehner
Chromosome separation during Drosophila male meiosis I requires separase-mediated cleavage of the homolog conjunction protein UNO.
PLoS Genetics
title Chromosome separation during Drosophila male meiosis I requires separase-mediated cleavage of the homolog conjunction protein UNO.
title_full Chromosome separation during Drosophila male meiosis I requires separase-mediated cleavage of the homolog conjunction protein UNO.
title_fullStr Chromosome separation during Drosophila male meiosis I requires separase-mediated cleavage of the homolog conjunction protein UNO.
title_full_unstemmed Chromosome separation during Drosophila male meiosis I requires separase-mediated cleavage of the homolog conjunction protein UNO.
title_short Chromosome separation during Drosophila male meiosis I requires separase-mediated cleavage of the homolog conjunction protein UNO.
title_sort chromosome separation during drosophila male meiosis i requires separase mediated cleavage of the homolog conjunction protein uno
url https://doi.org/10.1371/journal.pgen.1008928
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