Meiotic cohesin SMC1β provides prophase I centromeric cohesion and is required for multiple synapsis-associated functions.

Cohesin subunit SMC1β is specific and essential for meiosis. Previous studies showed functions of SMC1β in determining the axis-loop structure of synaptonemal complexes (SCs), in providing sister chromatid cohesion (SCC) in metaphase I and thereafter, in protecting telomere structure, and in synapsi...

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Main Authors: Uddipta Biswas, Cornelia Wetzker, Julian Lange, Eleni G Christodoulou, Michael Seifert, Andreas Beyer, Rolf Jessberger
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2013-01-01
Series:PLoS Genetics
Online Access:http://europepmc.org/articles/PMC3873225?pdf=render
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spelling doaj-c427810c0be1444aaca079fdf39c48a42020-11-25T00:24:49ZengPublic Library of Science (PLoS)PLoS Genetics1553-73901553-74042013-01-01912e100398510.1371/journal.pgen.1003985Meiotic cohesin SMC1β provides prophase I centromeric cohesion and is required for multiple synapsis-associated functions.Uddipta BiswasCornelia WetzkerJulian LangeEleni G ChristodoulouMichael SeifertAndreas BeyerRolf JessbergerCohesin subunit SMC1β is specific and essential for meiosis. Previous studies showed functions of SMC1β in determining the axis-loop structure of synaptonemal complexes (SCs), in providing sister chromatid cohesion (SCC) in metaphase I and thereafter, in protecting telomere structure, and in synapsis. However, several central questions remained unanswered and concern roles of SMC1β in SCC and synapsis and processes related to these two processes. Here we show that SMC1β substantially supports prophase I SCC at centromeres but not along chromosome arms. Arm cohesion and some of centromeric cohesion in prophase I are provided by non-phosphorylated SMC1α. Besides supporting synapsis of autosomes, SMC1β is also required for synapsis and silencing of sex chromosomes. In absence of SMC1β, the silencing factor γH2AX remains associated with asynapsed autosomes and fails to localize to sex chromosomes. Microarray expression studies revealed up-regulated sex chromosome genes and many down-regulated autosomal genes. SMC1β is further required for non-homologous chromosome associations observed in absence of SPO11 and thus of programmed double-strand breaks. These breaks are properly generated in Smc1β⁻/⁻ spermatocytes, but their repair is delayed on asynapsed chromosomes. SMC1α alone cannot support non-homologous associations. Together with previous knowledge, three main functions of SMC1β have emerged, which have multiple consequences for spermatocyte biology: generation of the loop-axis architecture of SCs, homologous and non-homologous synapsis, and SCC starting in early prophase I.http://europepmc.org/articles/PMC3873225?pdf=render
collection DOAJ
language English
format Article
sources DOAJ
author Uddipta Biswas
Cornelia Wetzker
Julian Lange
Eleni G Christodoulou
Michael Seifert
Andreas Beyer
Rolf Jessberger
spellingShingle Uddipta Biswas
Cornelia Wetzker
Julian Lange
Eleni G Christodoulou
Michael Seifert
Andreas Beyer
Rolf Jessberger
Meiotic cohesin SMC1β provides prophase I centromeric cohesion and is required for multiple synapsis-associated functions.
PLoS Genetics
author_facet Uddipta Biswas
Cornelia Wetzker
Julian Lange
Eleni G Christodoulou
Michael Seifert
Andreas Beyer
Rolf Jessberger
author_sort Uddipta Biswas
title Meiotic cohesin SMC1β provides prophase I centromeric cohesion and is required for multiple synapsis-associated functions.
title_short Meiotic cohesin SMC1β provides prophase I centromeric cohesion and is required for multiple synapsis-associated functions.
title_full Meiotic cohesin SMC1β provides prophase I centromeric cohesion and is required for multiple synapsis-associated functions.
title_fullStr Meiotic cohesin SMC1β provides prophase I centromeric cohesion and is required for multiple synapsis-associated functions.
title_full_unstemmed Meiotic cohesin SMC1β provides prophase I centromeric cohesion and is required for multiple synapsis-associated functions.
title_sort meiotic cohesin smc1β provides prophase i centromeric cohesion and is required for multiple synapsis-associated functions.
publisher Public Library of Science (PLoS)
series PLoS Genetics
issn 1553-7390
1553-7404
publishDate 2013-01-01
description Cohesin subunit SMC1β is specific and essential for meiosis. Previous studies showed functions of SMC1β in determining the axis-loop structure of synaptonemal complexes (SCs), in providing sister chromatid cohesion (SCC) in metaphase I and thereafter, in protecting telomere structure, and in synapsis. However, several central questions remained unanswered and concern roles of SMC1β in SCC and synapsis and processes related to these two processes. Here we show that SMC1β substantially supports prophase I SCC at centromeres but not along chromosome arms. Arm cohesion and some of centromeric cohesion in prophase I are provided by non-phosphorylated SMC1α. Besides supporting synapsis of autosomes, SMC1β is also required for synapsis and silencing of sex chromosomes. In absence of SMC1β, the silencing factor γH2AX remains associated with asynapsed autosomes and fails to localize to sex chromosomes. Microarray expression studies revealed up-regulated sex chromosome genes and many down-regulated autosomal genes. SMC1β is further required for non-homologous chromosome associations observed in absence of SPO11 and thus of programmed double-strand breaks. These breaks are properly generated in Smc1β⁻/⁻ spermatocytes, but their repair is delayed on asynapsed chromosomes. SMC1α alone cannot support non-homologous associations. Together with previous knowledge, three main functions of SMC1β have emerged, which have multiple consequences for spermatocyte biology: generation of the loop-axis architecture of SCs, homologous and non-homologous synapsis, and SCC starting in early prophase I.
url http://europepmc.org/articles/PMC3873225?pdf=render
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