Phosphoregulation of HORMA domain protein HIM-3 promotes asymmetric synaptonemal complex disassembly in meiotic prophase in Caenorhabditis elegans

In the two cell divisions of meiosis, diploid genomes are reduced into complementary haploid sets through the discrete, two-step removal of chromosome cohesion, a task carried out in most eukaryotes by protecting cohesion at the centromere until the second division. In eukaryotes without defined cen...

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Main Authors: Sato-Carlton, Aya (Author) , Nakamura-Tabuchi, Chihiro (Author) , Li, Xuan (Author) , Boog, Hendrik (Author) , Lehmer, Madison K. (Author) , Rosenberg, Scott C. (Author) , Barroso, Consuelo (Author) , Martinez-Perez, Enrique (Author) , Corbett, Kevin D. (Author) , Carlton, Peter Mark (Author)
Format: Article (Journal)
Language:English
Published: November 11, 2020
In: PLoS Genetics
Year: 2020, Volume: 16, Issue: 11
ISSN:1553-7404
DOI:10.1371/journal.pgen.1008968
Online Access:Verlag, lizenzpflichtig, Volltext: https://doi.org/10.1371/journal.pgen.1008968
Verlag, lizenzpflichtig, Volltext: https://journals.plos.org/plosgenetics/article?id=10.1371/journal.pgen.1008968
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Author Notes:Aya Sato-Carlton, Chihiro Nakamura-Tabuchi, Xuan Li, Hendrik Boog, Madison K. Lehmer, Scott C. Rosenberg, Consuelo Barroso, Enrique Martinez-Perez, Kevin D. Corbett, Peter Mark Carlton
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Summary:In the two cell divisions of meiosis, diploid genomes are reduced into complementary haploid sets through the discrete, two-step removal of chromosome cohesion, a task carried out in most eukaryotes by protecting cohesion at the centromere until the second division. In eukaryotes without defined centromeres, however, alternative strategies have been innovated. The best-understood of these is found in the nematode Caenorhabditis elegans: after the single off-center crossover divides the chromosome into two segments, or arms, several chromosome-associated proteins or post-translational modifications become specifically partitioned to either the shorter or longer arm, where they promote the correct timing of cohesion loss through as-yet unknown mechanisms. Here, we investigate the meiotic axis HORMA-domain protein HIM-3 and show that it becomes phosphorylated at its C-terminus, within the conserved “closure motif” region bound by the related HORMA-domain proteins HTP-1 and HTP-2. Binding of HTP-2 is abrogated by phosphorylation of the closure motif in in vitro assays, strongly suggesting that in vivo phosphorylation of HIM-3 likely modulates the hierarchical structure of the chromosome axis. Phosphorylation of HIM-3 only occurs on synapsed chromosomes, and similarly to other previously-described phosphorylated proteins of the synaptonemal complex, becomes restricted to the short arm after designation of crossover sites. Regulation of HIM-3 phosphorylation status is required for timely disassembly of synaptonemal complex central elements from the long arm, and is also required for proper timing of HTP-1 and HTP-2 dissociation from the short arm. Phosphorylation of HIM-3 thus plays a role in establishing the identity of short and long arms, thereby contributing to the robustness of the two-step chromosome segregation.
Item Description:Gesehen am 05.02.2021
Physical Description:Online Resource
ISSN:1553-7404
DOI:10.1371/journal.pgen.1008968