Multilayered mechanisms ensure that short chromosomes recombine in meiosis
Hajime Murakami,Isabel Lam,Isabel Lam,Pei-Ching Huang,Pei-Ching Huang,Jacquelyn Song,Megan van Overbeek,Scott Keeney +7 more
TLDR
This work demonstrates how Saccharomyces cerevisiae integrates multiple temporally distinct pathways to regulate the binding of Rec114 and Mer2 to chromosomes, thereby controlling the duration of a DSB-competent state.Abstract:
In most species, homologous chromosomes must recombine in order to segregate accurately during meiosis1. Because small chromosomes would be at risk of missegregation if recombination were randomly distributed, the double-strand breaks (DSBs) that initiate recombination are not located arbitrarily2. How the nonrandomness of DSB distributions is controlled is not understood, although several pathways are known to regulate the timing, location and number of DSBs. Meiotic DSBs are generated by Spo11 and accessory DSB proteins, including Rec114 and Mer2, which assemble on chromosomes3-7 and are nearly universal in eukaryotes8-11. Here we demonstrate how Saccharomyces cerevisiae integrates multiple temporally distinct pathways to regulate the binding of Rec114 and Mer2 to chromosomes, thereby controlling the duration of a DSB-competent state. The engagement of homologous chromosomes with each other regulates the dissociation of Rec114 and Mer2 later in prophase I, whereas the timing of replication and the proximity to centromeres or telomeres influence the accumulation of Rec114 and Mer2 early in prophase I. Another early mechanism enhances the binding of Rec114 and Mer2 specifically on the shortest chromosomes, and is subject to selection pressure to maintain the hyperrecombinogenic properties of these chromosomes. Thus, the karyotype of an organism and its risk of meiotic missegregation influence the shape and evolution of its recombination landscape. Our results provide a cohesive view of a multifaceted and evolutionarily constrained system that allocates DSBs to all pairs of homologous chromosomes.read more
Citations
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Ensuring meiotic DNA break formation in the mouse pseudoautosomal region
Laurent Acquaviva,Michiel Boekhout,Michiel Boekhout,Mehmet E. Karasu,Mehmet E. Karasu,Kevin Brick,Florencia Pratto,Tao Li,Megan van Overbeek,Liisa Kauppi,Liisa Kauppi,R. Daniel Camerini-Otero,Maria Jasin,Scott Keeney +13 more
TL;DR: The findings establish a mechanistic paradigm for the recombination of sex chromosomes during meiosis in mice by proposing that the repetitive DNA sequence of the PAR confers unique chromatin and higher-order structures that are crucial for recombination.
Journal ArticleDOI
Chromosome Organization in Early Meiotic Prophase.
Corinne Grey,Bernard de Massy +1 more
TL;DR: In this article, the axial elements are used to set the stage for efficient sister chromatid cohesion and meiotic recombination, necessary for the recognition of the homologous chromosomes.
Journal ArticleDOI
Mechanism and Control of Meiotic DNA Double-Strand Break Formation in S. cerevisiae.
TL;DR: In this article, the authors describe the mechanism of meiotic DSB formation based on recent advances in the characterization of the structure and function of DSB proteins and discuss regulatory pathways in the light of recent models.
Journal ArticleDOI
Chromosome-autonomous feedback down-regulates meiotic DNA break competence upon synaptonemal complex formation
TL;DR: The findings show that DSB number is regulated in a chromosome-autonomous fashion and provide insight into how homeostatic DSB controls respond to aneuploidy during meiosis.
Journal ArticleDOI
Let's get physical - mechanisms of crossover interference.
Lexy von Diezmann,Ofer Rog +1 more
TL;DR: In this article, the authors present a cell biological and biophysical perspective on crossover interference, summarizing the evidence that links interference to the spatial, dynamic, mechanical and molecular properties of meiotic chromosomes.
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A central role for cohesins in sister chromatid cohesion, formation of axial elements, and recombination during yeast meiosis.
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