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Reduced dosage of the chromosome axis factor Red1 selectively disrupts the meiotic recombination checkpoint in Saccharomyces cerevisiae

ABSTRACT: Meiotic chromosomes assemble characteristic “axial element” structures that are essential for fertility and provide the chromosomal context for meiotic recombination, synapsis and checkpoint signaling. Whether these meiotic processes are equally dependent on axial element integrity has remained unclear. Here, we investigated this question in S. cerevisiae using the putative condensin allele ycs4S. We show that the severe axial element assembly defects of this allele are explained by a linked mutation in the promoter of the major axial element gene RED1 that reduces Red1 protein levels to 20-25% of wild type. Intriguingly, the Red1 levels of ycs4S mutants support meiotic processes linked to axis integrity, including DNA double-strand break formation and deposition of the synapsis protein Zip1, at levels that permit 70% gamete survival. By contrast, the ability to elicit a meiotic checkpoint arrest is completely eliminated. This selective loss of checkpoint function is supported by a RED1 dosage series and is associated with the loss of most of the cytologically detectable Red1 from the axial element. Our results indicate separable roles for Red1 in building the structural axis of meiotic chromosomes and mounting a sustained recombination checkpoint response.

ORGANISM(S): Saccharomyces cerevisiae

PROVIDER: GSE87060 | GEO | 2017/07/18

SECONDARY ACCESSION(S): PRJNA343422

REPOSITORIES: GEO

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Transcription Dynamically Patterns the Meiotic Chromosome-Axis Interface

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Transcription Dynamically Patterns the Meiotic Chromosome-Axis Interface [ChIP-Seq]

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2015-08-06 | E-GEOD-69230 | biostudies-arrayexpress

Transcription Dynamically Patterns the Meiotic Chromosome-Axis Interface [ChIP-Seq]

Project description:Meiotic chromosomes are highly compacted yet remain transcriptionally active. To understand how chromosome folding accommodates transcription, we investigated the assembly of the axial element, the proteinaceous structure that compacts meiotic chromosomes and promotes recombination and fertility. We found that the axial-element proteins of budding yeast are flexibly anchored to chromatin by the ring-like cohesin complex and biased towards small chromosomes by a separate modulating mechanism that requires the conserved axial element component Hop1. The ubiquitous presence of cohesin at sites of convergent transcription provides well-dispersed points for axis attachment and thus compaction. Axis protein enrichment at these sites directly correlates with the propensity for recombination initiation nearby. Importantly, axis anchoring by cohesin is adjustable and readily displaced in the direction of transcription by the transcriptional machinery. We propose that such robust but flexible tethering allows the highly structured axial element to promote recombination while easily adapting to changes in chromosome activity.

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Transcription Dynamically Patterns the Meiotic Chromosome-Axis Interface [ChIP-chip]

Project description:Meiotic chromosomes are highly compacted yet remain transcriptionally active. To understand how chromosome folding accommodates transcription, we investigated the assembly of the axial element, the proteinaceous structure that compacts meiotic chromosomes and promotes recombination and fertility. We found that the axial-element proteins of budding yeast are flexibly anchored to chromatin by the ring-like cohesin complex and biased towards small chromosomes by a separate modulating mechanism that requires the conserved axial element component Hop1. The ubiquitous presence of cohesin at sites of convergent transcription provides well-dispersed points for axis attachment and thus compaction. Axis protein enrichment at these sites directly correlates with the propensity for recombination initiation nearby. Importantly, axis anchoring by cohesin is adjustable and readily displaced in the direction of transcription by the transcriptional machinery. We propose that such robust but flexible tethering allows the highly structured axial element to promote recombination while easily adapting to changes in chromosome activity.

2015-08-06 | GSE69230 | GEO

DNA replication and DSB factor binding in the meiotic S-phase checkpoint in budding yeast

Project description:During gamete formation, crossover recombination must occur on replicated DNA to ensure proper chromosome segregation in the first meiotic division. We identified a Mec1/ATR-dependent replication checkpoint in budding yeast that prevented the earliest stage of recombination, the programmed induction of DNA double-strand breaks (DSBs), when pre-meiotic DNA replication was delayed. The checkpoint suppressed DSBs through three complementary mechanisms: inhibition of Mer2 phosphorylation by Dbf4-dependent Cdc7 kinase, preclusion of chromosomal loading of Rec114 and Mre11, and lowered abundance of the Spo11 nuclease. Without this checkpoint, cells formed DSBs on partially replicated chromosomes. Importantly, such DSBs frequently failed to be repaired and impeded further DNA synthesis, leading to a rapid loss in cell viability. We conclude that a checkpoint-dependent constraint of DSB formation to duplicated DNA is critical not only for meiotic chromosome assortment, but also to protect genome integrity during gametogenesis. DSB factor association was measured in wild-type and checkpoint mutants strains under non-inducing or replication checkpoint inducing conditions. Additionally, DNA replication and helicase loading were measured in a replication and checkpoint deficient strain (cdc6-mn).

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Genome-wide binding site of Rec10 and Rec15 during meiosis

Project description:Higher-order chromosome structure is assumed to control various DNA-templated reactions in eukaryotes. Meiotic chromosomes implement developed structures called M-bM-^@M-^\axesM-bM-^@M-^] and M-bM-^@M-^\loopsM-bM-^@M-^]; both are suggested to tether each other, activating Spo11 to catalyze meiotic DNA double-strand breaks (DSBs) at recombination hotspots. We found that the Schizosaccharomyces pombe Spo11 homolog Rec12 and its partners form two distinct subcomplexes, DSBC (Rec6-Rec12-Rec14) and SFT (Rec7-Rec15-Rec24). Additionally, Mde2, whose expression is strictly regulated by the replication checkpoint, interacts with a component of each subcomplex. The SFT subcomplex binds to both axes via direct interaction of Rec15 with Rec10 in axes and DSB sites, hence axial Rec10 can partially tether DSB sites located in loops. Importantly, this multiprotein-based tethered axis-loop complex is destabilized in the absence of Mde2. We therefore propose a novel mechanism by which Mde2 functions as a recombination initiation mediator to tether axes and loops, in liaison with the meiotic replication checkpoint. ChIP-chip analyses of Rec10 (in wild type), Mde2 (in wild type and rec15M-bM-^HM-^F), and Rec15 (in wild type, rec10M-bM-^HM-^F, rec24M-bM-^HM-^F and mde2M-bM-^HM-^F) at meiosis 4 hours.

2012-07-27 | E-GEOD-31846 | biostudies-arrayexpress

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