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RNA sequence (RNA-seq) profiling of synthesized chromosome SynI in Saccharomyces cerevisiae

ABSTRACT: We designed and synthesized synI, which is ~21.4% shorter than native chrI, the smallest chromosome in Saccharomyces cerevisiae. SynI was designed for attachment to another synthetic chromosome due to concerns surrounding potential instability and karyotype imbalance, and is now attached to synIII, yielding the first synthetic yeast fusion chromosome. We constructed additional fusion chromosomes to investigate effects of fusions on nuclear function. We observed unexpected loops and twisted structures in chrIII-I and chrIX-III-I fusion chromosomes dependent on silencing protein Sir3. ChrI faces special challenges in assuring meiotic crossovers required for efficient homolog disjunction. Centromere deletions engineered into fusion chromosomes revealed opposing effects of core centromeres and pericentromeres in modulating deposition of meiotic recombination protein Red1. These effects extended over >100kb, to disproportionally promote meiotic recombination of small chromosomes like chrI. These findings reveal the power of synthetic genomics to uncover new biology and deconvolute complex biological systems.

ORGANISM(S): Saccharomyces cerevisiae

PROVIDER: GSE242509 | GEO | 2023/09/15

REPOSITORIES: GEO

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Long-range effects of centromeres on the binding of the meiotic chromosome axis factor Red1

Project description:A chromosome size-dependent bias in meiotic recombination is in place to ensure that homologous chromosome pairing occurs for all chromosomes, including the smallest ones. This bias is clearly detectable during the assembly of the meiotic protein axis, the structure that compacts meiotic chromosomes and promotes recombination.To investigate the origin of the size bias, we mapped genome-wide occupancy of the meiotic axis protein Red1 in yeast strains containing chromosome fusions and synthetic chromosomes. Meiosis studies of the fusion and synthetic chromosomes further revealed that core centromeres influence the deposition of the axial element protein Red1 over distances >100kb, while pericentromeric regions co-evolved to reduce Red1 binding near centromeres and spread out Red1 along the chromosomes.

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Topoisomerases modulate the timing of meiotic DNA breakage and chromosome morphogenesis in Saccharomyces cerevisiae

Project description:During meiotic prophase, concurrent transcription, recombination, and chromosome synapsis place substantial topological strain on chromosomal DNA, but the role of topoisomerases in this context remains poorly defined. Here, we analyzed the roles topoisomerases I and II (Top1 and Top2) during meiotic prophase in Saccharomyces cerevisiae. We show that both topoisomerases accumulate primarily in promoter-containing intergenic regions of actively transcribing genes, including many meiotic double-strand break (DSB) hotspots. Despite the comparable binding patterns, top1 and top2 mutations have different effects on meiotic recombination. TOP1 disruption delays DSB induction and shortens the window of DSB accumulation by an unknown mechanism. By contrast, temperature-sensitive top2-1 mutants exhibit a marked delay in meiotic chromosome remodeling and elevated DSB signals on synapsed chromosomes. The problems in chromosome remodeling were linked to altered Top2 binding patterns rather than a loss of Top2 catalytic activity and stemmed from a defect in recruiting the chromosome remodeler Pch2/TRIP13 to synapsed chromosomes. No chromosomal defects were observed in the absence of TOP1. Our results imply independent roles for topoisomerases I and II in modulating meiotic chromosome structure and recombination.

2020-03-06 | GSE131994 | GEO

LC-MS/MS analysis of immunoprecipitation samples of Tetrahymena meiotic proteins Melg1, Melg2, Melg3, and Tass1

Project description:In most eukaryotes, the meiotic chromosomal bouquet (comprising clustered chromosome ends) provides an ordered chromosome arrangement that facilitates pairing and recombination between homologous chromosomes. In the protist Tetrahymena thermophila, the meiotic prophase nucleus stretches enormously and chromosomes assume a bouquet-like arrangement in which telomeres and centromeres are attached to opposite poles of the nucleus. We have identified and characterized three meiosis-specific genes (MELG1-3) that control nuclear elongation and centromere and telomere clustering. Hence, to find out potential interactions, we did LC-MS/MS analysis for Melg1, Melg2, Melg3, and Tass1 (a partner of Melg3) immunoprecipitation samples.

2020-11-23 | PXD021813 | Pride

Dynamic Reorganization of the Genome Shapes the Recombination Landscape in Meiotic Prophase

Project description:In meiotic prophase, chromosomes are organized into compacted loop arrays to promote homolog pairing and recombination. Here, we probe the architecture of the mouse spermatocyte genome in early and late meiotic prophase using Hi-C. We show that early-prophase chromosomes are arranged as linear arrays of 0.8-1 Mb loops, which extend to 1.5-2 Mb in late prophase as chromosomes compact and homologs undergo synapsis. Topologically associating domains (TADs) are lost in meiotic prophase, suggesting that assembly of the meiotic chromosome axis dramatically reduces the dynamics of chromosome-associated cohesin complexes. While TADs are lost, physically-separated A and B compartments are maintained in meiotic prophase. Moreover, meiotic DNA breaks and inter-homolog crossovers preferentially form in the gene-dense A compartment, revealing a role for chromatin organization in meiotic recombination. Finally, direct detection of inter-homolog contacts genome-wide reveals the structural basis for homolog alignment and juxtaposition by the synaptonemal complex.

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ANKRD31 regulates spatiotemporal patterning of meiotic recombination initiation and ensures recombination between heterologous sex chromosomes in mice

Project description:Orderly segregation of chromosomes during meiosis requires that crossovers form between homologous chromosomes by recombination. Programmed DNA double-strand breaks (DSBs) initiate meiotic recombination. We identify ANKRD31 as a critical component of complexes of DSB-promoting proteins which assemble on meiotic chromosome axes. Genome-wide, ANKRD31 deficiency causes delayed recombination initiation. In addition, loss of ANKRD31 alters DSB distribution owing to reduced selectivity for sites that normally attract DSBs. Strikingly, ANKRD31 deficiency also abolishes uniquely high rates of recombination that normally characterize pseudoautosomal regions (PARs) of X and Y chromosomes. Consequently, sex chromosomes do not form crossovers leading to chromosome segregation failure in ANKRD31-deficient spermatocytes. These defects are accompanied by a genome-wide delay in assembling DSB-promoting proteins on axes and a loss of a pecialized PAR-axis domain that is highly enriched for DSB-promoting proteins. Thus, we propose a model for spatiotemporal patterning of recombination by ANKRD31-dependent control of axis-associated complexes of DSB-promoting proteins.

2019-06-07 | GSE126443 | GEO

Loss of DNA methylation affects recombination landscape in Arabidopsis

Project description:During sexual reproduction half of the genetic material is deposited in gametes and a complete set of chromosomes is restored upon fertilisation. Reduction of the genetic information prior gametogenesis occurs in meiosis where crossovers (COs) between homologous chromosomes secure an exchange of their genetic information. COs are not evenly distributed along chromosomes and are suppressed in chromosomal regions encompassing compact, hypermethylated centromeric and pericentromeric DNA. Therefore, it has been postulated that DNA hypermethylation is inhibitory to COs. Here by analysing meiotic recombination in mutant plants with hypomethylated DNA we observed unexpected and counterintuitive effects of the DNA methylation losses on COs distribution, further promoting recombination in the naturally hypomethylated euchromatic chromosome arms, while inhibiting it in heterochromatic regions encompassing centromeric and pericentromeric hypermethylated DNA. Importantly, the total number of COs was not affected, implying that the loss of DNA methylation only led to a global redistribution of COs along chromosomes. To determine by which mechanisms altered levels of DNA methylation influenced recombination, namely whether this occurred directly in cis or indirectly in trans by changing expression of genes encoding recombination components, we analysed COs distribution in WT lines with randomly scattered and well mapped hypomethylated chromosomal segments. Results of these experiments, supported by expression profiling data, suggest that DNA methylation affects meiotic recombination in cis. As DNA methylation is subjected to significant variation even within a single species, our results implicate that it could influence evolution of plant genomes through the control of meiotic recombination. 2 samples: Col, epiRIL12, with 3 replicates each

2012-03-12 | E-GEOD-34173 | biostudies-arrayexpress

Persistent DNA-break potential near telomeres increases initiation of meiotic recombination on short chromosomes

Project description:Faithful meiotic chromosome inheritance and fertility relies on the stimulation of meiotic crossover recombination by potentially genotoxic DNA double-strand breaks (DSBs). To avoid excessive damage, feedback mechanisms down-regulate DSBs on chromosomes that have successfully initiated crossover repair. In Saccharomyces cerevisiae, this regulation requires the removal of the conserved DSB-promoting protein Hop1/HORMAD during chromosome synapsis. Here, we identify privileged end-adjacent regions (EARs) spanning roughly 100 Kb near all telomeres that escape DSB downregulation. These regions retain Hop1 and continue to break in pachynema despite normal synaptonemal complex deposition. Differential retention of Hop1 requires the disassemblase Pch2/TRIP13, which preferentially removes Hop1 from telomere-distant sequences, and is modulated by the histone deacetylase Sir2 and the nucleoporin Nup2. Importantly, the uniform size of EARs among chromosomes contributes to disproportionately high DSB and repair signals on short chromosomes in pachynema, suggesting that EARs partially underlie the curiously high recombination rate of short chromosomes. Grant ID: Research grant #6-FY16-208 Grant title: Meiotic segregation of small chromosomes Funding Source: March of Dimes Foundation Affiliation: NEW YORK UNIVERSITY Name: Andreas Hochwagen

2019-01-10 | GSE105111 | GEO

Transcription Dynamically Patterns the Meiotic Chromosome-Axis Interface

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. 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 axial element to promote recombination while easily adapting to changes in chromosome activity.

2015-08-07 | GSE70112 | GEO

Loss of DNA methylation affects recombination landscape in Arabidopsis

2012-03-12 | GSE34173 | GEO

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. Two types of study were undertaken to understand the meiotic chromosomal axes assembly and its importance in DSB regulation in yeast. First, DSBs were mapped using ssDNA enrichment in strains isogenic for a dmc1 mutation, and also including rec8 deletion and pREC8-SCC1 in rec8 deletion. Second, the genome-wide distribution of meiotic or mitotic cohesin in meiosis was measured by ChIP-chip analysis in wild-type and pREC8-SCC1 in rec8 deletion.

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

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