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Molecular Biology and Evolution Feb 2019Meiotic recombination comprises crossovers and noncrossovers. Recombination, crossover in particular, shuffles mutations and impacts both the level of genetic...
Meiotic recombination comprises crossovers and noncrossovers. Recombination, crossover in particular, shuffles mutations and impacts both the level of genetic polymorphism and the speed of adaptation. In many species, the recombination rate varies across the genome with hot and cold spots. The hotspot paradox hypothesis asserts that recombination hotspots are evolutionarily unstable due to self-destruction. However, the genomic landscape of double-strand breaks (DSBs), which initiate recombination, is evolutionarily conserved among divergent yeast species, casting doubt on the hotspot paradox hypothesis. Nonetheless, because only a subset of DSBs are associated with crossovers, the evolutionary conservation of the crossover landscape could differ from that of DSBs. Here, we investigate this possibility by generating a high-resolution recombination map of the budding yeast Saccharomyces paradoxus through whole-genome sequencing of 50 meiotic tetrads and by comparing this recombination map with that of S. cerevisiae. We observe a 40% lower recombination rate in S. paradoxus than in S. cerevisiae. Compared with the DSB landscape, the crossover landscape is even more conserved. Further analyses indicate that the elevated conservation of the crossover landscape is explained by a near-subtelomeric crossover preference in both yeasts, which we find to be attributable at least in part to crossover interference. We conclude that the yeast crossover landscape is highly conserved and that the evolutionary conservation of this landscape can differ from that of the DSB landscape.
Topics: Biological Evolution; DNA Breaks, Double-Stranded; Heterozygote; Recombination, Genetic; Saccharomyces
PubMed: 30535029
DOI: 10.1093/molbev/msy233 -
G3 (Bethesda, Md.) Jun 2023Recombination allows for the exchange of genetic material between two parents, which plant breeders exploit to make improved cultivars. This recombination is not...
Recombination allows for the exchange of genetic material between two parents, which plant breeders exploit to make improved cultivars. This recombination is not distributed evenly across the chromosome. Recombination mostly occurs in euchromatic regions of the genome and even then, recombination is focused into clusters of crossovers termed recombination hotspots. Understanding the distribution of these hotspots along with the sequence motifs associated with them may lead to methods that enable breeders to better exploit recombination in breeding. To map recombination hotspots and identify sequence motifs associated with hotspots in soybean [Glycine max (L.) Merr.], two biparental recombinant inbred lines populations were genotyped with the SoySNP50k Illumina Infinium assay. A total of 451 recombination hotspots were identified in the two populations. Despite being half-sib populations, only 18 hotspots were in common between the two populations. While pericentromeric regions did exhibit extreme suppression of recombination, 27% of the detected hotspots were located in the pericentromeric regions of the chromosomes. Two genomic motifs associated with hotspots are similar to human, dog, rice, wheat, drosophila, and arabidopsis. These motifs were a CCN repeat motif and a poly-A motif. Genomic regions spanning other hotspots were significantly enriched with the tourist family of mini-inverted-repeat transposable elements that resides in <0.34% of the soybean genome. The characterization of recombination hotspots in these two large soybean biparental populations demonstrates that hotspots do occur throughout the soybean genome and are enriched for specific motifs, but their locations may not be conserved between different populations.
Topics: Humans; Animals; Dogs; Glycine max; Plant Breeding; Genome; Genotype; Recombination, Genetic
PubMed: 36999557
DOI: 10.1093/g3journal/jkad075 -
Molecular Cell Oct 2021Currently favored models for meiotic recombination posit that both noncrossover and crossover recombination are initiated by DNA double-strand breaks but form by...
Currently favored models for meiotic recombination posit that both noncrossover and crossover recombination are initiated by DNA double-strand breaks but form by different mechanisms: noncrossovers by synthesis-dependent strand annealing and crossovers by formation and resolution of double Holliday junctions centered around the break. This dual mechanism hypothesis predicts different hybrid DNA patterns in noncrossover and crossover recombinants. We show that these predictions are not upheld, by mapping with unprecedented resolution parental strand contributions to recombinants at a model locus. Instead, break repair in both noncrossovers and crossovers involves synthesis-dependent strand annealing, often with multiple rounds of strand invasion. Crossover-specific double Holliday junction formation occurs via processes involving branch migration as an integral feature, one that can be separated from repair of the break itself. These findings reveal meiotic recombination to be a highly dynamic process and prompt a new view of the relationship between crossover and noncrossover recombination.
Topics: Crossing Over, Genetic; DNA Breaks, Double-Stranded; DNA, Cruciform; DNA, Fungal; Meiosis; Recombinational DNA Repair; Saccharomyces cerevisiae; Saccharomyces cerevisiae Proteins; Sister Chromatid Exchange; Templates, Genetic
PubMed: 34453891
DOI: 10.1016/j.molcel.2021.08.003 -
Seminars in Cell & Developmental Biology Jun 2016The mycelial fungus Sordaria macrospora was first used as experimental system for meiotic recombination. This review shows that it provides also a powerful cytological... (Review)
Review
The mycelial fungus Sordaria macrospora was first used as experimental system for meiotic recombination. This review shows that it provides also a powerful cytological system for dissecting chromosome dynamics in wild-type and mutant meioses. Fundamental cytogenetic findings include: (1) the identification of presynaptic alignment as a key step in pairing of homologous chromosomes. (2) The discovery that biochemical complexes that mediate recombination at the DNA level concomitantly mediate pairing of homologs. (3) This pairing process involves not only resolution but also avoidance of chromosomal entanglements and the resolution system includes dissolution of constraining DNA recombination interactions, achieved by a unique role of Mlh1. (4) Discovery that the central components of the synaptonemal complex directly mediate the re-localization of the recombination proteins from on-axis to in-between homologue axis positions. (5) Identification of putative STUbL protein Hei10 as a structure-based signal transduction molecule that coordinates progression and differentiation of recombinational interactions at multiple stages. (6) Discovery that a single interference process mediates both nucleation of the SC and designation of crossover sites, thereby ensuring even spacing of both features. (7) Discovery of local modulation of sister-chromatid cohesion at sites of crossover recombination.
Topics: Chromosome Pairing; Fungal Proteins; Models, Biological; Recombination, Genetic; Sordariales; Synaptonemal Complex
PubMed: 26877138
DOI: 10.1016/j.semcdb.2016.02.012 -
Current Opinion in Genetics &... Dec 2021DNA breaks may arise accidentally in vegetative cells or in a programmed manner in meiosis. The usage of a DNA template makes homologous recombination potentially... (Review)
Review
DNA breaks may arise accidentally in vegetative cells or in a programmed manner in meiosis. The usage of a DNA template makes homologous recombination potentially error-free, however, recombination is not always accurate. Cells possess a remarkable capacity to tailor processing of recombination intermediates to fulfill a particular need. Vegetatively growing cells aim to maintain genome stability and therefore repair accidental breaks largely accurately, using sister chromatids as templates, into mostly non-crossovers products. Recombination in meiotic cells is instead more likely to employ homologous chromosomes as templates and result in crossovers to allow proper chromosome segregation and promote genetic diversity. Here we review models explaining the processing of recombination intermediates in vegetative and meiotic cells and its regulation, with a focus on MLH1-MLH3-dependent crossing-over during meiotic recombination.
Topics: Chromatids; Chromosome Segregation; DNA Breaks, Double-Stranded; DNA Repair; Homologous Recombination; Meiosis
PubMed: 34293660
DOI: 10.1016/j.gde.2021.06.012 -
Molecular Biology and Evolution Mar 2021Genetic recombination characterized by reciprocal exchange of genes on paired homologous chromosomes is the most prominent event in meiosis of almost all sexually...
Genetic recombination characterized by reciprocal exchange of genes on paired homologous chromosomes is the most prominent event in meiosis of almost all sexually reproductive organisms. It contributes to genome stability by ensuring the balanced segregation of paired homologs in meiosis, and it is also the major driving factor in generating genetic variation for natural and artificial selection. Meiotic recombination is subjected to the control of a highly stringent and complex regulating process and meiotic recombination frequency (MRF) may be affected by biological and abiotic factors such as sex, gene density, nucleotide content, and chemical/temperature treatments, having motivated tremendous researches for artificially manipulating MRF. Whether genome polyploidization would lead to a significant change in MRF has attracted both historical and recent research interests; however, tackling this fundamental question is methodologically challenging due to the lack of appropriate methods for tetrasomic genetic analysis, thus has led to controversial conclusions in the literature. This article presents a comprehensive and rigorous survey of genome duplication-mediated change in MRF using Saccharomyces cerevisiae as a eukaryotic model. It demonstrates that genome duplication can lead to consistently significant increase in MRF and rate of crossovers across all 16 chromosomes of S. cerevisiae, including both cold and hot spots of MRF. This ploidy-driven change in MRF is associated with weakened recombination interference, enhanced double-strand break density, and loosened chromatin histone occupation. The study illuminates a significant evolutionary feature of genome duplication and opens an opportunity to accelerate response to artificial and natural selection through polyploidization.
Topics: Crossing Over, Genetic; DNA Breaks, Double-Stranded; Gene Duplication; Meiosis; Models, Genetic; Ploidies; Saccharomyces cerevisiae
PubMed: 32898273
DOI: 10.1093/molbev/msaa219 -
Genetics, Selection, Evolution : GSE Jun 2021Meiotic recombination results in the exchange of genetic material between homologous chromosomes. Recombination rate varies between different parts of the genome,...
BACKGROUND
Meiotic recombination results in the exchange of genetic material between homologous chromosomes. Recombination rate varies between different parts of the genome, between individuals, and is influenced by genetics. In this paper, we assessed the genetic variation in recombination rate along the genome and between individuals in the pig using multilocus iterative peeling on 150,000 individuals across nine genotyped pedigrees. We used these data to estimate the heritability of recombination and perform a genome-wide association study of recombination in the pig.
RESULTS
Our results confirmed known features of the recombination landscape of the pig genome, including differences in genetic length of chromosomes and marked sex differences. The recombination landscape was repeatable between lines, but at the same time, there were differences in average autosome-wide recombination rate between lines. The heritability of autosome-wide recombination rate was low but not zero (on average 0.07 for females and 0.05 for males). We found six genomic regions that are associated with recombination rate, among which five harbour known candidate genes involved in recombination: RNF212, SHOC1, SYCP2, MSH4 and HFM1.
CONCLUSIONS
Our results on the variation in recombination rate in the pig genome agree with those reported for other vertebrates, with a low but nonzero heritability, and the identification of a major quantitative trait locus for recombination rate that is homologous to that detected in several other species. This work also highlights the utility of using large-scale livestock data to understand biological processes.
Topics: Animals; Female; Genetic Loci; Genetic Variation; Male; Pedigree; Recombination, Genetic; Swine
PubMed: 34171988
DOI: 10.1186/s12711-021-00643-0 -
Molecular Biology of the Cell May 2022Homologous recombination (HR) is an essential meiotic process that contributes to the genetic variation of offspring and ensures accurate chromosome segregation....
Homologous recombination (HR) is an essential meiotic process that contributes to the genetic variation of offspring and ensures accurate chromosome segregation. Recombination is facilitated by the formation and repair of programmed DNA double-strand breaks. These DNA breaks are repaired via recombination between maternal and paternal homologous chromosomes and a subset result in the formation of crossovers. HR and crossover formation is facilitated by synapsis of homologous chromosomes by a proteinaceous scaffold structure known as the synaptonemal complex (SC). Recent studies in yeast and worms have indicated that polo-like kinases (PLKs) regulate several events during meiosis, including DNA recombination and SC dynamics. Mammals express four active PLKs (PLK1-4), and our previous work assessing localization and kinase function in mouse spermatocytes suggested that PLK1 coordinates nuclear events during meiotic prophase. Therefore, we conditionally mutated in early prophase spermatocytes and assessed stages of HR, crossover formation, and SC processes. mutation resulted in increased RPA foci and reduced RAD51/DMC1 foci during zygonema, and an increase of both class I and class II crossover events. Furthermore, the disassembly of SC lateral elements was aberrant. Our results highlight the importance of PLK1 in regulating HR and SC disassembly during spermatogenesis.
Topics: Animals; Cell Cycle Proteins; Chromosome Pairing; DNA; Homologous Recombination; Male; Mammals; Meiosis; Mice; Protein Serine-Threonine Kinases; Proto-Oncogene Proteins; Spermatogenesis; Synaptonemal Complex; Polo-Like Kinase 1
PubMed: 35274968
DOI: 10.1091/mbc.E21-03-0115 -
Genetics Aug 2023It has long been known that the chiasmata are not independently distributed in most organisms, a phenomenon known as chiasma interference. In this paper, I suggest a...
It has long been known that the chiasmata are not independently distributed in most organisms, a phenomenon known as chiasma interference. In this paper, I suggest a model of chiasma interference that generalizes the Poisson model, the counting model, the Poisson-skip model, and the two-pathway counting model into a single framework, and use it to derive infinite series expressions for the sterility and recombination pattern probabilities in inversion homo- and heterokaryotypes, and a closed-form expression for the special case of the two-pathway counting model in homokaryotypes. I then use these expressions to perform maximum likelihood parameter estimations for recombination and tetrad data from various species. The results imply that the simpler counting models perform well compared to more complex ones, that interference works in a similar way in homo- and heterokaryotypes, and that the model fits well with data for the latter as well as the former. I also find evidence that the interference signal is broken by the centromere in some species, but not others, suggestions of negative interference in Aspergillus nidulans, and no consistent support for the theory that a second noninterfering chiasma pathway exists only in organisms that require double-strand break for synapsis. I suggest that the latter finding is at least partly due to issues involved in analyzing aggregate data from different experiments and individuals.
Topics: Humans; Crossing Over, Genetic; Centromere; Chromosome Pairing; Chromosome Inversion; Infertility; Meiosis
PubMed: 37378555
DOI: 10.1093/genetics/iyad120 -
DNA Research : An International Journal... Dec 2017Traditional plant breeding relies on meiotic recombination for mixing of parental alleles to create novel allele combinations. Detailed analysis of recombination...
Traditional plant breeding relies on meiotic recombination for mixing of parental alleles to create novel allele combinations. Detailed analysis of recombination patterns in model organisms shows that recombination is tightly regulated within the genome, but frequencies vary extensively along chromosomes. Despite being a model organism for fruit developmental studies, high-resolution recombination patterns are lacking in tomato. In this study, we developed a novel methodology to use low-coverage resequencing to identify genome-wide recombination patterns and applied this methodology on 60 tomato Recombinant Inbred Lines (RILs). Our methodology identifies polymorphic markers from the low-coverage resequencing population data and utilizes the same data to locate the recombination breakpoints in individuals by using a variable sliding window. We identified 1,445 recombination sites comprising 112 recombination prone regions enriched for AT-rich DNA motifs. Furthermore, the recombination prone regions in tomato preferably occurred in gene promoters over intergenic regions, an observation consistent with Arabidopsis thaliana, Zea mays and Mimulus guttatus. Overall, our cost effective method and findings enhance the understanding of meiotic recombination in tomato and suggest evolutionarily conserved recombination associated genomic features.
Topics: Genome, Plant; High-Throughput Nucleotide Sequencing; Solanum lycopersicum; Meiosis; Nucleotide Motifs; Polymorphism, Single Nucleotide; Recombination, Genetic; Sequence Analysis, DNA
PubMed: 28605512
DOI: 10.1093/dnares/dsx024