-
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 -
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 -
Proceedings. Biological Sciences Sep 2016Meiosis is an ancestral, highly conserved process in eukaryotic life cycles, and for all eukaryotes the shared component of sexual reproduction. The benefits and... (Review)
Review
Meiosis is an ancestral, highly conserved process in eukaryotic life cycles, and for all eukaryotes the shared component of sexual reproduction. The benefits and functions of meiosis, however, are still under discussion, especially considering the costs of meiotic sex. To get a novel view on this old problem, we filter out the most conserved elements of meiosis itself by reviewing the various modifications and alterations of modes of reproduction. Our rationale is that the indispensable steps of meiosis for viability of offspring would be maintained by strong selection, while dispensable steps would be variable. We review evolutionary origin and processes in normal meiosis, restitutional meiosis, polyploidization and the alterations of meiosis in forms of uniparental reproduction (apomixis, apomictic parthenogenesis, automixis, selfing) with a focus on plants and animals. This overview suggests that homologue pairing, double-strand break formation and homologous recombinational repair at prophase I are the least dispensable elements, and they are more likely optimized for repair of oxidative DNA damage rather than for recombination. Segregation, ploidy reduction and also a biparental genome contribution can be skipped for many generations. The evidence supports the theory that the primary function of meiosis is DNA restoration rather than recombination.
Topics: Animals; Biological Evolution; Eukaryota; Meiosis; Plants; Recombination, Genetic; Reproduction
PubMed: 27605505
DOI: 10.1098/rspb.2016.1221 -
Genes Sep 2021Plant cytogenetic studies have provided essential knowledge on chromosome behavior during meiosis, contributing to our understanding of this complex process. In this... (Review)
Review
Plant cytogenetic studies have provided essential knowledge on chromosome behavior during meiosis, contributing to our understanding of this complex process. In this review, we describe in detail the meiotic process in auto- and allopolyploids from the onset of prophase I through pairing, recombination, and bivalent formation, highlighting recent findings on the genetic control and mode of action of specific proteins that lead to diploid-like meiosis behavior in polyploid species. During the meiosis of newly formed polyploids, related chromosomes (homologous in autopolyploids; homologous and homoeologous in allopolyploids) can combine in complex structures called multivalents. These structures occur when multiple chromosomes simultaneously pair, synapse, and recombine. We discuss the effectiveness of crossover frequency in preventing multivalent formation and favoring regular meiosis. Homoeologous recombination in particular can generate new gene (locus) combinations and phenotypes, but it may destabilize the karyotype and lead to aberrant meiotic behavior, reducing fertility. In crop species, understanding the factors that control pairing and recombination has the potential to provide plant breeders with resources to make fuller use of available chromosome variations in number and structure. We focused on wheat and oilseed rape, since there is an abundance of elucidating studies on this subject, including the molecular characterization of the (wheat) and (oilseed rape) loci, which are known to play a crucial role in regulating meiosis. Finally, we exploited the consequences of chromosome pairing and recombination for genetic map construction in polyploids, highlighting two case studies of complex genomes: (i) modern sugarcane, which has a man-made genome harboring two subgenomes with some recombinant chromosomes; and (ii) hexaploid sweet potato, a naturally occurring polyploid. The recent inclusion of allelic dosage information has improved linkage estimation in polyploids, allowing multilocus genetic maps to be constructed.
Topics: Brassica napus; Chromosomes, Plant; Crossing Over, Genetic; Meiosis; Plant Breeding; Polyploidy; Triticum
PubMed: 34680912
DOI: 10.3390/genes12101517 -
The Plant Journal : For Cell and... Jul 2015During meiosis homologous chromosomes pair and undergo reciprocal genetic exchange, termed crossover. Meiotic recombination has a profound effect on patterns of genetic... (Review)
Review
During meiosis homologous chromosomes pair and undergo reciprocal genetic exchange, termed crossover. Meiotic recombination has a profound effect on patterns of genetic variation and is an important tool during crop breeding. Crossovers initiate from programmed DNA double-stranded breaks that are processed to form single-stranded DNA, which can invade a homologous chromosome. Strand invasion events mature into double Holliday junctions that can be resolved as crossovers. Extensive variation in the frequency of meiotic recombination occurs along chromosomes and is typically focused in narrow hotspots, observed both at the level of DNA breaks and final crossovers. We review methodologies to profile hotspots at different steps of the meiotic recombination pathway that have been used in different eukaryote species. We then discuss what these studies have revealed concerning specification of hotspot locations and activity and the contributions of both genetic and epigenetic factors. Understanding hotspots is important for interpreting patterns of genetic variation in populations and how eukaryotic genomes evolve. In addition, manipulation of hotspots will allow us to accelerate crop breeding, where meiotic recombination distributions can be limiting.
Topics: Crossing Over, Genetic; DNA Breaks, Double-Stranded; DNA, Single-Stranded; Epigenesis, Genetic; Fungi; Genetic Techniques; Genome; Homologous Recombination; Meiosis; Plants
PubMed: 25925869
DOI: 10.1111/tpj.12870 -
Science China. Life Sciences Mar 2015Meiotic recombination is a deeply conserved process within eukaryotes that has a profound effect on patterns of natural genetic variation. During meiosis homologous... (Review)
Review
Meiotic recombination is a deeply conserved process within eukaryotes that has a profound effect on patterns of natural genetic variation. During meiosis homologous chromosomes pair and undergo DNA double strand breaks generated by the Spo11 endonuclease. These breaks can be repaired as crossovers that result in reciprocal exchange between chromosomes. The frequency of recombination along chromosomes is highly variable, for example, crossovers are rarely observed in heterochromatin and the centromeric regions. Recent work in plants has shown that crossover hotspots occur in gene promoters and are associated with specific chromatin modifications, including H2A.Z. Meiotic chromosomes are also organized in loop-base arrays connected to an underlying chromosome axis, which likely interacts with chromatin to organize patterns of recombination. Therefore, epigenetic information exerts a major influence on patterns of meiotic recombination along chromosomes, genetic variation within populations and evolution of plant genomes.
Topics: Chromatin; Crossing Over, Genetic; Epigenesis, Genetic; Meiosis; Plants; Recombination, Genetic
PubMed: 25651968
DOI: 10.1007/s11427-015-4811-x -
Philosophical Transactions of the Royal... Dec 2017Meiosis is unusual among cell divisions in shuffling genetic material by crossovers among homologous chromosomes and partitioning the genome into haploid gametes.... (Review)
Review
Meiosis is unusual among cell divisions in shuffling genetic material by crossovers among homologous chromosomes and partitioning the genome into haploid gametes. Crossovers are critical for chromosome segregation in most eukaryotes, but are also an important factor in evolution, as they generate novel genetic combinations. The molecular mechanisms that underpin meiotic recombination and chromosome segregation are well conserved across kingdoms, but are also sensitive to perturbation by environment, especially temperature. Even subtle shifts in temperature can alter the number and placement of crossovers, while at greater extremes, structural failures can occur in the linear axis and synaptonemal complex structures which are essential for recombination and chromosome segregation. Understanding the effects of temperature on these processes is important for its implications in evolution and breeding, especially in the context of global warming. In this review, we first summarize the process of meiotic recombination and its reliance on axis and synaptonemal complex structures, and then discuss effects of temperature on these processes and structures. We hypothesize that some consistent effects of temperature on recombination and meiotic thermotolerance may commonly be two sides of the same coin, driven by effects of temperature on the folding or interaction of key meiotic proteins.This article is part of the themed issue 'Evolutionary causes and consequences of recombination rate variation in sexual organisms'.
Topics: Global Warming; Meiosis; Recombination, Genetic; Synaptonemal Complex; Temperature; Thermotolerance
PubMed: 29109229
DOI: 10.1098/rstb.2016.0470 -
Seminars in Cell & Developmental Biology Jun 2016During the first division of meiosis, segregation of homologous chromosomes reduces the chromosome number by half. In most species, sister chromatid cohesion and... (Review)
Review
During the first division of meiosis, segregation of homologous chromosomes reduces the chromosome number by half. In most species, sister chromatid cohesion and reciprocal recombination (crossing-over) between homologous chromosomes are essential to provide tension to signal proper chromosome segregation during the first meiotic division. Crossovers are not distributed uniformly throughout the genome and are repressed at and near the centromeres. Rare crossovers that occur too near or in the centromere interfere with proper segregation and can give rise to aneuploid progeny, which can be severely defective or inviable. We review here how crossing-over occurs and how it is prevented in and around the centromeres. Molecular mechanisms of centromeric repression are only now being elucidated. However, rapid advances in understanding crossing-over, chromosome structure, and centromere functions promise to explain how potentially deleterious crossovers are avoided in certain chromosomal regions while allowing beneficial crossovers in others.
Topics: Animals; Centromere; Chromosome Segregation; DNA Breaks, Double-Stranded; Gene Conversion; Humans; Meiosis; Recombination, Genetic
PubMed: 26849908
DOI: 10.1016/j.semcdb.2016.01.042 -
Annual Review of Genetics 2010Homologous recombination (HR) is required for accurate chromosome segregation during the first meiotic division and constitutes a key repair and tolerance pathway for... (Review)
Review
Homologous recombination (HR) is required for accurate chromosome segregation during the first meiotic division and constitutes a key repair and tolerance pathway for complex DNA damage, including DNA double-strand breaks, interstrand crosslinks, and DNA gaps. In addition, recombination and replication are inextricably linked, as recombination recovers stalled and broken replication forks, enabling the evolution of larger genomes/replicons. Defects in recombination lead to genomic instability and elevated cancer predisposition, demonstrating a clear cellular need for recombination. However, recombination can also lead to genome rearrangements. Unrestrained recombination causes undesired endpoints (translocation, deletion, inversion) and the accumulation of toxic recombination intermediates. Evidently, HR must be carefully regulated to match specific cellular needs. Here, we review the factors and mechanistic stages of recombination that are subject to regulation and suggest that recombination achieves flexibility and robustness by proceeding through metastable, reversible intermediates.
Topics: Animals; DNA Repair; Humans; Recombination, Genetic; Yeasts
PubMed: 20690856
DOI: 10.1146/annurev-genet-051710-150955 -
Genetics Dec 2018Meiotic recombination is a major driver of genome evolution by creating new genetic combinations. To probe the factors driving variability of meiotic recombination, we...
Meiotic recombination is a major driver of genome evolution by creating new genetic combinations. To probe the factors driving variability of meiotic recombination, we used a high-throughput method to measure recombination rates in hybrids between SK1 and a total of 26 strains from different geographic origins and habitats. Fourteen intervals were monitored for each strain, covering chromosomes VI and XI entirely, and part of chromosome I. We found an average number of crossovers per chromosome ranging between 1.0 and 9.5 across strains ("domesticated" or not), which is higher than the average between 0.5 and 1.5 found in most organisms. In the different intervals analyzed, recombination showed up to ninefold variation across strains but global recombination landscapes along chromosomes varied less. We also built an incomplete diallel experiment to measure recombination rates in one region of chromosome XI in 10 different crosses involving five parental strains. Our overall results indicate that recombination rate is increasingly positively correlated with sequence similarity between homologs (i) in DNA double-strand-break-rich regions within intervals, (ii) in entire intervals, and (iii) at the whole genome scale. Therefore, these correlations cannot be explained by effects only. We also estimated that and effects explained 38 and 17%, respectively, of the variance of recombination rate. In addition, by using a quantitative genetics analysis, we identified an inbreeding effect that reduces recombination rate in homozygous genotypes, while other interaction effects (specific combining ability) or additive effects (general combining ability) are found to be weak. Finally, we measured significant crossover interference in some strains, and interference intensity was positively correlated with crossover number.
Topics: Chromosomes, Fungal; Crossing Over, Genetic; DNA Breaks, Double-Stranded; Genome, Fungal; Genotype; Inbreeding; Meiosis; Recombination, Genetic; Saccharomyces cerevisiae
PubMed: 30291109
DOI: 10.1534/genetics.118.301644