High-resolution mapping of meiotic crossovers and non-crossovers in yeast

Abstract

Meiotic recombination plays a central role in the evolution of sexually reproducing organisms. The two recombination outcomes, crossover (CO) and noncrossover (NCO), increase genetic diversity, but have the potential to homogenize alleles by gene conversion. While CO rates are known to vary considerably across the genome, NCOs and gene conversions have only been identified in a handful of loci. To examine recombination genome-wide and at high spatial resolution, we generated maps of COs, CO-associated gene conversion and NCO gene conversion using dense genetic marker data collected from all four products of 56 yeast meioses. Our maps reveal differences in the distributions of COs and NCOs, showing more regions where either COs or NCOs are favoured than expected by chance. Furthermore, we detect evidence for interference between COs and NCOs, a phenomenon previously only known to occur between COs. Up to 1% of the genome of each meiotic product is subject to gene conversion in a single meiosis, with detectable bias towards GC nucleotides. The maps represent the first high-resolution, genome-wide characterization of the multiple outcomes of recombination in any organism. In addition, because NCO hot spots create holes of reduced linkage within haplotype blocks, our results stress the need to incorporate NCOs into genetic linkage analysis.

High-Resolution Mapping of Crossover Events in the Hexaploid Wheat Genome Suggests a Universal Recombination Mechanism

“…containing at least one gene feature (promoter, gene body, or terminator) confirming thus the results observed in yeast (Mancera et al 2008). At the whole-genome level, similar results were found with 2/3 of COs overlapping genes, as this is the case for most COs in plants (reviewed in Mercier et al 2015).…”

“…For cultivated crops, this implies a decrease of the breeding power in regions showing low CO rates (Rodgers-Melnick et al 2015). In human, Saccharomyces cerevisiae, Arabidopsis, and wheat, .80% of the recombination events occur in less than a quarter of the genome (Myers et al 2005;Chen et al 2008;Mancera et al 2008;Choi et al 2013;International Wheat Genome Sequencing Consortium 2014). This nonhomogeneity of CO distribution is the basis of the definition of recombination hotspots and coldspots (which have significantly high and low CO frequencies, respectively).…”

Recombination rate variation in closely related species

“…Other indirect quantitative approaches also exist, such as immunostaining as used by in Murid rodents and Double Strand Break (DSB) mapping, most commonly used in yeast (Gerton et al, 2000;Buhler et al, 2007;Mancera et al, 2008). Of course, choosing an approach is constrained by the organism and the resources available, and researchers must be aware of limitations when making generalizations and conclusions.…”

Detecting positive selection within genomes: the problem of biased gene conversion

“…These processes alter the probability with which a particular allele at a given locus is transmitted to the next generation, and hence its probability of fixation. For example, it has been shown in yeast that gene conversion events occurring during meiotic recombination result in the biased transmission of G and C (denoted by S, for strong) over A and T (W, for weak) alleles (Mancera et al 2008). There is indirect evidence that this form of meiotic drive (termed gBGC, for GC-biased gene conversion) affects genome evolution in many other taxa (Duret & Galtier 2009a).…”