Dissecting meiotic recombination based on tetrad analysis by single-microspore sequencing in maize

Li, Xiang; Li, Lin; Yan, Jianbing

doi:10.1038/ncomms7648

Cited by 114 publications

(169 citation statements)

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“…This is consistent with low levels of DNA methylation observed at Arabidopsis and maize crossover hot spots (Choi et al 2013;Wijnker et al 2013;RodgersMelnick et al 2015) and the widespread suppression of recombination in plant heterochromatin (Copenhaver et al 1999;Fu et al 2002;Liu et al 2009;Giraut et al 2011;Mayer et al 2012;Salomé et al 2012; The Tomato Genome Consortium 2012; Bauer et al 2013;Choulet et al 2014;Li et al 2015;Rodgers-Melnick et al 2015). We show that RdDM is associated with acquisition of H3K9me2 and increased nucleosome occupancy at the targeted hot spots.…”

Section: Discussionsupporting

confidence: 62%

“…Plant hot spots are observed at gene transcriptional start sites (TSSs) and transcriptional termination sites (TTSs) and require the histone variant H2A.Z for wild-type activity (Brown and Sundaresan 1991;Fu et al 2001;Saintenac et al 2011;Choi et al 2013;Drouaud et al 2013;Hellsten et al 2013;Li et al 2015). In contrast, crossovers are largely suppressed in repeat-rich heterochromatic regions in plant genomes (Copenhaver et al 1999;Wei et al 2009;Mayer et al 2012; The Tomato Genome Consortium 2012; Yelina et al 2012;Choulet et al 2014;Rodgers-Melnick et al 2015).…”

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confidence: 99%

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DNA methylation epigenetically silences crossover hot spots and controls chromosomal domains of meiotic recombination in Arabidopsis

et al. 2015

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During meiosis, homologous chromosomes undergo crossover recombination, which is typically concentrated in narrow hot spots that are controlled by genetic and epigenetic information. Arabidopsis chromosomes are highly DNA methylated in the repetitive centromeres, which are also crossover-suppressed. Here we demonstrate that RNA-directed DNA methylation is sufficient to locally silence Arabidopsis euchromatic crossover hot spots and is associated with increased nucleosome density and H3K9me2. However, loss of CG DNA methylation maintenance in met1 triggers epigenetic crossover remodeling at the chromosome scale, with pericentromeric decreases and euchromatic increases in recombination. We used recombination mutants that alter interfering and noninterfering crossover repair pathways ( fancm and zip4) to demonstrate that remodeling primarily involves redistribution of interfering crossovers. Using whole-genome bisulfite sequencing, we show that crossover remodeling is driven by loss of CG methylation within the centromeric regions. Using cytogenetics, we profiled meiotic DNA double-strand break (DSB) foci in met1 and found them unchanged relative to wild type. We propose that met1 chromosome structure is altered, causing centromere-proximal DSBs to be inhibited from maturation into interfering crossovers. These data demonstrate that DNA methylation is sufficient to silence crossover hot spots and plays a key role in establishing domains of meiotic recombination along chromosomes.

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Section: Discussionsupporting

confidence: 62%

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confidence: 99%

DNA methylation epigenetically silences crossover hot spots and controls chromosomal domains of meiotic recombination in Arabidopsis

et al. 2015

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“…Thus, historical CO events can be deduced from linkage disequilibrium analysis that measures the association of sets of markers on chromosomes in a population. Recently, whole-genome sequencing of four products of meiotic tetrads allowed fine-scale mapping of recombination break points (Wijnker et al, 2013;Li et al, 2015). COs also can be scored cytologically by counting chiasmata or recombination nodules, seen as electron-dense structures at recombination sites by electron microscopy (Anderson et al, 2003).…”

Section: Co Distributionmentioning

confidence: 99%

Understanding and Manipulating Meiotic Recombination in Plants

2017

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Meiosis is a specialized cell division, essential in most reproducing organisms to halve the number of chromosomes, thereby enabling the restoration of ploidy levels during fertilization. A key step of meiosis is homologous recombination, which promotes homologous pairing and generates crossovers (COs) to connect homologous chromosomes until their separation at anaphase I. These CO sites, seen cytologically as chiasmata, represent a reciprocal exchange of genetic information between two homologous nonsister chromatids. This gene reshuffling during meiosis has a significant influence on evolution and also plays an essential role in plant breeding, because a successful breeding program depends on the ability to bring the desired combinations of alleles on chromosomes. However, the number and distribution of COs during meiosis is highly constrained. There is at least one CO per chromosome pair to ensure accurate segregation of homologs, but in most organisms, the CO number rarely exceeds three regardless of chromosome size. Moreover, their positions are not random on chromosomes but exhibit regional preference. Thus, genes in recombination-poor regions tend to be inherited together, hindering the generation of novel allelic combinations that could be exploited by breeding programs. Recently, much progress has been made in understanding meiotic recombination. In particular, many genes involved in the process in Arabidopsis (Arabidopsis thaliana) have been identified and analyzed. With the coming challenges of food security and climate change, and our enhanced knowledge of how COs are formed, the interest and needs in manipulating CO formation are greater than ever before. In this review, we focus on advances in understanding meiotic recombination and then summarize the attempts to manipulate CO formation. Last, we pay special attention to the meiotic recombination in polyploidy, which is a common genomic feature for many crop plants.

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“…It is also possible to map recombination events at high resolution, by crossing strains with defined sequence polymorphisms, followed by wholegenome sequencing of the resulting progenies. High-resolution maps of genome-wide recombination events are now available for Saccharomyces cerevisiae, Drosophila, maize, and Theileria parva (Mancera et al, 2008;Comeron et al, 2012;Henson et al, 2012;Li et al, 2015;Rodgers-Melnick et al, 2015). Furthermore, highthroughput sequencing, combined with single-cell technology, contributed to the detection of meiotic recombination of single sperm (Lu et al, 2012b;Wang et al, 2012) and single oocyte (Hou et al, 2013) genotyping.…”

Section: Introductionmentioning

confidence: 99%

DNA Crossover Motifs Associated with Epigenetic Modifications Delineate Open Chromatin Regions in Arabidopsis

et al. 2015

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The rate of crossover, the reciprocal exchanges of homologous chromosomal segments, is not uniform along chromosomes differing between male and female meiocytes. To better understand the factors regulating this variable landscape, we performed a detailed genetic and epigenetic analysis of 737 crossover events in Arabidopsis thaliana. Crossovers were more frequent than expected in promoters. Three DNA motifs enriched in crossover regions and less abundant in crossover-poor pericentric regions were identified. One of these motifs, the CCN repeat, was previously unknown in plants. The A-rich motif was preferentially associated with promoters, while the CCN repeat and the CTT repeat motifs were preferentially associated with genes. Analysis of epigenetic modifications around the motifs showed, in most cases, a specific epigenetic architecture. For example, we show that there is a peak of nucleosome occupancy and of H3K4me3 around the CCN and CTT repeat motifs while nucleosome occupancy was lowest around the A-rich motif. Cytosine methylation levels showed a gradual decrease within ;2 kb of the three motifs, being lowest at sites where crossover occurred. This landscape was conserved in the decreased DNA methylation1 mutant. In summary, the crossover motifs are associated with epigenetic landscapes corresponding to open chromatin and contributing to the nonuniformity of crossovers in Arabidopsis.

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Dissecting meiotic recombination based on tetrad analysis by single-microspore sequencing in maize

Cited by 114 publications

References 55 publications

DNA methylation epigenetically silences crossover hot spots and controls chromosomal domains of meiotic recombination in Arabidopsis

DNA methylation epigenetically silences crossover hot spots and controls chromosomal domains of meiotic recombination in Arabidopsis

Understanding and Manipulating Meiotic Recombination in Plants

DNA Crossover Motifs Associated with Epigenetic Modifications Delineate Open Chromatin Regions in Arabidopsis

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