High-resolution crossover mapping reveals similarities and differences of male and female recombination in maize

Kianian, Penny M.A.; Wang, Minghui; Simons, Kristin; Ghavami, Farhad; He, Yan; Dukowic-Schulze, Stefanie; Sundararajan, Anitha; Sun, Qi; Pillardy, Jarosław; Mudge, Joann; Chen, Changbin; Kianian, Shahryar F.; Pawlowski, Wojciech P.

doi:10.1038/s41467-018-04562-5

Cited by 77 publications

(125 citation statements)

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“…SPO11-oligo sequencing in Arabidopsis and budding yeast has revealed meiotic DSB hotspots located in nucleosome-free regions associated with gene regulatory sequences (Choi et al, 2018;Pan et al, 2011). Crossovers in plants also positively associate with H3K4me3 and histone variant H2A.Z, which show 5′ enrichment at transcribed genes (Choi et al, 2013;Liu et al, 2009;Wijnker et al, 2013;He et al, 2017;Kianian et al, 2018). In budding yeast, H3K4me3 tethers DSB hotspots to the Mer2 axis protein via the COMPASS complex Spp1 subunit, showing how chromatin and axis organization can interact to promote meiotic recombination (Sommermeyer et al, 2013;Acquaviva et al, 2013).…”

Section: Introductionmentioning

confidence: 99%

Interacting Genomic Landscapes of REC8-Cohesin, Chromatin, and Meiotic Recombination in Arabidopsis

et al. 2020

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Section: Introductionmentioning

confidence: 99%

Interacting Genomic Landscapes of REC8-Cohesin, Chromatin, and Meiotic Recombination in Arabidopsis

et al. 2020

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“…This results in new combinations of alleles in the next generation that can generate novel phenotypic variation, which is the raw material for both natural and artificial selection [1][2][3] . In most organisms, the locations of COs along chromosomes do not form a random distribution [4][5][6][7][8][9][10][11] . Thus, the local CO rate governs the types of allelic combinations that can arise through sexual reproduction.…”

Section: Introductionmentioning

confidence: 99%

Linked-read sequencing of gametes allows efficient genome-wide analysis of meiotic recombination

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Rowan

Flood

et al. 2018

Preprint

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Meiotic crossovers (COs) ensure proper chromosome segregation and redistribute the genetic variation that is transmitted to the next generation. Existing methods for CO identification are challenged by large populations and the demand for genome-wide and fine-scale resolution. Taking advantage of linked-read sequencing, we developed a highly efficient method for genome-wide identification of COs at kilobase resolution in pooled recombinants. We first tested this method using a pool of Arabidopsis F 2 recombinants, and obtained results that recapitulated those identified from the same plants using individual whole-genome sequencing. By applying this method to a pool of pollen DNA from a single F 1 plant, we established a highly accurate CO landscape without generating or sequencing a single recombinant plant. The simplicity of this approach now enables the simultaneous generation and analysis of multiple CO landscapes and thereby allows for efficient comparison of genotypic and environmental effects on recombination, accelerating the pace at which the mechanisms for the regulation of recombination can be elucidated. CO detection using linked-read sequencing RESULTS CO breakpoint detection from bulk recombinantsTo establish a set of COs for verifying our method, we first performed whole-genome sequencing of 50 individual F 2 plants derived from a cross of two of the best-studied inbred lab strains of Arabidopsis, Col-0 and Ler and used the haplotype reconstruction software TIGER 33 to determine a benchmark set of 400 COs across all 50 genomes (Fig. 1 ; Materials and Methods;Supplementary Tables 1 and 2).We then bulked the identical 50 F 2 plants by pooling individual leaves of comparable size and extracting high molecular weight (HMW) DNA 37 (Fig. 1). After size selection and quality control ( Supplementary Fig. 1), we loaded 0.25 ng DNA into a 10X Genomics Chromium Controller. The Chromium Controller encapsulates millions of gel beads as GEMs (Gel bead in EMulsion), each of which is loaded with a small number of long DNA molecules. These long molecules are fragmented and ligated with GEM-specific DNA barcodes to generate a 10X library suitable for Illumina sequencing. This library, which we called P50L25, was whole-genome sequenced with 84 million 151 bp-read pairs ( Supplementary Table 1).CO detection using linked-read sequencing 5 After aligning the reads against the Col-0 reference sequence 38 using longranger (v2.2.2, 10X Genomics), we recovered 3.6 million molecules (≥1 kb) including 116 million reads using a newly developed computational tool, DrLink, which can be downloaded at https://github.com/schneebergerlab/DrLink (Fig. 2a; Materials and Methods). On average, these molecules identified by DrLink were ~45 kb in size and were covered by ~21 read pairs, leading to a molecule base coverage of ~0.16x ( Fig. 2b-d; Supplementary Table 1). To avoid chimeras resulting from the accidental co-occurrence of two independent, but closely-spaced molecules with identical barcodes, we selected molecules which were small...

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“…At the genome-wide scale, maize COs form a particular U-shape pattern, with COs increasing strongly toward chromosome ends ( Anderson et al, 2003 ; Li et al, 2015 ; Rodgers-Melnick et al, 2015 ; Kianian et al, 2018 ). Maize chromosomes have rather big pericentromeric heterochromatin regions that cover more than half of them ( Baucom et al, 2009 ; Wei et al, 2009 ).…”

Section: Crossing Over and Polaritymentioning

confidence: 99%

“…Four studies based on next-generation sequencing have mapped recombination events in maize (Table 3 ). Three studies have been published ( Li et al, 2015 ; Rodgers-Melnick et al, 2015 ; Kianian et al, 2018 ). Data from the fourth study was reported in Alina Ott’s Ph.D. dissertation, and a manuscript is in preparation ( Ott, 2017 ).…”

Section: Crossing Over and Polaritymentioning

confidence: 99%

A Critical Assessment of 60 Years of Maize Intragenic Recombination

et al. 2018

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Until the mid-1950s, it was believed that genetic crossovers did not occur within genes. Crossovers occurred between genes, the “beads on a string” model. Then in 1956, Seymour Benzer published his classic paper describing crossing over within a gene, intragenic recombination. This result from a bacteriophage gene prompted Oliver Nelson to study intragenic recombination in the maize Waxy locus. His studies along with subsequent work by others working with maize and other organisms described the outcomes of intragenic recombination and provided some of the earliest evidence that genes, not intergenic regions, were recombination hotspots. High-throughput genotyping approaches have since replaced single gene intragenic studies for characterizing the outcomes of recombination. These large-scale studies confirm that genes, or more generally genic regions, are the most active recombinogenic regions, and suggested a pattern of crossovers similar to the budding yeast Saccharomyces cerevisiae. In S. cerevisiae recombination is initiated by double-strand breaks (DSBs) near transcription start sites (TSSs) of genes producing a polarity gradient where crossovers preferentially resolve at the 5′ end of genes. Intragenic studies in maize yielded less evidence for either polarity or for DSBs near TSSs initiating recombination and in certain respects resembled Schizosaccharomyces pombe or mouse. These different perspectives highlight the need to draw upon the strengths of different approaches and caution against relying on a single model system or approach for understanding recombination.

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High-resolution crossover mapping reveals similarities and differences of male and female recombination in maize

Cited by 77 publications

References 61 publications

Interacting Genomic Landscapes of REC8-Cohesin, Chromatin, and Meiotic Recombination in Arabidopsis

Interacting Genomic Landscapes of REC8-Cohesin, Chromatin, and Meiotic Recombination in Arabidopsis

Linked-read sequencing of gametes allows efficient genome-wide analysis of meiotic recombination

A Critical Assessment of 60 Years of Maize Intragenic Recombination

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