Multiple loci contribute to genome-wide recombination levels in male mice

Murdoch, Brenda M.; Owen, Nichole; Shirley, Sofia; Crumb, Sara; Broman, Karl W.; Hassold, Terry

doi:10.1007/s00335-010-9303-5

Cited by 29 publications

(54 citation statements)

References 31 publications

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“…There are striking differences in global MLH1 frequency between inbred house mouse strains (Koehler et al 2002; Dumont and Payseur 2011a), and prior studies have established that this divergence carries a clear genetic basis (Murdoch et al 2010; Dumont and Payseur 2011b; Liu et al 2014). Ideally, to distinguish between the one-crossover-per-chromosome and one-crossover-per-chromosome-arm alternatives, one would rely on a nested series of Rb rearrangements on a common genetic background.…”

Section: Resultsmentioning

confidence: 99%

“…Association analyses (Kong et al 2004, 2008; Chowdhury et al 2009; Hunter et al 2016), genetic mapping in pedigrees and controlled crosses (Thomsen et al 2001; Murdoch et al 2010; Parvanov et al 2010; Dumont and Payseur 2011b), and candidate gene-driven approaches (Baudat et al 2010; Myers et al 2010) have recently led to the discovery of numerous recombination-modifying loci in diverse species, including the identification of individual genes. Multiple environmental variables, such as exposure to xenobiotic compounds (Susiarjo et al 2007; Vrooman et al 2015) and various measures of stress (Plough 1917; Parsons 1988; Singh et al 2015), have also been demonstrated to influence recombination rates.…”

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confidence: 99%

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Variation and Evolution of the Meiotic Requirement for Crossing Over in Mammals

Dumont

2017

Genetics

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The segregation of homologous chromosomes at the first meiotic division is dependent on the presence of at least one well-positioned crossover per chromosome. In some mammalian species, however, the genomic distribution of crossovers is consistent with a more stringent baseline requirement of one crossover per chromosome arm. Given that the meiotic requirement for crossing over defines the minimum frequency of recombination necessary for the production of viable gametes, determining the chromosomal scale of this constraint is essential for defining crossover profiles predisposed to aneuploidy and understanding the parameters that shape patterns of recombination rate evolution across species. Here, I use cytogenetic methods for in situ imaging of crossovers in karyotypically diverse house mice (Mus musculus domesticus) and voles (genus Microtus) to test how chromosome number and configuration constrain the distribution of crossovers in a genome. I show that the global distribution of crossovers in house mice is thresholded by a minimum of one crossover per chromosome arm, whereas the crossover landscape in voles is defined by a more relaxed requirement of one crossover per chromosome. I extend these findings in an evolutionary metaanalysis of published recombination and karyotype data for 112 mammalian species and demonstrate that the physical scale of the genomic crossover distribution has undergone multiple independent shifts from one crossover per chromosome arm to one per chromosome during mammalian evolution. Together, these results indicate that the chromosomal scale constraint on crossover rates is itself a trait that evolves among species, a finding that casts light on an important source of crossover rate variation in mammals.

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Section: Resultsmentioning

confidence: 99%

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confidence: 99%

Variation and Evolution of the Meiotic Requirement for Crossing Over in Mammals

Dumont

2017

Genetics

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“…Although differences in total number of CO per spermatocyte have been observed in strains of mice, this study is one of the first to evaluate different breeds of sheep [Murdoch et al, 2010;Fröhlich et al, 2015;. We hypothesized that the number of COs per spermatocyte not only differs within a breed, but also differs across breeds of sheep.…”

Section: Discussionmentioning

confidence: 97%

“…Although the total number of COs that occur in a meiotic cell is known to differ between strains of mice, this is only beginning to be evaluated in livestock species [Sandor et al, 2012;Murdoch et al, 2010;Poissant et al, 2010;Vozdova et al, 2013;Fröhlich et al, 2015;Ma et al, 2015;Johnston et al, 2016;Kadri et al, 2016;Sebestova et al, 2016]. In this study, the numbers of COs were quantified and their locations on the SC characterized in males from different breeds of sheep.…”

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confidence: 99%

Meiotic Recombination Differences in Rams from Three Breeds of Sheep in the US

Davenport

McKay²,

Fahey

et al. 2018

Cytogenet Genome Res

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Meiotic recombination is an important contributor to genetic variation and ensures proper chromosome segregation during gametogenesis. Previous studies suggest that at least 1 crossover (CO) per chromosome arm is important to avoid mis-segregation. While the total number of COs per spermatocyte is known to differ in mice, this is only beginning to be evaluated in sheep. This study used a cytogenetic approach to quantify and compare the number of COs per spermatocyte in rams from 3 breeds of sheep: Suffolk, Icelandic, and Targhee. In total, 2,758 spermatocytes and over 170,000 COs were examined. Suffolk rams exhibited the lowest mean number of COs (61.1 ± 0.15) compared to Icelandic (63.5 ± 0.27) and Targhee (65.9 ± 0.26) rams. Significant differences in the number of COs per spermatocyte were observed between Suffolk, Icelandic, and Targhee breeds as well as within each breed. Additionally, the number and location of COs were characterized for homologous chromosomes in a subset of spermatocytes for each ram. A positive correlation was identified between the number of COs and the length of the homologous chromosome pair. Suffolk and Icelandic rams exhibited up to 7 COs per chromosome, while Targhee rams exhibited up to 9. Further, distinct CO location preferences on homologous chromosome pairs with 1, 2, 3, and 4 COs were observed in all 3 breeds. These data in sheep will aid in elucidating the mechanism of mammalian meiotic recombination, an important contributor to genetic diversity.

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“…In particular, crossover frequency in male mice is known to vary across different inbred strains (Koehler et al 2002) and these differences have been exploited to map genetic loci affecting recombination rates in F 2 intercrosses (Murdoch et al 2010; Dumont and Payseur 2011). Finally, mutations at several genes are known to lead to pathological changes in recombination (Niedzwiedz et al 2004; Liebe et al 2006).…”

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confidence: 99%

High-Resolution Sex-Specific Linkage Maps of the Mouse Reveal Polarized Distribution of Crossovers in Male Germline

et al. 2014

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Since the publication of the first comprehensive linkage map for the laboratory mouse, the architecture of recombination as a basic biological process has become amenable to investigation in mammalian model organisms. Here we take advantage of high-density genotyping and the unique pedigree structure of the incipient Collaborative Cross to investigate the roles of sex and genetic background in mammalian recombination. Our results confirm the observation that map length is longer when measured through female meiosis than through male meiosis, but we find that this difference is modified by genotype at loci on both the X chromosome and the autosomes. In addition, we report a striking concentration of crossovers in the distal ends of autosomes in male meiosis that is absent in female meiosis. The presence of this pattern in both single- and double-recombinant chromosomes, combined with the absence of a corresponding asymmetry in the distribution of double-strand breaks, indicates a regulated sequence of events specific to male meiosis that is anchored by chromosome ends. This pattern is consistent with the timing of chromosome pairing and evolutionary constraints on male recombination. Finally, we identify large regions of reduced crossover frequency that together encompass 5% of the genome. Many of these “cold regions” are enriched for segmental duplications, suggesting an inverse local correlation between recombination rate and mutation rate for large copy number variants.

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Multiple loci contribute to genome-wide recombination levels in male mice

Cited by 29 publications

References 31 publications

Variation and Evolution of the Meiotic Requirement for Crossing Over in Mammals

Variation and Evolution of the Meiotic Requirement for Crossing Over in Mammals

Meiotic Recombination Differences in Rams from Three Breeds of Sheep in the US

High-Resolution Sex-Specific Linkage Maps of the Mouse Reveal Polarized Distribution of Crossovers in Male Germline

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