Characterization of recombination features and the genetic basis in multiple cattle breeds

Abstract

BackgroundCrossover generated by meiotic recombination is a fundamental event that facilitates meiosis and sexual reproduction. Comparative studies have shown wide variation in recombination rate among species, but the characterization of recombination features between cattle breeds has not yet been performed. Cattle populations in North America count millions, and the dairy industry has genotyped millions of individuals with pedigree information that provide a unique opportunity to study breed-level variations in recombination.ResultsBased on large pedigrees of Jersey, Ayrshire and Brown Swiss cattle with genotype data, we identified over 3.4 million maternal and paternal crossover events from 161,309 three-generation families. We constructed six breed- and sex-specific genome-wide recombination maps using 58,982 autosomal SNPs for two sexes in the three dairy cattle breeds. A comparative analysis of the six recombination maps revealed similar global recombination patterns between cattle breeds but with significant differences between sexes. We confirmed that male recombination map is 10% longer than the female map in all three cattle breeds, consistent with previously reported results in Holstein cattle. When comparing recombination hotspot regions between cattle breeds, we found that 30% and 10% of the hotspots were shared between breeds in males and females, respectively, with each breed exhibiting some breed-specific hotspots. Finally, our multiple-breed GWAS found that SNPs in eight loci affected recombination rate and that the PRDM9 gene associated with hotspot usage in multiple cattle breeds, indicating a shared genetic basis for recombination across dairy cattle breeds.ConclusionsCollectively, our results generated breed- and sex-specific recombination maps for multiple cattle breeds, provided a comprehensive characterization and comparison of recombination patterns between breeds, and expanded our understanding of the breed-level variations in recombination features within an important livestock species.Electronic supplementary materialThe online version of this article (10.1186/s12864-018-4705-y) contains supplementary material, which is available to authorized users.

Chromosome-wide distribution and characterization of intersubspecific meiotic noncrossovers in mice

“…The COs were highly abundant in the subtelomeric regions and at the 2 nd decile of the chromosomal lengths (Figure 5a) in agreement with the non-uniform spatial distribution previously described in male meiosis of mice 36,37 as well as of humans and other species 38–40 . The spatial chromosome-wide distribution of NCOs was significantly different from the CO distribution (P ≤ 0.0109, see Materials and Methods).…”

Molecular evolution of the meiotic recombination pathway in mammals

“…Five of the genes that exhibit signatures of positive selection across the mammalian phylogeny have been associated with interindividual variation in recombination rate within species: RAD21L (Kong et al 2014), REC8 (Sandor et al 2012;Johnston et al 2016Johnston et al , 2018, MSH4 (Kong et al 2014;Ma et al 2015;Kadri et al 2016;Shen et al 2018), RNF212 (Kong et al 2008;Chowdhury et al 2009;Fledel-Alon et al 2011;Sandor et al 2012;Johnston et al 2016;Kadri et al 2016;Petit et al 2017), and TEX11 (Murdoch et al 2010). However, as a group, recombination genes previously associated with intraspecific variation in the genome-wide recombination rate evolve at similar rates to recombination genes lacking such an association.…”

“…; Shen et al. ). Third, laboratory mice have proven instrumental in the identification and functional characterization of recombination genes (de Vries et al.…”

“…Genome-wide association studies are beginning to reveal the genetic basis of variation in recombination rate within species. Individual recombination rates have been associated with variants in specific genes in populations of Drosophila melanogaster (Hunter et al 2016), humans (Kong et al 2008(Kong et al , 2014Chowdhury et al 2009;Fledel-Alon et al 2011), domesticated cattle (Sandor et al 2012;Ma et al 2015;Kadri et al 2016;Shen et al 2018), domesticated sheep (Petit et al 2017), Soay sheep (Johnston et al 2016), and red deer (Johnston et al 2018). Variants in several of these genes correlate with recombination rate in multiple species, including RNF212 (Kong et al 2008;Chowdhury et al 2009;Fledel-Alon et al 2011;Sandor et al 2012;Johnston et al 2016;Kadri et al 2016;Petit et al 2017), RNF212B (Johnston et al 2016(Johnston et al , 2018Kadri et al 2016), REC8 (Sandor et al 2012;Johnston et al 2016Johnston et al , 2018, HEI10/CCNB1IP1 (Kong et al 2014;Petit et al 2017), MSH4 (Kong et al 2014;Ma et al 2015;Kadri et al 2016;Shen et al 2018), CPLX1 (Kong et al 2014;Ma et al 2015;Johnston et al 2016;Shen et al 2018) and PRDM9 (Fledel-Alon et al 2011;Sandor et al 2012;…”

“…First, the evolution of recombination rate has been measured along the mammalian phylogeny (Dumont and Payseur 2008;Segura et al 2013). Second, recombination rate variation has been associated with specific genes in mammalian populations (Kong et al 2008(Kong et al , 2014Chowdhury et al 2009;Sandor et al 2012;Ma et al 2015;Johnston et al 2016Johnston et al , 2018Kadri et al 2016;Petit et al 2017;Shen et al 2018). Third, laboratory mice have proven instrumental in the identification and functional characterization of recombination genes (de Vries et al 1999;Baudat et al 2000;Romanienko and Camerini-Otero 2000;Yang et al 2006;Ward et al 2007;Schramm et al 2011;Bisig et al 2012;Bolcun-Filas and Schimenti 2012;La Salle et al 2012;Kumar et al 2015;Finsterbusch et al 2016;Stanzione et al 2016).…”