Recombination in diverse maize is stable, predictable, and associated with genetic load

Abstract

Among the fundamental evolutionary forces, recombination arguably has the largest impact on the practical work of plant breeders. Varying over 1,000-fold across the maize genome, the local meiotic recombination rate limits the resolving power of quantitative trait mapping and the precision of favorable allele introgression. The consequences of low recombination also theoretically extend to the species-wide scale by decreasing the power of selection relative to genetic drift, and thereby hindering the purging of deleterious mutations. In this study, we used genotyping-by-sequencing (GBS) to identify 136,000 recombination breakpoints at high resolution within US and Chinese maize nested association mapping populations. We find that the pattern of cross-overs is highly predictable on the broad scale, following the distribution of gene density and CpG methylation. Several large inversions also suppress recombination in distinct regions of several families. We also identify recombination hotspots ranging in size from 1 kb to 30 kb. We find these hotspots to be historically stable and, compared with similar regions with low recombination, to have strongly differentiated patterns of DNA methylation and GC content. We also provide evidence for the historical action of GC-biased gene conversion in recombination hotspots. Finally, using genomic evolutionary rate profiling (GERP) to identify putative deleterious polymorphisms, we find evidence for reduced genetic load in hotspot regions, a phenomenon that may have considerable practical importance for breeding programs worldwide.recombination | maize | genetic load | deleterious mutations | methylation A lthough the selective pressures contributing to its origin and persistence continue to be debated, recombination is widely recognized for its roles in promoting the diversity necessary to respond to continually shifting environments, in addition to preventing the build-up of genetic load by decoupling linked deleterious and beneficial variants (1-3). In practice, increased local recombination enhances breeders' abilities to map quantitative traits and introduce favorable alleles into breeding lines.Recombination's importance has spurred interest in the causes and predictability of the local recombination frequency, which is usually characterized by hotspots with cross-over rates of up to several hundred-fold the genomic background (4-6). The predictability across diverse sources of germplasm is particularly salient in maize, a species with many large structural variants in which the average genetic distance between two inbred lines exceeds that between humans and chimpanzees (7). Moreover, elevated residual heterozygosity within low-recombining regions of maize recombinant inbred lines (RILs) suggests that heterosis in maize results from complementation of alternative deleterious alleles within these regions by dominant beneficial alleles segregating in repulsion (8-10). These low-recombination regions include the large [∼100 megabases (Mb)] pericentromeres harbored by all...

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

“…New wheat-genomic tools allow more resolute analysis of recombination pattern Whole-genome, fine-scale recombination studies in plants have only been conducted in species for which the genome sequence was available (Wu et al 2003;Liu et al 2009;Paape et al 2012;Rodgers-Melnick et al 2015;Shilo et al 2015). However, this mainly restricted such analyses to species with small and compact genomes with low rates of TEs.…”

“…In all eukaryotes studied so far, the distribution of COs is not homogeneous along the chromosomes (Lukaszewski and Curtis 1993;Tenaillon et al 2002;Saintenac et al 2009;Mayer et al 2012;Pan et al 2012;Choulet et al 2014;Choi and Henderson 2015;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).…”

“…Repeated sequences and recombination rate are correlated positively in Caenorhabditis elegans (Duret et al 2000) and negatively in the Drosophila melanogaster genome (Rizzon et al 2002). Even in the same species, in maize, insertion sites of the Mu transposon concentrate in the same regions as meiotic recombination (Liu et al 2009), while fine-scale studies at the bronze locus revealed a reduction of recombination in regions containing TEs, suggesting that retrotransposons are probably inert with regard to recombination because of methylation and the likely associated condensed chromatin (Dooner and Martínez-Férez 1997;He and Dooner 2009;Rodgers-Melnick et al 2015). In Arabidopsis, DNA methylation can silence CO hotspots and plays an essential role in forming domains of meiotic recombination along chromosomes (Yelina et al 2015).…”

Cassava haplotype map highlights fixation of deleterious mutations during clonal propagation

“…8). The evolutionarily constrained genome of cassava (104 Mb) was comparable to that of maize (111 Mb) 17 in size, but was smaller than that of humans (214 Mb) 16 and larger than that of Drosophila (88 Mb) 18 . GERP profiling also identified a remarkably asymmetric distribution of constrained sequence at the chromosome scale (Supplementary Fig.…”

“…3b and Supplementary Fig. 11) rather than being concentrated in low-recombination regions, as seen in humans 23 , fruit flies 24 , and maize 17 . Thus, recombination, which is presumably rare in a clonally propagated crop, does not effectively purge the mutation burden in cassava.…”