Recombination in maize is stable, predictable, and associated with genetic load: a joint study of the US and Chinese maize NAM populations

Authors: RODGERS-MELNICK, ELI - Cornell University; Bradbury, Peter; ELSHIRE, ROBERT - Agresearch; GLAUBITZ, JEFFREY - Cornell University; ARCHARYA, CHARLOTTE - Cornell University; MITCHELL, SHARON - Cornell University; LI, CHUNHUI - Chinese Academy Of Agricultural Sciences; LI, YONGXIANG - Chinese Academy Of Agriculture & Mechanical Sciences; Buckler, Edward - Ed

Submitted to: Proceedings of the National Academy of Sciences (PNAS)
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 2/6/2015
Publication Date: 3/24/2015
Publication URL: http://www.pnas.org/content/112/12/3823.abstract
Citation: Rodgers-Melnick, E., Bradbury, P., Elshire, R.J., Glaubitz, J.C., Archarya, C.B., Mitchell, S.E., Li, C., Li, Y., Buckler IV, E.S. 2015. Recombination in maize is stable, predictable, and associated with genetic load: a joint study of the US and Chinese maize NAM populations. Proceedings of the National Academy of Sciences. 112(12):3823.

Interpretive Summary: This is a study of genome-wide patterns of meiotic recombination in two distinct maize populations used by researchers internationally to map diverse quantitative traits. We use a novel application of genotyping-by-sequencing (GBS) technology to define the locations of 136,000 recombination breakpoints. Using this dataset, we observe that recombination is surprisingly stable across diverse lines and it is predictable from genomic features of maize reference genome, despite extensive structural variation among founder lines. There is evidence for several previous uncharacterized large inversions that completely suppress recombination in several families and several hundred newly identified recombination hotspots across the genome, associated with DNA hypomethylation, increased GC content, and fewer segregating deleterious alleles. This is the first direct evidence of a genome-wide inverse relationship between the recombination rate and the genetic load. We show that despite the tremendous diversity among NAM founders within and between these two families, recombination is remarkably consistent and associated with a number of genomic features on a fine scale, including probable deleterious variation.

Technical 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 United States and Chinese maize nested association mapping populations. We find that the pattern of crossovers 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 1kb to 30kb. We find these hotspots to be historically stable and, when compared to similar regions with low recombination, to have strongly differentiated patterns of DNA methylation and GC content. Using Genomic Evolutionary Rate Profiling (GERP) to identify putative deleterious polymorphsms, we also find evidence for reduced genetic load in hotpot regions, a phenomenon that may have considerable practical importance for breeding programs worldwide.