Recent history of artificial outcrossing facilitates whole-genome association mapping in elite inbred crop varieties

Abstract

Genomewide association studies depend on the extent of linkage disequilibrium (LD), the number and distribution of markers, and the underlying structure in populations under study. Outbreeding species generally exhibit limited LD, and consequently, a very large number of markers are required for effective whole-genome association genetic scans. In contrast, several of the world's major food crops are self-fertilizing inbreeding species with narrow genetic bases and theoretically extensive LD. Together these are predicted to result in a combination of low resolution and a high frequency of spurious associations in LD-based studies. However, inbred elite plant varieties represent a unique human-induced pseudo-outbreeding population that has been subjected to strong selection for advantageous alleles. By assaying 1,524 genomewide SNPs we demonstrate that, after accounting for population substructure, the level of LD exhibited in elite northwest European barley, a typical inbred cereal crop, can be effectively exploited to map traits by using whole-genome association scans with several hundred to thousands of biallelic SNPs.

Fig. 1.

PCOs of the SNP genotype data of 102 barley varieties. The full genotype data set is partitioned into foreign material (triangles), European two-row spring (squares), and winter (diamonds) varieties. The complete list of varieties is available in Table 1.

Fig. 2.

Diversity and LD in barley genome. (a) Distribution of PIC along the linkage map. PIC was averaged across a window of 25 adjacent loci with a step of one and plotted against the linkage map. Data points are colored by group of germplasm. (b) Decay of LD (r²) as a function of genetic distance (cM) between pairs of loci on individual chromosomes in European two-row spring barley. Loci with MAF < 0.1 were excluded from analysis. Only LD values with P < 0.001 are shown.

Fig. 3.

LD matrix of European two-row spring barley. Data points are colored by magnitude of LD (r²). LD is plotted along the cumulative linkage map of the barley genome with chromosome starting at multiples of 200 cM. (Inset) Variation in LD along the barley chromosome 3H, which correlates with the recombination (genetic distance) and physical map of centromeric region of 3H (23). BIN 6 of the linkage map encompasses ≈600 Mb of chromosome 3H including the centromere (CEN) (23, 24), and r² exhibits strong LD across the whole region.