Extreme population-dependent linkage disequilibrium detected in an inbreeding plant species, Hordeum vulgare

Abstract

In human genetics a detailed knowledge of linkage disequilibrium (LD) is considered a prerequisite for effective population-based, high-resolution gene mapping and cloning. Similar opportunities exist for plants; however, differences in breeding system and population history need to be considered. Here we report a detailed study of localized LD in different populations of an inbreeding crop species. We measured LD between and within four gene loci within the region surrounding the hardness locus in three different gene pools of barley (Hordeum vulgare). We demonstrate that LD extends to at least 212 kb in elite barley cultivars but is rapidly eroded in related inbreeding ancestral populations. Our results indicate that haplotype-based sequence analysis in multiple populations will provide new opportunities to adjust the resolution of association studies in inbreeding crop species.

Figure 1.

Plots of LD (r²) as a function of distance (in base pairs) between informative (f > 0.1) polymorphic sites in four different gene regions and three different gene pools.

Figure 2.

Representation of the intergenic space between 12 genes located in a contiguous 303-kb region surrounding the Ha locus. Median LD values across these regions for the cultivated sample are indicated. Coding sequence is represented by colored boxes and arrows designate gene orientation. Location of repetitive sequence is indicated by shaded boxes. Mini-inverted repetitive element insertions are represented by a vertical bar.

Figure 3.

Plots of LD (r²) as a function of distance (in kilobases) for the (a) cultivated, (b) landrace, and (c) wild (H. spontaneum) samples.

Figure 4.

Matrix of pairwise association between sites for the (a) cultivated, (b) landrace, and (c) wild (H. spontaneum) samples. Above the diagonal are r² values; below the diagonal are P-values.

Figure 5.

Plots of the median association value for each group of pairwise comparisons against the corresponding median distance. Groups are: within-gene comparisons (1–4 kb), comparisons between markers within hina and GSP (28–32 kb), comparisons between markers within hinb and hina (77–83 kb), comparisons between markers within GSP and PG2 (98–101 kb), comparisons between markers within hinb and GSP (107–113 kb), comparisons between markers within hina and PG2 (128–131 kb), and comparisons between markers within hinb and PG2 (207–212 kb).

Figure 6.

Distribution of −log P-values of pairwise association.

Figure 7.

Plots indicating pairs of sites that demonstrate deviation from the assumption of a constant recombination rate across the region for the (a) cultivated, (b) landrace, and (c) wild (H. spontaneum) samples. Above the diagonal, marginal likelihood ratios >2.0 are blue and red for pairs with more and less LD than expected, respectively. Below the diagonal are the minimum number of detectable recombination events normalized by physical distance between pairs of sites. Recombination rates of a magnitude of 10e⁻⁴ are indicated by blue as recombination rates increase. Recombination rates of a magnitude of 10e⁻³ are indicated by light yellow (1 × 10e⁻³), yellow (2 × 10e⁻³), gold (3 × 10e⁻³), light orange (4 × 10e⁻³), orange (5 × 10e⁻³), and red (6 × 10e⁻³). Recombination rates of a magnitude >7.0 × 10e⁻³ are purple. Gray boxes indicate the absence of detectable recombination.