Genomic analysis of differentiation between soil types reveals candidate genes for local adaptation in Arabidopsis lyrata

Abstract

Serpentine soil, which is naturally high in heavy metal content and has low calcium to magnesium ratios, comprises a difficult environment for most plants. An impressive number of species are endemic to serpentine, and a wide range of non-endemic plant taxa have been shown to be locally adapted to these soils. Locating genomic polymorphisms which are differentiated between serpentine and non-serpentine populations would provide candidate loci for serpentine adaptation. We have used the Arabidopsis thaliana tiling array, which has 2.85 million probes throughout the genome, to measure genetic differentiation between populations of Arabidopsis lyrata growing on granitic soils and those growing on serpentinic soils. The significant overrepresentation of genes involved in ion transport and other functions provides a starting point for investigating the molecular basis of adaptation to soil ion content, water retention, and other ecologically and economically important variables. One gene in particular, calcium-exchanger 7, appears to be an excellent candidate gene for adaptation to low CaratioMg ratio in A. lyrata.

Figure 1. Map of collection locations.

Figure 2. Distributions of hybridization intensities.

Probes with a perfect match in the draft A. lyrata genome have the highest mean intensity (red), and the corresponding mismatches for these probes have the next highest mean (orange). For probes without a match in the draft genome, intensities are still higher at perfect match (grey) than mismatch (purple) probes. Though some of these probes might have a matching DNA sequence in our populations, but not in the reference genome, many of these probes are probably comparisons between a single mismatch and a double mismatch, yet are still providing valuable information. Note that extreme values are not shown for both axes.

Figure 3. Histogram of t-test p-values between collection localities (bin size = 0.001).

Three combinations of our four populations were tested: test 1 is the soil type comparison (blue line) = serp1+serp2 vs. granite1+granite2. For comparison, we also computed the other two combinations of the four localities: test 2 (red line) = serp1+granite1 vs. serp2+granite2; test 3 (green line) = serp2+granite1 vs. serp1+granite2).

Figure 4. Sequencing of cax7 revealed a small region of high differentiation between soil types: 200 bp sliding windows of FST are shown in black.

Serpentine populations have much less polymorphism in this region that granitic populations (200 bp sliding windows of heterozygosity are shown in blue for serpentine, red for granite). Vertical lines delineate a region of 70 bp where 8 of 23 amino acids are polymorphic in granitic populations and fixed in serpentine populations.