Understanding the evolution of defense metabolites in Arabidopsis thaliana using genome-wide association mapping

With the improvement and decline in cost of high-throughput genotyping and phenotyping technologies, genome-wide association (GWA) studies are fast becoming a preferred approach for dissecting complex quantitative traits. Glucosinolate (GSL) secondary metabolites within Arabidopsis spp. can serve as a model system to understand the genomic architecture of quantitative traits. GSLs are key defenses against insects in the wild and the relatively large number of cloned quantitative trait locus (QTL) controlling GSL traits allows comparison of GWA to previous QTL analyses. To better understand the specieswide genomic architecture controlling plant-insect interactions and the relative strengths of GWA and QTL studies, we conducted a GWA mapping study using 96 A. thaliana accessions, 43 GSL phenotypes, and approximately 230,000 SNPs. Our GWA analysis identified the two major polymorphic loci controlling GSL variation (AOP and MAM) in natural populations within large blocks of positive associations encompassing dozens of genes. These blocks of positive associations showed extended linkage disequilibrium (LD) that we hypothesize to have arisen from balancing or fluctuating selective sweeps at both the AOP and MAM loci. These potential sweep blocks are likely linked with the formation of new defensive chemistries that alter plant fitness in natural environments. Interestingly, this GWA analysis did not identify the majority of previously identified QTL even though these polymorphisms were present in the GWA population. This may be partly explained by a nonrandom distribution of phenotypic variation across population subgroups that links population structure and GSL variation, suggesting that natural selection can hinder the detection of phenotype-genotype associations in natural populations.