Natural variation in root suberization is associated with local environment in Arabidopsis thaliana

Genetic signature of climate adaptation has been widely recognized across the genome of many organisms; however, the eco-physiological basis for linking genomic polymorphisms with local adaptations remains largely unexplored. Using a panel of 218 world-wide Arabidopsis accessions, we characterized the natural variation in root suberization by quantifying 16 suberin monomers. We explored the associations between suberization traits and 126 climate variables. We conducted genome-wide association analysis and integrated previous genotype-environment association (GEA) to identify the genetic bases underlying suberization variation and their involvements in climate adaptation. Root suberin content displays extensive variation across Arabidopsis populations and significantly correlates with local moisture gradients and soil characteristics. Specifically, enhanced suberization is associated with drier environments, higher soil cation-exchange capacity, and lower soil pH; higher proportional levels of very-long-chain suberin is negatively correlated with moisture availability, lower soil gravel content, and higher soil silt fraction. We identified 94 putative causal loci and experimentally proved that GPAT6 is involved in C16 suberin biosynthesis. Highly significant associations between the putative genes and environmental variables were observed. Roots appear highly responsive to environmental heterogeneity via regulation of suberization, especially the suberin composition. The patterns of suberization-environment correlation and the suberin-related GEA fit the expectations of local adaptation for the polygenic suberization trait.