Genotyping by Sequencing and Genome–Environment Associations in Wild Common Bean Predict Widespread Divergent Adaptation to Drought

Drought will reduce global crop production by >10% in 2050 substantially worsening global malnutrition. Breeding for resistance to drought will require accessing crop genetic diversity found in the wild accessions from the driest high stress ecosystems. Genome-environment associations (GEA) in crop wild relatives reveal natural adaptation, and therefore can be used to identify adaptive variation. We explored this approach in the food crop Phaseolus vulgaris L., characterizing 86 geo-referenced wild accessions using genotyping by sequencing (GBS) to discover single nucleotide polymorphisms (SNPs). The wild beans represented Mesoamerica, Guatemala, Colombia, Ecuador/Northern Peru and Andean groupings. We found high polymorphism with a total of 22,845 SNPs across the 86 accessions that confirmed genetic relationships for the groups. As a second objective, we quantified allelic associations with a bioclimatic-based drought index using 10 different statistical models that accounted for population structure. Based on the optimum model, 115 SNPs in 90 regions, widespread in all 11 common bean chromosomes, were associated with the bioclimatic-based drought index. A gene coding for an ankyrin repeat-containing protein and a phototropic-responsive NPH3 gene were identified as potential candidates. Genomic windows of 1 Mb containing associated SNPs had more positive Tajima's D scores than windows without associated markers. This indicates that adaptation to drought, as estimated by bioclimatic variables, has been under natural divergent selection, suggesting that drought tolerance may be favorable under dry conditions but harmful in humid conditions. Our work exemplifies that genomic signatures of adaptation are useful for germplasm characterization, potentially enhancing future marker-assisted selection and crop improvement.