Genetic control of pod dehiscence in domesticated common bean: Associations with range expansion and local aridity conditions

SignificancePlant domestication has radically modified crop morphology and development. Nevertheless, many crops continue to display some atavistic characteristics that were advantageous to their wild ancestors, such as pod dehiscence (PD). Domesticated common bean (Phaseolus vulgaris), a nutritional staple for millions of people globally, shows considerable variation in PD. Here, we identified multiple genetic regions controlling PD in common bean grown throughout geographically distributed lineages. For example, on chromosome Pv03, PvPdh1 shows a single base-pair substitution that is strongly associated with decreased PD and expansion of the crop into northern Mexico, where the arid conditions promote PD. The environmental dependency and genetic redundancy explain the maintenance of atavistic traits under domestication. Knowledge of PD genetics will assist in developing aridity-adapted varieties.AbstractA reduction in pod dehiscence (PD) is an important part of the domestication syndrome in legumes, including common bean. Despite this, many modern dry bean varieties continue to suffer yield reductions due to dehiscence, an atavistic trait, which is particularly problematic in hot, dry environments. To date, the genetic control of this important trait has been only partially resolved. Using QTL mapping and GWAS, we identified major PD QTLs in dry beans on chromosomes Pv03, Pv05, Pv08, and Pv09, three of which had not been described previously. We further determined that the QTL on chromosome Pv03, which is strongly associated with PD in Middle American beans, includes a dirigent-like candidate gene orthologous to Pod dehiscence 1 (Pdh1) of soybean. In this gene, we identified a substitution in a highly conserved amino acid that is unique to PD-resistant varieties. This allele is associated with the expansion of Middle American domesticated common beans into the arid environments of northern Mexico, resulting in a high allelic frequency in the domesticated ecogeographic race Durango. The polygenic redundancy and environmental dependency of PD resistance may explain the maintenance of this atavistic characteristic after domestication. Use of these alleles in breeding will reduce yield losses in arid growing conditions, which are predicted to become more widespread in coming decades.