Deep genotyping reveals specific adaptation footprints of conventional and organic farming in barley populations—an evolutionary plant breeding approach

Sustainable food production for a growing world population will pose a central challenge in the coming decades. Organic farming is among the feasible approaches to achieving this goal if the yield gap to conventional farming can be decreased. However, uncertainties exist to which extend—and for which phenotypes in particular—organic and conventional agro-ecosystems require differentiated breeding strategies. To answer this question, a heterogeneous spring barley population was established between a wild barley and an elite cultivar to examine this question. This initial population was divided into two sets and sown one in organic and the other in conventional managed agro-ecosystems, without any artificial selection for two decades. A fraction of seeds harvested each year was sown the following year. Various generations, up to the 23th were whole-genome pool-sequenced to identify adaptation patterns towards ecosystem and climate conditions in the allele frequency shifts. Additionally, a meta-data analysis was conducted to link genomic regions’ increased fitness to agronomically related traits. This long-term experiment highlights for the first time that allele frequency pattern difference between the conventional and organic populations grew with subsequent generations. Further, the organic-adapted population showed a higher genetic heterogeneity. The data indicate that adaptations towards new environments happen in few generations. Drastic interannual changes in climate are manifested in significant allele frequency changes. Particular wild form alleles were positively selected in both environments. Clustering these revealed an increased fitness associated with biotic stress resistance, yield physiology, and yield components in both systems. Additionally, the introduced wild alleles showed increased fitness related to root morphology, developmental processes, and abiotic stress responses in the organic agro-ecosystem. Concluding the genetic analysis, we demonstrate that breeding of organically adapted varieties should be conducted in an organically managed agro-ecosystem, focusing on root-related traits, to close the yield gap towards conventional farming.