A footptrint of plant eco-geographic adaptation on the composition of the barley rhizosphere bacterial microbiota

Background: The microbiota thriving in the rhizosphere, the thin layer of soil surrounding plant roots, plays a critical role in plant's adaptation to the environment. Domestication and breeding selection have progressively differentiated the microbiota of modern crops from the ones of their wild ancestors. However, the impact of ecogeographical constraints faced by domesticated plants and crop wild relatives on recruitment and maintenance of the rhizosphere microbiota remains to be fully elucidated. Methods: We grew twenty wild barley (Hordeum vulgare ssp. spontaneum) genotypes representing five distinct ecogeographic areas in the Israeli region, one of the sites of barley domestication, alongside four 'Elite' varieties (H. vulgare ssp. vulgare) in a reference agricultural soil under greenhouse conditions. At early stem elongation, rhizosphere specimens were collected, and stem and root dry weight measured. In parallel, we generated high-resolution 16S rRNA gene profiles of the rhizosphere and unplanted soil samples. Ecological indices and multivariate statistical analyses allowed us to identify 'host signatures' on the composition of the rhizosphere microbiota. Finally, we capitalise on single nucleotide polymporsphisms (SNPs) of the barley genome to correlate microbiota diversity and host genetic diversity. Results: Elite material outperformed the wild genotypes in aboveground biomass while, almost invariably, wild genotypes allocated more resources to belowground growth. These growth differential responses were associated to a differential microbial recruitment in the rhizosphere. The selective enrichment of individual bacterial members of microbiota mirrored the distinct ecogeographical constraints faced by the wild and domesticated plants. Unexpectedly, Elite varieties exerted a stronger genotype effect on the rhizosphere microbiota when compared with wild barley genotypes adapted to desert environments and this effect had a bias for Actinobacteria. Finally, in wild barley genotypes, we discovered a limited, but significant, correlation between microbiota diversity and host genomic diversity. Conclusions: Our results revealed a footprint of host's adaptation the environment on the assembly of the bacteria thriving at the root-soil interface. This recruitment cue layered atop of the distinct evolutionary trajectories of wild and domesticated plants and, at least in part, is encoded by the barley genome. This knowledge will be critical to further dissect microbiota contribution to plant's adaptation to the environment and to devise strategies for climate-smart agriculture.