The genetic architecture of Arabidopsis thaliana in response to native non-pathogenic leaf bacterial species revealed by GWA mapping in field conditions

Non-pathogenic bacteria can largely contribute to plant health by mobilizing and supplying nutrients and by providing protection against pathogens and resistance to abiotic stresses. Yet, the number of GWAS reporting the genetic architecture of the response to individual members of the beneficial microbiota remains limited. In this study, we established a GWAS under field conditions to estimate the level of genetic variation and the underlying genetic architecture, among 162 accessions of Arabidopsis thaliana originating from 54 natural populations located south-west of France, in response to 13 strains of seven of the most abundant and prevalent non-pathogenic bacterial species isolated from the leaf compartment of A. thaliana in the same geographical region. Using a high-throughput phenotyping methodology to score vegetative growth-related traits, extensive genetic variation was detected within our local set of A. thaliana accessions in response to these leaf bacteria, both at the species and strain levels. The presence of crossing reaction norms among strains indicates that declaring a strain as a plant-growth promoting bacterium is highly dependent on the host genotype tested. In line with the strong genotype-by-genotype interactions, we detected a complex and highly flexible genetic architecture between the 13 strains. Finally, the candidate genes underlying the QTLs revealed a significant enrichment in several biological pathways, including cell, secondary metabolism, signalling and transport. Altogether, plant innate immunity appears as a significant source of natural genetic variation in plant-microbiota interactions and opens new avenues for better understanding the ecologically relevant molecular dialog during plant-microbiota interactions.