The genetic architecture ofArabidopsis thalianain response to native non-pathogenic leaf bacterial species revealed by GWA mapping in field conditions

Abstract

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.

The Genetic Architecture of Adaptation to Leaf and Root Bacterial Microbiota inArabidopsis thaliana

“…( A ) Fraction of candidate genes obtained from a GWAS performed on the leaf bacterial communities of 200 Swedish A. thaliana accessions grown in the native habitats of four natural populations of A. thaliana in Sweden ( Brachi et al 2022 ) overlapping with GEA candidate genes. ( B ) Fraction of candidate genes obtained from a GWAS performed on the vegetative growth response of 162 accessions from southwest of France to 13 bacterial strains belonging to 7 of the 12 most prevalent and abundant leaf nonpathogenic bacterial species isolated from the leaf compartment of A. thaliana in the same geographical region ( Ramírez-Sánchez, Duflos, et al 2022 ) overlapping with GEA candidate genes. Large red, purple, orange, and black dots correspond to the fraction of overlapped GWA candidate genes with P < 0.001, P < 0.01, P < 0.05, and P > 0.05, respectively.…”

“…The second GWAS was conducted in a common garden located southwest of France on 162 whole-genome sequenced accessions of A. thaliana originating from 54 out of the 141 natural populations used in our study ( Ramírez-Sánchez, Duflos, et al 2022 ). Those accessions were challenged in field conditions with 13 bacterial strains belonging to seven of the 12 most abundant and prevalent leaf OTUs across our natural populations in southwest of France and phenotyped for diverse vegetative growth-related traits such as the rosette surface area and relative growth rate ( Ramírez-Sánchez, Duflos, et al 2022 ).…”

“…The second GWAS was conducted in a common garden located southwest of France on 162 whole-genome sequenced accessions of A. thaliana originating from 54 out of the 141 natural populations used in our study ( Ramírez-Sánchez, Duflos, et al 2022 ). Those accessions were challenged in field conditions with 13 bacterial strains belonging to seven of the 12 most abundant and prevalent leaf OTUs across our natural populations in southwest of France and phenotyped for diverse vegetative growth-related traits such as the rosette surface area and relative growth rate ( Ramírez-Sánchez, Duflos, et al 2022 ). Whatever the “plant compartment × seasonal group” combination considered, a significant overlap was detected between the list of 1,962 unique candidate genes located in the vicinity of the top SNPs associated with the response of vegetative growth-related traits to the 13 bacterial strains and the list of candidate genes identified by GEA analysis in our study ( fig.…”

“…A similar approach was adopted with a list of 1,962 candidate genes identified in a GWAS performed on 162 whole-genome sequenced accessions of A. thaliana originating from 54 out of the 141 natural populations used in our study ( Ramírez-Sánchez, Duflos, et al 2022 ). The 162 accessions were phenotyped in a common garden for their response to 13 bacterial strains belonging to seven of the 12 most abundant and prevalent leaf OTUs across our natural populations in southwest of France ( Ramírez-Sánchez, Duflos, et al 2022 ).…”