Plant genetic and root-associated microbial diversity modulate Lactuca sativa responsiveness to a soil inoculum under phosphate deficiency.

Microbial-based approaches offer a promising strategy to decrease the use of chemical fertilizers in agriculture. Among them, arbuscular mycorrhizal fungi (AMF), which extend root surface area and enhance phosphate uptake, and phosphate-solubilizing bacteria (PSB) are particularly relevant. However, their effectiveness depends strongly on plant genetic diversity. To identify genetic markers underlying plant responses to beneficial soil microbes, we studied a panel of 128 fully sequenced Lactuca sativa varieties under controlled phosphate-starvation conditions and treated with AMF and PSB. Lettuce genetic variation showed a strong effect on physiological and morphological responses to microbial inoculation. Genome-wide association studies identified specific genomic regions associated with changes in leaf phosphate content and shoot biomass following treatment. Beyond genetic factors, we observed shifts in fungal β-diversity and increased bacterial α-diversity associated with phenotypic variation. We also identified 44 amplicon sequence variants associated with agriculturally relevant traits. Among these, six bacterial strains were experimentally validated through in vitro and pot experiments for their effects on leaf phosphate concentration and shoot biomass. Overall, we highlighted key genetic, microbial, and physiological mechanisms that may enhance microbial treatments for improved plant phosphate management in lettuce.