Arabidopsis root defense barriers support beneficial interactions with rhizobacterium Pseudomonas simiae WCS417

Plant roots interact with pathogenic and beneficial microbes in the soil. While root defense barriers block pathogens, their roles in facilitating beneficial plant-microbe associations are understudied. Here, we examined the impact of specific root defense barriers on the well-known beneficial association between Arabidopsis thaliana and the plant growth-promoting rhizobacterium Pseudomonas simiae WCS417. Using 15 Arabidopsis mutants with alterations in structural (cutin, suberin, callose, and lignin) and chemical (camalexin and glucosinolates) defense barriers, we demonstrate that some barriers impact WCS417-mediated plant growth responses and its root colonization. Root exudates from Arabidopsis wild-type (WT) and mutant plants differentially affected the WCS417 transcriptome, with camalexin notably impacting bacterial motility and chemotaxis, which was also confirmed by in vitro studies. On the plant side, WCS417-induced transcriptome changes in the roots of defense barrier mutants were significantly different from those in WT plants, particularly affecting growth and defense-related processes. Specifically, the data indicated altered activity of reactive oxygen species in several of the defense barrier mutants, which was confirmed in planta. Our data suggest that various root defense barriers play a role in balancing growth and defense during this mutualistic interaction, thereby impacting the establishment and effectiveness of plant mutualists, extending their established role in disease resistance.