Coumarins link rhizobacteria perception in roots to systemic resistance in leaves

Abstract

Induced systemic resistance (ISR) is activated in leaves upon root colonization by beneficial microbes, yet the signals linking rhizosphere perception to shoot immunity remain unknown. In the Arabidopsis thaliana-Pseudomonas simiae WCS417 model interaction, the root-specific transcription factor MYB72 and its target gene BGLU42 regulate ISR and the production, activation, and root secretion of coumarins, specialized metabolites involved in plant iron (Fe) acquisition and rhizosphere microbiome assembly. Overexpression of BGLU42 confers constitutive ISR in leaves, suggesting a link between coumarin metabolism and systemic immunity. Here, two-photon multispectral imaging and targeted metabolite profiling revealed that, under Fe-sufficient conditions, WCS417 induces a distinct spatial pattern of F6’H1-dependent coumarin accumulation along the root system. These WCS417-induced coumarin signatures differed from those observed under Fe deficiency, indicating activation of a microbiota-specific coumarin metabolic program. Increased coumarin accumulation in roots was followed by a rise in coumarin levels in shoots. Time-resolved transcriptome profiling supported this metabolic reprogramming, showing rapid activation of Fe acquisition and coumarin biosynthesis genes in roots, including F6’H1, MYB72, and BGLU42, followed by delayed but similar transcriptional responses in shoots. Functional analyses demonstrated that coumarin biosynthesis is required for WCS417-ISR: the f6’h1 mutant failed to mount systemic resistance, whereas F6’H1 overexpression conferred constitutive resistance to bacterial and fungal pathogens. In addition, WCS417-mediated coumarin accumulation systemically modulated flg22-triggered reactive oxygen species production in leaves in an F6’H1-dependent manner. Together, our results identify coumarins as key mediators linking rhizobacterial perception in roots to systemic immune signaling and resistance in leaves.