Arabidopsis uses distinct coumarins and bacterial pathways for pH-adaptive iron acquisition.

Iron (Fe) limitation restricts plant growth in diverse soils, and root-associated microbes can alleviate plant Fe starvation. Whether plants integrate the edaphic environment and microbial activities into their Fe uptake strategies remains unclear. We show that bacterium-mediated alleviation of Fe deficiency in Arabidopsis functions at varying environmental pH and is taxonomically widespread among root microbiota isolates from soils with different edaphic profiles. This process is regulated by host-controlled and pH-adapted root exudation of different coumarin chemotypes. These exometabolites interact with root-associated bacteria to mobilize Fe either via bacterial siderophore-mediated chelation at circumneutral pH or redox-sensing-controlled, reduction-based pathways at acidic pH. The corresponding bacterial genes are prevalent in the root microbiota, and they likely evolved before the emergence of land plants. Our findings suggest that Fe malnutrition-induced exudation of redox-active metabolites by non-graminaceous plant species is a widespread adaptation for Fe mobilization from soil, mediated by the co-option of ancient microbial processes.