Cooperation between a root fungal endophyte and host-derived coumarin scopoletin mediates Arabidopsis iron nutrition

Summary Iron acquisition is a critical challenge for plants, especially in iron-deficient soils. Recent research underscores the importance of root-exuded coumarins in modulating the root microbiome community structure and facilitating iron uptake. However, interactions between root-associated fungi and coumarins in plant iron nutrition remain unknown. We investigated the mechanism by which a fungal endophyte, Macrophomina phaseolina (F80), enhances Arabidopsis iron nutrition. Fungal–coumarin interactions were assessed by profiling metabolites and measuring iron mobilisation in F80 cultures supplemented with specific coumarins, alongside quantifying growth performance and iron content in Arabidopsis coumarin-biosynthesis mutants inoculated with F80. Our findings reveal that an interaction between the coumarin scopoletin and F80 in the rhizosphere rescues plant growth under iron-limiting conditions by resolving the iron mobility bottleneck. F80 exhibits a capacity to modify scopoletin into iron-chelating catechol coumarin esculetin, thereby releasing available iron. We conclude that Arabidopsis -produced scopoletin functions as a precursor for fungal conversion into iron-chelating coumarins. By extending the role of coumarins from bacterial to fungal members of the root microbiota, this study places coumarins at the centre of commensal-mediated enhancement of plant iron nutrition across microbial kingdoms.