Antifungal biosynthesis by root-associated Streptomyces and Pseudomonas is elicited upon plant colonization

Plants are colonized by a diverse microbiome, with microorganisms residing inside and outside of plant tissues. Plants can harness the protective traits of their microbial inhabitants to ward off insect pests and fungal pathogens. However, current understanding of the role of commensal interactions on activating the desired microbial genomic traits remains limited. Here we show that biosynthesis of the antifungal 2,5-dihydro-L-phenylalanine (DHP) by the endophytic Streptomyces sp. PG2 is strongly induced upon colonization of Arabidopsis thaliana. DHP production protects the plant from infection by the fungal root pathogen Rhizoctonia solani, both in vitro and in vivo.. We identified the DHP biosynthetic gene cluster (BGC) and showed that heterologous expression of the BGC in the DHP non-producer Streptomyces coelicolor also conferred plant-inducible DHP production. The BGC was also found in plant-associated Gram-negative bacteria, and in Pseudomonas syringae FF5 we again observed strongly enhanced DHP production upon plant colonization. An ecology-inspired elicitor screen showed that L-valine and brassinosteroid hormones elicit DHP biosynthesis in the plant-beneficial Streptomyces sp. PG2, while L-valine also elicited DHP biosynthesis in S. coelicolor. In vivo experiments confirmed the stimulation of antifungal activity in Streptomyces sp. PG2 by L-valine, while brassinolide mutant plants showed reduced DHP induction. Conversely, neither L-valine nor brassinolide elicited the expression of the DHP BGC in the pathogenic P. syringae, revealing important divergence in the responses to plant signaling, which may reflect selectivity in how endosymbionts and pathogens respond to host cues. Collectively, our data demonstrate that plant colonization can elicit the biosynthetic potential of root-associated microbes, thereby enhancing plant resilience.