Nitrogen form-dependent microbial siderophore diversity shapes wheat-pathogen dynamics

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Abstract

Plants assimilate nitrogen (N) primarily as ammonium or nitrate, which exert strikingly opposite effects on soil-borne crop disease. Prior to host invasion, pathogens first encounter the resident microbial consortia of the rhizosphere, a critical frontline that determines the outcome of infection. A key hypothesis underpinning these interactions is that the two N forms shape microbial competition for iron through siderophore production. Yet, how this regulation operates remains unknown. Here, we integrate microbial genetics, metagenomics, transcriptomics and synthetic microbial communities to reveal that N form dictates dominant microbial iron-acquisition strategies in the wheat rhizosphere that modulates Fusarium crown rot (FCR) incidence. Ammonium selectively enriched commensal Proteobacteria carrying the asb gene cluster for petrobactin biosynthesis, thereby enhancing iron availability for the fungal pathogen Fusarium pseudograminearum and promoting disease. In contrast, nitrate recruited Actinobacteria-dominated communities encoding diverse non-asb siderophores that sequester iron and inhibit Fpg. A non-asb synthetic community significantly suppressed FCR and increased wheat yield, whereas a petrobactin-producing community exacerbated it. Mutant assays, fungal transcriptomic and global metagenome mining confirmed the specific role of the siderophore type in mediating pathogen suppression. Our results establish a mechanistic basis of nutrient–microbiome–pathogen interaction, linking N form and crop health via the ecology of iron competition. Given the global reliance on ammonium-based fertilizers, targeted modulation of N supply form offers an actionable framework to engineer protective rhizosphere microbiomes and sustainable nutritional strategies, thereby mitigating soil-borne diseases and strengthening agricultural resilience.

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