Pseudomonas chlororaphis YL21 synergistically controls Fusarium crown rot of wheat by reshaping rhizosphere microbiota and reprogramming host defense metabolism.

Fusarium crown rot (FCR) poses a major threat to wheat (Triticum aestivum L.) production worldwide, with severe outbreaks occurring in the Xinjiang Uygur Autonomous Region, China. As a soil-borne disease caused by Fusarium species, FCR is considered difficult to detect and manage, which often leads to poor control efficacy. Therefore, developing novel green biocontrol agents represents an urgent scientific challenge. Here, we report a rhizosphere bacterium, Pseudomonas chlororaphis YL21, which exhibits strong antagonistic activity against Fusarium spp. Inoculation with P. chlororaphis YL21 significantly reduced FCR severity and promoted plant growth. This strain produces proteases that inhibit pathogens, as well as plant growth-promoting factors including nitrogen fixation, siderophores, hydrogen cyanide (HCN), indole-3-acetic acid (IAA), and ammonia. ITS and 16S rRNA sequencing revealed that strain YL21 substantially reshaped the rhizosphere microbiota structure and promoted the enrichment of other beneficial microorganisms. RNA-Seq showed upregulation of plant hormone signal transduction and vitamin B6 metabolism pathways, as well as defense-related genes including PR1 and RPM1. Untargeted metabolomics revealed substantial metabolic changes in the wheat stem base following YL21 inoculation, with metabolites such as xanthoxylol, dihydrochelerythrine, and zeanic acid being significantly upregulated. Plants reprogrammed key metabolic pathways, including glucosinolate biosynthesis, ABC transporters, and the biosynthesis of various plant secondary metabolites, collectively indicating activated defense responses. This work elucidates the biocontrol mechanisms of P. chlororaphis against Fusarium by integrating metabolomics, transcriptomics, and microbiome analyses. Our findings lay a solid foundation for developing sustainable approaches to manage FCR in wheat.