Rhizoplane microbiome: niche-specific recruitment and plant defense priming against bacterial wilt disease.

The plant microbiome plays a pivotal role in host adaptation and disease suppression, yet niche-specific microbial responses to biotic stress, particularly within distinct plant compartments, remain poorly understood. Here, we revealed that bacterial wilt disease (BWD) induced pronounced niche-specific microbiome alterations in tobacco, with the rhizoplane (RP) emerging as a critical hub for beneficial microbial recruitment and defense coordination. Utilizing 16S and ITS amplicon sequencing across 6 distinct plant niches, we observed significantly enhanced bacterial diversity and a striking enrichment of potentially beneficial microbes in the RP under BWD stress. Eight potent antagonistic bacterial strains were isolated from this key niche, with Stenotrophomonas sp. ASV61 and Chryseobacterium sp. ASV172 demonstrating robust in vitro biocontrol potential and confirming in vivo plant resistance and growth promotion. We further elucidated the superior biocontrol mechanisms of Chryseobacterium sp. ASV172, attributing its superior efficacy to enhanced colonization and flexirubin-mediated antagonism. Crucially, plant transcriptomic profiling unveiled that these beneficial microbes engaged in a signaling dialogue with host plants, dynamically modulating defense hormone pathways. While Ralstonia alone manipulated host defenses by sustaining salicylic acid responses, antagonistic strains re-directed the plant toward robust jasmonic acid signaling, thereby restoring a more effective defense posture. Collectively, our findings underscore the disproportionate importance of the RP over the rhizosphere in assembling a resilient microbiome against soil-borne diseases, paving the way for targeted RP microbiome engineering strategies for sustainable disease management.