Soil acidification dismantles a citrulline-mediated microbe-metabolite-host defense axis in watermelon, exacerbating Fusarium wilt.

Soil acidification disrupts the structure and function of soil microbiomes, resulting in increased vulnerability to soil-borne pathogens. While the link between soil acidification and disease susceptibility is well-established, the mechanisms underlying the suppression of plant defense remain poorly understood. In this study, we found that soil acidification perturbed the co-evolved assembly process of endophytic microbiomes in watermelon roots, leading to the collapse of a critical microbe-metabolite-host defense axis essential for resistance against Fusarium oxysporum f. sp. niveum (FON). Integrated field surveys and multi-omics analyses revealed that acidification-induced dysbiosis in the root endophytic microbiomes, characterized by the depletion of keystone Pseudomonas species (Pseudomonadaceae), strongly correlated with increased Fusarium wilt incidence. Central to this interaction was citrulline, a metabolite produced by root Pseudomonas endophytes that functioned as a symbiotic effector promoting bacterial colonization and a defense modulator inhibiting FON-induced oxidative burst. Disruption of citrulline biosynthesis abolished these protective effects, whereas exogenous citrulline application restored disease resistance. These findings underscored the role of root endophyte-derived citrulline in sustaining microbial fitness and plant defense, revealing a tripartite interaction impacted by soil acidification. Collectively, this study provides insights for developing microbiome-based strategies to enhance sustainable crop protection in degraded agroecosystems.