Plant-Mediated Soil Sickness: Steering the Rhizosphere into a Pathogenic Niche.

Abstract

Continuous monoculture of <i>Panax notoginseng</i> leads to severe replant disease, yet the mechanisms by which root exudates mediate rhizosphere microbiome assembly and pathogen enrichment remain poorly understood. Here, we demonstrate that long-term root exudate accumulation acts as an ecological filter, driving the fungal community toward a phylogenetically impoverished, pathogen-dominated state. Specifically, exudates enriched the soil-borne pathogen <i>Fusarium</i> while reducing the abundance of potentially antagonistic fungi. In contrast, bacterial communities exhibited higher resilience, with exudates selectively enriching oligotrophic taxa such as <i>Terrimonas</i> and <i>MND1</i>, but suppressing nitrifying bacteria (e.g., <i>Nitrospira</i>) and plant-growth-promoting rhizobacteria (PGPR). Microbial functional profiling revealed a shift in nitrogen cycling, characterized by suppressed nitrification and enhanced nitrate reduction. Crucially, co-occurrence network analysis identified bacterial taxa strongly negatively correlated with <i>Fusarium</i>, providing a synthetic community blueprint for biocontrol strategies. Our study establishes a mechanistic link between root exudate accumulation and negative plant-soil feedback in monoculture systems, highlighting microbiome reprogramming as a key driver of replant disease. These insights offer novel avenues for manipulating rhizosphere microbiomes to sustain crop productivity in intensive agricultural systems.