Mechanism of Action of Fusarium oxysporum CCS043 Utilizing Allelochemicals for Rhizosphere Colonization and Enhanced Infection Activity in Rehmannia glutinosa

<i>Rehmannia glutinosa</i> is an important medicinal herb; but its long-term cultivation often leads to continuous cropping problems. The underlying cause can be attributed to the accumulation of and alterations in root exudates; which interact with soil-borne pathogens; particularly <i>Fusarium oxysporum</i>; triggering disease outbreaks that severely affect its yield and quality. It is therefore crucial to elucidate the mechanisms by which root exudates induce <i>F. oxysporum</i> CCS043 outbreaks. In this study; the genome of <i>F. oxysporum</i> CCS043 from <i>R. glutinosa's</i> rhizosphere microbiota was sequenced and assembled de novo; resulting in a 47.67 Mb genome comprising 16,423 protein-coding genes. Evolutionary analysis suggests that different <i>F. oxysporum</i> strains may adapt to the host rhizosphere microecosystem by acquiring varying numbers of specific genes while maintaining a constant number of core genes.The allelopathic effects of ferulic acid; verbascoside; and catalpol on <i>F. oxysporum</i> CCS043 were examined at the physiological and transcriptomic levels. The application of ferulic acid was observed to primarily facilitate the proliferation and growth of <i>F. oxysporum</i> CCS043; whereas verbascoside notably enhanced the biosynthesis of infection-related enzymes such as pectinase and cellulase. Catalpol demonstrated a moderate level of allelopathic effects in comparison to the other two. Furthermore; 10 effectors were identified by combining the genomic data. Meanwhile; it was found that among the effector-protein-coding genes; ChiC; VRDA; csn; and chitinase exhibited upregulated expression across all treatments. The expression patterns of these key genes were validated using qRT-PCR. Transient overexpression of the two effector-encoding genes in detached <i>R. glutinosa</i> leaves provided further confirmation that ChiC (GME8876_g) and csn (GME9251_g) are key effector proteins responsible for the induction of hypersensitive reactions in <i>R. glutinosa</i> leaf cells. This study provides a preliminary indication that the use of allelochemicals by <i>F. oxysporum</i> CCS043 can promote its own growth and proliferation and enhance infection activity. This finding offers a solid theoretical basis and data support for elucidating the fundamental causes of fungal disease outbreaks in continuous cropping of <i>R. glutinosa</i> and for formulating effective mitigation strategies.