Microbiome shifts during <i>Fusarium oxysporum</i> and <i>F. solani</i> (syn. <i>Neocosmospora solani</i> )—induced <i>Ligusticum chuanxiong</i> root rot: endophtic bacterial protective responses and fungal pathogenic tendencies

Root rot disease is a globally significant threat to the health of diverse economically important crops. Understanding shifts in the plant microbiome during disease progression can aid in identifying beneficial microbes with disease-resistant potential and developing ecofriendly biocontrol strategies. However, microbiome changes during root rot progression in the medicinal plant <i>Ligusticum chuanxiong</i> remain poorly understood. This study aimed to investigate the response of host-associated microbiomes to pathogen stress (<i>Fusarium oxysporum</i> and <i>F. solani</i> syn. <i>Neocosmospora solani</i>) during <i>L. chuanxiong</i> root rot. The diversity, composition, function, and network interactions of bacterial and fungal communities were examined using high-throughput sequencing and network analysis in healthy rhizomes, healthy layers of diseased rhizomes, rotten layers of diseased rhizomes, and rhizosphere and non-rhizosphere soils. The bacterial diversity decreased as root rot progressed in end ophytic (from 0.72 to 0.38) and rhizosphere soils (from 0.80 to 0.68), whereas the fungal diversity showed no significant changes. The diseased samples were enriched with root rot pathogens and other potential pathogens, such as the soil bacterium <i>Pectobacterium</i> and the soil fungus <i>Gibberella</i>, whereas beneficial taxa, including endophytic <i>Bacillus</i> and <i>Trichoderma</i>, and soil-dwelling <i>Candidatus_Solibacter</i> and <i>Beauveria</i>, were significantly reduced. Notably, in the healthy layers of diseased rhizomes, which represent a "transitional phase", fungal communities resembled those in rotten tissues with increased pathogenic taxa (<i>e.g.</i>, <i>Ceratocystis</i> and <i>Plectosphaerella</i>), whereas bacterial communities were more similar to healthy rhizomes and enriched in beneficial genera (<i>e.g.</i>, <i>Microbacterium</i> and <i>Variovorax</i>). Functional prediction indicated suppressed bacterial activity and enhanced fungal saprotrophy in rotten rhizomes. The cross-kingdom network complexity decreased in both endophytic and soil microbial communities during root rot, while positive correlations within endophytic networks increased. Overall, as root rot progresses, the stability and competitive interactions within endophytic and soil microbiomes of <i>L. chuanxiong</i> weaken. Early in infection, endophytic bacterial and fungal communities exhibit divergent responses: bacteria likely contribute to disease resistance, whereas fungi may promote pathogenesis. This findings suggest that a more beneficial role for endophytic bacteria in controlling <i>L. chuanxiong</i> root rot. Restoring microbial community complexity may offer a viable biocontrol strategy. Our findings provide a theoretical foundation for future identification of specific beneficial microbes and the development of safe biocontrol approaches.