Trehalose-mediated reshaping of the rhizosphere microbiome drives tea root rot progression

Tea (Camellia sinensis [L.] Kuntze) is one of the most economically important crops and as a traditional medicinal plant in the world. The long-term continuous cropping and inappropriate management have led to frequent outbreaks of soil-borne diseases such as root rot, which pose a serious threat to the sustainable development of the tea industry. However, the pathogenesis of tea root rot remains poorly understood. In this study, two novel pathogen fungi, Paraconiothyrium cyclothyrioides F8 and Apiotrichum sporotrichoides F17, were isolated and identified from diseased tea roots. Microbiome analysis revealed significant restructuring of the rhizosphere microbial community in diseased tea plants, with a significant reduction in the abundance of Basidiomycota and marked enrichment of pathogen such as Fusarium and Apiotrichum. Meanwhile, the abundances of beneficial fungi (e.g., Saitozyma and Trichoderma) and bacteria (e.g., Bacillus and Sporosarcina) were significantly decreased. Further investigation demonstrated that root exudate trehalose exhibited prominent bidirectional regulatory effect through promoted the growth of pathogen, while simultaneously inhibiting biofilm formation, rhizosphere colonization at specific concentrations and weakened the biocontrol functions of the beneficial antagonistic bacteria Sporosarcina pasteurii T21 and Lysinibacillus sp. T23, facilitating the formation of a rhizosphere chemical environment that "aids enemies and harms allies" and thereby exacerbating disease occurrence. This study emphasized the dominant role of plant metabolites such as trehalose in driving the assembly of rhizosphere microbial communities from a disease-suppressive to a disease-conducive state, as well as in disease development. The findings provide a novel theoretical perspective for the microbiological regulation of tea root rot and offer theoretical and practical bases for tea root rot disease green prevention and control.