Compartments of roots and mature leaves are key hubs in the connectivity of tea-plant mycobiomes and are influenced by environmental factors and host age.

Understanding the tripartite consortium of crop, mycobiome, and environment is necessary to advance smart farming. Owing to their life cycle of hundreds of years, tea plants are excellent models for studying these entwined relationships; however, observations on this globally important cash crop with numerous health benefits are still rudimentary. Here, the fungal taxa along the soil-tea plant continuum in tea gardens of different ages in famous high-quality tea-growing regions in China were characterized using DNA metabarcoding. Using machine learning, we dissected the spatiotemporal distribution, co-occurrence patterns, assembly, and their associations in different compartments of tea-plant mycobiomes, and further explored how these potential interactions were driven by environmental factors and tree age, and how they influenced the market prices of tea. The results revealed that Compartment niche differentiation was the key driving force behind variation in the tea-plant mycobiome. The mycobiome of roots had the highest specific proportion and convergence and almost did not overlap with the soil. The enrichment ratio of developing leaves to root mycobiome increased with increasing tree age, while mature leaves showed the highest value in the Laobanzhang (LBZ) tea garden with top market prices and displayed the strongest depletion effect on mycobiome association along the soil-tea plant continuum. The balance between determinism and stochasticity in the assembly process was co-driven by compartment niches and life cycle variation. Fungal guild analysis showed that altitude indirectly affected market prices of tea by mediating the abundance of the plant pathogen. The relative importance of plant pathogen and ectomycorrhizae could be used to assess the age of tea. Biomarkers were mainly distributed in soil compartments, and Clavulinopsis miyabeana, Mortierella longata, and Saitozyma sp. may affect the spatiotemporal dynamics of tea-plant mycobiomes and their ecosystem services. Soil properties (mainly total potassium) and tree age indirectly affected the developing leaves via positively influencing the mycobiome of mature leaves. In contrast, the climate directly and significantly drove the mycobiome composition of the developing leaves. Moreover, the proportion of negative correlations in the co-occurrence network positively regulated tea-plant mycobiome assembly, which significantly affected the market prices of tea in the structural equation model with network complexity as hub. These findings indicate that mycobiome signatures play pivotal roles in the adaptive evolution and fungal disease control of tea plants and can help develop better agricultural practices that focus on both plant health and financial profits, and provide a new strategy for assessing tea quality grade and age.