Linking Plant Metabolomics with Fungal Functional Dynamics Reveals a Noncanonical S-R-C Adaptive Trajectory

Phyllosphere plant-fungal interactions are crucial for crop health, yet how leaf metabolite dynamics interplay with fungal functional succession remains unclear. Using field-based holo-omics, we show that developmental shifts in sorghum leaf metabolomes drive a noncanonical temporal trajectory of fungal life-history strategies from stress-tolerator (S), through ruderal (R), to competitor (C). Young leaves deploy antifungal metabolites that select for stress-tolerators (S-strategists) with expanded genomes. A transient increase in maltose abundance during flowering promotes the proliferation of fast-growing ruderal (R-) strategists. As plants mature, competitive (C-) strategists rely on secondary metabolism to persist in crowded communities. We further detect asynchrony between taxonomic and functional beta diversities, and a drop in the taxonomic one coincides with upregulated expression of fungal genes encoding secreted carbohydrate-active enzymes and effectors. Collectively, these findings identify developmental stage-specific leaf metabolomes as key determinants of phyllosphere fungal adaptation and functioning.