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

ABSTRACT 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.