Host filtering overrides simulated climate change: plant species identity shapes phyllosphere fungal communities and putative pathogen proportions in an alpine meadow.

UNLABELLED: Phyllosphere fungal communities play critical ecological roles in plant fitness and nutrient cycling in terrestrial ecosystems. However, the influences of multifactorial climate change on foliar mycobiomes across distinct plant functional groups remain poorly understood. To elucidate this, we used an 11-year field manipulation experiment to assess the impacts of simulated warming (+2.0°C) and altered precipitation (-50%, ambient, and +50%) on foliar fungal α-diversity, β-diversity, and functional guilds across four co-occurring alpine host plants: a forb (Aster diplostephioides), a grass (Elymus nutans), a legume (Oxytropis kansuensis), and a sedge (Kobresia humilis), combining ITS1 metabarcoding with compositional bias-corrected modeling (Analysis of Compositions of Microbiomes with Bias Correction 2). We found that host plant species identity acted as the overriding ecological filter, explaining 34.1% of community variation ([Formula: see text]) and predominantly governing putative pathogen proportions ([Formula: see text]; forb > grass > sedge > legume). In contrast, climate manipulation impacts were strictly host-dependent: experimental warming significantly elevated fungal OTU richness solely in the legume O. kansuensis ([Formula: see text]), while restructuring community β-diversity exclusively in O. kansuensis ([Formula: see text], [Formula: see text]) and the sedge K. humilis ([Formula: see text], [Formula: see text]). In addition, while precipitation shifts minimally affected broad-scale diversity, both climate factors induced fine-scale taxonomic turnover in specific lineages (notably Aureobasidium, Cladosporium, Vishniacozyma, and Colletotrichum); crucially, overall guild-level putative pathogen proportions remained resilient against all climate treatments and their interactions ([Formula: see text]). Our findings suggest that host intrinsic filtering and functional buffering outweigh direct short-term climatic pressures, and emphasize that future alpine foliar disease vulnerability will be predominantly mediated by climate-driven shifts in host plant community dominance rather than direct climatic stimulation of potential pathogens.

IMPORTANCE: The phyllosphere represents a vital ecological interface where fungal communities dictate plant fitness and ecosystem functioning, yet their vulnerability to concurrent warming and altered precipitation remains poorly understood in fragile alpine biomes. Here, we demonstrate that host plant species identity serves as the overriding ecological filter structuring foliar fungal communities, overriding direct short-term climatic stressors and effectively buffering potential pathogen burdens. Climate warming and precipitation shifts induced only fine-scale, host-specific adjustments in individual fungal lineages rather than triggering broad functional pathogen outbreaks. These findings provide critical evidence that future alpine foliar disease dynamics under global change will be primarily mediated by climate-driven shifts in host plant community composition rather than direct climatic acceleration of pathogen proliferation. This work highlights the imperative of integrating species-specific plant-microbe interactions into ecological forecasting and conservation frameworks for vulnerable alpine ecosystems.