Successional dynamics from fungal pathogen dominance to beneficial bacterial enrichment along leaf ontogeny

Abstract The phyllosphere microbiome is integral to host health and productivity, yet how these communities assemble during leaf ontogeny remains poorly understood. We examined bacterial and fungal communities of Hevea brasiliensis leaves across six developmental stages using a space-for-time substitution design. Our results showed that plant developmental stage had a profound influence on the microbial diversity, composition, and interkingdom networks, exerting a much stronger effect on the epiphytic than the endophytic compartment. Bacterial diversity increased progressively from the bud to the deciduous stage, whereas fungal diversity exhibited a sharp decline before recovering. This transient fungal decline was coupled with the transient dominance of putative pathogens (peaking at ∼53% relative abundance) in the early expanding leaves. During leaf expansion and maturation, community assembly shifted from stochastic dominance to deterministic processes, a transition most pronounced in the bacterial community (peaking at ∼80% determinism). Concurrently, network analysis revealed a topological turnover towards a balanced, highly connected architecture in the stable stage. This structural complexity underpinned peak ecological stability, characterized by extensive negative associations and the recruitment of stabilizing keystones, including the plant-beneficial genus Massilia. Furthermore, biomarker analysis confirmed a distinct functional turnover: early stages were defined by pathogen signals, whereas late stages were characterized by the progressive accumulation of beneficial taxa (e.g. Sphingomonas and Massilia). Collectively, our findings suggest that leaf ontogeny orchestrates microbiome assembly through deterministic selection, shaping a succession from pathogen-dominated stochastic communities to stable, beneficial-enriched networks. These insights provide a theoretical foundation for manipulating microbiome succession to enhance sustainable forest health.