Small world but large differences: cultivar-specific secondary metabolite-mediated phyllosphere fungal homeostasis in tea plant (Camellia sinensis)

Phyllosphere microbes are closely linked to plant health and are important for the maintenance of host community stability. Tea plants (Camellia sinensis) can synthesize abundant secondary metabolites (SMs), however, it is unclear how they affect tea plant phyllosphere homeostasis. We investigated the effects of secondary metabolites of two tea plant cultivars (Longjing43 and Zhongcha108) that have different levels of resistance to anthracnose on the composition, function, assembly and network of phyllosphere fungi. We found that the phyllosphere fungal compositions of Longjing43 and Zhongcha108 were distinct, with certain fungal pathogens significantly enriched in the susceptible cultivar Longjing43 (e.g., Fusarium), which had a higher relative abundance of phytopathogenic functional groups. In addition, the phyllosphere fungal community assembly of the resistant cultivar Zhongcha108 with a higher habitat niche breadth was more influenced by stochastic processes. More importantly, the fungal network of Zhongcha108 exhibited higher complexity and stability, indicating a more resilient network structure. Random forest and partial least squares path models revealed that secondary metabolites, fungal community diversity, composition and function essentially determined network stability. (−)-Epigallocatechin-3-gallate (EGCG) and caffeine (CAF) were the most important predictors of phyllosphere fungal network stability in 2018 and 2019, respectively. Rare fungal taxa were particularly important in maintaining phyllosphere homeostasis. Our study suggests that secondary metabolites may mediate phyllosphere fungal homeostasis in tea plants. These findings highlight the importance of secondary metabolites in shaping the phyllosphere fungal community and provide ideas for regulating plant resistance to pathogenic fungi.