Complex associations between cross-kingdom microbial endophytes and host genotype in ash dieback disease dynamics

Tree pathogens are a major threat to forest ecosystems. Conservation management strategies can exploit natural mechanisms of resistance, such as tree genotype and host‐associated microbial communities. However, fungal and bacterial communities are rarely looked at in the same framework, particularly in conjunction with host genotype. Here, we explore these relationships and their influence on ash dieback disease, caused by the pathogen Hymenoscyphus fraxineus, in European common ash trees. We collected leaves from UK ash trees and used microsatellite markers to genotype trees, quantitative PCR to quantify H. fraxineus infection load and ITS and 16S rRNA amplicon sequencing to identify fungal and bacterial communities, respectively. There was a significant association between H. fraxineus infection intensity and ash leaf fungal and bacterial community composition. Higher infection levels were positively correlated with fungal community alpha‐diversity, and a number of fungal and bacterial genera were significantly associated with infection presence and intensity. Under higher infection loads, leaf microbial networks were characterized by stronger associations between fewer members than those associated with lower infection levels. Together these results suggest that H. fraxineus disrupts stable endophyte communities after a particular infection threshold is reached, and may enable proliferation of opportunistic microbes. We identified three microbial genera associated with an absence of infection, potentially indicating an antagonistic relationship with H. fraxineus that could be utilized in the development of anti‐pathogen treatments. Host genotype did not directly affect infection, but did significantly affect leaf fungal community composition. Thus, host genotype could have the potential to indirectly affect disease susceptibility through genotype × microbiome interactions, and should be considered when selectively breeding trees. Synthesis. We show that the diver