Elevated O3 concentrations alter the compartment-specific microbial communities inhabiting rust-infected poplars

Elevated ozone (O₃) can affect the susceptivity of plants to rust pathogens. However, the collective role of microbiomes involved in such interaction remains largely elusive. We exposed two cultivated poplar clones exhibiting differential O₃ sensitivities, to non-filtered ambient air (NF), NF + 40 ppb or NF + 60 ppb O₃-enriched air in field open-top chambers and then inoculated Melampsora larici-populina urediniospores to study their response to rust infection and to investigate how microbiomes inhabiting four compartments (phyllosphere, rhizosphere, root endosphere, bulk soil) are involved in this response. We found that hosts with higher O₃ sensitivity had significantly lower rust severity than hosts with lower sensitivity. Furthermore, the effect of increased O₃ on the diversity and composition of microbial communities was highly dependent on poplar compartments, with the microbial network complexity patterns being completely opposite between the two clones. Notably, microbial source analysis estimated that phyllosphere fungal communities predominately derived from root endosphere and vice versa, suggesting a potential transmission mechanism between plant above- and below-ground systems. These promising results suggest that further investigations are needed to better understand the interactions of abiotic and biotic stresses on plant performance and the role of the microbiome in driving these changes.