Elevated Ozone Concentration and Nitrogen Addition Increase Poplar Rust Severity by Shifting the Phyllosphere Microbial Community

Tropospheric ozone and nitrogen deposition are two major environmental pollutants. A great deal of research has focused on the negative impacts of elevated O(3) and the complementary effect of soil N addition on the physiological properties of trees. However, it has been overlooked how elevated O(3) and N addition affect tree immunity in face of pathogen infection, as well as of the important roles of phyllosphere microbiome community in host–pathogen–environment interplay. Here, we examined the effects of elevated O(3) and soil N addition on poplar leaf rust [Melampsora larici-populina] severity of two susceptible hybrid poplars [clone ‘107’: Populus euramericana cv. ‘74/76’; clone ‘546’: P. deltoides Í P. cathayana] in Free-Air-Controlled-Environment plots, in addition, the link between Mlp-susceptibility and changes in microbial community was determined using Miseq amplicon sequencing. Rust severity of clone ‘107’ significantly increased under elevated O(3) or N addition only; however, the negative impact of elevated O(3) could be significantly mitigated when accompanied by N addition, likewise, this trade-off was reflected in its phyllosphere microbial α-diversity responding to elevated O(3) and N addition. However, rust severity of clone ‘546’ did not differ significantly in the cases of elevated O(3) and N addition. Mlp infection altered microbial community composition and increased its sensitivity to elevated O(3), as determined by the markedly different abundance of taxa. Elevated O(3) and N addition reduced the complexity of microbial community, which may explain the increased severity of poplar rust. These findings suggest that poplars require a changing phyllosphere microbial associations to optimize plant immunity in response to environmental changes.