Elevated ozone concentration and nitrogen addition increase poplar rust severity by shifting the phyllosphere microbial community

Abstract

The tropospheric ozone and nitrogen deposition are two major environmental pollutants. Numerous studies have focused on the negative impacts of elevated O3 and the complementary effect of soil N addition to tree physiological characteristics. However, it was notoriously ignored of how elevated O3 with 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 O3 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 × P. cathayana) in Free-Air-Controlled-Environment plots, besides, 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 O3 or N addition only, however, the negative impact of elevated O3 could be significantly alleviated when simultaneously conducting N addition, likewise, this trade-off was also found in its phyllosphere microbial α-diversity responding to elevated O3 and N addition. However, the rust severity of clone ‘546’ did not significantly differ in the cases of elevated O3 and N addition. Mlp-infection altered microbial community composition and increased its sensitivity to elevated O3 assessed by significantly different abundance of taxa. Elevated O3 and N addition reduced the complexity of microbial community, which may explain the increased severity of poplar rust. These findings demonstrated that poplars need shifting phyllosphere microbial associations to optimize plant immunity in response to environmental changes.