Abstract

Nitrogen (N) is an essential nutrient that strongly influences plant growth and development, and its availability can affect plant susceptibility to fungal pathogens. Poplar is a tree species widely distributed around the world. It is severely threatened by Melampsora larici-populina Kleb., a biotrophic pathogen which is the most destructive foliar pathogen of poplar trees and leads to significant biomass losses. Research on the interaction between Populus and M. larici-populina remains limited. We assessed the impact of N deficiency on foliar disease development caused by rust and to elucidate underlying physiological and molecular mechanisms in poplar, thereby providing insights into the relationship between plant nutrition and disease susceptibility. We performed an analysis of host physiological traits and plant-pathogen interaction transcriptomics in poplar trees under N deficiency and rust infection. Notably, N-deficient poplar trees showed reduced rust disease development, whereas N-sufficient poplar trees infected with rust accumulated higher levels of reactive oxygen species (ROS) and nitric oxide (NO). Both N deficiency and rust infection increased secondary metabolite accumulation in poplar leaves. Furthermore, dual RNA-seq analysis of the poplar–rust interaction identified numerous differentially expressed genes (DEGs) in poplar trees. The positive correlation in gene expression between N-deficient and rust-infected poplar suggests that similar response pathways are activated under both conditions. In contrast, an adequate N supply increased susceptibility to the pathogen. Under N-sufficient conditions, rust infection preferentially activated biotic stress-response genes while suppressing growth. N-deficient poplar conditions accumulated more antioxidant compounds, enhancing resistance by creating a less favorable environment for pathogen development. Consistently, genes in M. larici-populina associated with pathogen invasion and proliferation were down