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Marssonina brunnea, the causative pathogen of Marssonina leaf spot of poplars (MLSP), devastates poplar plantations by forming black spots on leaves and defoliating trees. Although MLSP has been studied for over 30 years, the key genes that function during M. brunnea infection and their effects on plant growth are poorly understood. Here, we used multigene association studies to investigate the effects of key genes in the plant-pathogen interaction pathway, as revealed by transcriptome analysis, on photosynthesis and growth in a natural population of 435 Populus tomentosa individuals. By analyzing transcriptomic changes during three stages of infection, we detected 628 transcription factor genes among the 7,611 differentially expressed genes that might be associated with basal defense responses. Gene Ontology and Kyoto Encyclopedia of Genes and Genomes enrichment analyses revealed that transcriptomic changes across different stages of infection lead to the reprogramming of metabolic processes possibly related to defense activation. We identified 29,399 common single-nucleotide polymorphisms (SNPs) within 221 full-length genes in plant-pathogen interaction pathways that were significantly associated with photosynthetic and growth traits. We also detected 4,460 significant epistatic pairs associated with stomatal conductance, tree diameter, and tree height. Epistasis analysis uncovered significant interactions between 2,561 SNP-SNP pairs from different functional modules in the plant-pathogen interaction pathway, revealing possible genetic interactions. This analysis revealed many key genes that function during M. brunnea infection and their potential roles in mediating photosynthesis and plant growth, shedding light on genetic interactions between functional modules in the plant-pathogen interaction pathway.

Key Genes and Genetic Interactions of Plant-Pathogen Functional Modules in Poplar Infected by Marssonina brunnea