Transcriptional Insight Into Brassica napus Resistance Genes LepR3 and Rlm2-Mediated Defense Response Against the Leptosphaeria maculans Infection

The phytopathogenic fungus Leptosphaeria maculans causes the blackleg disease on Brassica napus, resulting in severe loss of rapeseed production. Breeding of resistant cultivars containing race-specific resistance genes is provably effective to combat this disease. While two allelic resistance genes LepR3 and Rlm2 recognizing L. maculans avirulence genes AvrLm1 and AvrLm2 at plant apoplastic space have been cloned in B. napus, the downstream gene expression network underlying the resistance remains elusive. In this study, transgenic lines expressing LepR3 and Rlm2 were created in the susceptible “Westar” cultivar and inoculated with L. maculans isolates containing different sets of AvrLm1 and AvrLm2 for comparative transcriptomic analysis. Through grouping the RNA-seq data based on different levels of defense response, we find LepR3 and Rlm2 orchestrate a hierarchically regulated gene expression network, consisting of induced ABA acting independently of the disease reaction, activation of signal transduction pathways with gradually increasing intensity from compatible to incompatible interaction, and specifically induced enzymatic and chemical actions contributing to hypersensitive response with recognition of AvrLm1 and AvrLm2. This study provides an unconventional investigation into LepR3 and Rlm2-mediated plant defense machinery and adds novel insight into the interaction between surface-localized receptor-like proteins (RLPs) and apoplastic fungal pathogens.