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.