Whole-Genome Analysis Uncovers Long-Noncoding RNAs Regulating Rhizoctonia solani Resistance via Metabolic Pathways in Rice

Rice sheath blight is a devastating disease caused by Rhizoctonia solani. The systematic studies on long-noncoding
RNAs (lncRNAs)-mediated gene regulation during rice defense against R. solani are limited. Here, we identified 833 R. solani-responsive lncRNAs in rice that clustered
into eight distinct expression modules. We predicted 551 mRNAs targeted
by 366 pathogen-responsive lncRNAs, uncovering 648 potential cis-regulatory relationships. Functional analysis linked
these cis-regulated targets to metabolic pathways,
especially terpenoid, jasmonic acid, and tryptophan pathways. Additionally,
40 lncRNAs functioned as competing endogenous RNAs (ceRNAs), sponging
22 miRNAs to regulate 73 mRNAs enriched in metabolism. Further exploration
of lncRNA-associated enzymatic candidates identified three key metabolic
nodes: OsKSL12 and OsSANRL.1 in the cis-network and
OsCYP87C2 in the ceRNA network. Genetic knockout experiments confirmed
that these enzymes are associated with the rice defense against R. solani. Notably, sanguinarine (SG) metabolized
by OsSANRL.1 exhibited antifungal activity. Our study elucidates the
lncRNA-mediated regulatory networks underlying rice defense, with
a focus on metabolic reprogramming during infection by R. solani.