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.