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.

水稻纹枯病（rice sheath blight）是由立枯丝核菌（Rhizoctonia solani）引发的毁灭性病害。目前针对水稻抵御立枯丝核菌过程中长链非编码RNA（long non-coding RNA，lncRNA）介导的基因调控机制的系统性研究仍较为匮乏。本研究在水稻中鉴定出833个应答立枯丝核菌的长链非编码RNA，这些RNA可聚类为8个不同的表达模块。我们预测了366个应答病原菌的长链非编码RNA所靶向的551个mRNA，共揭示出648个潜在的顺式调控关联。功能富集分析将这些顺式调控靶标关联到多条代谢通路，尤其是萜类（terpenoid）、茉莉酸（jasmonic acid）以及色氨酸（tryptophan）代谢通路。此外，有40个长链非编码RNA充当竞争内源RNA（competing endogenous RNA，ceRNA），通过作为分子海绵吸附22个微小RNA（microRNA，miRNA）来调控73个富集于代谢过程的mRNA。进一步对与长链非编码RNA相关的候选酶类进行挖掘，鉴定出3个关键代谢节点：顺式调控网络中的OsKSL12与OsSANRL.1，以及竞争内源RNA网络中的OsCYP87C2。基因敲除实验证实，这些酶类与水稻抵御立枯丝核菌的过程密切相关。值得注意的是，血根碱（sanguinarine，SG）经OsSANRL.1代谢后，展现出抗真菌活性。本研究阐明了水稻抵御立枯丝核菌过程中长链非编码RNA介导的调控网络，重点揭示了病原菌侵染过程中的代谢重编程现象。