Evolutionarily conserved 12-oxophytodienoate reductase trans-lncRNA pair affects disease resistance in tea (Camellia sinensis) via the jasmonic acid signaling pathway

Long non-coding RNAs (lncRNAs) have gathered significant attention due to their pivotal role in plant growth, development, and biotic and abiotic stress resistance. Despite this, there is still little understanding regarding the functions of lncRNA in these domains in the tea plant (Camellia sinensis), mainly attributable to the insufficiencies in gene manipulation techniques for tea plants. In this study, we designed a novel strategy to identify evolutionarily conserved trans-lncRNA (ECT-lncRNA) pairs in plants. We used highly consistent base sequences in the exon-overlapping region between trans-lncRNAs and their target gene transcripts. Based on this method, we successfully screened 24 ECT-lncRNA pairs from at least two or more plant species. In tea, as observed in model plants such as Arabidopsis, alfalfa, potatoes, and rice, there exists a trans-lncRNA capable of forming an ECT-lncRNA pair with transcripts of the 12-oxophytodienoate reductase (OPR) family, denoted as the OPRL/OPR pair. Considering evolutionary perspectives, the OPRL gene cluster in each species likely originates from a replication event of the OPR gene cluster. Gene manipulation and gene expression analysis revealed that CsOPRL influences disease resistance by regulating CsOPR expression in tea plants. Furthermore, the knockout of StOPRL1 in Solanum tuberosum led to aberrant growth characteristics and strong resistance to fungal infection. This study provides insights into a strategy for the screening and functional verification of ECT-lncRNA pairs.