Analysis of lncRNA–mRNA pairs induced by Colletotrichum camelliae reveals Cslnc170 as a regulator of CsLOX4 in tea plants

Fungal diseases such as anthracnose substantially affect the growth of tea (Camellia sinensis) plants. Understanding disease-resistance mechanisms and identifying resistance genes will aid in breeding resistant varieties. Noncoding RNAs, including long noncoding RNAs (lncRNAs), play critical roles in regulating plant immunity by influencing target gene expression; however, their role in disease resistance of tea plants remains underexplored. Here, we used RNA sequencing to identify differentially expressed lncRNAs and mRNAs in C. sinensis following infection with Colletotrichum camelliae. Our analysis revealed 524 antisense lncRNA-mRNA pairs and 3,588 cis-acting lncRNA-mRNA pairs involved in photosynthesis, amino acid biosynthesis, fatty acid metabolism, and secondary metabolism pathways such as flavonoid biosynthesis. Among these, we identified the cis-acting pair Cslnc170-CsLOX4 (encoding a 13-lipoxygenase) as a key regulator of disease resistance. The Cslnc170 gene (1,581 bp) lies 9,254 bp downstream of the CsLOX4 gene, a member of the 13-lipoxygenase family. Functional studies showed that Cslnc170 activates CsLOX4 expression via loop 4 of its secondary structure and the CsLOX4 promoter region (930 to 952 bp). Agrobacterium-mediated overexpression and antisense-oligonucleotide-mediated silencing experiments confirmed that the Cslnc170-CsLOX4 pair enhances resistance to anthracnose in tea leaves. These findings provide insights into the regulatory role of lncRNA-mRNA pairs, offering potential targets for improving disease resistance in tea plants.