Comprehensive analysis of lncRNAs and mRNAs in Vitis vinifera defense mechanisms against multiple pathogens

Long non-coding RNAs (lncRNAs) are critical regulators of plant immunity, yet their roles in broad-spectrum resistance of Vitis vinifera (grapevine) against multiple pathogens remain underexplored. In the present study, we investigated the functional roles of grapevine lncRNAs during infection with five pathogens, including Lasiodiplodia theobromae, Xylella fastidiosa, Flavescence dorée, Erysiphe necator and Plasmopara viticola.

We identified 7752 candidate lncRNAs through transcriptome analyses of grapevine infected by five pathogens, including fungi, bacteria, oomycetes and phytoplasmas. These lncRNAs regulated key immune-related pathways, such as plant-pathogen interaction, mitogen-activated protein kinase signaling pathway-plant and plant hormone signal transduction. Subsequently, specific lncRNA-mRNA pairs induced by each pathogen were identified by differential expression, co-expression network and expression trend analyses. The results showed that the specific pairs were linked to pathogen resistance, targeting immune-related genes, such as UDP-glycosyltransferase, ethylene-responsive transcription factor, glycosyltransferase 2, GDSL esterase lipase, thaumatin-like protein, cytochrome P450 malectin receptor-like protein kinase and glycoside hydrolase chitinase. In addition, broad-spectrum resistance was associated with 254 lncRNAs regulating 324 functional genes, including leucine-rich repeat proteins and transcription factors.

This comprehensive dataset advances understanding of grapevine immunity, highlighting lncRNAs as potential targets for breeding pathogen-resistant grapevine varieties and fostering sustainable viticulture practices. Furthermore, we intend to explore the functional mechanisms of these broad-spectrum resistance genes, such as by using CRISPR (i.e. clustered regularly interspaced short palindromic repeats) for functional validation, identifying their promoter binding sites, screening for interacting proteins using yeast two-hybrid assays and constructing regulatory networks via bioinformatics approaches. © 2025 Society of Chemical Industry.