The lncRNA47980-miR5303-FBA41 module modulates tomato disease resistance by fine-tuning reactive oxygen species and phytohormone levels

Tomato (Solanum lycopersicum), a globally important fruit and vegetable crop with diverse germplasm, frequently suffers from yield and quality losses due to late blight caused by Phytophthora infestans. Non-coding RNAs (ncRNAs) have been shown to play essential roles in plant disease resistance. In a previous study, we demonstrated that lncRNA47980 positively regulates tomato resistance; however, the underlying mechanism remained unclear. Here, we demonstrate that lncRNA47980 functions as an endogenous target mimic (eTM) of miR5303, thereby alleviating its inhibitory effect on F-box associated protein 41 (FBA41). MiR5303 levels were significantly elevated in lncRNA47980 knockout mutants compared with wild-type (WT) plants. Moreover, introducing an 8-point mutation in the miR5303-binding region of lncRNA47980 abolished the interaction, further confirming its role as an eTM for miR5303. Genetic analyses showed that knockout of miR5303 enhanced resistance, whereas its overexpression impaired resistance. Moreover, miR5303 directly cleaved transcripts of its target gene FBA41, whose overexpression conferred enhanced resistance and was localized in chloroplasts. lncRNA47980, miR5303, and FBA41 dynamically regulated reactive oxygen species levels by modulating the level of antioxidant enzymes and related genes in a time-dependent manner. Furthermore, they influenced the expression of downstream defense-related genes by altering salicylic acid and jasmonic acid levels. Lignin content determination revealed that FBA41 and lncRNA47980 overexpression plants accumulated significantly more lignin than WT, while miR5303 overexpression reduced lignin accumulation. Our findings demonstrate that the lncRNA47980-miR5303-FBA41 regulatory module enhances tomato resistance to P. infestans by orchestrating multiple defense pathways, offering valuable insights for crop improvement and disease management strategies.