Long non-coding RNA lncRNA39042 enhances late blight resistance in tomato by modulating its flanking defense genes

Tomato is an essential horticultural and commercial crop, with increasingly Phytophthora infestans encroached, which seriously restrict the quality and productivity. Prior studies have reported that long non-coding RNAs (lncRNAs) play an important role in planta immune response, however, the function of key lncRNAs in response tomato resistant to P. infestans remain to be explored. Here, we identified Sl-lncRNA39042, a 311-bp sense-stranded lncRNA, as a positive regulator of tomato resistance to late blight, regarding that the observation that overexpression of Sl-lncRNA39042 significantly reduced the relative lesion area, whereas its silencing led to a notable increase. Consistent with this, the expression of SlPRs was potentiated in leaves transiently overexpressing Sl-lncRNA39042 but attenuated in Sl-lncRNA39042-silenced leaves upon P. infestans infection. Subsequently, we further found that the expression patterns of SlPI-like and SlPAL-like, two genes located within 100 kb flanking of Sl-lncRNA39042, closely mirrored that of the lncRNA and showed a significant positive correlation. Moreover, both SlPI-like and SlPAL-like were upregulated in leaves transiently overexpressing Sl-lncRNA39042 and downregulated in Sl-lncRNA39042-silenced leaves, suggesting that Sl-lncRNA39042 modulates their expression. Further, we demonstrated that overexpression of either SlPI-like or SlPAL-like significantly enhanced tomato resistance to late blight. Collectively, these results strongly suggest that P. infestans-inducible Sl-lncRNA39042 confers late blight resistance in tomato by activating the expression of SlPI-like and SlPAL-like. These findings expand understanding of the role of lncRNAs in tomato against P. infestans and provide new insights for disease-resistant breeding.