Function identification of miR394 in tomato resistance to Phytophthora infestans.

KEY MESSAGE: MiR394 plays a negative role in tomato resistance to late blight. The lncRNA40787 severing as an eTM for miR394 to regulate LCR and exerting functions in tomato resistance. Tomato (Solanum lycopersicum), which was used as model species for studying the mechanism of plant disease defense, is susceptible to multiple pathogens. Non-coding RNA (ncRNA) has a pivotal role in plants response to biological stresses. It has previously been observed that the expression level of miR394 changed significantly after the infection of various pathogens. However, there has been no detailed investigation of the accumulated or suppressed mechanism of miR394. Our previous study predicted three lncRNAs (lncRNA40787, lncRNA27177, and lncRNA42566) that contain miR394 endogenous target mimics (eTM), which may exist as the competitive endogenous RNAs (ceRNAs) of miR394. In our study, the transcription levels of these three lncRNAs were strongly up-regulated in tomato upon infection with P. infestans. In contrast with the three lncRNAs, the accumulation of miR394 was significantly suppressed. Based on the expression pattern, and value of minimum free energy (mfes) that represents the binding ability between lncRNA and miRNA, lncRNA40787 was chosen for further investigation. Results showed that overexpression of lncRNA40787 reduced the expression of miR394 along with decreased lesion area and enhanced disease resistance. Overexpression of miR394, however, decreased the expression of its target gene Leaf Curling Responsiveness (LCR), and suppressed the synthesis components genes of jasmonic acid (JA), depressing the resistance of tomato to P. infestans infection. Taken together, our findings indicated that miR394 can be decoyed by lncRNA40787, and negatively regulated the expression of LCR to enhance tomato susceptibility under P. infestans infection. Our study provided detailed information on the lncRNA40787-miR394-LCR regulatory network and serves as a reference for future research.