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The ubiquitous lipid-derived molecules N-acylethanolamines (NAEs) have multiple immune functions in mammals, but their roles and mechanisms in plant defense response during changing environment remain largely unclear. Here, we found that exogenous NAE18:0 and NAE18:2 promoted defense against the necrotrophic pathogen Botrytis cinerea but suppressed defense to the hemi-biotrophic pathogen Pseudomonas syringae pv. tomato (Pst) DC3000 in tomato. The knocking-down and overexpression function analysis of the pathogen-responsive NAE synthetic gene PHOSPHOLIPASE Dγ (PLDγ) and hydrolytic gene FATTY ACID AMID HYDROLASE 1 (FAAH1) revealed that the NAE pathway is crucial for plant defense response. Using exogenous applications and SA-abolished NahG plants, we unveiled the antagonistic relationship between NAE and SA in plant defense response. Elevated CO2 and temperature significantly changed the NAE pathway in response to pathogens, while inhibition of the NAE pathway led to the alternation of environment-mediated defense variations against Pst DC3000 in tomato, indicating that NAE pathway is associated with plant defense variations in response to elevated CO2 and temperature. The results herein reveal a new function of NAE in plant defense, and its involvement in environment-mediated defense variation in tomato. These findings shed light on the NAE-based plant defense, which may have relevance to crop disease management in future changing climate.

With global climate change, plants are frequently being exposed to various stresses, such as pathogen attack, drought, and extreme temperatures. Transcription factors (TFs) play crucial roles in numerous plant biological processes; however, the functions of many tomato (Solanum lycopersicum L.) TFs that regulate plant responses to multiple stresses are largely unknown. Here, using an RNA-seq approach, we identified SlNAP1, a NAC TF-encoding gene, which was strongly induced by various stresses. By generating SlNAP1 transgenic lines and evaluating their responses to biotic and abiotic stresses in tomato, we found that SlNAP1-overexpressing plants showed significantly enhanced defense against two widespread bacterial diseases, leaf speck disease, caused by Pseudomonas syringae pv. tomato (Pst) DC3000, and root-borne bacterial wilt disease, caused by Ralstonia solanacearum. In addition, SlNAP1 overexpression dramatically improved drought tolerance in tomato. Although the SlNAP1-overexpressing plants were shorter than the wild-type plants during the early vegetative stage, eventually, their fruit yield increased by 10.7%. Analysis of different hormone contents revealed a reduced level of physiologically active gibberellins (GAs) and an increased level of salicylic acid (SA) and abscisic acid (ABA) in the SlNAP1-overexpressing plants. Moreover, EMSAs and ChIP-qPCR assays showed that SlNAP1 directly activated the transcription of multiple genes involved in GA deactivation and both SA and ABA biosynthesis. Our findings reveal that SlNAP1 is a positive regulator of the tomato defense response against multiple stresses and thus may be a potential breeding target for improving crop yield and stress resistance.