CAS1-synthesized β-Caryophyllene enhances broad-spectrum stress resistance in tomatoes

Plants have evolved a variety of regulatory mechanisms to adapt to changing environment conditions. Secondary metabolites play a crucial role in these adaptive processes. However, little is known about whether specific secondary metabolites confer broad-spectrum resistance to various biotic and abiotic stresses. In this study, we compared the cultivated tomato Solanum lycopersicum L. Ailsa Craig (AC) with the wild tomato Solanum habrochaites S.Knapp & D.M.Spooner LA1777. We found that wild tomato LA1777 exhibited stronger resistance than cultivated tomato AC under cold, drought, salt stresses, and attack by the insect Helicoverpa armigera. Comparative metabolomic analysis of cultivated tomato AC and wild tomato LA1777 revealed significantly higher levels of terpenoid compounds, particularly sesquiterpenes in wild tomato LA1777. Transcriptomic analysis of the terpenoid synthase gene family, combined with virus-induced gene silencing, identified β-Caryophyllene synthase 1 (ShCAS1) as essential for β-Caryophyllene production in wild tomato LA1777 under cold stress. Silencing ShCAS1 compromised the plant's resistance to cold, drought, salt stresses and H. armigera attack in wild tomato LA1777, while exogenous application of β-Caryophyllene enhanced resistance to these stresses in cultivated tomato AC. These findings underscore the significant role of ShCAS1-synthesized β-Caryophyllene in conferring broad-spectrum resistance in tomatoes, suggesting that this compound could be a key target for breeding or biotechnological approaches aimed at improving the resilience of crops to diverse environmental challenges.