TOR balances plant growth and cold tolerance by orchestrating amino acid-derived metabolism in tomato

The target of rapamycin (TOR) kinase is a central signaling hub that plays a crucial role in precisely orchestrating plant growth and development. It is increasingly evident that TOR also has a significant impact on plant stress responses. This suggests that TOR is intricately involved in maintaining the balance between plant growth and stress responses. Nevertheless, despite the observed effects, the specific mechanisms through which TOR operates in these processes remain obscure. In this study, we investigated how the tomato (Solanum lycopersicum) TOR (SlTOR) affects plant growth and cold responses. We demonstrated that the inhibition of SlTOR transcriptionally primes cold stress responses, consequently enhancing tomato cold tolerance. Furthermore, a widely targeted metabolomics analysis revealed the disruption of amino acid metabolism homeostasis under cold stress upon SlTOR inhibition. This disruption led to the accumulation of two important defense metabolites: salicylic acid (SA) and putrescine (Put). Subsequent gain- and loss-of-function analyses validated the crucial roles of salicylic acid and putrescine in enhancing tomato cold tolerance. Our study provides a mechanistic framework that elucidates how SlTOR modulates amino acid-related metabolism to enhance tomato cold tolerance, which sheds light on the complex interplay between growth and stress responses orchestrated by TOR. Overall design: To investigate the biological function of tomato TOR in the regulation of transcriptional reprogramming. Four biological replicates of 10-day-old tomato seedlings were treated with or without 5 µM Torin2. We then proformed gene expression profiling analysis using data obtained from RNA-seq. Comparative gene expression profiling analysis was further carried out between mock-treated (m) and Torin2-treated (T) tomato seedlings.