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

Abstract

The target of rapamycin (TOR) kinase is a central signaling hub that plays a crucial role in precisely orchestrating plant growth, development, and 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 SlTOR inhibition transcriptionally primes cold stress responses, consequently enhancing tomato cold tolerance. A widely targeted metabolomics analysis revealed the disruption of amino acid metabolism homeostasis under cold stress upon SlTOR inhibition, which led to the accumulation of two important cryoprotective metabolites: salicylic acid (SA) and putrescine (Put). Next, we discovered SlPGH1 (2-PHOSPHO-D-GLYCERATE HYDRO-LYASE) as a direct substrate of SlTOR. Inhibiting SlTOR led to increased SlCBF1 (C-REPEAT-BINDING FACTOR 1) expression via SlPGH1, potentially triggering the activation of cold-responsive genes and subsequent metabolic alterations. 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.