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 1) 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.

Acknowledgements

This study was supported by the National Natural Science Foundation of China (grant no. 32170308 to L.F.) and the funding from Shanghai Jiao Tong University (grant no. WH220415006 to L.F.). The authors thank Dr Ruohe Yin (Shanghai Jiao Tong University, Shanghai, China) for the tomato seeds, and Prof. Yan Xiong (Fujian Agriculture and Forestry University, Fuzhou, China) for their critical comments and suggestions.

Author contributions

Z.L. and L.F. planned and designed the research. Z.L., L.Y., Y.W., and L.F. performed experiments and analyzed data. Z.L. and L.F. wrote the manuscript. R.Z. and S.Y. participated in the experimental design and manuscript discussion and revision. All authors contributed with inputs and revisions. Z.L. and L.Y. contributed equally to this work.

Data availability statement

The data underlying this article are available in the article and in its online supplementary material.

Conflict of interests

The authors declare no competing interests.

Supplementary information

Supplementary data is available at Horticulture Research online.

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