SlTOR negatively regulates cold stress responses

Plants often face a trade-off between growing and surviving under stress. In this study, researchers uncovered how the target of rapamycin (TOR) kinase in tomatoes plays a central role in navigating this balance. They found that inhibiting (Solanum lycopersicum) TOR (SlTOR) not only suppressed growth pathways but also activated cold-responsive genes and boosted the accumulation of key metabolites—salicylic acid (SA) and putrescine (Put)—that enhance cold tolerance. A downstream protein, SlPGH1, was identified as a crucial mediator linking TOR activity to cold-induced gene expression and metabolic changes. This discovery offers a comprehensive mechanism for how TOR fine-tunes amino acid-derived metabolism to help tomato plants survive chilling temperatures.

Plants continually adjust their growth and defense responses to survive in challenging environments. Under cold stress, this balance becomes especially critical, as resources must be redirected from growth to survival. The target of rapamycin (TOR) kinase, a well-known regulator of growth and metabolism in eukaryotes, has recently been implicated in plant stress responses. Although prior research suggested that TOR might influence cold tolerance, its exact role and mechanism remained unclear. Tomato, a heat-loving crop, is highly vulnerable to chilling temperatures, making it an ideal model to study this trade-off. Due to these challenges, a deeper investigation into how TOR controls plant cold responses was urgently needed.

A research team from Shanghai Jiao Tong University has published a study (DOI: 10.1093/hr/uhae253) on September 5, 2024, in Horticulture Research, which sheds light on the molecular mechanisms through which TOR kinase regulates cold tolerance in tomato plants. By combining transcriptomic, metabolomic, and genetic approaches, the researchers demonstrated how (Solanum lycopersicum) TOR (SlTOR) inhibition not only enhanced cold resistance but also orchestrated a metabolic shift toward protective compounds like salicylic acid (SA) and putrescine (Put). The findings reveal a previously uncharacterized signaling axis—SlTOR–SlPGH1–SlCBF1—that bridges growth suppression and cold defense activation.

To uncover how TOR balances growth and stress responses, researchers generated TOR-silenced tomato plants and treated them with specific TOR inhibitors (Torin2 and AZD8055). Inactivation of SlTOR led to significant root growth arrest but also triggered the expression of cold-responsive genes such as SlCBF1, SlCAMTA3, and SlZAT10. Under cold conditions (4°C), TOR inhibition enhanced cold tolerance, as evidenced by reduced electrolyte leakage and lower levels of reactive oxygen species. Widely targeted metabolomics profiling revealed that SlTOR suppression during cold stress induced a major shift in amino acid metabolism, diverting metabolic flux toward the synthesis of cryoprotective compounds including SA, Put, and flavonoids. A key finding was the identification of SlPGH1 as a direct TOR substrate. TOR phosphorylation of SlPGH1 influences its regulation of CBF1, a master cold-responsive transcription factor. Virus-induced gene silencing (VIGS) further validated the role of SlPGH1, ICS1, ADC1, and ADC2 in mediating TOR-dependent cold tolerance. This comprehensive analysis demonstrates that TOR actively orchestrates transcriptome and metabolome reprogramming under stress, coordinating growth repression with enhanced defense.

“This study provides a mechanistic framework for how plants navigate the growth-defense dilemma,” said Dr. Liwen Fu, the corresponding author. “By identifying the TOR–PGH1–CBF1 signaling cascade, we revealed how a single kinase can fine-tune transcriptional and metabolic networks to enhance survival under cold stress. Our findings also highlight the significance of amino acid-derived metabolites, especially SA and Put, in fortifying stress resilience. This discovery opens up new avenues for breeding or engineering climate-resilient crops.”

Understanding how TOR modulates cold tolerance has far-reaching implications for agriculture, particularly for thermophilic crops like tomato that are sensitive to climate-induced cold snaps. The discovery of TOR's role in rewiring amino acid metabolism suggests potential targets for genetic manipulation or chemical priming to improve crop resilience. By manipulating the TOR–PGH1–CBF1 axis or enhancing SA and Put production, researchers may be able to develop tomato varieties better suited for cooler climates or extreme weather. More broadly, this study contributes to the foundational knowledge required for balancing yield and stress resistance in future crop improvement strategies.

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References

DOI

10.1093/hr/uhae253

Original Source URL

https://doi.org/10.1093/hr/uhae253

Funding information

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.).

About Horticulture Research

Horticulture Research is an open access journal of Nanjing Agricultural University and ranked number one in the Horticulture category of the Journal Citation Reports ™ from Clarivate, 2023. The journal is committed to publishing original research articles, reviews, perspectives, comments, correspondence articles and letters to the editor related to all major horticultural plants and disciplines, including biotechnology, breeding, cellular and molecular biology, evolution, genetics, inter-species interactions, physiology, and the origination and domestication of crops.