Climate change has intensified the frequency of sudden low-temperature events, posing serious risks to crops such as tomato, a species originating from tropical and subtropical regions that is highly sensitive to chilling. Plants respond by activating cold-responsive genes and accumulating metabolites that minimize cellular damage, but these protective strategies often come at the cost of reduced growth and yield. Previous studies hinted that The target of rapamycin (TOR) signaling networks regulate both development and stress responses, yet the precise mechanism governing the trade-off remained poorly understood. Due to these challenges, there is a pressing need to investigate how TOR orchestrates growth and cold tolerance in tomato.
A research team from Shanghai Jiao Tong University has uncovered how target of rapamycin (SlTOR) balances tomato growth and cold tolerance. The study was published (DOI: 10.1093/hr/uhae253) on September 5, 2024 in Horticulture Research. The findings demonstrate that suppressing SlTOR activity primes transcriptional and metabolic responses that enhance resistance to chilling. By linking amino acid metabolism with stress-responsive gene networks, the work provides new mechanistic insights into how crops can be better equipped to endure low-temperature stress.
Using estradiol-inducible RNA interference and chemical inhibitors (Torin2, AZD8055), the researchers silenced SlTOR in tomato seedlings. RNA-seq analysis identified over 2,000 differentially expressed genes, with growth-related pathways suppressed and defense-related pathways enhanced. Notably, cold-responsive genes including SlCAMTA3, SlCBF1, and SlZAT10 were strongly upregulated, confirming SlTOR's role as a negative regulator of chilling responses. Electrolyte leakage and reactive oxygen species assays further showed that SlTOR-suppressed plants sustained less cellular damage under cold stress.
Metabolomics profiling revealed extensive reprogramming: most amino acid biosynthesis pathways were downregulated, while aromatic amino acid derivatives surged. Levels of salicylic acid (SA), Put, and flavonoids increased significantly, compounds already known to function as cryoprotectants. Genetic silencing of biosynthetic enzymes (SlICS1, SlADC1, SlADC2) confirmed the importance of these metabolites, as plants lacking them became susceptible to cold. Mechanistic studies identified SlPGH1, a glycolytic enzyme and direct substrate of SlTOR, which regulates SlCBF1 expression. The SlTOR–SlPGH1–SlCBF1 axis emerged as a key regulatory pathway that couples transcriptome rewiring with metabolite accumulation, thereby enabling tomatoes to survive low temperatures while moderating growth.
“Plants constantly face a trade-off between growing and defending themselves,” said Dr. Liwen Fu, senior author of the study. “Our work shows that TOR is not just a growth promoter but also a switch that can reroute metabolism when stress arises. By uncovering the SlTOR–SlPGH1–SlCBF1 axis, we provide a clearer picture of how tomatoes adapt to chilling. These findings are important because they open the possibility of fine-tuning TOR signaling to protect crops from cold events without severely compromising yield potential.”
This research highlights TOR signaling as a promising target for agricultural innovation. Modulating SlTOR activity could enable breeders and biotechnologists to develop tomato varieties with improved tolerance to cold snaps, reducing crop losses in vulnerable regions. Beyond tomatoes, the mechanism may extend to other crops where TOR orchestrates similar growth–defense trade-offs. By manipulating metabolic fluxes toward protective compounds such as SA, Put, and flavonoids, farmers may gain plants that are both productive and stress-resilient. These insights lay the groundwork for designing climate-ready crops capable of thriving under increasingly unpredictable environmental conditions.
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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.