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Integrative modeling of cold and light signaling in tomato: unraveling the transcriptional network governing cold
Jian-Ping Tao1,2, Ting Huang1,3, Zhi-Hang Hu1
1College of Horticulture, State Key Laboratory of Crop Genetics & Germplasm Enhancement and Utilization, Key Laboratory of Horticultural Crop Biology and Germplasm Creation in East China of the Ministry of Agriculture and Rural Affairs, Nanjing Agricultural University, Nanjing, Jiangsu 210095, China.
Abstract:
The integration of light and cold signaling is critical for cold acclimation in plants, but the regulatory complexity of the underlying transcriptional network remains poorly understood. To systematically dissect this interplay in tomato (Solanum lycopersicum), we constructed a computational model that merges the core cold-responsive inducer of CBF expression 1 (ICE1)-C-repeat binding factor (CBF)-cold regulated factors (COR) pathway with light-sensitive modules, including the constitutive photomorphogenic 1 (COP1)-elongated hypocotyl 5 (HY5)-MYB domain protein 15 (MYB15) cascade and the phytochrome-phytochrome interacting factor 4 (PIF4)-GA-INSENSITIVE 4 (GIA4) regulatory axis. Simulations successfully reproduced the experimentally observed gene expression dynamics across different photoperiods and revealed that phytochrome activity is co-modulated by both light quality and temperature. Our model predicts that a low red/far-red ratio enhances the expression of CBF, whereas cold treatment stabilizes phyA and phyB proteins, jointly promoting cold tolerance. Additionally, the PIF4-GAI4 negative feedback loop is shown to generate sustained oscillations in SlPIF4's expression, and the cold-responsive gene SlCOR413 is predicted to exhibit low-temperature-induced oscillatory behavior. This integrative framework provides a systems-level tool for dissecting light-cold crosstalk and offers a basis for rationally engineering cold tolerance in horticultural crops through targeted modulation of transcriptional networks.
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