Cold-Induced CBF–PIF3 Interaction Enhances Freezing Tolerance by Stabilizing the phyB Thermosensor in Arabidopsis

• Published in: Molecular plant Vol. 13; no. 6; pp. 894 - 906
• Main Authors: Jiang, Bochen, Shi, Yiting, Peng, Yue, Jia, Yuxin, Yan, Yan, Dong, Xiaojing, Li, Hui, Dong, Jie, Li, Jigang, Gong, Zhizhong, Thomashow, Michael F., Yang, Shuhua
• Format: Journal Article
• Language: English
• Published: England Elsevier Inc 01.06.2020
• Subjects: Adaptation, Physiological - genetics; Arabidopsis; Arabidopsis - genetics; Arabidopsis - physiology; Arabidopsis Proteins - genetics; Arabidopsis Proteins - metabolism; Basic Helix-Loop-Helix Transcription Factors - genetics; Basic Helix-Loop-Helix Transcription Factors - metabolism; CBFs; Freezing; freezing tolerance; Gene Expression Regulation, Plant; phyB; Phytochrome B - metabolism; PIFs; Protein Binding; Protein Stability; Proteolysis; Stress, Physiological; CBFs; PIFs; phyB; Arabidopsis; freezing tolerance
• ISSN: 1674-2052; 1752-9867
• DOI: 10.1016/j.molp.2020.04.006

Growth inhibition and cold-acclimation strategies help plants withstand cold stress, which adversely affects growth and survival. PHYTOCHROME B (phyB) regulates plant growth through perceiving both light and ambient temperature signals. However, the mechanism by which phyB mediates the plant response to cold stress remains elusive. Here, we show that the key transcription factors mediating cold acclimation, C-REPEAT BINDING FACTORs (CBFs), interact with PHYTOCHROME-INTERACTING FACTOR 3 (PIF3) under cold stress, thus attenuating the mutually assured destruction of PIF3–phyB. Cold-stabilized phyB acts downstream of CBFs to positively regulate freezing tolerance by modulating the expression of stress-responsive and growth-related genes. Consistent with this, phyB mutants exhibited a freezing-sensitive phenotype, whereas phyB-overexpression transgenic plants displayed enhanced freezing tolerance. Further analysis showed that the PIF1, PIF4, and PIF5 proteins, all of which negatively regulate plant freezing tolerance, were destabilized by cold stress in a phytochrome-dependent manner. Collectively, our study reveals that CBFs–PIF3–phyB serves as an important regulatory module for modulating plant response to cold stress. This study reveals that the key transcription factors of cold signaling, CBFs, interact with PIF3 to stabilize the thermosensor phyB. Cold stablized phyB promotes the phytochrome-dependent degradation of PIF1, PIF4, and PIF5 and enhances freezing tolerance. Thus, this study unravels an important role for the CBFs–PIF3–phyB module in regulating freezing tolerance in Arabidopsis.