Plasma Membrane CRPK1-Mediated Phosphorylation of 14-3-3 Proteins Induces Their Nuclear Import to Fine-Tune CBF Signaling during Cold Response

• Published in: Molecular cell Vol. 66; no. 1; pp. 117 - 128.e5
• Main Authors: Liu, Ziyan, Jia, Yuxin, Ding, Yanglin, Shi, Yiting, Li, Zhen, Guo, Yan, Gong, Zhizhong, Yang, Shuhua
• Format: Journal Article
• Language: English
• Published: United States Elsevier Inc 06.04.2017
• Subjects: 14-3-3 proteins; 14-3-3 Proteins - genetics; 14-3-3 Proteins - metabolism; Active Transport, Cell Nucleus; Adaptation, Physiological; Arabidopsis; Arabidopsis - enzymology; Arabidopsis - genetics; Arabidopsis Proteins - genetics; Arabidopsis Proteins - metabolism; CBF proteins; Cell Membrane - enzymology; Cell Nucleus - enzymology; cold stress; Cold Temperature; cold tolerance; Cold-Shock Response; cytosol; Enzyme Activation; freezing; gene overexpression; Genotype; Membrane Fluidity; membrane proteins; mutants; Mutation; Phenotype; Phosphorylation; physiological transport; Plants, Genetically Modified; plasma membrane; Proteasome Endopeptidase Complex - metabolism; protein kinase CRPK1; protein kinases; Protein Kinases - genetics; Protein Kinases - metabolism; Protein Stability; Protein-Serine-Threonine Kinases - genetics; Protein-Serine-Threonine Kinases - metabolism; Proteolysis; Signal Transduction; Thermosensing; Time Factors; Transcription Factors - genetics; Transcription Factors - metabolism; transgenic plants; protein kinase CRPK1; 14-3-3 proteins; cold stress; CBF proteins; Arabidopsis; phosphorylation
• ISSN: 1097-2765; 1097-4164; 1097-4164
• DOI: 10.1016/j.molcel.2017.02.016

In plant cells, changes in fluidity of the plasma membrane may serve as the primary sensor of cold stress; however, the precise mechanism and how the cell transduces and fine-tunes cold signals remain elusive. Here we show that the cold-activated plasma membrane protein cold-responsive protein kinase 1 (CRPK1) phosphorylates 14-3-3 proteins. The phosphorylated 14-3-3 proteins shuttle from the cytosol to the nucleus, where they interact with and destabilize the key cold-responsive C-repeat-binding factor (CBF) proteins. Consistent with this, the crpk1 and 14-3-3κλ mutants show enhanced freezing tolerance, and transgenic plants overexpressing 14-3-3λ show reduced freezing tolerance. Further study shows that CRPK1 is essential for the nuclear translocation of 14-3-3 proteins and for 14-3-3 function in freezing tolerance. Thus, our study reveals that the CRPK1-14-3-3 module transduces the cold signal from the plasma membrane to the nucleus to modulate CBF stability, which ensures a faithfully adjusted response to cold stress of plants. [Display omitted] •Cold activates the plasma membrane-localized protein kinase CRPK1•CRPK1 interacts with and phosphorylates 14-3-3 proteins•Phosphorylated 14-3-3 proteins translocate from the cytosol to the nucleus•In the nucleus, 14-3-3 proteins interact with CBFs and promote their degradation How the plasma membrane senses and transduces cold signals remains unknown. Liu et al. demonstrate that the cold-activated plasma membrane CRPK1 phosphorylates 14-3-3 proteins, which are imported from the cytosol to the nucleus and interact with CBF proteins to promote their destabilization, thus fine-tuning CBF-dependent cold signaling.