Plasma Membrane CRPK1-Mediated Phosphorylation of 14-3-3 Proteins Induces Their Nuclear Import to Fine-Tune CBF Signaling during Cold Response.
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.
State Key Laboratory of Plant Physiology and Biochemistry, College of Biological Sciences, China Agricultural University, Beijing 100193, China.
Ziyan
Z
Liu
State Key Laboratory of Plant Physiology and Biochemistry, College of Biological Sciences, China Agricultural University, Beijing 100193, China.
Yuxin
Y
Jia
State Key Laboratory of Plant Physiology and Biochemistry, College of Biological Sciences, China Agricultural University, Beijing 100193, China.
Yanglin
Y
Ding
State Key Laboratory of Plant Physiology and Biochemistry, College of Biological Sciences, China Agricultural University, Beijing 100193, China.
Yiting
Y
Shi
State Key Laboratory of Plant Physiology and Biochemistry, College of Biological Sciences, China Agricultural University, Beijing 100193, China.
Zhen
Z
Li
State Key Laboratory of Plant Physiology and Biochemistry, College of Biological Sciences, China Agricultural University, Beijing 100193, China.
Yan
Y
Guo
State Key Laboratory of Plant Physiology and Biochemistry, College of Biological Sciences, China Agricultural University, Beijing 100193, China.
Zhizhong
Z
Gong
State Key Laboratory of Plant Physiology and Biochemistry, College of Biological Sciences, China Agricultural University, Beijing 100193, China. Electronic address: yangshuhua@cau.edu.cn.
Shuhua
S
Yang
D048948:14-3-3 Proteins / Q000235:genetics / Q000378:metabolism*; D021581:Active Transport, Cell Nucleus; D000222:Adaptation, Physiological; D017360:Arabidopsis / Q000201:enzymology* / Q000235:genetics; D029681:Arabidopsis Proteins / Q000235:genetics / Q000378:metabolism*; D002462:Cell Membrane / Q000201:enzymology*; D002467:Cell Nucleus / Q000201:enzymology*; D003080:Cold Temperature; D058639:Cold-Shock Response; D004789:Enzyme Activation; D005838:Genotype; D008560:Membrane Fluidity; D009154:Mutation; D010641:Phenotype; D010766:Phosphorylation; D030821:Plants, Genetically Modified; D046988:Proteasome Endopeptidase Complex / Q000378:metabolism; D011494:Protein Kinases / Q000235:genetics / Q000378:metabolism*; D017346:Protein Serine-Threonine Kinases / Q000235:genetics / Q000378:metabolism*; D055550:Protein Stability; D059748:Proteolysis; D015398:Signal Transduction; D013697:Thermosensing; D013997:Time Factors; D014157:Transcription Factors / Q000235:genetics / Q000378:metabolism*
D048948:14-3-3 Proteins; D029681:Arabidopsis Proteins; D014157:Transcription Factors; D011494:Protein Kinases; C000622384:CRPK1 protein, Arabidopsis; D017346:Protein Serine-Threonine Kinases; D046988:Proteasome Endopeptidase Complex; C061553:ATP dependent 26S protease
14-3-3 proteins; Arabidopsis; CBF proteins; cold stress; phosphorylation; protein kinase CRPK1