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Mitogen-activated protein kinase cascades are important signaling modules that convert environmental stimuli into cellular responses. We show that MPK3, MPK4, and MPK6 are rapidly activated after cold treatment. The mpk3 and mpk6 mutants display increased expression of CBF genes and enhanced freezing tolerance, whereas constitutive activation of the MKK4/5-MPK3/6 cascade in plants causes reduced expression of CBF genes and hypersensitivity to freezing, suggesting that the MKK4/5-MPK3/6 cascade negatively regulates the cold response. MPK3 and MPK6 can phosphorylate ICE1, a basic-helix-loop-helix transcription factor that regulates the expression of CBF genes, and the phosphorylation promotes the degradation of ICE1. Interestingly, the MEKK1-MKK2-MPK4 pathway constitutively suppresses MPK3 and MPK6 activities and has a positive role in the cold response. Furthermore, the MAPKKK YDA and two calcium/calmodulin-regulated receptor-like kinases, CRLK1 and CRLK2, negatively modulate the cold activation of MPK3/6. Our results uncover important roles of MAPK cascades in the regulation of plant cold response.
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•The MKK4/5-MPK3/6 cascade negatively regulates freezing tolerance•The MEKK1-MKK2-MPK4 cascade positively regulates freezing tolerance•MPK3/6-mediated phosphorylation of ICE1 promotes ICE1 degradation•CRLK1 and CRLK2 suppress the cold activation of MPK3/6
ICE1 is a central regulator of the plant cold response, and its levels are tightly controlled. Zhao et al. show that cold-activated MPK3 and MPK6 phosphorylate ICE1 and promote its degradation, thus negatively regulating the cold response, whereas MPK4 positively regulates the cold response by constitutively suppressing MPK3 and MPK6 activity.