Apple B-box protein BBX37 regulates jasmonic acid mediated cold tolerance through the JAZ-BBX37-ICE1-CBF pathway and undergoes MIEL1-mediated ubiquitination and degradation.

The plant hormone jasmonic acid (JA) is involved in the cold stress response, and the inducer of CBF expression 1 (ICE1)- C-repeat binding factor (CBF) regulatory cascade plays a key role in the regulation of cold stress tolerance. In this study, we showed that a novel B-box (BBX) protein MdBBX37 positively regulates JA-mediated cold-stress resistance in apple. We found that MdBBX37 bound to the MdCBF1 and MdCBF4 promoters to activate their transcription, and also interacted with MdICE1 to enhance the transcriptional activity of MdICE1 on MdCBF1, thus promoting its cold tolerance. Two JA signaling repressors, MdJAZ1 and MdJAZ2 (JAZ, JAZMONATE ZIM-DOMAIN), interacted with MdBBX37 to repress the transcriptional activity of MdBBX37 on MdCBF1 and MdCBF4, and also interfered with the interaction between MdBBX37 and MdICE1, thus negatively regulating JA-mediated cold tolerance. E3 ligase MdMIEL1 (MIEL1, MYB30-Interacting E3 Ligase1) reduced MdBBX37-improved cold resistance by mediating ubiquitination and degradation of the MdBBX37 protein. The data reveal that MIEL1 and JAZ proteins co-regulate JA-mediated cold stress tolerance through the BBX37-ICE1-CBF module in apple. These results will aid further examination of the post-translational modification of BBX proteins and the regulatory mechanism of JA-mediated cold stress tolerance.