Brassinosteroid signaling regulator BIM1 integrates brassinolide and jasmonic acid signaling during cold tolerance in apple

Although brassinolide (BR) and jasmonic acid (JA) play essential roles in the regulation of cold stress responses, the molecular basis of their crosstalk remains elusive. Here, we show a key component of BR signaling in apple (Malus x domestica), BR INSENSITIVE1 (BRI1)-EMS-SUPPRESSOR1 (BES1)-INTERACTING MYC-LIKE PROTEIN1 (MdBIM1), increases cold tolerance by directly activating expression of C-REPEAT BINDING FACTOR1 (MdCBF1) and forming a complex with C-REPEAT BINDING FACTOR2 (MdCBF2) to enhance MdCBF2-activated transcription of cold-responsive genes. Two repressors of JA signaling, JAZMONATE ZIM-DOMAIN1 (MdJAZ1) and JAZMONATE ZIM-DOMAIN2 (MdJAZ2), interact with MdBIM1 to integrate BR and JA signaling under cold stress. MdJAZ1 and MdJAZ2 reduce MdBIM1-promoted cold stress tolerance by attenuating transcriptional activation of MdCBF1 expression by MdBIM1 and interfering with the formation of the MdBIM1-MdCBF2 complex. Furthermore, the E3 ubiquitin ligase ARABIDOPSIS T & Oacute; XICOS en LEVADURA73 (MdATL73) decreases MdBIM1-promoted cold tolerance by targeting MdBIM1 for ubiquitination and degradation. Our results not only reveal crosstalk between BR and JA signaling mediated by a JAZ-BIM1-CBF module but also provide insights into the posttranslational regulatory mechanism of BR signaling. A brassinosteroid signaling regulator may act as a molecular bridge integrating brassinolide and jasmonic acid signaling to regulate cold tolerance via a C-repeat binding factor-dependent pathway.

Automated summary

In apple, a key component of BR signaling, MdBIM1, increases cold tolerance by activating the expression of CBF genes and forming complexes with MdCBF2. The repressors of JA signaling, MdJAZ1 and MdJAZ2, interact with MdBIM1 to integrate BR and JA signaling under cold stress. The E3 ubiquitin ligase MdATL73 targets MdBIM1 for degradation, reducing cold tolerance. This study reveals the crosstalk between BR and JA signaling and provides insights into the posttranslational regulation of BR signaling.