Apple SINA E3 ligase MdSINA3 negatively mediates JA-triggered leaf senescence by ubiquitinating and degrading the MdBBX37 protein.

Jasmonic acid (JA) induces chlorophyll degradation and leaf senescence. B-box (BBX) proteins play important roles in the modulation of leaf senescence, but the molecular mechanism of BBX protein-mediated leaf senescence remains to be further studied. Here, we identified the BBX protein MdBBX37 as a positive regulator of JA-induced leaf senescence in Malus domestica (apple). Further studies showed that MdBBX37 interacted with the senescence regulatory protein MdbHLH93 to enhance its transcriptional activation on the senescence-associated gene MdSAG18, thereby promoting leaf senescence. Moreover, the JA signaling repressor MdJAZ2 interacted with MdBBX37 and interfered with the interaction between MdBBX37 and MdbHLH93, thereby negatively mediating MdBBX37-promoted leaf senescence. In addition, the E3 ubiquitin ligase MdSINA3 delayed MdBBX37-promoted leaf senescence through targeting MdBBX37 for degradation. The MdJAZ2-MdBBX37-MdbHLH93-MdSAG18 and MdSINA3-MdBBX37 modules realized the precise modulation of JA on leaf senescence. In parallel, our data demonstrate that MdBBX37 was involved in abscisic acid (ABA)- and ethylene-mediated leaf senescence through interacting with the ABA signaling regulatory protein MdABI5 and ethylene signaling regulatory protein MdEIL1, respectively. Taken together, our results not only reveal the role of MdBBX37 as an integration node in JA-, ABA- and ethylene-mediated leaf senescence, but also provide new insights into the post-translational modification of BBX proteins.