MdZFP7 integrates JA and GA signals via interaction with MdJAZ2 and MdRGL3a in regulating anthocyanin biosynthesis and undergoes degradation by the E3 ubiquitin ligase MdBRG3.

Abstract

Jasmonic acid (JA) and gibberellin (GA) coordinate many aspects of plant growth and development, including anthocyanin biosynthesis. However, the crossover points of JA and GA signals and the pathways through which they interact to regulate anthocyanin biosynthesis are poorly understood. Here, we investigated the molecular mechanism by which the zinc finger protein (ZFP) transcription factor Malus domestica ZFP7 (MdZFP7) regulates anthocyanin biosynthesis by integrating JA and GA signals at the transcriptional and post-translational levels. MdZFP7 is a positive regulator of anthocyanin biosynthesis, which fulfills its role by directly activating the expression of MdMYB1 and enhancing the transcriptional activation of MdWRKY6 on the target genes MdDFR and MdUF3GT. MdZFP7 integrates JA and GA signals by interacting with the JA repressor apple JASMONATE ZIM-DOMAIN2 (MdJAZ2) and the GA repressor apple REPRESSOR-of-ga1-3-like 3a (MdRGL3a). MdJAZ2 weakens the transcriptional activation of MdMYB1 by MdZFP7 and disrupts the MdZFP7-MdWRKY6 interaction, thereby reducing the anthocyanin biosynthesis promoted by MdZFP7. MdRGL3a contributes to the stimulation of anthocyanin biosynthesis by MdZFP7 by sequestering MdJAZ2 from the MdJAZ2-MdZFP7 complex. The E3 ubiquitin ligase apple BOI-related E3 ubiquitin-protein ligase 3 (MdBRG3), which is antagonistically regulated by JA and GA, targets the ubiquitination degradation of MdZFP7. The MdBRG3-MdZFP7 module moves the crosstalk of JA and GA signals from the realm of transcriptional regulation and into the protein post-translational modification. In conclusion, this study not only elucidates the node-role of MdZFP7 in the integration of JA and GA signals, but also describes the transcriptional and post-translational regulatory network of anthocyanin biosynthesis with MdZFP7 as the hub.