Phosphorylation-Coupled Proteolysis of the Transcription Factor MYC2 Is Important for Jasmonate-Signaled Plant Immunity

Abstract

As a master regulator of jasmonic acid (JA)–signaled plant immune responses, the basic helix-loop-helix (bHLH) Leu zipper transcription factor MYC2 differentially regulates different subsets of JA–responsive genes through distinct mechanisms. However, how MYC2 itself is regulated at the protein level remains unknown. Here, we show that proteolysis of MYC2 plays a positive role in regulating the transcription of its target genes. We discovered a 12-amino-acid element in the transcription activation domain (TAD) of MYC2 that is required for both the proteolysis and the transcriptional activity of MYC2. Interestingly, MYC2 phosphorylation at residue Thr328, which facilitates its turnover, is also required for the MYC2 function to regulate gene transcription. Together, these results reveal that phosphorylation-coupled turnover of MYC2 stimulates its transcription activity. Our results exemplify that, as with animals, plants employ an “activation by destruction” mechanism to fine-tune their transcriptome to adapt to their ever-changing environment.

Author Summary

The plant hormone jasmonic acid (JA) regulates a wide range of plant immune responses involving genome-wide transcriptional reprogramming that are regulated by the basic helix-loop-helix (bHLH) Leu zipper transcription factor MYC2. As a master regulator of JA signaling, MYC2 differentially regulates the transcription of different branches of JA–responsive genes through distinct molecular mechanisms. Here, we provide evidence that phosphorylation-dependent turnover of MYC2 is coupled with its function. We show that, during JA response, high accumulation of the MYC2 protein correlates with peaked expression of early wound-responsive genes that are positively regulated by MYC2, whereas low accumulation of the MYC2 protein correlates with peaked expression of late pathogen-responsive genes that are negatively regulated by MYC2. We discovered a 12-amino-acid element in the transcription activation domain of MYC2 that is required for both the proteolysis and the transcriptional activity of MYC2. Interestingly, MYC2 phosphorylation at residue Thr328, which facilitates its turnover, is also important for the MYC2 function to regulate transcription. Together, these results reveal that phosphorylation and turnover of MYC2 are tightly linked with its function to regulate the transcription of JA–responsive genes. Our results exemplify that plants employ proteolysis-coupled transcription as mechanism to fine-tune their responses to versatile stresses.