A SnRK1-JMJ15-CRF6 coregulatory module gages mitochondrial functional status to mitigate growth-defense trade-off in Arabidopsis

Mitochondrion is a signaling organelle sensing environmental changes and integrating cellular responses via retrograde signalling. However, it is still largely unknown how mitochondria help plants cope with adversity while it powers plant growth. In this work, we identify two new targets of plant SNF1-Related Kinase1 (SnRK1), namely histone H3K4me3 demethylase JMJ15 and transcription factor CRF6. We show that JMJ15 and CRF6 are required for reprograming transcription in response to Antimycin A (AA)-induced mitochondrial stress. A functional module of JMJ15 and CRF6 with SnRK1 that measures mitochondrial status is supported by the AA-promoted nuclear translocation of SnRK1a, a-subunit of SnRK1 under mitochondrial stress, and the physical interaction of SnRK1a with JMJ15 and CRF6, and high correlation of transcriptome changes resulted from the genetic inactivation of JMJ15 and CRF6 with the ones from the plant overexpressing SnRK1a under normal and AA stress conditions. We show that SnRK1a phosphorylates and destabilize JMJ15 to inhibit its H3K27me3 demethylase activity. While SnRK1a does not phosphorylated CRF6, it promotes CRF6 degradation via proteasome pathway. CRF6 interacts with JMJ15, and prevents JMJ15 from phosphorylation dependent degradation, offering a feedback loop to antagonize the action of SnRK1a. Our findings indicate a new mechanism in which a histone demethylase mediated epigenetic regulation and a transcription factor govern cytokine and oxidative stress signalling are implicated in SnRK1-integrated transcriptional network to mitigate growth-defense trade-offs under mitochondrial dysfunction. Overall design: mRNA profiles of 10-day old WT, snrk1a, jmj15, crf6 and SnRK1a overexpression plants were generated by deep sequencing, in triplicate.