The SnRK1-JMJ15-CRF6 module integrates energy and mitochondrial signaling to balance growth and the oxidative stress response in Arabidopsis.

Mitochondria support plant growth and adaptation via energy production and signaling pathways. However, how mitochondria control the transition between growth and stress response is largely unknown in plants. Using molecular approaches, we identified the histone H3K4me3 demethylase JMJ15 and the transcription factor CRF6 as targets of SnRK1 in Arabidopsis. By analyzing antimycin A (AA)-triggered mitochondrial stress, we explored how SnRK1, JMJ15, and CRF6 form a regulatory module that gauges mitochondrial status to balance growth and the oxidative stress response. SnRK1a1, a catalytic α-subunit of SnRK1, phosphorylates and destabilizes JMJ15 to inhibit its H3K4me3 demethylase activity. While SnRK1a1 does not phosphorylate CRF6, it promotes its degradation via the proteasome pathway. CRF6 interacts with JMJ15 and prevents its SnRK1a1 phosphorylation-dependent degradation, forming an antagonistic feedback loop. SnRK1a1, JMJ15, and CRF6 are required for transcriptional reprogramming in response to AA stress. The transcriptome profiles of jmj15 and crf6 mutants were highly correlated with those of plants overexpressing SnRK1a1 under both normal and AA stress conditions. Genetic analysis revealed that CRF6 acts downstream of SnRK1 and JMJ15. Our findings identify the SnRK1-JMJ15-CRF6 module that integrates energy and mitochondrial signaling for the growth-defense trade-off, highlighting an epigenetic mechanism underlying mitonuclear communication.