JMJ27-mediated histone H3K9 demethylation positively regulates drought-stress responses in Arabidopsis

Dimethylation of histone H3 at lysine 9 (H3K9me2) is associated with heterochromatinization and transcriptional gene silencing in plants. The activation of sets of genes by drought stress is correlated with reduced H3K9me2 levels, but the role of H3K9 methylation in the regulation of drought-stress responses remains elusive. Here, we show that the Jumonji domain-containing H3K9 demethylase JMJ27 positively regulates drought-stress responses through its histone demethylase activity. RNA-seq analysis identified JMJ27-regulated genes, including positive regulators of drought stress GALACTINOL SYNTHASE 2 (GOLS2) and RESPONSE TO DESICCATION 20 (RD20). Genetic analysis demonstrated that JMJ27 positively regulates drought-stress responses at least partly through GOLS2 and RD20. JMJ27 directly associated with GOLS2 and RD20, and protected these loci from silencing by reducing H3K9me2 levels under normal conditions. REGULATORY PARTICLE NON-ATPASE 1a (RPN1a), a subunit of the 26S proteasome, interacted with JMJ27 and negatively regulated JMJ27 accumulation. Drought stress diminished RPN1a abundance, resulting in increased JMJ27 abundance. The drought stress-promoted occupancy of JMJ27 at GOLS2 and RD20 chromatin may reinforce their transcriptional induction by locally reducing the H3K9me2 levels. These results indicate that the RPN1a-JMJ27 module precisely regulates dynamic H3K9me2 deposition plasticity, ensuring proper adaptation to drought stress in Arabidopsis.