Arabidopsis histone H3K4 demethylase JMJ17 functions in dehydration stress response

Summary Under dehydration in plants, antagonistic activities of histone 3 lysine 4 (H3K4) methyltransferase and histone demethylase maintain a dynamic and homeostatic state of gene expression by orientating transcriptional reprogramming toward growth or stress tolerance. However, the histone demethylase that specifically controls histone methylation homeostasis under dehydration stress remains unknown. Here, we document that a histone demethylase, JMJ 17, belonging to the KDM 5/ JARID 1 family, plays crucial roles in response to dehydration stress and abscisic acid ( ABA ) in Arabidopsis thaliana . jmj17 loss‐of‐function mutants displayed dehydration stress tolerance and ABA hypersensitivity in terms of stomatal closure. JMJ 17 specifically demethylated H3K4me1/2/3 via conserved iron‐binding amino acids in vitro and in vivo . Moreover, H3K4 demethylase activity of JMJ 17 was required for dehydration stress response. Systematic combination of genome‐wide chromatin immunoprecipitation coupled with massively parallel DNA sequencing (Ch IP ‐seq) and RNA ‐sequencing ( RNA ‐seq) analyses revealed that a loss‐of‐function mutation in JMJ 17 caused an ectopic increase in genome‐wide H3K4me3 levels and activated a plethora of dehydration stress‐responsive genes. Importantly, JMJ 17 bound directly to the chromatin of OPEN STOMATA 1 ( OST 1 ) and demethylated H3K4me3 for the regulation of OST 1 mRNA abundance, thereby modulating the dehydration stress response. Our results demonstrate a new function of a histone demethylase under dehydration stress in plants.