C-terminal domains of histone demethylase JMJ14 interact with a pair of NAC transcription factors to mediate specific chromatin association

Jumonji C (JmjC) domain-containing protein 14 (JMJ14) is an H3K4-specific histone demethylase that has important roles in RNA-mediated gene silencing and flowering time regulation in Arabidopsis. However, how JMJ14 is recruited to its target genes remains unclear. Here, we show that the C-terminal FYRN (F/Y-rich N terminus) and FYRC (F/Y-rich C terminus) domains of JMJ14 are required for RNA silencing and flowering time regulation. Chromatin binding of JMJ14 is lost upon deletion of its FYRN and FYRC domains, and H3K4me3 is increased. FYRN and FYRC domains interact with a pair of NAC (NAM, ATAF, CUC) domain-containing transcription factors, NAC050 and NAC052. Genome-wide chromatin immunoprecipitation analysis revealed that JMJ14 and NAC050/052 share a set of common target genes with CTTGNNNNNCAAG consensus sequences. Mutations in either NAC052 or NAC050 impair RNA-mediated gene silencing. Together, our findings demonstrate an important role of FYRN and FYRC domains in targeting JMJ14 through direct interaction with NAC050/052 proteins, which reveals a novel mechanism of histone demethylase recruitment.