The evening complex component ELF3 recruits H3K4me3 demethylases to repress PHYTOCHROME INTERACTING FACTOR4 and 5 in Arabidopsis

Abstract In Arabidopsis (Arabidopsis thaliana), light and circadian clock signaling converge on PHYTOCHROME-INTERACTING FACTORS (PIFs) 4 and 5 to produce a daily rhythm of hypocotyl elongation. PIF4 and PIF5 expression is repressed at dusk by the evening complex (EC), consisting of EARLY FLOWERING3 (ELF3), ELF4, and LUX ARRHYTHMO (LUX). Here, we report that ELF3 recruits the JUMONJI (JMJ) H3K4me3 demethylases JMJ17 and JMJ18 to the PIF4 and PIF5 loci in the evening to remove their H3K4me3 marks. The association of JMJ17 and JMJ18 with the 2 genomic loci depends on the EC, and the H3K4me3 marks are enriched in the elf3 and jmj17 jmj18 mutants. Half of the globally differentially expressed genes are overlapping in elf3 and jmj17 jmj18. Cleavage Under Targets and Tagmentation sequencing analysis identified 976 H3K4me3-enriched loci in elf3. Aligning the H3K4me3-enriched loci in elf3 to genes with increased expression in elf3 and jmj17 jmj18 identified 179 and 176 target loci, respectively. Half of the loci are targeted by both ELF3 and JMJ17/JMJ18. This suggests a strong connection between the 2 JMJ proteins and EC function. Our studies reveal that an array of key genes in addition to PIF4 and PIF5 are repressed by the EC through the H3K4me3 demethylation pathway.