The PRR–EC complex and SWR1 chromatin remodeling complex function cooperatively to repress nighttime hypocotyl elongation by modulating PIF4 expression in Arabidopsis

The circadian clock entrained by environmental light–dark cycles enables plants to fine-tune diurnal growth and developmental responses. Here, we show that physical interactions among evening clock components, including PSEUDO-RESPONSE REGULATOR 5 (PRR5), TIMING OF CAB EXPRESSION 1 (TOC1), and the Evening Complex (EC) component EARLY FLOWERING 3 (ELF3), define a diurnal repressive chromatin structure specifically at the PHYTOCHROME-INTERACTING FACTOR 4 (PIF4) locus in Arabidopsis. These three clock components act interdependently as well as independently to repress nighttime hypocotyl elongation, as hypocotyl elongation rate dramatically increased specifically at nighttime in the prr5-1 toc1-21 elf3-1 mutant, concomitantly with a substantial increase in PIF4 expression. Transcriptional repression of PIF4 by ELF3, PRR5, and TOC1 is mediated by the SWI2/SNF2-RELATED (SWR1) chromatin remodeling complex, which incorporates histone H2A.Z at the PIF4 locus, facilitating robust epigenetic suppression of PIF4 during the evening. Overall, these findings demonstrate that the PRR–EC–SWR1 complex represses hypocotyl elongation at night through a distinctive chromatin domain covering PIF4 chromatin. This study reports that the core circadian clock components PRR5, TOC1, and ELF3 interact with each other and cooperatively regulate PIF4 expression, and the PRR–EC complex diurnally recruits the SWR1 complex to PIF4 chromatin to repress its expression in the evening.