Pseudo Response Regulators Regulate Photoperiodic Hypocotyl Growth by RepressingPIF4/5Transcription(1)([OPEN])

The circadian clock measures and conveys daylength information to control rhythmic hypocotyl growth in photoperiodic conditions to achieve optimal fitness, but it operates through largely unknown mechanisms. Here, we show that Pseudo Response Regulators (PRRs) coordinate with the Evening Complex (EC), a transcriptional repressor complex within the clock core oscillator, to specifically regulate photoperiodic hypocotyl growth in Arabidopsis (Arabidopsis thaliana). Intriguingly, a distinct daylength could shift the expression phase and extend the expression duration of PRRs. Multiple lines of evidence have further demonstrated that PRRs directly bind the promoters ofPHYTOCHROME-INTERACTING FACTOR4(PIF4) andPIF5to repress their expression, hence PRRs act as transcriptional repressors of the positive growth regulatorsPIF4andPIF5. Importantly, mutation or truncation of the TIMING OF CAB EXPRESSION1 (TOC1) DNA binding domain, without compromising its physical interaction with PIFs, still caused long hypocotyl growth under short days, highlighting the essential role of the PRR-PIFtranscriptional module in photoperiodic hypocotyl growth. Finally, genetic analyses have demonstrated thatPIF4andPIF5are epistatic toPRRsin the regulation of photoperiodic hypocotyl growth. Collectively, we propose that, upon perceiving daylength information, PRRs cooperate with EC to directly repressPIF4andPIF5transcription together with their posttranslational regulation of PIF activities, thus forming a complex regulatory network to mediate circadian clock-regulated photoperiodic growth. Pseudo Response Regulator proteins and the Evening Complex transmit daylength information to regulate photoperiodic hypocotyl growth by directly repressing transcription of key growth regulators