Pseudo Response Regulators Regulate Photoperiodic Hypocotyl Growth by Repressing <i>PIF4</i>/<i>5</i> Transcription

Abstract

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 (<i>Arabidopsis thaliana</i>). 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 of <i>PHYTOCHROME-INTERACTING FACTOR4</i> (<i>PIF4</i>) and <i>PIF5</i> to repress their expression, hence PRRs act as transcriptional repressors of the positive growth regulators <i>PIF4</i> and <i>PIF5</i> 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<i>-PIF</i> transcriptional module in photoperiodic hypocotyl growth. Finally, genetic analyses have demonstrated that <i>PIF4</i> and <i>PIF5</i> are epistatic to <i>PRRs</i> in the regulation of photoperiodic hypocotyl growth. Collectively, we propose that, upon perceiving daylength information, PRRs cooperate with EC to directly repress <i>PIF4</i> and <i>PIF5</i> transcription together with their posttranslational regulation of PIF activities, thus forming a complex regulatory network to mediate circadian clock-regulated photoperiodic growth.