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 (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 of PHYTOCHROME-INTERACTING FACTOR4 (PIF4) and PIF5 to repress their expression, hence PRRs act as transcriptional repressors of the positive growth regulators PIF4 and PIF5 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-PIF transcriptional module in photoperiodic hypocotyl growth. Finally, genetic analyses have demonstrated that PIF4 and PIF5 are epistatic to PRRs in the regulation of photoperiodic hypocotyl growth. Collectively, we propose that, upon perceiving daylength information, PRRs cooperate with EC to directly repress PIF4 and PIF5 transcription together with their posttranslational regulation of PIF activities, thus forming a complex regulatory network to mediate circadian clock-regulated photoperiodic growth.
Highlights
Seedlings of terrestrial flowering plants display diel rhythmic growth upon responding to recurring natural stimuli immediately after protruding from the soil
Since EARLY FLOWERING 3 (ELF3) has been shown to interact with PHYTOCHROME-INTERACTING FACTOR4 (PIF4) to regulate hypocotyl growth independent of Evening Complex (EC) (Nieto et al, 2015), we further examined the genetic relationship between Pseudo Response Regulators (PRRs) and EC by using LUX, a DNA binding protein in EC (Hazen et al, 2005; Nusinow et al, 2011)
PIF4 and PIF5 have been characterized as potential targets of PRR5 and
Summary
Seedlings of terrestrial flowering plants display diel rhythmic growth upon responding to recurring natural stimuli immediately after protruding from the soil. Photoperiod information, which reflects seasonal changes, can be processed by circadian clock-dependent mechanisms to shape the gene expression pattern, with an acrophase at a specific time of the day, to modulate a wide range of plant growth and developmental processes, including flowering time (Yanovsky and Kay, 2002; Valverde et al, 2004; Sawa et al, 2007; Sawa and Kay, 2011; Andres and Coupland, 2012; Lee et al, 2017). The length of the hypocotyl is reversely associated with daylength, which has long been considered as a coordinative mechanism between the circadian clock and daily photoreception (Nozue et al, 2007; Niwa et al, 2009; Nomoto et al, 2012). The regulatory network underlying this coordinative mechanism is largely unknown
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