Molecular convergence of clock and photosensory pathways through PIF3–TOC1 interaction and co-occupancy of target promoters

Abstract

A mechanism for integrating light perception and the endogenous circadian clock is central to a plant's capacity to coordinate its growth and development with the prevailing daily light/dark cycles. Under short-day (SD) photocycles, hypocotyl elongation is maximal at dawn, being promoted by the collective activity of a quartet of transcription factors, called PIF1, PIF3, PIF4, and PIF5 (phytochromeinteracting factors). PIF protein abundance in SDs oscillates as a balance between synthesis and photoactivated-phytochrome-imposed degradation, with maximum levels accumulating at the end of the long night. Previous evidence shows that elongation under diurnal conditions (as well as in shade) is also subjected to circadian gating. However, the mechanism underlying these phenomena is incompletely understood. Here we show that the PIFs and the core clock component Timing of CAB expression 1 (TOC1) display coincident cobinding to the promoters of predawn-phased, growthrelated genes under SD conditions. TOC1 interacts with the PIFs and represses their transcriptional activation activity, antagonizing PIF-induced growth. Given the dynamics of TOC1 abundance (displaying high postdusk levels that progressively decline during the long night), our data suggest that TOC1 functions to provide a direct output from the core clock that transiently constrains the growth-promoting activity of the accumulating PIFs early postdusk, thereby gating growth to predawn, when conditions for cell elongation are optimal. These findings unveil a previously unrecognized mechanism whereby a core circadian clock output signal converges immediately with the phytochrome photosensory pathway to coregulate directly the activity of the PIF transcription factors positioned at the apex of a transcriptional network that regulates a diversity of downstream morphogenic responses.PIFs | photoperiod | TOC1 | circadian clock | gating of growth G iven the importance of solar energy to plants, they have evolved sophisticated photosensory-response systems to monitor and adapt to the diurnal photoperiod (1). This environmental parameter provides a precise index of the progression of the earth's seasons and the time of the day and thereby a signal that regulates a spectrum of growth and developmental responses (such as elongation growth, flowering, and dormancy) appropriate to the prevailing conditions.The photoreceptors in the phytochrome family (phyA-E in Arabidopsis) are the primary sensors of this signal (2, 3). These chromoproteins regulate two pathways in parallel that converge to control the morphogenic response: (i) the phytochromeinteracting factor (PIF) pathway, whereby the photoactivatedphytochrome molecules bind to and induce the degradation of the PIF proteins (notably the PIF1, PIF3, PIF4, and PIF5 quartet, a subfamily of basic helix-loop-helix transcription factors), thereby altering the expression of the PIF direct-target genes and the cognate downstream transcriptional network (4, 5), and (ii) the circadian clock, whereby the phytochromes entrain t...

PSEUDO RESPONSE REGULATORs stabilize CONSTANS protein to promote flowering in response to day length

“…This elegant system directly couples CO stability and function in photoperiodic flowering to cycling circadian‐clock components, ensuring that CO only binds to and activates FT transcription at specific times during the day dependent on day length. Since CO and PRRs contain similar CCT DNA‐binding domains (Matsushika et al , 2000; Gendron et al , 2012), PRRs might also bind along with CO to the FT promoter and contribute to the control of FT transcription, as was recently shown for the interaction between PRRs and PIF transcription factors on their target genes (Soy et al , 2016; Zhu et al , 2016). Morning FT expression is more pronounced when plants are exposed to shade (Wollenberg et al , 2008), suggesting that specific PRRs might also control this process by coupling a distinct flowering signal to CO protein stability or FT induction in the morning.…”

Phytochromes and Phytochrome Interacting Factors

“…PIF3 also interacts with TOC1, and this interaction optimizes the temporal regulation of diurnal growth of hypocotyl elongation (Soy et al, 2016). Similar to PIF1, PIF3 represses chlorophyll biosynthesis and photosynthesis in etiolated seedlings (Stephenson et al, 2009).…”

Circadian Clock and Photoperiodic Flowering in Arabidopsis: CONSTANS Is a Hub for Signal Integration

“…1). In addition, TOC1 interacts with PHYTOCHROME INTERACTING FACTOR3, which binds to G-box, to repress transcription of their co-target genes (Soy et al, 2016). TOC1-dependent repression is gradually removed toward the end of the night by TOC1 protein degradation controlled by ZTL E3 ubiquitin ligase and its homologs, FKF1 and LKP2 (Más et al, 2003;Baudry et al, 2010; Fig.…”