Current Biology
Volume 28, Issue 2, 22 January 2018, Pages 311-318.e5
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Circadian Waves of Transcriptional Repression Shape PIF-Regulated Photoperiod-Responsive Growth in Arabidopsis

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Highlights

  • Circadian waves transcriptionally control the PIF-regulated diurnal gene network

  • The clock components PRR9/7/5/1 sequentially gate PIF-promoted growth from morning onward

  • CDF5 is antagonistically targeted by PRRs and PIFs to restrict growth to dawn

  • CDF5 promotes cell elongation downstream of the PRR/PIF module

Summary

Plants coordinate their growth and development with the environment through integration of circadian clock and photosensory pathways. In Arabidopsis thaliana, rhythmic hypocotyl elongation in short days (SD) is enhanced at dawn by the basic-helix-loop-helix (bHLH) transcription factors PHYTOCHROME-INTERACTING FACTORS (PIFs) directly inducing expression of growth-related genes [1, 2, 3, 4, 5, 6]. PIFs accumulate progressively during the night and are targeted for degradation by active phytochromes in the light, when growth is reduced. Although PIF proteins are also detected during the day hours [7, 8, 9, 10], their growth-promoting activity is inhibited through unknown mechanisms. Recently, the core clock components and transcriptional repressors PSEUDO-RESPONSE REGULATORS PRR9/7/5 [11, 12], negative regulators of hypocotyl elongation [13, 14], were described to associate to G boxes [15], the DNA motifs recognized by the PIFs [16, 17], suggesting that PRR and PIF function might converge antagonistically to regulate growth. Here we report that PRR9/7/5 and PIFs physically interact and bind to the same promoter region of pre-dawn-phased, growth-related genes, and we identify the transcription factor CDF5 [18, 19] as target of this interplay. In SD, CDF5 expression is sequentially repressed from morning to dusk by PRRs and induced pre-dawn by PIFs. Consequently, CDF5 accumulates specifically at dawn, when it induces cell elongation. Our findings provide a framework for recent TIMING OF CAB EXPRESSION 1 (TOC1/PRR1) data [5, 20] and reveal that the long described circadian morning-to-midnight waves of the PRR transcriptional repressors (PRR9, PRR7, PRR5, and TOC1) [21] jointly gate PIF activity to dawn to prevent overgrowth through sequential regulation of common PIF-PRR target genes such as CDF5.

Keywords

plant diurnal growth
hypocotyl elongation
gating of plant responses
phytochrome-interacting factors PIFs
circadian clock
pseudo-response regulators PRRs
TOC1
cycling DOF factor CDF5
transcriptional regulation
Arabidopsis

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