Circadian waves of transcriptional repression shape PIF-regulated photoperiod-responsive growth in arabidopsis

Guiomar Martín, Arnau Rovira, Nil Veciana, Judit Soy, Gabriela Toledo-Ortiz, Charlotte M M Gommers, Marc Boix, Rossana Henriques, Eugenio G Minguet, David Alabadí, Karen J Halliday, Pablo Leivar, Elena Monte

Research output: Contribution to journalArticlepeer-review

Abstract

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 [1-6]. 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 [7-10], 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.

Original languageEnglish
Article number29337078
Pages (from-to)311-318.e5
Number of pages14
JournalCurrent biology : CB
Volume28
Issue number2
Early online date11 Jan 2018
DOIs
Publication statusPublished - 22 Jan 2018

Keywords

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

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