Circadian Entrainment in Arabidopsis by the Sugar-Responsive Transcription Factor bZIP63

Alexander Frank, Cleverson C. Matiolli, Américo J.C. Viana, Timothy J. Hearn, Jelena Kusakina, Fiona E. Belbin, David Wells Newman, Aline Yochikawa, Dora L. Cano-Ramirez, Anupama Chembath, Kester Cragg-Barber, Michael J. Haydon, Carlos T. Hotta, Michel Vincentz, Alex A.R. Webb*, Antony N. Dodd

*Corresponding author for this work

Research output: Contribution to journalArticle (Academic Journal)peer-review

35 Citations (Scopus)
366 Downloads (Pure)

Abstract

Synchronization of circadian clocks to the day-night cycle ensures the correct timing of biological events. This entrainment process is essential to ensure that the phase of the circadian oscillator is synchronized with daily events within the environment [1], to permit accurate anticipation of environmental changes [2, 3]. Entrainment in plants requires phase changes in the circadian oscillator, through unidentified pathways, which alter circadian oscillator gene expression in response to light, temperature, and sugars [4–6]. To determine how circadian clocks respond to metabolic rhythms, we investigated the mechanisms by which sugars adjust the circadian phase in Arabidopsis [5]. We focused upon metabolic regulation because interactions occur between circadian oscillators and metabolism in several experimental systems [5, 7–9], but the molecular mechanisms are unidentified. Here, we demonstrate that the transcription factor BASIC LEUCINE ZIPPER63 (bZIP63) regulates the circadian oscillator gene PSEUDO RESPONSE REGULATOR7 (PRR7) to change the circadian phase in response to sugars. We find that SnRK1, a sugar-sensing kinase that regulates bZIP63 activity and circadian period [10–14] is required for sucrose-induced changes in circadian phase. Furthermore, TREHALOSE-6-PHOSPHATE SYNTHASE1 (TPS1), which synthesizes the signaling sugar trehalose-6-phosphate, is required for circadian phase adjustment in response to sucrose. We demonstrate that daily rhythms of energy availability can entrain the circadian oscillator through the function of bZIP63, TPS1, and the KIN10 subunit of the SnRK1 energy sensor. This identifies a molecular mechanism that adjusts the circadian phase in response to sugars. Frank et al. identify mechanisms by which the Arabidopsis circadian clock entrains to sugars. Metabolic adjustment of circadian phase involves trehalose-6-phosphate, SnRK1 subunit KIN10 and the transcription factor bZIP63. bZIP63 regulates the circadian clock gene PSEUDORESPONSE REGULATOR7. This sets the circadian phase in light and dark cycles.

Original languageEnglish
Pages (from-to)2597-2606.e6
Number of pages16
JournalCurrent Biology
Volume28
Issue number16
Early online date2 Aug 2018
DOIs
Publication statusPublished - 20 Aug 2018

Keywords

  • Circadian rhythms
  • signal transduction
  • metabolism

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