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

Research output: Contribution to journalArticle

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, 5, 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, 8, 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, 11, 12, 13, 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.
Original languageEnglish
Pages (from-to)2597-2606.e6
JournalCurrent Biology
Volume28
Issue number16
Early online date2 Aug 2018
DOIs
Publication statusPublished - 20 Aug 2018

Fingerprint

Arabidopsis
Sugars
Circadian Clocks
Transcription Factors
transcription factors
sugars
Sucrose
trehalose
phosphates
circadian rhythm
Clocks
Phosphotransferases
sucrose
Gene Expression
Light
Temperature
energy
phase transition
Metabolism
Gene expression

Bibliographical note

© 2018 The Authors. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).

Keywords

  • circadian rhythms
  • signal transduction
  • metabolism
  • sugar signaling

Cite this

Frank, A., Matiolli, C. C., Viana, A. J. C., Hearn, T. J., Kusakina, J., Belbin, F. E., ... Dodd, A. N. (2018). Circadian Entrainment in Arabidopsis by the Sugar-Responsive Transcription Factor bZIP63. Current Biology, 28(16), 2597-2606.e6. https://doi.org/10.1016/j.cub.2018.05.092
Frank, Alexander ; Matiolli, Cleverson C ; Viana, Américo J C ; Hearn, Timothy J ; Kusakina, Jelena ; Belbin, Fiona E ; Wells Newman, David ; Yochikawa, Aline ; Cano-Ramirez, Dora L ; Chembath, Anupama ; Cragg-Barber, Kester ; Haydon, Michael J ; Hotta, Carlos T ; Vincentz, Michel ; Webb, Alex A R ; Dodd, Antony N. / Circadian Entrainment in Arabidopsis by the Sugar-Responsive Transcription Factor bZIP63. In: Current Biology. 2018 ; Vol. 28, No. 16. pp. 2597-2606.e6.
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Frank, A, Matiolli, CC, Viana, AJC, Hearn, TJ, Kusakina, J, Belbin, FE, Wells Newman, D, Yochikawa, A, Cano-Ramirez, DL, Chembath, A, Cragg-Barber, K, Haydon, MJ, Hotta, CT, Vincentz, M, Webb, AAR & Dodd, AN 2018, 'Circadian Entrainment in Arabidopsis by the Sugar-Responsive Transcription Factor bZIP63', Current Biology, vol. 28, no. 16, pp. 2597-2606.e6. https://doi.org/10.1016/j.cub.2018.05.092

Circadian Entrainment in Arabidopsis by the Sugar-Responsive Transcription Factor bZIP63. / Frank, Alexander; Matiolli, Cleverson C; Viana, Américo J C; Hearn, Timothy J; Kusakina, Jelena; Belbin, Fiona E; Wells Newman, David; Yochikawa, Aline; Cano-Ramirez, Dora L; Chembath, Anupama; Cragg-Barber, Kester; Haydon, Michael J; Hotta, Carlos T; Vincentz, Michel; Webb, Alex A R; Dodd, Antony N.

In: Current Biology, Vol. 28, No. 16, 20.08.2018, p. 2597-2606.e6.

Research output: Contribution to journalArticle

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T1 - Circadian Entrainment in Arabidopsis by the Sugar-Responsive Transcription Factor bZIP63

AU - Frank, Alexander

AU - Matiolli, Cleverson C

AU - Viana, Américo J C

AU - Hearn, Timothy J

AU - Kusakina, Jelena

AU - Belbin, Fiona E

AU - Wells Newman, David

AU - Yochikawa, Aline

AU - Cano-Ramirez, Dora L

AU - Chembath, Anupama

AU - Cragg-Barber, Kester

AU - Haydon, Michael J

AU - Hotta, Carlos T

AU - Vincentz, Michel

AU - Webb, Alex A R

AU - Dodd, Antony N

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Y1 - 2018/8/20

N2 - 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, 5, 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, 8, 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, 11, 12, 13, 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.

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Frank A, Matiolli CC, Viana AJC, Hearn TJ, Kusakina J, Belbin FE et al. Circadian Entrainment in Arabidopsis by the Sugar-Responsive Transcription Factor bZIP63. Current Biology. 2018 Aug 20;28(16):2597-2606.e6. https://doi.org/10.1016/j.cub.2018.05.092