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

Abstract

SummarySynchronization 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.

ABA signalling is regulated by the circadian clock component LHY

“…There are many interactions between circadian rhythms and cell signalling pathways. In addition to circadian gating, there are interactions between the circadian oscillator and Ca 2+ signalling (Martí Ruiz et al ., ), sugar signalling (Haydon et al ., ; Frank et al ., ), protein phosphorylation (Choudhary et al ., ), phytohormone signalling (Hanano et al ., ), and signalling between organelles (Noordally et al ., ). The circadian oscillator regulates auxin signals that control development (Covington & Harmer, ; Voß et al ., ), and there are bidirectional interactions between the circadian oscillator component TIMING OF CAB2 EXPRESSION1 (TOC1) and ABA signalling (Legnaioli et al ., ).…”

Cryptochromes integrate green light signals into the circadian system

“…Exogenous sucrose has previously been used to saturate plants' circadian responses to photoassimilates (Frank et al, ; Haydon et al, ; Haydon et al, ; Philippou et al, ). Interestingly, exogenous sucrose was sufficient to mask the cry1 circadian defect under constant green light but not constant blue light (Figures c and S4b).…”

“…Although our data suggest a role for cryptochromes in green light perception, recent work has emphasized the contribution of photoassimilates to circadian timing (Frank et al, 2018;Haydon et al, 2013;Haydon et al, 2017;Philippou, Ronald, Sanchez-Villarreal, Davis, & Davis, 2019). In order to assess the contribution of photosynthesis towards circadian rhythmicity under constant green light, we assessed circadian rhythms in the presence of CO 2 -depleted air, and/or by supplying exogenous sucrose within the growth media to saturate the cellular response to photosynthetically derived sucrose ( Figures 2d and 4).…”

Retrograde signalling as an informant of circadian timing

“…SnRK1 activity is additionally repressed by the accumulation of trehalose-6-phosphate, which serves as a molecular indicator of intracellular sucrose (Figueroa & Lunn, 2016). Overexpression of AKIN10 extends the circadian period in the light (Shin et al, 2017;Frank et al, 2018), suggesting that the control of this subunit is sufficient to change circadian timing. Importantly, SnRK1 regulates the activity of bZIP63, a transcription factor that activates PRR7 transcription (Mair et al, 2015;Frank et al, 2018).…”

“…Importantly, SnRK1 regulates the activity of bZIP63, a transcription factor that activates PRR7 transcription (Mair et al, 2015;Frank et al, 2018). As a consequence, the regulation of SnRK1 activity by trehalose-6phosphate provides a mechanism by which intracellular sugar levels can be interpreted by the circadian system (Frank et al, 2018).…”