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Summary 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., Graphical Abstract, Highlights • The transcription factor bZIP63 binds and regulates the circadian clock gene PRR7 • bZIP63 is required for adjustment of circadian period by sugars • Trehalose-6-phosphate metabolism and KIN10 signaling regulate circadian period • Sugar signals establish the correct circadian phase in light and dark cycles, 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.

Emerging seedlings respond to environmental conditions such as light and temperature to optimize their establishment. Seedlings grow initially through elongation of the hypocotyl, which is regulated by signalling pathways that integrate environmental information to regulate seedling development. The hypocotyls of Arabidopsis thaliana also elongate in response to sucrose. Here, we investigated the role of cellular sugar-sensing mechanisms in the elongation of hypocotyls in response to sucrose. We focused upon the role of SnRK1, which is a sugar-signalling hub that regulates metabolism and transcription in response to cellular energy status. We also investigated the role of TPS1, an enzyme that synthesizes the signalling sugar trehalose-6-phosphate (Tre6P) that is proposed to regulate SnRK1 activity. Under light/dark cycles, we found that sucrose-induced hypocotyl elongation did not occur in tps1 mutants and overexpressors of KIN10 (AKIN10/SnRK1.1), a catalytic subunit of SnRK1. We demonstrate that the magnitude of sucrose-induced hypocotyl elongation depends on the day length and light intensity. We identified roles for auxin and gibberellin signalling in sucrose-induced hypocotyl elongation under short photoperiods. We found that sucrose-induced hypocotyl elongation under light/dark cycles does not involve another proposed sugar sensor, HEXOKINASE1, or the circadian oscillator. Our study identifies novel roles for KIN10 and TPS1 in mediating a signal that underlies sucrose-induced hypocotyl elongation in light/dark cycles.