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.

All plant productivity, including the food that we eat, arises from the capture of solar energy by plants. At most latitudes sunlight is available for only part of the 24 h day due to the rotation of the planet. This rhythmic and predictable alteration in the environment has driven the evolution of the circadian clock, which has an extremely pervasive influence upon plant molecular biology, physiology and phenology. A number of recent studies have demonstrated that the circadian clock is integrated very closely with photosynthesis and its metabolic products. We consider the coupling of the circadian oscillator with carbohydrate biochemistry and the connections between the nuclear-encoded circadian clock and processes within chloroplasts. We describe how this might provide adaptations to optimize plant performance in an environment that varies both predictably upon a daily and seasonal basis, and unpredictably due to the weather.

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 signaling pathways that integrate environmental information to regulate seedling development. The hypocotyls of Arabidopsis (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 Suc. We focused upon the role of SnRK1, which is a sugar-signaling hub that regulates metabolism and transcription in response to cellular energy status. We also investigated the role of TPS1, which synthesizes the signaling sugar trehalose-6-P that is proposed to regulate SnRK1 activity. Under light/dark cycles, we found that Suc-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 Suc-induced hypocotyl elongation depends on the day length and light intensity. We identified roles for auxin and gibberellin signaling in Suc-induced hypocotyl elongation under short photoperiods. We found that Suc-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 Suc-induced hypocotyl elongation in light/dark cycles.

Summary We investigated the signalling pathways that regulate chloroplast transcription in response to environmental signals. One mechanism controlling plastid transcription involves nuclear‐encoded sigma subunits of plastid‐encoded plastid RNA polymerase. Transcripts encoding the sigma factor SIG5 are regulated by light and the circadian clock. However, the extent to which a chloroplast target of SIG5 is regulated by light‐induced changes in SIG5 expression is unknown. Moreover, the photoreceptor signalling pathways underlying the circadian regulation of chloroplast transcription by SIG5 are unidentified.We monitored the regulation of chloroplast transcription in photoreceptor and sigma factor mutants under controlled light regimes in Arabidopsis thaliana.We established that a chloroplast transcriptional response to light intensity was mediated by SIG5; a chloroplast transcriptional response to the relative proportions of red and far red light was regulated by SIG5 through phytochrome and photosynthetic signals; and the circadian regulation of chloroplast transcription by SIG5 was predominantly dependent on blue light and cryptochrome.Our experiments reveal the extensive integration of signals concerning the light environment by a single sigma factor to regulate chloroplast transcription. This may originate from an evolutionarily ancient mechanism that protects photosynthetic bacteria from high light stress, which subsequently became integrated with higher plant phototransduction networks.

Herbicides increase crop yields by allowing weed control and harvest management. Glyphosate is the most widely-used herbicide active ingredient, with $11 billion spent annually on glyphosate-containing products applied to >350 million hectares worldwide, using about 8.6 billion kg of glyphosate. The herbicidal effectiveness of glyphosate can depend upon the time of day of spraying. Here, we show that the plant circadian clock regulates the effectiveness of glyphosate. We identify a daily and circadian rhythm in the inhibition of plant development by glyphosate, due to interaction between glyphosate activity, the circadian oscillator and potentially auxin signalling. We identify that the circadian clock controls the timing and extent of glyphosate-induced plant cell death. Furthermore, the clock controls a rhythm in the minimum effective dose of glyphosate. We propose the concept of agricultural chronotherapy, similar in principle to chronotherapy in medical practice. Our findings provide a platform to refine agrochemical use and development, conferring future economic and environmental benefits.