Circadian clocks are believed to confer an advantage to plants, but the nature of that advantage has been unknown. We show that a substantial photosynthetic advantage is conferred by correct matching of the circadian clock period with that of the external light-dark cycle. In wild type and in long- and short-circadian period mutants of Arabidopsis thaliana, plants with a clock period matched to the environment contain more chlorophyll, fix more carbon, grow faster, and survive better than plants with circadian periods differing from their environment. This explains why plants gain advantage from circadian control.
Ca(2+) signals are a core regulator of plant cell physiology and cellular responses to the environment. The channels, pumps, and carriers that underlie Ca(2+) homeostasis provide the mechanistic basis for generation of Ca(2+) signals by regulating movement of Ca(2+) ions between subcellular compartments and between the cell and its extracellular environment. The information encoded within the Ca(2+) transients is decoded and transmitted by a toolkit of Ca(2+)-binding proteins that regulate transcription via Ca(2+)-responsive promoter elements and that regulate protein phosphorylation. Ca(2+)-signaling networks have architectural structures comparable to scale-free networks and bow tie networks in computing, and these similarities help explain such properties of Ca(2+)-signaling networks as robustness, evolvability, and the ability to process multiple signals simultaneously.
Transcriptional feedback loops are a feature of circadian clocks in both animals and plants. We show that the plant circadian clock also incorporates the cytosolic signaling molecule cyclic adenosine diphosphate ribose (cADPR). cADPR modulates the circadian oscillator's transcriptional feedback loops and drives circadian oscillations of Ca2+ release. The effects of antagonists of cADPR signaling, manipulation of cADPR synthesis, and mathematical simulation of the interaction of cADPR with the circadian clock indicate that cADPR forms a feedback loop within the plant circadian clock.
Circadian clocks are 24-h timing devices that phase cellular responses; coordinate growth, physiology, and metabolism; and anticipate the day-night cycle. Here we report sensitivity of the Arabidopsis thaliana circadian oscillator to sucrose, providing evidence that plant metabolism can regulate circadian function. We found that the Arabidopsis circadian system is particularly sensitive to sucrose in the dark. These data suggest that there is a feedback between the molecular components that comprise the circadian oscillator and plant metabolism, with the circadian clock both regulating and being regulated by metabolism. We used also simulations within a three-loop mathematical model of the Arabidopsis circadian oscillator to identify components of the circadian clock sensitive to sucrose. The mathematical studies identified GIGANTEA (GI) as being associated with sucrose sensing. Experimental validation of this prediction demonstrated that GI is required for the full response of the circadian clock to sucrose. We demonstrate that GI acts as part of the sucrose-signaling network and propose this role permits metabolic input into circadian timing in Arabidopsis.he Arabidopsis thaliana circadian clock confers growth and competitive advantage (1). The phase of circadian rhythms in plants is adjusted by light signals to entrain the clock to dawn and dusk (2). Additionally, it has been proposed that the Arabidopsis circadian clock is sensitive to nitrogen acting as a nutritional cue (3) and phytohormones, possibly as an input from stress signaling and growth pathways (4). In Arabidopsis, circadian oscillations are generated and maintained by interlocking transcriptionaltranslational feedback loops and posttranslational regulation (1,(5)(6)(7)(8). In the morning, light activates the expression of two Myblike transcription factors, CIRCADIAN CLOCK ASSOCIATED 1 (CCA1) and LATE ELONGATED HYPOCOTYL (LHY), leading to expression of PSEUDO RESPONSE REGULATORS (PRR) 7 and 9, which in turn repress CCA1 and LHY expression. This "morning" loop of the oscillator is connected to "evening" expressed genes through direct repression of the expression of TIMING OF CAB EXPRESSION 1 (TOC1/PRR1) by binding of LHY/CCA1 to the TOC1 promoter. TOC1 is expressed in the evening and feeds back to activate LHY/CCA1 through an unknown pathway. TOC1 physically interacts with and antagonizes CCA1 HIKING EXPEDITION (CHE), a transcriptional repressor of CCA1 (9). CCA1 and LHY are also coupled with TOC1 through GIGANTEA (GI). LHY/CCA1 repress GI and GI forms a loop with TOC1, GI activating TOC1 and TOC1 repressing GI. GI encodes a protein of unknown biochemical function but in blue light, GI physically interacts with and stabilizes ZEITLUPE (10), an F-box protein that targets TOC1 for degradation (11). To entrain the circadian oscillator, signals are incorporated from light, second messengers, and metabolites to alter circadian clock gene expression and modulate circadian function (7,(12)(13)(14)(15).Carbohydrates are a major energy store in most forms ...
The occurrence, activity and plasticity of the CAM pathway is described from an introductory viewpoint, framed by the use of the four "Phases" of CAM as comparative indicators of the interplay between environmental constraints and internal molecular and biochemical regulation. Having described a number of "rules" which seem to govern the CAM cycle and apply uniformly to most species, a number of key regulatory points can then be identified. These include temporal separation of carboxylases, based on the circadian expression of key genes and their control by metabolites. The role of a circadian oscillator and interplay between tonoplast and nuclear control are central to maintaining the CAM cycle. Control of reserve carbohydrates is often neglected, but the importance of daily partitioning (for growth and the subsequent night-time CAM activity) and use at night is shown to drive the CAM cycle. Finally, it is shown that the genotypic and phenotypic plasticity in patterns of CAM expression is mediated partly by environmental conditions and molecular signalling, but also by diffusive constraints in succulent tissues. A transformation system is now required to allow these key areas of control to be elucidated.
Circadian clocks are signalling networks that enhance an organism's relationship with the rhythmic environment. The plant circadian clock modulates a wide range of physiological and biochemical events, such as stomatal and organ movements, photosynthesis and induction of flowering. Environmental signals regulate the phase and period of the plant circadian clock, which results in an approximate synchronization of clock outputs with external events. One of the consequences of circadian control is that stimuli of the same strength applied at different times of the day can result in responses of different intensities. This is known as 'gating'. Gating of a signal may allow plants to better process and react to the wide range and intensities of environmental signals to which they are constantly subjected. Light signalling, stomatal movements and low-temperature responses are examples of signalling pathways that are gated by the circadian clock. In this review, we describe the many levels at which the circadian clock interacts with responses to the environment. We discuss how environmental rhythms of temperature and light intensity entrain the circadian clock, how photoperiodism may be regulated by the relationship between environmental rhythms and the phasing of clock outputs, and how gating modulates the sensitivity of the clock and other responses to environmental and physiological signals. Finally, we describe evidence that the circadian clock can increase plant fitness.
Circadian timekeeping in plants increases photosynthesis and productivity. There are circadian oscillations in the abundance of many chloroplast-encoded transcripts, but it is not known how the circadian clock regulates chloroplast transcription or the photosynthetic apparatus. We show that, in Arabidopsis, nuclear-encoded SIGMA FACTOR5 (SIG5) controls circadian rhythms of transcription of several chloroplast genes, revealing one pathway by which the nuclear-encoded circadian oscillator controls rhythms of chloroplast gene expression. We also show that SIG5 mediates the circadian gating of light input to a chloroplast-encoded gene. We have identified an evolutionarily conserved mechanism that communicates circadian timing information between organelles with distinct genetic systems and have established a new level of integration between eukaryotic circadian clocks and organelles of endosymbiotic origin.
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.
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