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First published online March 18, 2004; 10.1105/tpc.020214 © 2004 American Society of Plant Biologists Circadian and Diurnal Calcium Oscillations Encode Photoperiodic Information in ArabidopsisDepartment of Plant Sciences, University of Cambridge, Cambridge CB2 3EA, United Kingdom 3 To whom correspondence should be addressed. E-mail alex.webb{at}plantsci.cam.ac.uk; fax 44 (0)1223 333953.
We have tested the hypothesis that circadian oscillations in the concentration of cytosolic free calcium ([Ca2+]cyt) can encode information. We imaged oscillations of [Ca2+]cyt in the cotyledons and leaves of Arabidopsis (Arabidopsis thaliana) that have a 24-h period in light/dark cycles and also constant light. The amplitude, phase, and shape of the oscillations of [Ca2+]cyt and [Ca2+]cyt at critical daily time points were controlled by the light/dark regimes in which the plants were grown. These data provide evidence that 24-h oscillations in [Ca2+]cyt encode information concerning daylength and light intensity, which are two major regulators of plant growth and development.
Calcium is a ubiquitous second messenger involved in the transduction of many environmental and developmental stimuli in plants and animals (Trewavas, 1999  ; Sanders et al., 2002; Schuster et al., 2002). In response to diverse stimuli, cells generate transient increases in the concentration of cytosolic free calcium ([Ca2+]cyt) that vary in amplitude, frequency, duration, cellular location, and timing (McAinsh et al., 1995; McAinsh and Hetherington, 1998; Trewavas, 1999; Berridge et al., 2000; Evans et al., 2001; Allen et al., 2001). Important information regarding the nature of the stimulus may therefore be encoded in the different spatiotemporal profiles of [Ca2+]cyt increases (McAinsh and Hetherington, 1998; Sanders et al., 2002; Schuster et al., 2002). The majority of stimuli tested to date result in single, rapid [Ca2+]cyt spikes (also called bursts) or in complex [Ca2+]cyt oscillations recurring with a period of 1 to 20 min (Sanders et al., 2002; Schuster et al., 2002). However, longer-term [Ca2+]cyt oscillations, characterized by a period of  24 h, occur in the cytosol and chloroplast of Nicotiana plumbaginifolia, in the cytosol of Arabidopsis (Arabidopsis thaliana; Johnson et al., 1995), and in the cytosol of neurons of the mouse suprachiasmatic nucleus, which is the primary circadian pacemaker in mammals (Ikeda et al., 2003). These circadian rhythms of [Ca2+]cyt are believed to be involved in signaling to or from the endogenous circadian clock (Gómez and Simón, 1995; Trewavas, 1999; Webb, 2003), although their precise role remains unclear (Sai and Johnson, 1999). One possibility is that circadian oscillations of [Ca2+]cyt encode information in a manner analogous to the short-period oscillations of [Ca2+]cyt induced by extracellular signals. Known regulators of circadian behavior include light duration and intensity. Thus, circadian oscillations of [Ca2+]cyt might have the potential to encode temporal information about the daily duration and intensity of light, which are two major regulators of plant growth and development.
Eukaryotic circadian clocks have similar basic structures; input pathways integrate environmental cues such as the daily (24-h) cycle of alternating light and dark intervals and temperature to entrain a core molecular oscillator that, in turn, regulates multiple output pathways and transduces temporal information (Harmer et al., 2001
Circadian Oscillations of [Ca2+]cyt in the Leaves of Arabidopsis Aequorin bioluminescence was measured in vivo, using photon-counting imaging (Figure 1). Seedlings in LL had circadian oscillations in aequorin luminescence that increased during the subjective day to a peak value and decreased during the subjective night to a minimum. The circadian alteration in the bioluminescent signal was localized to the cotyledons and the emerging leaves (Figure 1). The changes in aequorin bioluminescence reflected alterations in [Ca2+]cyt because oscillations of luminescence were not detected when we imaged untransformed plants treated with coelenterazine or transformed plants without coelenterazine. The oscillations were not a consequence of alterations in the abundance of cytosolic aequorin because the total aequorin pool measured using antibodies (Johnson et al., 1995 ) and photon counting of the luminescence of the entire pool following discharge in excess Ca2+ (data not shown) did not change in a circadian manner. No differences in growth rate, flowering time, and morphology were detected between wild-type and transgenic plants, demonstrating that transgene insertion and expression had no effect on circadian behavior (data not shown). The period of the [Ca2+]cyt oscillations was 24 h and predicted both subjective dawn and subjective dusk, which are characteristics of circadian rhythms (Millar and Kay, 1996).
The mean whole-plant [Ca2+]cyt typically oscillated between 100 nmol L–1 at the trough and 300 nmol L–1 at the peak. However, this may be an underestimate of the peak of [Ca2+]cyt occurring in individual cells in response to circadian signals because (1) the [Ca2+]cyt of different populations of cells oscillate with different circadian phases (Wood et al., 2001), and (2) individual cells in a population can have different circadian phases (see Webb, 2003). The multiple phases of individual cells in the plant and any cells not responding will result in the mean peak whole-plant [Ca2+]cyt being lower than the peak of [Ca2+]cyt attained in the cells.
The Amplitude of Circadian Oscillations of [Ca2+]cyt Is Modulated by Photon Flux Density
The Phase of Circadian Oscillations of [Ca2+]cyt Is Modulated by the Photoperiod of Entrainment We tested whether circadian [Ca2+]cyt oscillations were modulated by changes in daylength (photoperiod). Seedlings were entrained in 6L/18D, 8L/16D, 12L/12D, 16L/8D, and 20L/4D. Seedlings entrained in 6L/18D, 8L/16D, 12L/12D, and 16L/8D had free-running rhythms in aequorin luminescence (Figure 3) with an approximate period of 24 h (Figure 4B). By contrast, seedlings entrained in 20L/4D had no rhythmic component to the bioluminescence signal (Figures 4A and 4B). The phase of the circadian [Ca2+]cyt oscillations was dependent on the entrainment photoperiod, with peak [Ca2+]cyt occurring later per 24-h cycle in plants entrained in long photoperiods than in plants entrained in short photoperiods (Figure 5A). The luminescence of seedlings entrained in 6L/18D peaked at a mean of 4.09 ± 0.19 h (n = 24) after subjective dawn for circadian cycle 2 (24 to 48 h after transfer to LL). Seedlings entrained in 8L/16D had peak luminescence at 5.39 ± 0.22 h (n = 36) after subjective dawn, seedlings entrained in 12L/12D had peak luminescence at 6.59 ± 0.37 h (n = 44) after subjective dawn, and seedlings entrained in 16L/8D were maximally luminescent 8.16 ± 0.90 h (n = 24) after subjective dawn, for circadian cycle 2. Thus, the longer the photoperiod during entrainment, the later the peak luminescence after subjective dawn in LL. This trend was repeated in the subsequent cycles of circadian free-run (e.g., cycle 3, from 48 to 72 h, and cycle 4, from 72 to 96 h after transfer to LL). The timing of minimum luminescence in LL was unaffected by the entrainment daylength and occurred 19 to 20 h after subjective dawn in seedlings from all entrainment regimes (Figure 5C). Consequently, the circadian [Ca2+]cyt oscillations were asymmetric, and the asymmetry depended on the entrainment photoperiod because the longer the photoperiod, the shorter the time difference between maximum and minimum [Ca2+]cyt. Therefore, the daylength during entrainment controlled both the phase and the shape (symmetry) of the [Ca2+]cyt oscillations during circadian free-run in LL.
The photoperiod-dependent phase shift of the circadian [Ca2+]cyt rhythms had significant consequences for [Ca2+]cyt at subjective dusk. At subjective dusk, relative luminescence (as a percentage of the maximum luminescence for each circadian cycle) was dependent on the duration of the entrainment photoperiod. The relative luminescence at subjective dusk of seedlings entrained to 6L/18D was 72.59 ± 10.92% (n = 24), that of seedlings entrained in 8L/16D was 59.82 ± 11.95% (n = 36), that of seedlings entrained in 12L/12D was 55.06 ± 11.10% (n = 44), and for seedlings entrained to 16L/8D, relative luminescence was 24.17 ± 8.91% (n = 24). Thus, at subjective dusk, [Ca2+]cyt was relatively high in plants entrained in short photoperiods and low in plants entrained in long photoperiods. These differences in [Ca2+]cyt at subjective dusk are a consequence of photoperiodic entrainment. Conversely, at subjective dawn, there was no significant difference in relative luminescence for seedlings entrained in the different LD regimes. We next tested whether the phase and shape of circadian [Ca2+]cyt oscillations were set by the length of the dark period by transferring the seedlings to LL after a dark period equal to that they were entrained in (12 h) or following a final dark period that had been extended by 5 h (17 h total; Figure 6A). Extending the length of the final dark period did not alter the circadian period. The period estimate of the circadian rhythm of seedlings transferred to LL after a 5-h delay was 22.6 ± 1.47 h (n = 4), which was not significantly different to that of seedlings transferred to LL without delay; 21.9 ± 1.85 h (n = 10). Extending the length of the final dark period resulted in a shift in phase of the oscillations relative to each other, but the phase of the rhythms relative to the final subjective dawn was unaffected (Figure 6B). The timing of maximum luminescence relative to subjective dawn in the first three circadian cycles was not significantly different between the treatments (Figure 6B). The characteristics of the circadian luminescence oscillations were therefore determined by the entrainment regime and not by the length of the final dark period.
Leaf [Ca2+]cyt Oscillations in LD Cycles Are Modulated by Photoperiod and Light Intensity Although important information regarding biological clocks is obtained from studying organisms under constant conditions, such conditions are largely artificial. We therefore examined [Ca2+]cyt dynamics in more natural LD cycles to determine, firstly, whether [Ca2+]cyt oscillations with a 24-h period exist under these conditions and, secondly, whether the [Ca2+]cyt oscillations encode environmental information. Arabidopsis expressing aequorin was grown in 8L/16D or 16L/8D and luminescence measured in these same LD regimes rather than in LL (Figure 7). Plants grown in 16L/8D were exposed to a PFD of 60 µmol m–2 s–1. Plants grown in the 8L/16D regime were exposed to 60 µmol m–2 s–1 or to 110 µmol m–2 s–1, thus the latter received similar daily integrated photons as plants in 16L/8D.
Seedlings in LD had [Ca2+]cyt oscillations that were strikingly similar to those observed in circadian free-run (LL). In LD, [Ca2+]cyt increased during the day to a peak value, peaked before dusk, and then decreased to a minimum during the dark period. The period of the [Ca2+]cyt oscillations in LD also was 24 h. Importantly, the timing of peak luminescence (phase) in LD was consistent with that in LL and dependent on the photoperiod (Figure 7). At dusk, the relative luminescence of seedlings in 8L/16D was 59.57 ± 15.02% (n = 22) compared with 24.89 ± 4.34% (n = 22) in 16L/8D. The relative intensity at subjective dusk was very similar whether measured in LD or LL. Seedlings entrained to 8L/16D had dusk relative luminescence values of 59% in both LD and in LL. Moreover, the relative luminescence at subjective or true dusk of seedlings entrained to 16L/8D was 24% in both LL and LD. Additionally, the amplitude of the [Ca2+]cyt oscillations in LD was consistently larger in the higher PFD (Figure 7A). These data demonstrate that leaf [Ca2+]cyt oscillates with a period of 24 h in light and dark cycles that are characteristic of natural environments and that the pattern of these oscillations was dependent on the photoperiod and the intensity of light.
We have examined both the location and potential for information encoding in circadian oscillations of [Ca2+]cyt. The spatial resolution provided by photon-counting imaging enabled localization of circadian [Ca2+]cyt oscillations to the leaves and cotyledons of Arabidopsis in both LL and LD. It is likely that both the epidermal and mesophyll cells contribute to the circadian oscillations of [Ca2+]cyt in the leaves (Wood et al., 2001 ). However, the imaging system we used did not allow us to investigate the localization of the [Ca2+]cyt oscillations at a cellular level. These data demonstrate that the circadian oscillations of [Ca2+]cyt reported previously for whole plants (Johnson et al., 1995) are present in the photosynthetic organs, where light stimuli are perceived and integrated.
The localization of 24-h oscillations of [Ca2+]cyt to the cotyledons and leaves suggests that they might have a role in transducing circadian and photoperiodic information (Lumsden, 1998
Previously, circadian oscillations in [Ca2+]cyt have been detected in N. plumbaginifolia and in Arabidopsis (Johnson et al., 1995 Our data provide new evidence that circadian and photoperiodic information can be encoded in the pattern of [Ca2+]cyt oscillations in both circadian free-run in LL and in LD cycles. This has important implications for understanding signaling in plants. We have demonstrated that the phase (or timing of the peak of [Ca2+]cyt) and shape of free-running circadian oscillations of [Ca2+]cyt in LL were dependent on the length of the light and dark cycles during entrainment. The peak of [Ca2+]cyt after subjective dawn in LL occurred later in those plants that had been entrained to long light periods than the peak in plants entrained to short light periods. These data demonstrate that the phase of the circadian oscillations of [Ca2+]cyt was sensitive to the length of the light and/or dark cycles during entrainment. However, the timing of the trough of [Ca2+]cyt relative to subjective dawn was not altered by the photoperiodic entrainment.
Another effect of the phase shift of the [Ca2+]cyt rhythms was that the timing of the peak was altered in relation to subjective dusk. The peak of [Ca2+]cyt in LL in plants entrained to 6L/18D occurred at the end of the subjective light period, 0 to 2 h before subjective dusk. By comparison, the peak in plants entrained to 16L/8D occurred in the middle of the subjective light period, 6 to 8 h before subjective dusk. Plants entrained in 6L/18D therefore emitted
These data demonstrate that the entrainment photoperiod regulates the phase and shape of the circadian [Ca2+]cyt oscillations and importantly, the [Ca2+]cyt at subjective dusk. It is therefore possible that these characteristics of circadian [Ca2+]cyt oscillations encode information that affects the integration and outcomes of Ca2+-based signaling networks (Berridge et al., 2000
Two aspects of circadian [Ca2+]cyt oscillations in Arabidopsis seedlings, the phase and the amplitude of the oscillations, are modulated by light quantity and entrainment photoperiod. The modulation of the phase and amplitude of circadian oscillations of [Ca2+]cyt by environmental stimuli is consistent with the hypothesis that information is encoded in the dynamics of circadian [Ca2+]cyt oscillations (Jaffe, 1991 We also imaged the daily [Ca2+]cyt dynamics of the leaves and cotyledons of seedlings in light and dark cycles more representative of the natural environment. The [Ca2+]cyt oscillations in LD were strikingly similar to those observed in LL: [Ca2+]cyt rose during the day, peaked several hours after dawn, and then decreased, attaining a minimal value during the night. Additionally, the photoperiod-dependent phase shift of [Ca2+]cyt oscillations and amplitude modulation observed in LL occurred also in LD. In 8L/16D, the peak [Ca2+]cyt occurred at 6 h after dawn but in 16L/8D, the peak [Ca2+]cyt occurred at 8 h after dawn. Higher PFD in 8L/16D increased the amplitude of the oscillations in [Ca2+]cyt, in agreement with our observations of circadian [Ca2+]cyt oscillations in LL, but PFD did not affect the phase of the [Ca2+]cyt oscillations in LD. Thus, the effects of daylength on [Ca2+]cyt in LD were because of the duration of the light and dark cycles and not the amount of light to which the seedlings were exposed. These data demonstrate that [Ca2+]cyt in cotyledon and leaf cells oscillated with a 24-h period in LD cycles and that the phase of these oscillations was sensitive to the entrainment regime and the amplitude was sensitive to PFD. Importantly, the level of [Ca2+]cyt at dusk was relatively high in plants in short days and low in plants in long days. This observation strongly suggests that [Ca2+]cyt oscillations in LD are not directly regulated by light but are instead associated with the circadian clock and may play a role in circadian signaling in response to LD cycles.
There was one major difference between the oscillations of [Ca2+]cyt in LL and those in LD. The luminescence of seedlings in LD did not increase significantly before dawn but only rose after illumination. This difference between the Ca2+ dynamics of plants in LD or in LL can be explained by the observation that [Ca2+]cyt is arrhythmic in darkness (Johnson et al., 1995
The slow rates of increase and decrease of [Ca2+]cyt in LD suggest that the daily [Ca2+]cyt oscillations were not generated as an immediate, acute response to illumination but instead by a complex signaling network cued to LD cycles and the circadian clock (Millar and Kay, 1996
Perhaps one of the most important plant responses regulated by daylength is the photoperiodic transition from vegetative growth to the development of flowers (Yanovsky and Kay, 2002
Seedling Growth and Photoperiodic Entrainment Transgenic Arabidopsis seeds (ecotype Wassilewskija) that constitutively express the apoaequorin cDNA under the control of the 35S promoter of Cauliflower mosaic virus were surface-sterilized and germinated on solid medium (0.5x Murashige and Skoog medium and 0.8% (w/v) agar, pH = 6.8) in clusters of 15 to 20 plants. Surface sterilization was performed by rinsing seeds for 1 min in 100% ethanol, then by incubating seeds for 10 min in 50% (v/v) sodium hypochlorite, followed by two washes in sterile water. Seed germination was synchronized by vernalization at 4°C for 2 d in the dark. Seedlings were grown in white light at a PFD of 60 µmol m–2 s–1 at 19°C for 11 d. During the growth period, seedlings were entrained to several photoperiods: 6L/18D, 8L/16D, 12L/12D, 16L/8D, or 20L/4D. Plants were then transferred to 60 µmol m–2 s–1 or 110 µmol m–2 s–1 of LL for imaging circadian [Ca2+]cyt oscillations under circadian free-run conditions. In a separate protocol, plants remained under the appropriate entrainment regime for measurement of [Ca2+]cyt dynamics under LD conditions. During the dark period, plants were handled in a dark room under green safelight.
Imaging Aequorin Bioluminescence
The integrated 8-bit photon-counting images were processed using the Photek IFS32 software. Regions of interest, based on the bright-field image, were demarcated around each seedling cluster, and total photon counts (luminescence) were quantified. Rhythms of aequorin luminescence, corresponding to rhythms in [Ca2+]cyt, were analyzed using two methods. First, the fast Fourier transform–nonlinear least-squares method (FFT-NLLS) described by Plautz et al. (1997)
Estimation of the Total Aequorin Pool and Magnitude of the Oscillations in [Ca2+]cyt
The long time scale of the measurements compromise estimation of [Ca2+]cyt based on the rate of aequorin consumption as a proportion of the total pool (Johnson et al., 1995
To generate a calibration curve, we used data obtained from photon-counting imaging of 7-d-old aequorin-expressing seedlings irrigated with 100, 150, 200, or 300 mol m–3 NaCl in Murashige and Skoog medium (n = 20; F. Tracy and M. Tester, personal communication). Functional aequorin had been generated by overnight incubation with 10 µmol L–1 coelenterazine in the dark. The seedlings were imaged continuously before, during, and after perfusion with NaCl containing solution. A time-resolved integration graph of the integrated photon count s–1 was plotted, and the peak fold increase in light was calculated. Previously, the mean peak [Ca2+]cyt increase in response to 100, 150, 200, or 300 mol L–1 NaCl in Murashige and Skoog medium had been measured using photon-counting luminometry calibrated exactly as described in Fricker et al. (1999
We thank Marc Knight of the University of Oxford (Oxford, UK) Department of Plant Sciences for his kind gift of Arabidopsis expressing apoaequorin, and Carl H. Johnson of Vanderbilt University (Nashville, TN) and Enid MacRobbie and Julia Davies (University of Cambridge, Cambridge, UK) for their helpful comments on the manuscript. We thank Francis Tracey and Mark Tester (University of Cambridge) for providing access to their unpublished data. We also acknowledge the financial support of the Broodbank Fellowship Trust of the University of Cambridge (to J.L.), the Royal Society of London, and the Biotechnology and Biological Sciences Research Council of the United Kingdom (to A.A.R.W).
1 These authors contributed equally to this work. 
2 Current address: School of Biological Sciences, The University of Exeter, Washington Signer Laboratories, Perry Road, Exeter EX4 4QG, UK. The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantcell.org) is: Alex A.R. Webb (alex.webb{at}plantsci.cam.ac.uk). Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.020214. Received December 18, 2003; accepted January 30, 2004.
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