JXB Advance Access originally published online on March 31, 2003
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Journal of Experimental Botany, Vol. 54, No. 386, pp. 1471-1479,
May 1, 2003
© 2003 Oxford University Press
Contribution of C3 carboxylation to the circadian rhythm of carbon dioxide uptake in a Crassulacean acid metabolism plant Kalanchoë daigremontiana
Received 22 August 2002; Accepted 16 February 2003
1 Adam Mickiewicz University, Biology Department, Al. Niepodleg
o
ci 14, 61-714 Pozna
, Poland
2 Technische Universität-Darmstadt, Institut für Botanik, Fachbereich Biologie, Schnittspahnstr. 3-5, D-64287 Darmstadt, Germany
3 To whom correspondence should be addressed. twyka{at}amu.edu.pl
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Abstract |
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During the endogenous circadian rhythm of carbon dioxide uptake in continuous light by a Crassula cean acid metabolism plant, Kalanchoë daigremontiana, the two carboxylating enzymes, phosphoenolpyruvate carboxylase (PEPC) and ribulose 1,5 bisphosphate carboxylase/oxygenase (Rubisco), are active simultaneously, although, until now, only the role of PEPC in generating the rhythm has been acknowledged. According to the established model, the rhythm is primarily regulated at the PEPC activity level, modulated by periodic compartmentation of its inhibitor, malate, in the vacuole and controlled by tension/relaxation of the tonoplast. However, the circadian accumulation of malic acid (the main indicator of PEPC activity) dampened significantly within the first few periods without affecting the rhythm’s amplitude. Moreover, the amount of malate accumulated during a free-running oscillation was several-fold lower than the amount expected if PEPC were the key carboxylating enzyme, based on a 1:1 stoichiometry of CO2 and malate. Together with the observation that rates of CO2 uptake under continuous light were higher than in darkness, the evidence shows that C3 carboxylation greatly contributes to the generation of rhythmic CO2 uptake in continuous light in this ‘obligate’ CAM plant. Because the shift from predominantly CAM to predominantly C3 carboxylation is smooth and does not distort the trajectory of the rhythm, its control probably arises from a robust network of oscillators, perhaps also involving stomata.
Key words: Circadian rhythm, Crassulacean acid metabolism, Kalanchoë, photosynthesis.
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Introduction |
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Carbon dioxide uptake by Crassulacean acid metabolism plants is accomplished by two carboxylases, with the cytoplasmic enzyme phosphoenolpyruvate carboxylase (PEPC) operating mainly during the night when stomata are open and the products of CO2 fixation (malate or citrate, or both) are accumulated in the vacuole (phase I; Osmond, 1978). When, during the day, PEPC is down-regulated by malate entering the cytoplasm from the vacuole, the second carboxylating enzyme, ribulose-1–5-bisphosphate carboxylase (Rubisco), is active in the chloroplasts and consumes CO2 derived from the decarboxylation of malate. Stomata at that time are tightly closed (phase III). These two cardinal phases of CAM are separated by the transitional phases II and IV, which take place at, respectively, the beginning and end of the light period and feature simultaneous operation of both carboxylating enzymes (Griffiths et al., 1990). In spite of a considerable variation among different species and a pronounced plasticity in response to environmental conditions or developmental stage (Dodd et al., 2002), this multiphasic rhythm of gas exchange, together with the nocturnal acidification of the vacuole, constitutes the essence of Crassulacean acid metabolism. The regulation of transitions between the different phases remains one of the key issues in CAM research. It is now clear that it involves both metabolic feedbacks and endogenous clock mechanisms (Carter et al., 1996; Borland et al., 1999; Lüttge, 2000; Nimmo, 2000).
In several CAM species (e.g. in the genera Kalanchoë and Clusia) the rhythms of carbon dioxide uptake (JCO2) and stomatal conductance (gH2O) persist concurrently for many days under continuous light and steady temperature conditions (Wilkins, 1984; Lüttge and Beck, 1992; H Duarte, TU Darmstadt, personal communication). The oscillations are generated by an endogenous clock mechanism, and, accordingly, display a considerable temperature compensation of the period (Anderson and Wilkins, 1989; Lüttge and Beck, 1992) and the entrainability by light (Bohn et al., 2001) and temperature (Grams et al., 1997; Lüttge et al., 1996). As with other biological clock systems, research has focused on identifying the central oscillator responsible for driving the rhythm, mostly using Kalanchoë species. A number of the rhythm’s properties indicate that the observed oscillations of carbon dioxide uptake are manifestations of the fluctuating activity of phosphoenolpyruvate carboxylase. First, a similar rhythm also occurs in the dark, where, in initially CO2-free air, rhythmic CO2 outputs are observed (Wilkins, 1992). Second, on-line 13C discrimination values exhibited a rhythmic variation, concurrent in phase with JCO2, indicating a rhythmic activity of PEP carboxylase (Grams et al., 1997). Lastly, a successful model exists, which simulates the rhythmic behaviour of carbon flow based solely on changes in PEPC activity, which are controlled by the cytoplasmic malate level (Blasius et al., 1999). In this model, periodic malate accumulation in the vacuole, and its release back into the cytoplasm, where it reversibly inhibits PEP carboxylase, are both dependent on tonoplast permeability to malate, which itself is a function of fluidity, or ‘state of order’ of the tonoplast membrane. Shifts of tonoplast fluidity are triggered by changes in the vacuolar turgor, which, in turn, depends on the vacuolar malate content (Lüttge et al., 1975; Rygol et al., 1987). The model provided an excellent agreement between the simulated time-course of JCO2 and gH2O and the actual gas exchange measurements in Kalanchoë daigremontiana, as well as accurately reproducing the effects of temperature changes on the expression of the rhythm (Grams et al., 1997; Beck et al., 2001).
Despite extensive investigation conducted into the phenomenology and mechanism of the endogenous gas exchange rhythm in Kalanchoë, there is little understanding of the position of Rubisco activity in the overall carboxylation scheme in continuous light, perhaps because research has been largely entrained by the early studies conducted in the dark (Wilkins, 1959, 1962). It is possible that the activity of Rubisco remains entirely complementary to the activity of PEP-carboxylase, which, due to its high affinity for CO2, diverts this substrate away from Rubisco at peaks of gas exchange, not unlike the situation in phase II and late phase IV of the diurnal CAM cycle (Fischer and Kluge, 1984; Griffiths et al., 1990). Peaks of Rubisco activity would then occur during the minima of overt CO2 uptake when vacuolar malate is being decarboxylated behind more or less closed stomata. So far, however, the time-course of Rubisco activity in continuous light has not been directly probed in any CAM plant. Recently, an alternative suggestion has been advanced that the circadian JCO2 rhythms in CAM plants are actually an expression of oscillating C3, rather than CAM carboxylation (Dodd et al., 2002). It is certainly possible that Rubisco activity itself is under circadian control in CAM plants in continuous light. Circadian regulation of C3 photosynthesis has been found in several plants and cyanobacteria (Hennessey and Field, 1991; Iwasaki and Kondo, 2000; Lüttge, 2002a; Staiger, 2002), although explicit clock models capable of producing self-sustaining oscillations are lacking.
The objective of this paper is to examine the evidence for rhythmic activity of C3 carboxylation during the free running rhythm of CO2 uptake in continuous light in Kalanchoë daigremontiana. Based on original results and on new interpretation of published data, it is argued that Rubisco activity accounts for a considerable fraction of the rhythm’s amplitude.
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Materials and methods |
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Plants of Kalanchoë daigremontiana Hamet et Perrier de la Bathie (Crassulaceae) were propagated vegetatively from stock maintained in a greenhouse at Technische Universität-Darmstadt (Germany) and grown in pots filled with peat-based compost. Supplementary illumination was provided by 400 W HQI-T lamps (Osram, Munich, Germany) to extend the light period to 12 h. When the plants were about 50–60 cm tall and had 4–5 pairs of fully formed leaves, they were transferred into a controlled environment phytotron chamber (12/12 h light/dark, 28/21 °C light/dark, 70% relative humidity) and adapted to chamber conditions for at least 7 d before being used for measurements.
Leaf gas exchange was measured using an open minicuvette system (Walz GmbH, Effeltrich, Germany) operating in the differential mode described in Lüttge and Beck (1992). The youngest fully expanded leaf, while still attached to the plant, was sealed in a plexiglass climate-controlled cuvette. A thermocouple was placed in contact with the lower leaf surface to allow feedback control of leaf temperature through the adjustment of the temperature of air entering the cuvette. The relative humidity of incoming air was controlled by bubbling it through water and then cooling it in a Peltier unit to the desired dew point. Relative air humidities during the light and dark periods were set always to maintain a steady vapour pressure deficit of 1.6 kPa. Gas flow through the cuvette was set to 2.2 l min–1. Illumination was maintained at PPFD=120 µmol m–2 s–1 measured at leaf level, except for a single time series where PPFD=187 µmol m–2 s–1. Carbon dioxide and water vapour concentration in air leaving the cuvette, as well as environmental variables inside the cuvette (RH, leaf temperature and PPFD level) were automatically logged every 5 min and later CO2 uptake rate, stomatal conductance and intercellular CO2 concentration were calculated according to Farquhar and Sharkey (1982).
Seven independent time series of gas exchange measurements were obtained. The protocol adopted for gas exchange studies started with 4 d of 12/12 h light/dark photoperiod (referred to as LD throughout this paper), with leaf temperatures maintained at 28/21 °C (light/dark). At the end of the final dark period the light was turned on and maintained continuously for up to 14 d (referred to as LL), while leaf temperature was held at 24 °C. After the completion of every time series the leaf was harvested and its area determined by tracing the leaf outline on paper and comparing the weight of the traced area with a reference.
During one of the gas exchange runs, leaf tissue samples were collected in order to determine variation in malate content. The samples were obtained from similar-aged leaves of additional plants, which were maintained in an adjacent growth chamber. To provide the best possible match of environmental conditions between the leaf on which gas exchange was being measured and the leaves sampled for malate, selected leaves, while still attached to the plant, were immobilized at the level which provided uniform illumination (PPFD=109–118 µmol m–2 s–1). Relative air humidity was set to 70%. To maintain leaf temperature at the target level, air temperature in the walk-in chamber was set at a level slightly lower than that in the gas exchange cuvette. Leaf temperature was monitored by a thermocouple attached to its lower side and recorded continuously by a pen recorder. Sampling took place at two stages of the time series: during the last dark period, and during the fourth free-running oscillation of JCO2 in continuous light. First, at –8 and 0 h from the start of continuous light, leaf discs 9 mm in diameter were excised from five leaves. Likewise, at 74 h after the start of LL, and every 3 h thereafter until 98 h, leaf discs were excised from each of eight additional leaves. The discs were immediately frozen in liquid nitrogen and stored at –80 °C. After weighing, grinding in liquid nitrogen, heating to 95 °C for 10 min, and homogenizing for 5 min in an ultrasound homogenizer, samples were diluted to 1 ml with double-distilled H2O, and centrifuged at 13 000 rpm for 5 min. The malate level in the samples was determined using enzymatic reactions with malate dehydrogenase and glutamate-oxaloacetate transaminase according to Möllering (1974). A double set of standards was run with each determination, and samples were analysed in duplicate and average values were used.
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Results |
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Under alternating light/dark conditions leaves of Kalanchoe daigremontiana exhibited the typical four phases of CAM gas exchange. In continuous light, all seven leaves performed co-ordinated circadian oscillations of CO2 uptake and stomatal conductance, as shown in Fig. 1 for a representative time series. Figure 2 illustrates details of gas exchange pattern in LD and during the transient in LL, i.e. from onset of continuous light to the first peak (for clarity only JCO2 values are plotted). In all runs the transient reproduced the three daytime phases (II, III and IV) of CAM during the first 12 h in LL, followed by continued net CO2 uptake until the peak during the subjective night. This first circadian peak of JCO2 was always higher than the peak expressed during the dark period, although the magnitude of the difference varied among time series.
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Circadian oscillations were also evident in the ratio of calculated internal to external CO2 concentration (Fig. 3). Phases of this rhythm were the reverse of JCO2 and gH2O phases. Their amplitude appeared to be greater under the lower light level, where peaks reached or slightly exceeded the value of 1, indicating an enrichment of air in substomatal spaces in CO2 above the atmospheric level (Fig. 3A versus B). It was, however, not possible to calculate the ci/ca ratio for the earliest h under continuous light, because of the tight stomatal closure.
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In the single time series, in which the relationship between malate accumulation and CO2 uptake was examined, the integrated CO2 uptake during the last dark period before LL was 54.13 µM g–1 FW (Fig. 4A). During the same period, the leaves accumulated on average 86.52 µM g–1 FW malate (Fig. 4A, C). Given the expected 1:1 stoichiometry of CO2 and malate when PEPC is the only carboxylating enzyme, the 37% excess of malate must have originated from the recycling of mesophyll respiratory CO2. During the fourth free-running oscillation, malate accumulation (the difference between the highest and lowest content, i.e. between hours 83 and 95) was only 18.91 µM g–1 FW (Fig. 4B, D) while integrated CO2 uptake during the corresponding time was 126.44 µM g–1 FW, i.e. the bulk (85%) of all fixed carbon was not accounted for by malate.
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Discussion |
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Under relatively low levels of continuous light and at a defined temperature leaves of Kalanchoë daigremontiana perform self-sustained circadian oscillations of JCO2 and gH2O (Fig. 1; Lüttge and Beck, 1992; Grams et al., 1997). When LD and the first hours of LL are compared (Fig. 2), the endogenous rhythm of gas exchange in all the runs was initiated after a brief burst of CO2 uptake (phase II of CAM) followed by a 5–7 h transient of steady near-zero level of net carbon dioxide uptake. The latter corresponds to the classical phase III of CAM, when CO2 released from decarboxylated malate behind closed stomata is consumed as the substrate for Rubisco. The rapid opening of stomata that follows the depletion of malate, accompanied by a steep rise in CO2 uptake is then equivalent to phase IV, in which C3 fixation predominates, but PEPC also becomes activated. Under LD, Rubisco activity would subsequently be terminated by the onset of darkness, while carboxylation through PEPC would continue through the night. However, under the artificial conditions when light is maintained beyond normal daytime, carboxylation by both enzymes could, in principle, continue, contributing to the overall CO2 uptake. The additive action of the two carboxylases results in the self-sustaining oscillations of JCO2. The search for a master switch of the overt JCO2 rhythm must therefore consider the controls of both carboxylating systems. On the one hand, published evidence clearly shows that PEPC activity oscillates in a circadian manner. The online 13CO2 discrimination measured over two free-running oscillations of gas exchange revealed CAM-like values at times of maximal gas exchange and C3-like values at times of the minima (Grams et al., 1997). Moreover, phase shifts induced by temperature and the modes of rhythm reinitiation after the removal of inhibitory low or high temperatures are all consistent with the role of vacuolar malate content and the movement of malate between cell compartments in regulating the circadian activity of PEPC (Wilkins, 1992; Lüttge, 2000, 2002a). On the other hand, all published empirical measurements of malate level and enzyme activity fluctuation are limited to the first 1–3 cycles after the removal of the external timer. The endogenous oscillations of gas exchange in LL may, however, continue for over a dozen periods so the initial few days may merely represent a transient. At any rate it is not clear how representative this initial period is of the entire time series.
At the same time, there is little understanding of the behaviour of Rubisco activity throughout the endogenous CO2 uptake rhythm. In continuous light the normal mechanism for switching off Rubisco is absent and one may expect that its activity might be mainly regulated by the availability of CO2 or, hypothetically, by an endogenous clock mechanism exercising control at either the light harvesting or carbon reduction stage (Liu et al., 1996; Millar and Kay, 1996). So far, the question of relative contributions of both carboxylating enzymes to circadian oscillations of JCO2 has remained elusive, but some insights can be gathered from examining the stoichiometry of CO2 uptake and malate accumulation.
Under both LD and LL conditions, the principal and most straightforward index of CAM activity is the oscillation of malate level. Accumulation of malate during a night period reflects the net fixation by PEPC of CO2, whether it is taken up from the atmosphere or derived from mesophyll respiration. Similarly, during a single circadian period of JCO2 in LL, the yield of accumulated malate should be equivalent to net CO2 fixation by PEPC. Under these experimental conditions, the bulk (85%) of carbon fixed during the fourth free-running oscillation was not accounted for by malate accumulation (Fig. 4). That balance of carbon must then have been assimilated directly through the C3 pathway.
These data also illustrate that the amount of malate accumulated on a circadian basis in continuous light was lower than malate gain in the dark. Although this does not necessarily apply to the first oscillation in LL (Rascher, 2001), a review of published reports of malate levels in Kalanchoë leaves under LL clearly shows a fast dampening of malate fluctuations with each consecutive cycle of JCO2 (Fig. 5). One important implication of this trend is that in LL the vacuolar capacity for malate storage is not entirely used. This suggests that functioning of the tonoplast tension/relaxation mechanism proposed previously as the endogenous clock’s master switch (Blasius et al., 1999) may be limited when LL conditions are extended for a longer time. The dampening of malate oscillations is more rapid than the dampening of the overt JCO2 rhythm (Figs 1, 4 and source publications for Fig. 5) revealing a growing contribution of Rubisco to the oscillations. It must be noted, however, that reduced malate oscillation in LL does not necessarily imply a decrease in overall enzymatic activity of PEPC. This is because any malate formed may be immediately decarboxylated in a futile manner resulting in no net accumulation of malate, but also no effect on net CO2 flow into the leaf.
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Indirect evidence for the decreasing ratio of net CAM/C3 carboxylation in LL is also provided by the low values of internal CO2 concentration, which at the time of narrowing of stomatal pores show only slight enrichment over the atmospheric level (Fig. 3). By stark contrast, when CAM is fully operational (i.e. under LD conditions) daytime stomatal closure during phase III of CAM (Osmond, 1978) is associated with, and indeed caused by, greatly elevated substomatal CO2 originating from decarboxylation of the accumulated malate. Enrichment of substomatal air in CO2 over the atmospheric level can, at that time, be considerable (reviewed in Lüttge, 2002b). In the present study it was not possible to calculate the internal concentration of CO2 in phase III under LD due to the tight stomatal closure. However, the progressively higher circadian minima of gH2O observed after transition from LD to continuous light (Fig. 1) are consistent with a dampening of malate decarboxylation and low circadian amplitude of ci. Nevertheless, peaks of the ci/ca ratio at JCO2 minima did occur, and also slightly exceeded the value of one, clearly indicating times of increased malate decarboxylation. The oscillation pattern of ci/ca was much less pronounced in the single time series with elevated PPFD (Fig. 3B), compared with the six data sets obtained at lower light (Fig. 3A). Such difference most likely reflects the variable degree of light saturation of C3 photosynthesis with the higher light level, allowing a faster consumption of CO2 as it is being released from malate. The fact that the ci depletion at times of peak JCO2 was less under higher light is best explained by the much greater stomatal conductance (over 200 mM H2O m–2 s–1) compared with values under 100 mM m–2 s–1 in the low light experiments (data not shown). The greater oscillation of ci in low light need not, therefore, imply stronger PEPC activity peaks, but rather greater stomatal resistance. Such a positive response of stomata to light intensity would be another argument for the prevalence of the C3 photosynthetic mode in extended continuous light.
Lastly, maximal carbon uptake rates in continuous light are often higher than the rates measured in the dark (Figs 1, 2 this study; Fig. 4 in Lüttge and Ball, 1978; Fig. 6Ba in Lüttge and Beck, 1992; Rascher, 2001), evidently because of an additional contribution of Rubisco to overall carbon dioxide uptake. Given the much reduced amplitude of malate fluctuations, the bulk of net carbon uptake is gradually taken over by the C3 pathway. Notably, the dampening of CAM and the rise of direct C3 carboxylation has little effect on phase relations of the JCO2 rhythm, with peaks occurring at regular circadian intervals. The usual complementarity of temporal activity patterns of the two enzymes appears, therefore, to be lost in continuous light. This is further supported by the finding that starch oscillations which are the inverse of malate oscillations in LD, cease after the first cycle in LL (Buchanan-Bollig, 1984). Consistent with the usual substrate saturation of PEPC (Ting, 1994), and the probable substrate competition against Rubisco, the dampening of peaks of net PEPC activity would probably stimulate the activity of Rubisco at those times, assuming that CO2 supply rather than light is initially the limiting factor. Although the issue of light limitation was not explicitly tested here, in the several time series published for K. daigremontiana by Lüttge and Beck, the maximal rate of CO2 uptake increased up to PPFDs of 120–150 µM m–2 s–1 (Lüttge and Beck, 1992; Fig. 3A, B), which are close to those used in the present study. Light saturation at such low PPFDs was explained by these authors by an adaptation of their plants to winter growing conditions in the greenhouse which was also the case with this study’s plants. It remains to be verified whether the present results are reproducible in plants raised under strong light, especially that the specific activity of PEPC in K. daigremontiana is known to be much greater in the summer than in winter (Pilon-Smits et al., 1991). Notwithstanding the uncertainty over the issue of light and CO2 limitation, the gradual switchover between CAM and C3 rhythm in LL is probably associated with a decline in the intensity of substrate competition between these two enzymatic systems.
These considerations lead to the question of overall regulation of the overt JCO2 rhythm that might account for the maintenance of the rhythm in both the presence and absence of CAM. As is becoming increasingly clear, overt self-sustaining rhythms are not necessarily driven by single central clock mechanisms, such as might operate at a gene level, but rather are directed by complex regulatory networks integrated in space and time (Rascher et al., 2001; Lüttge, 2002a). Which element of the network dominates may depend on the phase of the cycle and the time elapsed from its initiation. It appears that the regulatory mechanism controlling the carboxylation through PEPC becomes dysfunctional at a relatively early stage, possibly even beginning during the first endogenous cycle. It must then be functionally replaced by another, C3-related oscillator. The fact that the transition is smooth and does not disturb the trajectory or affect the period of the overt rhythm could be explained by the CAM and C3 oscillators being in phase. However, peaks of JCO2 are clearly associated with subjective night-time (Fig. 1) i.e. the time when C3 photosynthesis might be expected to be down-regulated, should it be subject to circadian control, as shown for several C3 plants (Kreps and Kay, 1997; Staiger, 2002). It appears then that the generation of rhythmic net CO2 uptake is not merely based on the circadian control of individual enzymes, but rather reflects the output of a complex network of dynamic sources and sinks, probably interacting in a less hierarchical and unidirectional manner than traditional models of circadian rhythms suggest (Lillo et al., 2001; Roennenberg et al., 1998). For instance, there is growing evidence that single rhythms can be controlled by several autonomous oscillators (Johnson, 2001). As stomata are known to exhibit circadian oscillations (Webb, 1998; Gorton et al., 1989), the coupling of stomatal and mesophyll clocks in CAM plants needs to be further elucidated. Experimental set-ups should be created to uncouple the individual oscillators and evaluate their potential for self-sustained operation in isolation and in concert.
Hence, it is postulated here that an endogenous rhythm of carbon dioxide uptake in a CAM plant, Kalanchoë daigremontiana, is only initially a result of rhythmic carboxylation through the PEPC enzyme, which is gradually replaced by rhythmic C3 carboxylation. A normally CAM obligate species under continuous light then becomes a C3 plant, much as demonstrated by Friemert et al. (1988) under temperature treatments not conducive to malate storage. The established model of tonoplast acting as a circadian switch of JCO2 (Blasius et al., 1999) is then probably limited to LD and the initial hours of LL, but does not seem to describe the entire free-running rhythm.
The current findings are supplemented by intriguing observations with the C3/CAM intermediate Clusia minor L. Both in the C3-state and in the CAM-state endogenous rhythmicity of gas exchange, JCO2 and gH2O, rapidly dampens out after 3–4 oscillations, and the application of LD thereafter shows that C. minor has fully returned from CAM to normal C3-photosynthesis during the time in LL, clearly showing a rapid down-regulation of PEPC (Lüttge and Duarte, 2002). Finally, experiments with pulses of CO2-free air during LL with K. daigremontiana generate observations on phase-responses of JCO2 (TP Wyka, personal observation) which are not consistent with the oscillatory model of CAM with the vacuolar malate content and tonoplast permeability, and hence PEPC activity, as the only beat oscillator or hysteresis switch mentioned above (Blasius et al., 1999). This emphasizes the high complexity of the biological clock mechanism of CAM and indicates a considerable buffering of overt gas exchange rhythm as compared to its much more dynamic metabolic components.
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Acknowledgements |
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We thank H Duarte for contributing his expert help with gas exchange measurements and in the laboratory. Thanks are due to A Bohn and two anonymous reviewers for commenting on the manuscript. TW gratefully acknowledges support by the Alexander-von-Humboldt Foundation.
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References |
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