Circadian Rhythmicity: Is the “Biological Clock” Hardware or Software?

Lüttge, Ulrich

doi:10.1007/978-3-642-55819-1_13

Cited by 30 publications

(22 citation statements)

References 274 publications

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“…These are all individual elements of the CAM-related part of the oscillatory machinery. In addition, many components of the C3 photosynthetic apparatus are also regulated in a circadian manner (Lu¨ttge 2002). It appears that, in parallel to a shift in relative contribution of the two carboxylases to J C , the contribution of the CAM timing mechanism may be limited to the early times of .…”

Section: Discussionmentioning

confidence: 99%

“…Notwithstanding an extensive variation related to species characteristics, developmental stage of the photosynthetic organ, and environmental influences (Dodd et al 2002), this rhythm of carbon dioxide uptake and stomatal opening resulting from a dual carboxylation system constitutes the essence of CAM. The regulation of transitions between the different phases involves a complex interplay of metabolic fluxes, environmental signals and one or several circadian pacemakers (Winter and Smith 1996;Nimmo 2000;Lu¨ttge 2000Lu¨ttge , 2002.…”

Section: Introductionmentioning

confidence: 99%

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Perturbations of malate accumulation and the endogenous rhythms of gas exchange in the Crassulacean acid metabolism plant Kalancho� daigremontiana: testing the tonoplast-as-oscillator model

Wyka

Böhn

Duarte

et al. 2004

Planta

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In continuous light, leaves of the Crassulacean acid metabolism (CAM) plant Kalanchoë daigremontiana Hamet et Perrier exhibit a circadian rhythm of CO2 uptake, stomatal conductance and leaf-internal CO2 pressure. According to a current quantitative model of CAM, the pacemaking mechanism involves periodic turgor-related tension and relaxation of the tonoplast, which determines the direction of the net flux of malate between the vacuole and the cytoplasm. Cytoplasmic malate, in turn, through its inhibitory effect on phospho enolpyruvate carboxylase, controls the rate of CO2 uptake. According to this mechanism, when the accumulation of malate is disrupted by removing CO2 from the ambient air, the induction of a phase delay with respect to an unperturbed control plant is expected. First, using the mathematical model, such phase delays were observed in numerical simulations of three scenarios of CO2 removal: (i) starting at a trough of CO2 uptake, lasting for about half a cycle (ca. 12 h in vivo); (ii) with the identical starting phase, but lasting for 1.5 cycles (ca. 36 h); and (iii) starting while CO2 increases, lasting for half a cycle again. Applying the same protocols to leaves of K. daigremontiana in vivo did not induce the predicted phase shifts, i.e. after the end of the CO2 removal the perturbed rhythm adopted nearly the same phase as that of the control plant. Second, when leaves were exposed to a nitrogen atmosphere for three nights prior to onset of continuous light to prevent malate accumulation, a small, 4-h phase advance was observed instead of a delay, again contrary to the model-based expectations. Hence, vacuolar malic acid accumulation is ruled out as the central pacemaking process. This observation is in line with our earlier suggestion [T.P. Wyka, U. Lüttge (2003) J Exp Bot 54:1471-1479] that in extended continuous light, CO2 uptake switches gradually from a CAM-like to a C3-like mechanism, with oscillations of the two CO2 uptake systems being tightly coordinated. It appears that the circadian rhythm of gas exchange in this CAM plant emerges from one or several devices that are capable of generating temporal information in a robust manner, i.e. they are protected from even severe metabolic perturbations.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Perturbations of malate accumulation and the endogenous rhythms of gas exchange in the Crassulacean acid metabolism plant Kalancho� daigremontiana: testing the tonoplast-as-oscillator model

Wyka

Böhn

Duarte

et al. 2004

Planta

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“…CAM represents an noteworthy example of circadian clock specialisation and is one of the best-characterised physiological rhythms in plants (Wilkins 1992;Lüttge 2003;Wyka et al 2004). The presence of the CAM enzymatic machinery within a single cell requires strict temporal control of the competing carboxylation reactions by PEPC and RUBISCO.…”

Section: Circadian Clock Specialisation During Cam Evolutionmentioning

confidence: 99%

Evolution along the crassulacean acid metabolism continuum

Silvera

Neubig

Whitten

et al. 2010

Functional Plant Biol.

193

199

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Abstract. Crassulacean acid metabolism (CAM) is a specialised mode of photosynthesis that improves atmospheric CO 2 assimilation in water-limited terrestrial and epiphytic habitats and in CO 2 -limited aquatic environments. In contrast with C 3 and C 4 plants, CAM plants take up CO 2 from the atmosphere partially or predominantly at night. CAM is taxonomically widespread among vascular plants and is present in many succulent species that occupy semiarid regions, as well as in tropical epiphytes and in some aquatic macrophytes. This water-conserving photosynthetic pathway has evolved multiple times and is found in close to 6% of vascular plant species from at least 35 families. Although many aspects of CAM molecular biology, biochemistry and ecophysiology are well understood, relatively little is known about the evolutionary origins of CAM. This review focuses on five main topics: (1) the permutations and plasticity of CAM, (2) the requirements for CAM evolution, (3) the drivers of CAM evolution, (4) the prevalence and taxonomic distribution of CAM among vascular plants with emphasis on the Orchidaceae and (5) the molecular underpinnings of CAM evolution including circadian clock regulation of gene expression.

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“…The physiology and biochemistry of the circadian rhythm of CAM CO 2 fixation is relatively well characterized (Wilkins, 1992;Lü ttge, 2000Lü ttge, , 2003. Phosphoenolpyruvate carboxylase (PEPc) catalyzes primary CO 2 fixation in CAM plants.…”

mentioning

confidence: 99%

“…One proposal considers that the movement of malate into and out of the vacuole, with the tonoplast functioning as a discrete hysteresis switch, could itself form the basis of the CAM circadian oscillator (Wilkins, 1992;Lü ttge, 2000Lü ttge, , 2003. Computer modeling of this biophysical oscillator has demonstrated that it could sustain robust rhythmicity of CAM over a range of temperatures (Lü ttge, 2000).…”

mentioning

confidence: 99%

Conservation and Divergence of Circadian Clock Operation in a Stress-Inducible Crassulacean Acid Metabolism Species Reveals Clock Compensation against Stress

et al. 2005

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One of the best-characterized physiological rhythms in plants is the circadian rhythm of CO2 metabolism in Crassulacean acid metabolism (CAM) plants, which is the focus here. The central components of the plant circadian clock have been studied in detail only in Arabidopsis (Arabidopsis thaliana). Full-length cDNAs have been obtained encoding orthologs of CIRCADIAN CLOCK-ASSOCIATED1 (CCA1)/LATE ELONGATED HYPOCOTYL (LHY), TIMING OF CAB EXPRESSION1 (TOC1), EARLY FLOWERING4 (ELF4), ZEITLUPE (ZTL), FLAVIN-BINDING KELCH REPEAT F-BOX1 (FKF1), EARLY FLOWERING3 (ELF3), and a partial cDNA encoding GIGANTEA in the model stress-inducible CAM plant, Mesembryanthemum crystallinum (Common Ice Plant). TOC1 and LHY/CCA1 are under reciprocal circadian control in a manner similar to their regulation in Arabidopsis. ELF4, FKF1, ZTL, GIGANTEA, and ELF3 are under circadian control in C3 and CAM leaves. ELF4 transcripts peak in the evening and are unaffected by CAM induction. FKF1 shows an abrupt transcript peak 3 h before subjective dusk. ELF3 transcripts appear in the evening, consistent with their role in gating light input to the circadian clock. Intriguingly, ZTL transcripts do not oscillate in Arabidopsis, but do in M. crystallinum. The transcript abundance of the clock-associated genes in M. crystallinum is largely unaffected by development and salt stress, revealing compensation of the central circadian clock against development and abiotic stress in addition to the well-known temperature compensation. Importantly, the clock in M. crystallinum is very similar to that in Arabidopsis, indicating that such a clock could control CAM without requiring additional components of the central oscillator or a novel CAM oscillator.

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Circadian Rhythmicity: Is the “Biological Clock” Hardware or Software?

Cited by 30 publications

References 274 publications

Perturbations of malate accumulation and the endogenous rhythms of gas exchange in the Crassulacean acid metabolism plant Kalancho� daigremontiana: testing the tonoplast-as-oscillator model

Perturbations of malate accumulation and the endogenous rhythms of gas exchange in the Crassulacean acid metabolism plant Kalancho� daigremontiana: testing the tonoplast-as-oscillator model

Evolution along the crassulacean acid metabolism continuum

Conservation and Divergence of Circadian Clock Operation in a Stress-Inducible Crassulacean Acid Metabolism Species Reveals Clock Compensation against Stress

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