How to tell the time: the regulation of phosphoenolpyruvate carboxylase in Crassulacean acid metabolism (CAM) plants

Abstract

Crassulacean acid metabolism (CAM) plants exhibit persistent circadian rhythms of CO(2) metabolism. These rhythms are driven by changes in the flux through phosphoenolpyruvate carboxylase, which is regulated by reversible phosphorylation in response to a circadian oscillator. This article reviews progress in our understanding of the circadian expression of phosphoenolpyruvate carboxylase kinase.

Phosphorylation of Phosphoenolpyruvate Carboxylase Is Essential for Maximal and Sustained Dark CO2 Fixation and Core Circadian Clock Operation in the Obligate Crassulacean Acid Metabolism Species Kalanchoë fedtschenkoi

“…This work on a C 4 species surprised the wider community because decades of prior work had argued that PPC phosphorylation by PPCK was vital for alleviating malate/aspartate inhibition of PPC in planta and thus for optimizing photosynthetic CO 2 fixation in C 4 and CAM species (Vidal and Chollet, 1997;Nimmo, 2003). These findings have become all the more surprising in the light of recent work on the evolution of the PPCK gene family in C 3 and C 4 species of Flaveria (Aldous et al, 2014).…”

“…Since the first discovery of PPCK activity and its circadian control in 1991 (Carter et al, 1991), through the subsequent cloning and characterization of the gene encoding this remarkable protein kinase in 1999 (Hartwell et al, 1999), there has been a long-held assumption that this circadian clock-controlled kinase is crucial for the temporal coordination and optimization of nocturnal atmospheric CO 2 fixation in CAM species, and the associated persistent circadian rhythm of CO 2 exchange observed under constant conditions in CAM species such as K. fedtschenkoi and K. daigremontiana (Wilkins, 1992;Nimmo, 2003;Wyka et al, 2004;Hartwell, 2006). However, it has not been possible previously to perturb genetically the level of PPCK activity and dark period PPC phosphorylation in a CAM species; thus, it has not been possible to test the validity of this long held assumption about the pivotal role of PPCK in the circadian control of CAM.…”

“…For a CAM leaf, as the dark period progresses, the vacuolar storage capacity for malic acid reaches its limit, and malate begins to accumulate in the cytosol where it feeds back to inhibit PPC activity. In K. fedtschenkoi, the K i of PPC for malate was found to be increased by dark period phosphorylation of the enzyme on an N-terminal serine residue catalyzed by the activity of a specific, Ca 2+ -independent protein kinase, named PPC kinase (PPCK) (Carter et al, 1991;Hartwell et al, 1999;Nimmo, 2000Nimmo, , 2003. The circadian clock controls PPCK transcript levels and activity, such that they peak during the dark period (Hartwell et al, 1996(Hartwell et al, , 1999Taybi et al, 2000;Boxall et al, 2005;Theng et al, 2008).…”

Circadian rhythms are associated with variation in photosystem II function and photoprotective mechanisms

“…Circadian regulation of physiological traits has been documented in a large number of studies across both species and photosynthetic syndromes (Dodd et al, ; Faure et al, ; Graf et al, ; McClung, ; Nimmo, ), and delayed fluorescence expresses circadian oscillations and is a proposed proxy for circadian rhythms (Gould et al, ). Nevertheless, circadian regulation of the light reactions of photosynthesis is not yet well‐understood (Dodd et al, ).…”

Plasticity of crassulacean acid metabolism at subtropical latitudes: a pineapple case study

“…Such conditions may occur frequently during winter. Low night temperature may reduce PEPC activity, however, it also causes a marked decline in the sensitivity of the enzyme to malate inhibition, which thereby facilitates fixation of CO 2 under restrictive conditions (Nimmo ), indicating that relatively low night temperatures may not be the major limitation to pineapple growth at high latitudes.…”