Posttranslational Regulation of Phosphoenolpyruvate Carboxylase in C₄ and Crassulacean Acid Metabolism Plants

Abstract

Control of C4 photosynthesis and Crassulacean acid metabolism (CAM) is, in part, mediated by the diel regulation of phosphoenolpyruvate carboxylase (PEPC) activity. The nature of this regulation of PEPC in the leaf cell cytoplasm of C4 and CAM plants is both metabolite-related and posttranslational. Specifically, the regulatory properties of the enzyme vary in accord with the physiological activity of C4 photosynthesis and CAM: PEPC is less sensitive to feedback inhibition by L-malate under light (C4 plants) or Based on physiological and biochemical considerations, it is evident that PEPC activity must be regulated by light + dark transitions in C4 and CAM species in order to: (a) coordinate C4-and C3-photosynthetic carbon metabolism in response to light intensity in C4 plants (7, 10); (b) avoid futile decarboxylation/carboxylation cycling during the day in CAM plants (21); and (c) minimize uncontrolled utilization of glycolytic PEP during the dark in C4 plants (2, 7). While light-induced changes in the cytoplasmic levels of known metabolite effectors (e.g. glucose 6-P, L-malate, triose-P) likely contribute to the overall regulation of PEPC activity (5, 7, 21), recent attention has focused on the diel regulation of this enzyme's activity in C4 and CAM species by posttranslational modification. In this review we summarize the recent developments in this latter area of research and discuss the molecular mechanism(s) involved in this regulatory process.GENERAL PROPERTIES OF THE REGULATORY PROCESS The initial interest in the posttranslational modulation of PEPC activity came from work on the diel regulation of CAM. The enzyme responsible for the initial fixation of atmospheric CO2 by CAM plants in darkness is PEPC, which, like the C4 isoform, is activated allosterically by glucose 6-P and feedback inhibited by L-malate (7,21 (20,29).

Phosphoenolpyruvate Carboxylase Kinase in Tobacco Leaves Is Activated by Light in a Similar but Not Identical Way as in Maize

“…Two seemingly different scenarios exist for modulating the activity of PEPC-PK in C, and CAM leaves. In the former, light activates and darkness inactivates the kinase in vivo (Echevarria et al, 1990;Jiao and Chollet, 1991;Nimmo, 1993). Moreover, treatment of C, leaves with inhibitors of photosynthesis or cytosolic protein synthesis prevents this light activation of PEPC-PK (Jiao et al, 1991a;Bakrim et al, 1992Bakrim et al, , 1993Jiao and Chollet, 1992;Li and Chollet, 1993), implicating the involvement of photosynthesis and protein turnover in the light-signal transduction pathway.…”

“…It is well established that PEPC in C, and CAM leaves is regulated by reversible protein phosphorylation and that this process in turn is controlled by a highly regulated protein-Ser/Thr kinase (Jiao and Chollet, 1991;Nimmo, 1993;Huber et al, 1994;Lepiniec et al, 1994). Two seemingly different scenarios exist for modulating the activity of PEPC-PK in C, and CAM leaves.…”

Multiple cDNAs of phosphoenolpyruvate car☐ylase in the C4 dicotFlaveria trinervia

“…There is evidence that this part of the enzyme is involved in phosphoenolpyruvate binding and catalytic activity [2,17]. The serine-15 residue of the maize PEPCase undergoes reversible phosphorylation during light/dark transitions which is correlated with changes in the activation state of the enzyme [3]. The structural motif Lys/Arg-X-X-Ser of this phosphorylation site i~ also present at the corresponding position of the F. trinervia enzyme.…”

“…The structural motif Lys/Arg-X-X-Ser of this phosphorylation site i~ also present at the corresponding position of the F. trinervia enzyme. Thus, this element is shared by the C4 and CAM isoforms but is lacking in the C:isoenzyme [3,18].…”

“…malate or aspartate, act as feedback-inhibitors [1,2]. The PEPCase of C4 plants is also subject to a light/dark regulation which is mediated by reversible phosphorylation of a single serine residue in the amino-terminal part of the enzyme [3].…”