PHOSPHO<i>ENOL</i>PYRUVATE CARBOXYLASE: A Ubiquitous, Highly Regulated Enzyme in Plants

Chollet, Raymond; Vidal, Jean; O’Leary, Marion H.

doi:10.1146/annurev.arplant.47.1.273

Cited by 644 publications

(605 citation statements)

References 136 publications

(204 reference statements)

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“…A number of studies thus far have shown that CAM-specific PEPC1 transcripts in a 553 facultative CAM plant show higher abundance at night (Cushman et al, 2008), whereas in C 3 554 and C 4 plants, these transcripts are more abundant during the day (Chollet et al, 1996). Previous 555 findings suggest that the PEPC activity is increased at night; however, its protein abundance 556 pattern varies over the diel cycle in facultative CAM species (Häusler et al, 2000).…”

Section: Cam In Agave 552mentioning

confidence: 99%

Transcript, protein and metabolite temporal dynamics in the CAM plant Agave

et al. 2016

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Already a proven mechanism for drought resilience, crassulacean acid metabolism (CAM) is a specialized type of photosynthesis that maximizes water-use efficiency by means of an inverse (compared to C 3 and C 4 photosynthesis) day/ night pattern of stomatal closure/opening to shift CO 2 uptake to the night, when evapotranspiration rates are low. A systems-level understanding of temporal molecular and metabolic controls is needed to define the cellular behaviour underpinning CAM. Here, we report high-resolution temporal behaviours of transcript, protein and metabolite abundances across a CAM diel cycle and, where applicable, compare the observations to the well-established C 3 model plant Arabidopsis. A mechanistic finding that emerged is that CAM operates with a diel redox poise that is shifted relative to that in Arabidopsis. Moreover, we identify widespread rescheduled expression of genes associated with signal transduction mechanisms that regulate stomatal opening/closing. Controlled production and degradation of transcripts and proteins represents a timing mechanism by which to regulate cellular function, yet knowledge of how this molecular timekeeping regulates CAM is unknown. Here, we provide new insights into complex post-transcriptional and -translational hierarchies that govern CAM in Agave. These data sets provide a resource to inform efforts to engineer more efficient CAM traits into economically valuable C 3 crops.T he water-use efficiency of Agave spp. hinges on crassulacean acid metabolism (CAM), a specialized mode of photosynthesis that evolved from ancestral C 3 photosynthesis in response to water and CO 2 limitation 1 and is found in ∼6.5% of higher plants. Whereas C 3 photosynthesis produces a three-carbon (3-C) molecule for carbon fixation during the day, CAM generates a four-carbon organic acid from carbon fixation at night. In CAM, this nocturnal carboxylation reaction is catalysed by phosphoenolpyruvate carboxylase (PEPC), and the 3-C substrate phosphoenolpyruvate (PEP) is supplied by the glycolytic breakdown of carbohydrate formed during the previous day. The nocturnally accumulated malic acid is stored overnight in a central vacuole, and during the subsequent day malate is decarboxylated to release CO 2 at an elevated concentration for Rubisco in the chloroplast. The diel separation of carboxylases in CAM is accompanied by an inverse (compared with C 3 and C 4 photosynthesis-performing species) day/night pattern of stomatal closure/ opening that results in improved water-use efficiency (CO 2 fixed per unit water lost) that is up to sixfold higher than that of C 3 photosynthesis plants and up to threefold higher than that of C 4 photosynthesis plants under comparable conditions 2 .The frequent emergence of CAM from C 3 photosynthesis throughout evolutionary history implies that all of the enzymes required for CAM are homologues of ancestral forms found in C 3 species 1,3 . As such, the CAM pathway has been identified as a target for synthetic biology because it offers the potential to engin...

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Section: Cam In Agave 552mentioning

confidence: 99%

Transcript, protein and metabolite temporal dynamics in the CAM plant Agave

et al. 2016

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“…PEPC is a highly regulated enzyme that is allosterically activated by Glc-6-P and triose-P and inhibited by L-malate and Asp (Schuller et al, 1990). Furthermore, the sensitivity of the protein to allosteric regulation is modified by its phosphorylation state (Chollet et al, 1996). When phosphorylated, the protein is less sensitive to allosteric regulation.…”

Section: Is Cellular Metabolism Specialized During Cluster-root Carbomentioning

confidence: 99%

Developmental Physiology of Cluster-Root Carboxylate Synthesis and Exudation in Harsh Hakea. Expression of Phosphoenolpyruvate Carboxylase and the Alternative Oxidase

Shane¹,

Cramer²,

et al. 2004

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Harsh hakea (Hakea prostrata R.Br.) is a member of the Proteaceae family, which is highly represented on the extremely nutrientimpoverished soils in southwest Australia. When phosphorus is limiting, harsh hakea develops proteoid or cluster roots that release carboxylates that mobilize sparingly soluble phosphate in the rhizosphere. To investigate the physiology underlying the synthesis and exudation of carboxylates from cluster roots in Proteaceae, we measured O 2 consumption, CO 2 release, internal carboxylate concentrations and carboxylate exudation, and the abundance of the enzymes phosphoenolpyruvate carboxylase and alternative oxidase (AOX) over a 3-week time course of cluster-root development. Peak rates of citrate and malate exudation were observed from 12-to 13-d-old cluster roots, preceded by a reduction in cluster-root total protein levels and a reduced rate of O 2 consumption. In harsh hakea, phosphoenolpyruvate carboxylase expression was relatively constant in cluster roots, regardless of developmental stage. During cluster-root maturation, however, the expression of AOX protein increased prior to the time when citrate and malate exudation peaked. This increase in AOX protein levels is presumably needed to allow a greater flow of electrons through the mitochondrial electron transport chain in the absence of rapid ATP turnover. Citrate and isocitrate synthesis and accumulation contributed in a major way to the subsequent burst of citrate and malate exudation. Phosphorus accumulated by harsh hakea cluster roots was remobilized during senescence as part of their efficient P cycling strategy for growth on nutrient impoverished soils.In some plant species, a shortage of phosphorus induces the development of dense clusters of determinate branch roots (rootlets) that arise, en masse, from a localized region of the parent root axis. These short-lived structures have been termed proteoid roots because they were first described for Proteaceae (Purnell, 1960) but have since been found in a wide range of other species and families and are now often referred to as cluster roots . Most of our advances in cluster-root biology have been derived from studies of the crop species Lupinus albus (Fabaceae family) (Gardner et al

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“…Nitrate assimilation and organic acid metabolism also respond to changes of cellular pH. Alkalization leads to post-translational inhibition of NIA (Kaiser & BrendleBehnisch 1995;Botrel & Kaiser 1997), and activates PEPC by decreasing sensitivity to feedback inhibition by malate (Chollet, Vidal & O'Leary 1996;Nimmo 2000).…”

Section: Introductionmentioning

confidence: 99%

Influence of malate and 2-oxoglutarate on the NIA transcript level and nitrate reductase activity in tobacco leaves

Muller¹,

Scheible²,

Stitt³

et al. 2001

Plant Cell Environ

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slightly accelerated by 2-oxoglutarate. (iv) Plants were placed in the dark for 60 h to reduce NIA activity to the limit of detection, and leaf discs were then incubated in the dark on sucrose to achieve a photosynthesis-independent increase of NIA activity. This was strongly inhibited by malate. (v) It is concluded that malate inhibits NIA expression, affecting both the NIA transcript level and NIA activity. Although the results are consistent with a role for 2-oxoglutarate in the regulation of NIA expression, the impact is less marked and no endogenous changes of 2-oxoglutarate were found that are likely to have a significant effect on NIA expression.

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PHOSPHOENOLPYRUVATE CARBOXYLASE: A Ubiquitous, Highly Regulated Enzyme in Plants

Cited by 644 publications

References 136 publications

Transcript, protein and metabolite temporal dynamics in the CAM plant Agave

Transcript, protein and metabolite temporal dynamics in the CAM plant Agave

Developmental Physiology of Cluster-Root Carboxylate Synthesis and Exudation in Harsh Hakea. Expression of Phosphoenolpyruvate Carboxylase and the Alternative Oxidase

Influence of malate and 2-oxoglutarate on the NIA transcript level and nitrate reductase activity in tobacco leaves

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