Pyruvate,Pi Dikinase and NADP-Malate Dehydrogenase in C4 Photosynthesis: Properties and Mechanism of Light/Dark Regulation

Edwards, Gerald E.; Nakamoto, Hitoshi; Burnell, James N.; Hatch, M.D.

doi:10.1146/annurev.pp.36.060185.001351

Cited by 196 publications

(92 citation statements)

References 61 publications

(107 reference statements)

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“…First, chloroplast PPDKs accumulate in excess, constituting approximately 7% to 10% of the protein content of mesophyll cells (Baer and Schrader, 1985;Edwards et al, 1985), ensuring that a sufficient supply of PPDKs is available for C 4 photosynthesis, as required. Our results demonstrate that even when PPDK activity reaches its maximum level (when the phosphorylation level at Thr-527 reaches its minimum) at a light intensity of 800 mmol m -2 s -1 , approximately one-third of the total of PPDK is still phosphorylated ( Fig.…”

Section: Discussionmentioning

confidence: 99%

Posttranslational Modification of Maize Chloroplast Pyruvate Orthophosphate Dikinase Reveals the Precise Regulatory Mechanism of Its Enzymatic Activity

Chen

Wang

et al. 2014

Plant Physiol.

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In C 4 plants, pyruvate orthophosphate dikinase (PPDK) activity is tightly dark/light regulated by reversible phosphorylation of an active-site threonine (Thr) residue; this process is catalyzed by PPDK regulatory protein (PDRP). Phosphorylation and dephosphorylation of PPDK lead to its inactivation and activation, respectively. Here, we show that light intensity rather than the light/dark transition regulates PPDK activity by modulating the reversible phosphorylation at Thr-527 (previously termed Thr-456) of PPDK in maize (Zea mays). The amount of PPDK (unphosphorylated) involved in C 4 photosynthesis is indeed strictly controlled by light intensity, despite the high levels of PPDK protein that accumulate in mesophyll chloroplasts. In addition, we identified a transit peptide cleavage site, uncovered partial amino-terminal acetylation, and detected phosphorylation at four serine (Ser)/Thr residues, two of which were previously unknown in maize. In vitro experiments indicated that Thr-527 and Ser-528, but not Thr-309 and Ser-506, are targets of PDRP. Modeling suggests that the two hydrogen bonds between the highly conserved residues Ser-528 and glycine-525 are required for PDRP-mediated phosphorylation of the active-site Thr-527 of PPDK. Taken together, our results suggest that the regulation of maize plastid PPDK isoform (C 4 PPDK) activity is much more complex than previously reported. These diverse regulatory pathways may work alone or in combination to fine-tune C 4 PPDK activity in response to changes in lighting.

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Section: Discussionmentioning

confidence: 99%

Posttranslational Modification of Maize Chloroplast Pyruvate Orthophosphate Dikinase Reveals the Precise Regulatory Mechanism of Its Enzymatic Activity

Chen

Wang

et al. 2014

Plant Physiol.

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“…About 50% of pyruvate in maize leaves was in mesophyll cells under high light intensity (26). If we assume that 60% of the Chl in maize leaves is in mesophyll chloroplasts (16) with a stromal volume of 25 Ald-L-' and tentatively that 40 to 80% of pyruvate in mesophyll cells is in the mesophyll chloroplasts under high light intensity, then 300 nmol pyruvate-mg-' Chl corresponded to 5 to 10 mm of pyruvate in mesophyll chloroplasts which is far above the Km for pyruvate of pyruvate,Pi dikinase (0.25 mM) (6). Thus, the level of pyruvate does not limit the activity of pyruvate,Pi dikinase under high light intensity.…”

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confidence: 94%

Changes in Levels of Intermediates of the C₄ Cycle and Reductive Pentose Phosphate Pathway under Various Light Intensities in Maize Leaves

Usuda¹

1987

Plant Physiol.

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The rate of CO2 assimilation and levels of metabolites of the C4 cycle and reductive pentose phosphate pathway in attached leaves of maize (Zea mays L.) were (17,18,25). However, recent reports revealed that there were up to 30-fold differences in PEP carboxylase activity during dark to light transitions in maize when assayed in simulated conditions of dark or light or in the presence of effectors (5, 13). Studies of metabolite levels during induction in maize leaves (9, 20, 28) provided a basis for in vitro simulation ofconditions in vivo. The total level of the C4 cycle intermediates (malate, aspartate, pyruvate, PEP, and alanine) increased during induction (28) and also with increasing CO2 concentration (31,32) as the photosynthesis rate increased. These findings suggested that input of carbon into the C4 cycle and an increase in the total level of the C4 cycle intermediates is required to increase the photosynthetic rate in maize leaves (9,28,31,32).Although the influence of light intensity on metabolite levels in C4 plants has not been reported, this is an important environmental factor controlling C4 photosynthesis. Thus, the purpose of this study was to measure changes in photosynthetic metabolite levels in maize leaves under steady-state photosynthesis with varying light intensities.Recently, studies have been conducted on changes in photosynthetic metabolite levels during the induction period (9,20,28), and under steady-state photosynthesis with normal atmospheric conditions (19, 26) and with varying CO2 concentration (31) in maize leaves. These studies have increased our understanding of C4 photosynthesis and they provide a new approach to research in C4 plant. In part they have shown that there are sufficient concentration gradients between the mesophyll and bundle sheath to facilitate intercellular transport of certain C4 cycle intermediates by diffusion during C4 photosynthesis (19,

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“…Low extractable activities, often only just sufficient to support in vivo rates of photosynthesis, have been reported frequently (Long, 1983;Edwards et al, 1985). PPDK catalyzes the regeneration of PEP as the primary acceptor of atmospheric CO 2 from pyruvate, ATP, and phosphate in C 4 photosynthesis.…”

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Cool C4 Photosynthesis: Pyruvate Pi Dikinase Expression and Activity Corresponds to the Exceptional Cold Tolerance of Carbon Assimilation inMiscanthus×giganteus

et al. 2008

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The bioenergy feedstock grass Miscanthus 3 giganteus is exceptional among C 4 species for its high productivity in cold climates. It can maintain photosynthetically active leaves at temperatures 6°C below the minimum for maize (Zea mays), which allows it a longer growing season in cool climates. Understanding the basis for this difference between these two closely related plants may be critical in adapting maize to colder weather. When M. 3 giganteus and maize grown at 25°C were transferred to 14°C, light-saturated CO 2 assimilation and quantum yield of photosystem II declined by 30% and 40%, respectively, in the first 48 h in these two species. The decline continued in maize but arrested and then recovered partially in M. 3 giganteus. Within 24 h of the temperature transition, the pyruvate phosphate dikinase (PPDK) protein content per leaf area transiently declined in M. 3 giganteus but then steadily increased, such that after 7 d the enzyme content was significantly higher than in leaves growing in 25°C. By contrast it declined throughout the chilling period in maize leaves. Rubisco levels remained constant in M. 3 giganteus but declined in maize. Consistent with increased PPDK protein content, the extractable PPDK activity per unit leaf area (V max,ppdk ) in cold-grown M. 3 giganteus leaves was higher than in warm-grown leaves, while V max,ppdk was lower in coldgrown than in warm-grown maize. The rate of light activation of PPDK was also slower in cold-grown maize than M. 3 giganteus. The energy of activation (E a ) of extracted PPDK was lower in cold-grown than warm-grown M. 3 giganteus but not in maize. The specific activities and E a of purified recombinant PPDK from M. 3 giganteus and maize cloned into Escherichia coli were similar. The increase in PPDK protein in the M. 3 giganteus leaves corresponded to an increase in PPDK mRNA level. These results indicate that of the two enzymes known to limit C 4 photosynthesis, increase of PPDK, not Rubisco content, corresponds to the recovery and maintenance of photosynthetic capacity. Functionally, increased enzyme concentration is shown to increase stability of M. 3 giganteus PPDK at low temperature. The results suggest that increases in either PPDK RNA transcription and/or the stability of this RNA are important for the increase in PPDK protein content and activity in M. 3 giganteus under chilling conditions relative to maize.

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Pyruvate,Pi Dikinase and NADP-Malate Dehydrogenase in C4 Photosynthesis: Properties and Mechanism of Light/Dark Regulation

Cited by 196 publications

References 61 publications

Posttranslational Modification of Maize Chloroplast Pyruvate Orthophosphate Dikinase Reveals the Precise Regulatory Mechanism of Its Enzymatic Activity

Posttranslational Modification of Maize Chloroplast Pyruvate Orthophosphate Dikinase Reveals the Precise Regulatory Mechanism of Its Enzymatic Activity

Changes in Levels of Intermediates of the C₄ Cycle and Reductive Pentose Phosphate Pathway under Various Light Intensities in Maize Leaves

Cool C4 Photosynthesis: Pyruvate Pi Dikinase Expression and Activity Corresponds to the Exceptional Cold Tolerance of Carbon Assimilation inMiscanthus×giganteus

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Pyruvate,Pi Dikinase and NADP-Malate Dehydrogenase in C4 Photosynthesis: Properties and Mechanism of Light/Dark Regulation

Cited by 196 publications

References 61 publications

Posttranslational Modification of Maize Chloroplast Pyruvate Orthophosphate Dikinase Reveals the Precise Regulatory Mechanism of Its Enzymatic Activity

Posttranslational Modification of Maize Chloroplast Pyruvate Orthophosphate Dikinase Reveals the Precise Regulatory Mechanism of Its Enzymatic Activity

Changes in Levels of Intermediates of the C4 Cycle and Reductive Pentose Phosphate Pathway under Various Light Intensities in Maize Leaves

Cool C4 Photosynthesis: Pyruvate Pi Dikinase Expression and Activity Corresponds to the Exceptional Cold Tolerance of Carbon Assimilation inMiscanthus×giganteus

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Changes in Levels of Intermediates of the C₄ Cycle and Reductive Pentose Phosphate Pathway under Various Light Intensities in Maize Leaves