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ABSTRACT Rubisco, the most prevalent protein on Earth, catalyzes both a reaction that initiates C3 carbon fixation, and a reaction that initiates photorespiration, which stimulates protein synthesis. Regulation of the balance between these reactions under atmospheric CO2 fluctuations remains poorly understood. We have hypothesized that vascular plants maintain organic carbon‐to‐nitrogen homeostasis by adjusting the relative activities of magnesium and manganese in chloroplasts to balance carbon fixation and nitrate assimilation rates. The following examined the influence of magnesium and manganese on carboxylation and oxygenation for rubisco purified from two ecotypes of Plantago lanceolataL.: one adapted to the elevated CO2 atmospheres that occur near a natural CO2 spring and the other adapted to more typical CO2 atmospheres that occur nearby. The plastid DNA coding for the large unit of rubisco was similar in both ecotypes. The kinetics of rubiscos from the two ecotypes differed more when associated with manganese than magnesium. Specificity for CO2over O2 (Sc/o) for rubisco from both ecotypes was higher when the enzymes were bound to magnesium than manganese. Differences in the responses of rubisco from P. lanceolata to the metals may account for the adaptation of this species to different CO2 environments.
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Metals and other ligands balance carbon fixation and photorespiration in chloroplasts
Abstract The behavior of many plant enzymes depends on the metals and other ligands to which they are bound. A previous study demonstrated that tobacco Rubisco binds almost equally to magnesium and manganese and rapidly exchanges one metal for the other. The present study characterizes the kinetics of Rubisco and the plastidial malic enzyme when bound to either metal. When Rubisco purified from five C3species was bound to magnesium rather than manganese, the specificity for CO2over O2, (Sc/o) increased by 25% and the ratio of the maximum velocities of carboxylation / oxygenation (Vcmax/Vomax) increased by 39%. For the recombinant plastidial malic enzyme, the forward reaction (malate decarboxylation) was 30% slower and the reverse reaction (pyruvate carboxylation) was three times faster when bound to manganese rather than magnesium. Adding 6‐phosphoglycerate and NADP+inhibited carboxylation and oxygenation when Rubisco was bound to magnesium and stimulated oxygenation when it was bound to manganese. Conditions that favored RuBP oxygenation stimulated Rubisco to convert as much as 15% of the total RuBP consumed into pyruvate. These results are consistent with a stromal biochemical pathway in which (1) Rubisco when associated with manganese converts a substantial amount of RuBP into pyruvate, (2) malic enzyme when associated with manganese carboxylates a substantial portion of this pyruvate into malate, and (3) chloroplasts export additional malate into the cytoplasm where it generates NADH for assimilating nitrate into amino acids. Thus, plants may regulate the activities of magnesium and manganese in leaves to balance organic carbon and organic nitrogen as atmospheric CO2fluctuates.
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- Award ID(s):
- 1904535
- PAR ID:
- 10531945
- Publisher / Repository:
- Wiley-Blackwell
- Date Published:
- Journal Name:
- Physiologia Plantarum
- Volume:
- 176
- Issue:
- 4
- ISSN:
- 0031-9317
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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