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Photosynthetic Characteristics of Portulaca grandiflora, a Succulent C₄ Dicot ¹

CELLULAR COMPARTMENTATION OF ENZYMES AND ACID METABOLISM

Department of Biochemistry, University of Georgia, Athens, Georgia 30602, Richard B. Russell Agricultural Research Center, United States Department of Agriculture, Science and Education Administration, Agricultural Research, P. O. Box 5677, Athens, Georgia 30613

The succulent, cylindrical leaves of the C₄ dicot Portulaca grandiflora possess three distinct green cell types: bundle sheath cells (BSC) in radial arrangement around the vascular bundles; mesophyll cells (MC) in an outer layer adjacent to the BSC; and water storage cells (WSC) in the leaf center. Unlike typical Kranz leaf anatomy, the MC do not surround the bundle sheath tissue but occur only in the area between the bundle sheath and the epidermis. Intercellular localization of photosynthetic enzymes was characterized using protoplasts isolated enzymatically from all three green cell types.

Like other C₄ plants, P. grandiflora has ribulose 1,5-bisphosphate carboxylase and the decarboxylating enzyme, NADP⁺-malic enzyme, in the BSC. Unlike other C₄ plants, however, phosphoenolpyruvate carboxylase, pyruvate, Pi dikinase, and NADP⁺-malate dehydrogenase of the C₄ pathway were present in all three green cell types, indicating that all are capable of fixing CO₂ via phosphoenolpyruvate carboxylase and regenerating phosphoenolpyruvate. Other enzymes were about equally distributed between MC and BSC similar to other C₄ plants. The enzyme profile of the WSC was similar to that of the MC but with reduced activity in most enzymes, except mitochondrion-associated enzymes.

Intracellular localization of enzymes was studied in organelles partitioned by differential centrifugation using mechanically ruptured mesophyll and bundle sheath protoplasts. Phosphoenolpyruvate carboxylase was a cytosolic enzyme in both cells; whereas, ribulose 1,5-bisphosphate carboxylase and NADP⁺-malic enzyme were exclusively compartmentalized in the bundle sheath chloroplasts. NADP⁺-malate dehydrogenase, pyruvate, Pi dikinase, aspartate aminotransferase, 3-phosphoglycerate kinase, and NADP⁺-triose-P dehydrogenase were predominantly localized in the chloroplasts while alanine aminotransferase and NAD⁺-malate dehydrogenase were mainly present in the cytosol of both cell types. Based on enzyme localization, a scheme of C₄ photosynthesis in P. grandiflora is proposed.

Well-watered plants of P. grandiflora exhibit a diurnal fluctuation of total titratable acidity, with an amplitude of 61 and 54 microequivalent per gram fresh weight for the leaves and stems, respectively. These changes were in parallel with changes in malic acid concentration in these tissues. Under severe drought conditions, diurnal changes in both titratable acidity and malic acid concentration in both leaves and stems were much reduced. However, another C₄ dicot Amaranthus graecizans (nonsucculent) did not show any diurnal acid fluctuation under the same conditions. These results confirm the suggestion made by Koch and Kennedy (Plant Physiol. 65: 193-197, 1980) that succulent C₄ dicots can exhibit an acid metabolism similar to Crassulacean acid metabolism plants in certain environments.

¹ Supported in part by Grant PCM 770 8548 from the National Science Foundation.

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