Photosynthetica 2000, 38(3):385-391 | DOI: 10.1023/A:1010969419962
Changes in Properties of Phosphoenolpyruvate Carboxylase with Induction of Crassulacean Acid Metabolism (CAM) in the C4 Plant Portulaca Oleracea
- 1 Department of Botany, Faculty of Science at Sohag, South Valley University, Sohag, Egypt
Aiming at understanding the odd case of CAM expression by a C4 plant, some properties of phosphoenolpyruvate carboxylase (PEPC, EC 4.1.1.31, orthophosphate: oxaloacetate carboxylyase, phosphorylating) were comparatively studied in leaves of CAM-expressing and non-expressing Portulaca oleracea L. plants. CAM expression was induced by growing plants under an 8-h photoperiod and under water-stress. CAM induction in leaves of these plants (designated as CAM) is indicated by the nocturnal acidification and by the clear diurnal oscillation pattern and amplitude of acidity, malic acid, and PEPC activity characteristic of CAM plants. Treatment of the other plant group (designated as C4) by growth under a 16-h photoperiod and well-watered conditions did not induce expression of the tested criteria of CAM in plants. In these C4 plants, the mentioned CAM criteria were undetectable. PEPC from CAM and C4Portulaca responded differently to any of the studied assay conditions or effectors. For example, extent and timing of sensitivity of PEPC to pH change, inhibition by malate, activation by glucose-6-phosphate or inorganic phosphate, and the enzyme affinity to the substrate PEP were reversed with induction of CAM from the C4-P. oleracea. These contrasting responses indicate distinct kinetic and regulatory properties of PEPC of the two modes. Thus by shifting to CAM in the C4Portulaca a new PEPC isoform may be synthesised to meet CAM requirements. Simultaneous occurrence of both C4 and CAM is suggested in P. oleracea when challenged with growth under stress.
Additional key words: malic acid
Prepublished online: April 1, 2000; Published: October 1, 2000 Show citation
| ACS | AIP | APA | ASA | Harvard | Chicago | Chicago Notes | IEEE | ISO690 | MLA | NLM | Turabian | Vancouver |
References
- Bradford, M.M.: A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding.-Anal. Biochem. 72: 248-254, 1976.
Go to original source... - Brulfert, J., Arrabaca, M.C., Guerrier, D., Queiroz, O.: Changes in the isozymic pattern of phosphoenolpyruvate carboxylase. An early step in photoperiodic control of Crassulacean acid metabolism level.-Planta 146: 129-133, 1979.
Go to original source... - Brulfert, J., Müller, D., Kluge, M., Queiroz, O.: Photoperiodism and Crassulacean acid metabolism. I. Immunological and kinetic evidences for different patterns of phosphoenolpyruvate carboxylase isoforms in photoperiodically inducible and non-inducible Crassulacean acid metabolism plants.-Planta 154: 326-331, 1982.
Go to original source... - Brulfert, J., Queiroz, O.: Photoperiodism and Crassulacean acid metabolism. III. Different characteristics of the photoperiod-sensitive and non-sensitive isoforms of phosphoenolpyruvate carboxylase and Crassulacean acid metabolism operation.-Planta 154: 339-343, 1982.
Go to original source... - Carter, P.J., Nimmo, H.G., Fewson, C.A., Wilkins, M.B.: Circadian rhythms in the activity of a plant protein kinase.-EMBO J. 10: 2063-2068, 1991.
Go to original source... - Carter, P.J., Wilkins, M.B., Nimmo, H.G., Fewson, C.A.: Effects of temperature on the activity of phosphoenolpyruvate carboxylase and on the control of CO2 fixation in Bryophyllum fedtschenkoi.-Planta 196: 375-380, 1995a.
Go to original source... - Carter, P.J., Wilkins, M.B., Nimmo, H.G., Fewson, C.A.: The role of temperature in the regulation of the circadian-rhythm of CO2 fixation in Bryophyllum fedtschenkoi.-Planta 196: 381-386, 1995b.
Go to original source... - Chollet, R., Vidal, J., O'Leary, M.H.: Phosphoenolpyruvate carboxylase: A ubiquitous, highly regulated enzyme in plants.-Annu. Rev. Plant Physiol. Plant mol. Biol. 47: 273-298, 1996.
Go to original source... - Chu, C., Dai, Z., Ku, M.S.B., Edwards, G.E.: Induction of Crassulacean acid metabolism in the facultative halophyte Mesembryanthemum crystallinum by abscissic acid.-Plant Physiol. 93: 1253-1260, 1990.
Go to original source... - Cushman, J.C. Bohnert, H.J.: Crassulacean acid metabolism: Molecular genetics.-Annu. Rev. Plant Physiol. Plant mol. Biol. 50: 305-332, 1999.
Go to original source... - Cushman, J.C., Taybi, T., Bohnert, H.J.: Induction of crassulacean acid metabolism - molecular aspects.-In: Leegood, R.C., Sharkey, T.D., Caemmerer, S. von (ed.): Photosynthesis: Physiology and Metabolism. (In press). Kluwer Academic Publ., Dordrecht 1999.
Go to original source... - Fernández, M.D., Pieters, A., Azkue, M., Rengifo, E., Tezara, W., Woodward, F.I., Herrera, A.: Photosynthesis in plants of four tropical species growing under elevated CO2.-Photosynthetica 37: 587-599, 1999.
Go to original source... - Foster, J.G., Edwards, G.E., Winter, K.: Changes in levels of phosphoenolpyruvate carboxylase with induction of Crassulacean acid metabolism in Mesembryanthemum crystallinum L.-Plant Cell Physiol. 23: 585-594, 1982.
- Gonzalez, M.C., Osuna, L., Echevarra, O.C., Vidal, J., Cejudo, F.J.: Expression and localization of phosphoenolpyruvate carboxylase in developing and germinating wheat grains.-Plant Physiol. 116: 1249-1258, 1998.
Go to original source... - Greenway, H., Winter, K., Lûttge, G.: Phosphoenolpyruvate carboxylase during development of Crassulacean acid metabolism and during a diurnal cycle in Mesembryanthemum crystallinum.-J. exp. Bot. 29: 547-559, 1978.
Go to original source... - Guralnick, L.J., Jackson, M.D.: Crassulacean acid metabolism activity in the family Portulacaceae.-Plant Physiol. 102(Suppl.): 139, 1993.
- Gutmann, I., Wahlefeld, A.W.: L-malate determination with malate dehydrogenase and NAD.-In: Bergmeyer, H.U. (ed.): Methods of Enzymatic Analysis. Vol. 3. Pp. 1585-1589. Verlag Chemie, Weinheim 1974.
- Hanscom, Z., III, Ting, I.P.: Responses of succulents to plant water stress.-Plant Physiol. 61: 327-330, 1978.
Go to original source... - Hartwell, J., Smith, L.H., Wilkins, M.B., Jenkins, G.I., Nimmo, H.G.: Higher plant phosphoenolpyruvate carboxylase kinase is regulated at the level of translatable mRNA in response to light or a circadian rhythm.-Plant J. 10: 1071-1078, 1996.
Go to original source... - Herppich, W., Herppich, M., Willert, D.J. von: The irreversible C3 to CAM shift in well-watered and salt-stressed plants of Mesembryanthemum crystallinum is under strict ontogenetic control.-Bot. Acta 105: 34-40, 1992.
Go to original source... - Holthe, P.A., Patel, A., Ting, I.P.: The occurrence of CAM in Peperomia.-Selbyana 13: 77-87, 1992.
- Holtum, J.A.M., Winter, K.: Activity of enzymes of carbon metabolism during the induction of Crassulacean acid metabolism in Mesembryanthemum crystallinum L.-Planta 155: 8-16, 1982.
Go to original source... - Keeley, J.E.: Diel acid fluctuations in C4 amphibious grasses.-Photosynthetica 35: 273-277, 1998.
Go to original source... - Koch, K.E., Kennedy, R.A.: Characteristics of Crassulacean acid metabolism in the succulent C4 dicot Portulaca oleracea L.-Plant Physiol. 65: 193-197, 1980.
Go to original source... - Koch, K.E., Kennedy, R.A.: Crassulacean acid metabolism in the succulent C4 dicot, Portulaca oleracea L. under natural environmental conditions.-Plant Physiol. 69: 757-761, 1982.
Go to original source... - Kraybill, A.A., Martin, C.E.: Crassulacean acid metabolism in three species of the C4 genus Portulaca.-Int. J. Plant Sci. 157: 103-109, 1996.
Go to original source... - Ku, S.-B., Shieh, Y.-J., Reger, B.J., Black, C.C.: Photosynthetic characteristics of Portulaca grandiflora, a succulent C4 dicot. Cellular compartmentation of enzymes and acid metabolism.-Plant Physiol. 68: 1037-1080, 1981.
Go to original source... - Lillo, C., Smith, L.H., Nimmo, H.G., Wilkins, M.B.: Regulation of nitrate reductase and phosphoenolpyruvate carboxylase activities in barley leaf protoplasts.-Planta 200: 181-185, 1996.
Go to original source... - Mazen, A.M.A.: Changes in levels of phosphoenolpyruvate carboxylase with induction of Crassulacean acid metabolism (CAM)-like behavior in the C4 plant Portulaca oleracea.-Physiol. Plant. 98: 111-116, 1996.
Go to original source... - McNaughton, G.A.L., MacKintosh, C., Fewson, C.A., Wilkins, M.B., Nimmo, H.G.: Illumination increases the phosphorylation state of maize leaf phosphoenolpyruvate carboxylase by causing an increase in the activity of a protein kinase.-Biochim. biophys. Acta 1093: 189-195, 1991.
Go to original source... - Milburn, T.R., Peason, D.J., Ndegwe, N.A.: Crassulacean Acid Metabolism under natural tropical conditions.-New Phytol. 67: 883-897, 1968.
Go to original source... - Nishio, J.N., Ting, I.P.: Carbon flow and metabolic specialization in the tissue layers of the Crassulacean acid metabolism plant, Peperomia camptotricha.-Plant Physiol. 84: 600-604, 1987.
Go to original source... - Olivares, E., Urich, R., Montes, G., Coronel, I., Herrera, A.: Occurrence of Crassulacean acid metabolism in Cissus trifoliata L. (Vitaceae).-Oecologia 61: 358-362, 1984.
Go to original source... - Pierre, J.N., Queiroz, O.: Regulation of glycolysis and level of the Crassulacean acid metabolism.-Planta 144: 143-151, 1978.
Go to original source... - Queiroz, O., Morel, C.: Photoperiodism and enzyme activity. Towards a model for the control of circadian metabolic rhythms in the crassulacean acid metabolism.-Plant Physiol. 53: 596-602, 1974.
Go to original source... - Schuber, M., Kluge, M.: In situ studies on Crassulacean Acid Metabolism in Sedum acer L. and Sedum mite Gil.-Oecologia 50: 82-87, 1981.
Go to original source... - Smith, L.H., Lillo, C., Nimmo, H.G., Wilkins, M.B.: Light regulation of phosphoenolpyruvate carboxylase in barley mesophyll protoplasts is modulated by protein synthesis and calcium, and not necessarily correlated with phosphoenolpyruvate carboxylase kinase activity.-Planta 200: 174-180, 1996.
Go to original source... - Svensson, P., Blasing, O.E., Westhoff, P.: Evolution of the enzymatic characteristics of C4 phosphoenolpyruvate carboxylase - a comparison of the orthologous PPCA phosphoenolpyruvate carboxylases of Flaveria trinervia (C4) and Flaveria pringlei (C3).-Eur. J. Biochem. 246: 452-460, 1997.
Go to original source... - Ting, I.P.: Crassulacean acid metabolism.-Annu. Rev. Plant Physiol. 36: 595-622, 1985.
Go to original source... - Ting, I.P., Patel, A., Sipes, D.L., Reid, P.D., Walling, L.L.: Differential expression of photosynthesis genes in leaf tissue layers of Peperomia as revealed by tissue printing.-Amer. J. Bot. 81: 414-422, 1994.
Go to original source... - Vidal, J., Chollet, R.: Regulatory phosphorylation of C4 PEP carboxylase.-Trends Plant Sci. 2: 230-241, 1997.
Go to original source... - Walker, R.P., Leegood, R.C.: Phosphorylation of phosphoenolpyruvate carboxykinase in plants. Studies in plants with C4 photosynthesis and Crassulacean acid metabolism and in germinating seeds.-Biochem. J. 317: 653-658, 1996.
Go to original source... - Winter, K.: Effect of different CO2 regimes on the induction of Crassulacean acid metabolism in Mesembryanthemum crystallinum L.-Aust. J. Plant Physiol. 6: 589-594, 1979.
Go to original source... - Winter, K.: Change in properties of phosphoenolpyruvate carboxylase from the crassulacean acid metabolism plant Mesembryanthemum crystallinum after isolation.-Aust. J. Plant Physiol. 8: 115-119, 1981.
Go to original source... - Winter, K.: Properties of phosphoenolpyruvate carboxylase in rapidly prepared, desalted leaf extracts of the Crassulacean acid metabolism plant Mesembryanthemum crystallinum L.-Planta 154: 298-308, 1982.
Go to original source... - Winter, K., Foster, J.G., Edwards, G.E., Holtum, J.A.M.: Intracellular localization of enzymes of carbon metabolism in Mesembryanthemum crystallinum exhibiting C3 photosynthetic characteristics or performing Crassulacean acid metabolism.-Plant Physiol. 69: 300-307, 1982.
Go to original source... - Winter, K., Troughton, J.H.: Carbon assimilation pathways in Mesembryanthemum nodiflorum L. under natural conditions.-Z. Pflanzenphysiol. 88: 153-162, 1978.
Go to original source...




