Temperature Modulation of the Activity and Malate Inhibition of the Phosphoenolpyruvate Carboxylase from Leaves of Alternanthera pungens, Compared to that of Lycopersicom esculentum
American Journal of BioScience
Volume 2, Issue 6, November 2014, Pages: 238-243
Received: Nov. 24, 2014; Accepted: Dec. 11, 2014; Published: Dec. 18, 2014
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Bhaskarrao Chinthapalli, Department of Biology, College of Natural Sciences, Arba Minch University, Arba Minch, P.O. Box 21, Ethiopia
D. S. Vijaya Chitra, Department of Biology, College of Natural Sciences, Arba Minch University, Arba Minch, P.O. Box 21, Ethiopia
Agepati S. Raghavendra, Department of Plant Sciences, School of Life Sciences, University of Hyderabad, Prof. C.R Rao Road, Gachibowli, Hyderabad 500 046, Andhra Pradesh, India
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Temperature caused marked modulation of phosphoenolpyruvate carboxylase (PEPC, EC in leaf discs of Alternanthera pungens (C4 plant) as well as Lycopersicon esculentum (C3 species). The optimal incubation temperature for PEPC activity in A. pungens was 45 °C compared to 30 °C in L. esculentum. A. pungens lost nearly 61% of PEPC activity on exposure to a low temperature of 15 °C, compared to only about a 33% loss in the case of L. esculentum. The C4 enzyme was less sensitive to supra-optimal temperature and more sensitive to sub-optimal temperature than that of the C3 species. Further as the temperature was raised from 15 °C to 50 °C, there was a sharp decrease in malate sensitivity of PEPC. The extent of such a decrease in C4 plants was more than that in C3 species. Arrhenius plots that were constructed by plotting the activity of PEPC against the reciprocal of temperature in the absence or presence of malate exhibited abrupt changes or “break-points” at only one point of 17oC in A. pungens while at two points corresponding 17oC and 27oC in case of L. esculentum. The activation energy of PEPC from A. pungens was less compared to that of L. esculentum in the temperature range of 10 to 27oC. However, the activation energy of PEPC from A. pungens was less than that of L. esculentum above the temperature of 27oC. The activation energy increased by 2 to 4 fold at temperatures below 17oC, in case of both A. pungens and L. esculentum. Thus, our results show the activity and malate sensitivity of PEPC can be influenced in relation to high temperature tolerance of C4 plants, which can be physiologically significant.
Temperature, Malate Sensitivity, Cold Sensitivity, PEPC, Arrhenius Plots, Activation Energy
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Bhaskarrao Chinthapalli, D. S. Vijaya Chitra, Agepati S. Raghavendra, Temperature Modulation of the Activity and Malate Inhibition of the Phosphoenolpyruvate Carboxylase from Leaves of Alternanthera pungens, Compared to that of Lycopersicom esculentum, American Journal of BioScience. Vol. 2, No. 6, 2014, pp. 238-243. doi: 10.11648/j.ajbio.20140206.18
L. Lepiniec, J. Vidal, R. Chollet, P. Gadal and C. Crétin, “Phosphoenolpyruvate carboxylase: Structure, regulation and evolution,” Plant Science Vol. 99, 1994, pp. 111-124. doi.org/10.1016/0168-9452(94)90168-6
A. V. Rajagopalan, M. T. Devi and A. S. Raghavendra, “Molecular biology of C4 phosphoenolpyruvate carboxylase: structure, regulation and genetic engineering,” Photosynthesis Research, 1994, Vol. 39, pp. 115-135. doi.10.1007/BF00029380
J. Vidal and R. Chollet, (1997) Regulatory phosphorylation of C4 PEP carboxylase. Trends Plant Science, Vol. 2, 1997, pp. 230-237. doi.org/10.1016/S1360-1385(97)89548-9
H. G. Nimmo, “The regulation of phosphoenolpyruvate carboxylase in CAM plants,” Trends in Plant Science, Vol. 5, 2000, pp. 75-80. doi.org/10.1016/S1360-1385(99)01543-5
M. Matsuoka, R. T. Furbank, H. Fukayama and M. Miyao, “Molecular engineering of C4 photosynthesis,” Annual Review of Plant Physiology and Plant Molecular Biology Vol. 52, 2001, pp. 297-314. doi:10.1146/annurev.arplant.52.1.297
B. Chinthapalli, A. S. Raghavendra, A. R. Rishi and A. Goyal, “Phosphoenolpyruvate carboxylase from C4 plants: Properties and regulation,” In: A. Goyal, S. L. Mehta, M. L. Lodha, Eds., Reviews in Plant Biochemistry and Biotechnology, New Delhi, Vol. 1, 2002, pp. 143-160
J. Vidal, S. Coursol and J-N. Pierre, “Reversible phosphorylation in the regulation of photosynthetic phosphoenolpyruvate carboxylase in C4 plants,” In: E-M. Aro and B. Andersson, Eds., Advances in Photosynthesis and Respiration, “Regulation of Photosynthesis.” Kluwer Academic Publishers, The Netherlands, Vol. 11, 2002, pp. 363-375
Y. Kai, H. Matsumura and K. Izui, “Phosphoenolpyruvate carboxylase: three-dimensional structure and molecular mechanisms,” Archives of Biochemistry and Biophysics, Vol. 414, 2003, pp. 170-179. doi.org/10.1016/S0003-9861(03)00170-X
P Svensson, O. E. Bläsing and P. Westhoff, “Evolution of C4 phosphoenolpyruvate carboxylase,” Achieves Biochemistry Biophysics, Vol. 414, 2003, 180-188. doi.org/10.1016/S0003-9861(03)00165-6
J. Murmu, B. Chinthapalli and A. S. Raghavendra, “Phosphoenolpyruvate carboxylase from leaves of C4 plants: Biochemistry and molecular biology of regulation,” Indian Journal of Plant Physiology, Special Issue, 2003, pp. 164-173.
T. Sugiyama, M. R. Schmitt, S. B. Ku and G. E. Edwards, “Differences in cold liability of pyruvate, Pi dikinase among C4 species,” Plant Cell Physiology Vol. 20, 1979, pp. 965-971
J. A. Berry and O. Björkman, “Photosynthetic responses and adaptation to temperature in higher plants,” Annual Review of Plant Physiology, Vol. 31, 1980, pp. 491-543. doi:10.1146/annurev.pp.31.060180.002423
S. P. Long, “Environmental responses,” In: R. F. Sage and R. K. Monson, Eds., “C4 Plant Biology,” Academic Press, San Diego, 1999, pp. 215-249
C. Potvin and J. P. Simon, “The evolution of cold temperature adaptation among population of a widely distributed C4 weed: barnyard grass,” Evolutionary Trends in Plants, Vol. 4, 1990, 98-105
J. N. Burnell, “A comparative study of the cold sensitivity of pyruvate Pi dikinase in Flaveria species,” Plant Cell Physiology, Vol. 31, 1990, pp. 295-297. doi.10.1007/BF00037024
Y-C. Du, A. Nose and K. Wasano, “Thermal characteristics of C4 photosynthetic enzymes from leaves of three sugarcane species differing in cold sensitivity,” Plant Cell Physiology, Vol. 40, 1999a, pp. 298-304
J. P. Krall, G. E. Edwards and C. S. Andreo, “Protection of pyruvate, Pi dikinase from maize against cold liability by compatible solutes,” Plant Physiology, Vol. 89, pp. 280-285. doi:10.1104/pp.89.1.280
Y-C. Du, A. Nose and K. Wasano, “Effects of chilling temperature on photosynthetic rates, photosynthetic enzyme activities and metabolite levels in three sugarcane species,” Plant Cell Environment, Vol. 22, 1999b, pp. 317-324. doi:10.1046/j.1365-3040.1999.00415.x
P. J. Phillips and J. R. McWilliam, “Thermal responses of the primary carboxylating enzymes from C3 and C4 plants adapted to contrasting temperature environments,” In: M. D. Hatch, C. B. Osmond and R. O. Slatyer, Eds., “Photosynthesis and Photorespiration,” Wiley-Interscience, New York 1971, pp. 97-104.
E. Selinioti, Y. Manetas and N. A. Gavalas, “Cooperative effects of light and temperature on the activity of phosphoenolpyruvate carboxylase from Amaranthus paniculatus L.,” Plant Physiology Vol. 82, 1986, pp. 518-522. doi.org/10.1104/pp.82.2.518
J. P. Krall and G. E. Edwards, “PEP carboxylase from two C4 species of Panicum with markedly different, susceptibilities to cold inactivation,” Plant cell Physiology, Vol. 34, 1993, pp. 1-11
R. Chollet, J. Vidal and M. H. O’Leary, “Phosphoenolpyruvate carboxylase: a ubiquitous, highly regulated enzyme in plants,” Annual Review of Plant Physiology and Plant Molecular Biology, Vol. 47, 1996, pp. 273-298. doi:10.1146/annurev.arplant.47.1.273
K. Parvathi, A. S. Bhagwat, Y. Ueno, K. Izui and A. S. Raghavendra, “Illumination increases the affinity of phosphoenolpyruvate carboxylase to bicarbonate in leaves of a C4 plant, Amaranthus hypochondriacus,” Plant Cell Physiology, Vol. 41, 2000, pp. 905-910. doi:10.1093/pcp/pcd012
B. Chinthapalli, J. Murmu and A. S. Raghavendra, “Dramatic difference in the responses of phosphoenolpyruvate carboxylase to temperature in leaves of C3 and C4 plants,” Journal of Experimental Botany, Vol. 54, pp. 707-14. doi:10.1093/jxb/erg078
K. Izui, H. Matsumura, T. Furumoto and Y. Kai, “Phospho enolpyruvate carboxylase: a new era of structural biology,” Annual Reviews of Plant Biology, Vol. 55, 2004, pp. 69–84. doi.10.1146/annurev.arplant.55.031903.141619
J. N. Pierre, J. L. Preito, P. Gadal and J. Vidal, “In situ C4 phosphoenolpyruvate carboxylase activity and kinetic properties in isolated Digitaria sanguinalis mesophyll cells,” Photosynthesis Research, Vol. 79, 2004, pp. 349-355.doi.10.1023/B:PRES.0000017179.31351.f0
G. Grammatikopoulos and Y. Manetas, “Diurnal changes in phosphoenolpyruvate carboxylase and pyruvate, orthophosphate dikinase properties in the natural environment: interplay of light and temperature in a C4 thermophile,” Physiologia Plantarum, Vol. 80, 1990, 593–597. doi: 10.1111/j.1399-3054.1990.tb05683.x
K. U. Avasthi, K. Izui and A. S. Raghavendra, “Interplay of light and temperature during the in planta modulation of C4 phosphoenolpyruvate carboxylase from the leaves of Amaranthus hypochondriacus L.: diurnal and seasonal effects manifested at molecular levels,” Journal of Experimental Botany, Vol. 62, No. 3, 2011, pp. 1017–1026. doi:10.1093/jxb/erq333
D. I. Arnon, “Copper enzymes in isolated chloroplasts. Polyphenol oxidase in Beta vulgaris,” Plant Physiology, Vol. 24, 1949, 1-15. doi.org/10.1104/pp.24.1.1
P. Casati, M. V. Lara and C. S. Andreo, “Induction of a C4 like mechanism of CO2 fixation in Egeria densa, a submerged aquatic species,” Plant Physiology, Vol. 123, 2000, pp. 1611-1621. doi.org/10.1104/pp.123.4.1611
P. J. Carter, M. B. Wilkins, H. G. Nimmo and C. A. Fewson, “Effects of temperature on the activity of phosphoenolpyruvate carboxylase and on the control of CO2 fixation in Bryophyllum fedtschenkoi,” Planta, Vol. 196, 1995, pp. 375-380. doi.10.1007/BF00201398
M-X. Wu and R. T. Wedding, “Temperature effects on phosphoenolpyruvate carboxylase from a CAM and a C4 plant. A comparative study,” Plant Physiology, Vol. 85. 1987, pp. 497-501. doi.org/10.1104/pp.85.2.497
J. R. McWilliam and P. J. Ferrar, “Photosynthetic adaptation of higher plants to thermal stress,” In: RL Bieleski, A. R. Ferguson, M. M. Cresswell, Eds., “Mechanisms of Regulation of Plant Growth,” Bulletin 12, Royal Society of New Zealand, Wellington, 1974, pp. 467-476.
D. Graham, D. G. Hockley and B. D. Patterson, “Temperature effects on phosphoenolpyruvate carboxylase from chilling-sensitive and chilling resistant plants,” In: J. M. Lyons, J. K. Raison Eds., “Low Temperature Stress in Crop Plants. The Role of the Membrane,” Academic Press, New York, 1979, pp. 187-202.
A. Laisk and G. E. Edwards, “CO2 and temperature-dependent induction in C4 photosynthesis: an approach to the hierarchy of rate-limiting processes,” Australian Journal Plant Physiology, Vol. 24, 1997, pp. 505-516. doi:10.1071/PP97011
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