This Article Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via CrossRef Citing Articles via Google Scholar Google Scholar Articles by Holaday, A. S. Articles by Leegood, R. C. Search for Related Content PubMed PubMed Citation Articles by Holaday, A. S. Articles by Leegood, R. C. Agricola Articles by Holaday, A. S. Articles by Leegood, R. C.

Metabolism and Enzymology

Changes in Activities of Enzymes of Carbon Metabolism in Leaves during Exposure of Plants to Low Temperature ¹

Department of Biological Sciences, Texas Tech University, Box 4149, Lubbock, Texas 79409-3131, Robert Hill Institute and Department of Animal and Plant Sciences, University of Sheffield, Sheffield, S10 2UQ, United Kingdom

The aim of this study was to determine the response of photosynthetic carbon metabolism in spinach and bean to low temperature. (a) Exposure of warm-grown spinach and bean plants to 10°C for 10 days resulted in increases in the total activities of a number of enzymes, including ribulose 1,5-bisphosphate carboxylase (Rubisco), stromal fructose 1,6 bisphosphatase (Fru 1,6-P₂ase), sedoheptulose 1,7-bisphosphatase (Sed 1,7-P₂ase), and the cytosolic Fru 1,6-P₂ase. In spinach, but not bean, there was an increase in the total activity of sucrose-phosphate synthase. (b) The CO₂-saturated rates of photosynthesis for the cold-acclimated spinach plants were 68% greater at 10°C than those for warm-acclimated plants, whereas in bean, rates of photosynthesis at 10°C were very low after exposure to low temperature. (c) When spinach leaf discs were transferred from 27 to 10°C, the stromal Fru 1,6-P₂ase and NADP-malate dehydrogenase were almost fully activated within 8 minutes, and Rubisco reached 90% of full activation within 15 minutes of transfer. An initial restriction of Calvin cycle fluxes was evident as an increase in the amounts of ribulose 1,5-bisphosphate, glycerate-3-phosphate, Fru 1,6-P₂, and Sed 1,7-P₂. In bean, activation of stromal Fru 1,6-P₂ase was weak, whereas the activation state of Rubisco decreased during the first few minutes after transfer to low temperature. However, NADP-malate dehydrogenase became almost fully activated, showing that no loss of the capacity for reductive activation occurred. (d) Temperature compensation in spinach evidently involves increases in the capacities of a range of enzymes, achieved in the short term by an increase in activation state, whereas long-term acclimation is achieved by an increase in the maximum activities of enzymes. The inability of bean to activate fully certain Calvin cycle enzymes and sucrose-phosphate synthase, or to increase nonphotochemical quenching of chlorophyll fluorescence at 10°C, may be factors contributing to its poor performance at low temperature.

This article has been cited by other articles:

				M. Rapala-Kozik, E. Kowalska, and K. Ostrowska Modulation of thiamine metabolism in Zea mays seedlings under conditions of abiotic stress J. Exp. Bot., November 1, 2008; 59(15): 4133 - 4143. [Abstract] [Full Text] [PDF]

				K. Nakayama, K. Okawa, T. Kakizaki, T. Honma, H. Itoh, and T. Inaba Arabidopsis Cor15am Is a Chloroplast Stromal Protein That Has Cryoprotective Activity and Forms Oligomers Plant Physiology, May 1, 2007; 144(1): 513 - 523. [Abstract] [Full Text] [PDF]

				L. J. Sweetlove, A. Lytovchenko, M. Morgan, A. Nunes-Nesi, N. L. Taylor, C. J. Baxter, I. Eickmeier, and A. R. Fernie Mitochondrial uncoupling protein is required for efficient photosynthesis PNAS, December 19, 2006; 103(51): 19587 - 19592. [Abstract] [Full Text] [PDF]

				T. Hewezi, M. Leger, W. El Kayal, and L. Gentzbittel Transcriptional profiling of sunflower plants growing under low temperatures reveals an extensive down-regulation of gene expression associated with chilling sensitivity J. Exp. Bot., September 1, 2006; 57(12): 3109 - 3122. [Abstract] [Full Text] [PDF]

				M. Tamoi, M. Nagaoka, Y. Miyagawa, and S. Shigeoka Contribution of Fructose-1,6-bisphosphatase and Sedoheptulose-1,7-bisphosphatase to the Photosynthetic Rate and Carbon Flow in the Calvin Cycle in Transgenic Plants Plant Cell Physiol., March 1, 2006; 47(3): 380 - 390. [Abstract] [Full Text] [PDF]

				K. Hikosaka, K. Ishikawa, A. Borjigidai, O. Muller, and Y. Onoda Temperature acclimation of photosynthesis: mechanisms involved in the changes in temperature dependence of photosynthetic rate J. Exp. Bot., January 1, 2006; 57(2): 291 - 302. [Abstract] [Full Text] [PDF]

				Y.-P. Cen and R. F. Sage The Regulation of Rubisco Activity in Response to Variation in Temperature and Atmospheric CO2 Partial Pressure in Sweet Potato Plant Physiology, October 1, 2005; 139(2): 979 - 990. [Abstract] [Full Text] [PDF]

				K. Hikosaka Nitrogen Partitioning in the Photosynthetic Apparatus of Plantago asiatica Leaves Grown Under Different Temperature and Light Conditions: Similarities and Differences Between Temperature and Light Acclimation Plant Cell Physiol., August 1, 2005; 46(8): 1283 - 1290. [Abstract] [Full Text] [PDF]

				D. S. Kubien, S. von Caemmerer, R. T. Furbank, and R. F. Sage C4 Photosynthesis at Low Temperature. A Study Using Transgenic Plants with Reduced Amounts of Rubisco Plant Physiology, July 1, 2003; 132(3): 1577 - 1585. [Abstract] [Full Text] [PDF]

				R. F. Sage Variation in the kcat of Rubisco in C3 and C4 plants and some implications for photosynthetic performance at high and low temperature J. Exp. Bot., April 1, 2002; 53(369): 609 - 620. [Abstract] [Full Text] [PDF]

				P. Payton, R. Webb, D. Kornyeyev, R. Allen, and A. S. Holaday Protecting cotton photosynthesis during moderate chilling at high light intensity by increasing chloroplastic antioxidant enzyme activity J. Exp. Bot., December 1, 2001; 52(365): 2345 - 2354. [Abstract] [Full Text] [PDF]

				R. E. Hausler, T. Rademacher, J. Li, V. Lipka, K. L. Fischer, S. Schubert, F. Kreuzaler, and H.-J. Hirsch Single and double overexpression of C4-cycle genes had differential effects on the pattern of endogenous enzymes, attenuation of photorespiration and on contents of UV protectants in transgenic potato and tobacco plants J. Exp. Bot., September 1, 2001; 52(362): 1785 - 1803. [Abstract] [Full Text] [PDF]

				L. A. Wanner and O. Junttila Cold-Induced Freezing Tolerance in Arabidopsis Plant Physiology, June 1, 1999; 120(2): 391 - 400. [Abstract] [Full Text]

				A. Strand, V. Hurry, S. Henkes, N. Huner, P. Gustafsson, P. Gardeström, and M. Stitt Acclimation of Arabidopsis Leaves Developing at Low Temperatures. Increasing Cytoplasmic Volume Accompanies Increased Activities of Enzymes in the Calvin Cycle and in the Sucrose-Biosynthesis Pathway Plant Physiology, April 1, 1999; 119(4): 1387 - 1398. [Abstract] [Full Text]

				T. Yamasaki, T. Yamakawa, Y. Yamane, H. Koike, K. Satoh, and S. Katoh Temperature Acclimation of Photosynthesis and Related Changes in Photosystem II Electron Transport in Winter Wheat Plant Physiology, March 1, 2002; 128(3): 1087 - 1097. [Abstract] [Full Text] [PDF]