PLANT PHYSIOLOGY , Vol 109, Issue 1 15-30, Copyright © 1995 by American Society of Plant Biologists

WHOLE PLANT, ENVIRONMENTAL, AND STRESS PHYSIOLOGY

Cold Acclimation of Arabidopsis thaliana (Effect on Plasma Membrane Lipid Composition and Freeze-Induced Lesions)

M. Uemura, R. A. Joseph and P. L. Steponkus
Department of Soil, Crop and Atmospheric Sciences, Cornell University, Ithaca, New York 14853

Maximum freezing tolerance of Arabidopsis thaliana L. Heyn (Columbia) was attained after 1 week of cold acclimation at 2[deg]C. During this time, there were significant changes in both the lipid composition of the plasma membrane and the freeze-induced lesions that were associated with injury. The proportion of phospholipids increased from 46.8 to 57.1 mol% of the total lipids with little change in the proportions of the phospholipid classes. Although the proportion of di-unsaturated species of phosphatidylcholine and phosphatidylethanolamine increased, mono-unsaturated species were still the preponderant species. The proportion of cerebrosides decreased from 7.3 to 4.3 mol% with only small changes in the proportions of the various molecular species. The proportion of free sterols decreased from 37.7 to 31.2 mol%, but there were only small changes in the proportions of sterylglucosides and acylated sterylglucosides. Freezing tolerance of protoplasts isolated from either nonacclimated or cold-acclimated leaves was similar to that of leaves from which the protoplasts were isolated (-3.5[deg]C for nonacclimated leaves; -10[deg]C for cold-acclimated leaves). In protoplasts isolated from nonacclimated leaves, the incidence of expansion-induced lysis was [less than or equal to]10% at any subzero temperature. Instead, freezing injury was associated with formation of the hexagonal II phase in the plasma membrane and subtending lamellae. In protoplasts isolated from cold-acclimated leaves, neither expansion-induced lysis nor freeze-induced formation of the hexagonal II phase occurred. Instead, injury was associated with the "fracture-jump lesion," which is manifested as localized deviations of the plasma membrane fracture plane to subtending lamellae. The relationship between the freeze-induced lesions and alterations in the lipid composition of the plasma membrane during cold acclimation is discussed.

This article has been cited by other articles:

				R. Inatsugi, H. Kawai, Y. Yamaoka, Y. Yu, A. Sekiguchi, M. Nakamura, and I. Nishida Isozyme-Specific Modes of Activation of CTP:Phosphorylcholine Cytidylyltransferase in Arabidopsis thaliana at Low Temperature Plant Cell Physiol., October 1, 2009; 50(10): 1727 - 1735. [Abstract] [Full Text] [PDF]

				M. Fujiwara, S. Hamada, M. Hiratsuka, Y. Fukao, T. Kawasaki, and K. Shimamoto Proteome Analysis of Detergent-Resistant Membranes (DRMs) Associated with OsRac1-Mediated Innate Immunity in Rice Plant Cell Physiol., July 1, 2009; 50(7): 1191 - 1200. [Abstract] [Full Text] [PDF]

				A. Minami, M. Fujiwara, A. Furuto, Y. Fukao, T. Yamashita, M. Kamo, Y. Kawamura, and M. Uemura Alterations in Detergent-Resistant Plasma Membrane Microdomains in Arabidopsis thaliana During Cold Acclimation Plant Cell Physiol., February 1, 2009; 50(2): 341 - 359. [Abstract] [Full Text] [PDF]

				T. Yamazaki, Y. Kawamura, A. Minami, and M. Uemura Calcium-Dependent Freezing Tolerance in Arabidopsis Involves Membrane Resealing via Synaptotagmin SYT1 PLANT CELL, December 1, 2008; 20(12): 3389 - 3404. [Abstract] [Full Text] [PDF]

				T. Yamazaki, Y. Kawamura, and M. Uemura Cryobehavior of the Plasma Membrane in Protoplasts Isolated from Cold-Acclimated Arabidopsis Leaves is Related to Surface Area Regulation Plant Cell Physiol., June 1, 2008; 49(6): 944 - 957. [Abstract] [Full Text] [PDF]

				M. Rapacz, B. Wolanin, K. Hura, and M. Tyrka The Effects of Cold Acclimation on Photosynthetic Apparatus and the Expression of COR14b in Four Genotypes of Barley (Hordeum vulgare) Contrasting in their Tolerance to Freezing and High-light Treatment in Cold Conditions Ann. Bot., April 1, 2008; 101(5): 689 - 699. [Abstract] [Full Text] [PDF]

				Y. Fujioka, N. N. Noda, K. Fujii, K. Yoshimoto, Y. Ohsumi, and F. Inagaki In Vitro Reconstitution of Plant Atg8 and Atg12 Conjugation Systems Essential for Autophagy J. Biol. Chem., January 25, 2008; 283(4): 1921 - 1928. [Abstract] [Full Text] [PDF]

				W. Li, R. Wang, M. Li, L. Li, C. Wang, R. Welti, and X. Wang Differential Degradation of Extraplastidic and Plastidic Lipids during Freezing and Post-freezing Recovery in Arabidopsis thaliana J. Biol. Chem., January 4, 2008; 283(1): 461 - 468. [Abstract] [Full Text] [PDF]

				J.-W. Nam and T. J. Kappock Cloning and transcriptional analysis of Crepis alpina fatty acid desaturases affecting the biosynthesis of crepenynic acid J. Exp. Bot., April 1, 2007; 58(6): 1421 - 1432. [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]

				S. J. Halperin and K. L. Koster Sugar effects on membrane damage during desiccation of pea embryo protoplasts J. Exp. Bot., July 1, 2006; 57(10): 2303 - 2311. [Abstract] [Full Text] [PDF]

				R. Yano, M. Nakamura, T. Yoneyama, and I. Nishida Starch-Related {alpha}-Glucan/Water Dikinase Is Involved in the Cold-Induced Development of Freezing Tolerance in Arabidopsis Plant Physiology, June 1, 2005; 138(2): 837 - 846. [Abstract] [Full Text] [PDF]

				S. Jackowski and P. Fagone CTP:Phosphocholine Cytidylyltransferase: Paving the Way from Gene to Membrane J. Biol. Chem., January 14, 2005; 280(2): 853 - 856. [Full Text] [PDF]

				B. Schade, G. Jansen, M. Whiteway, K. D. Entian, and D. Y. Thomas Cold Adaptation in Budding Yeast Mol. Biol. Cell, December 1, 2004; 15(12): 5492 - 5502. [Abstract] [Full Text] [PDF]

				R. Swarup, J. Kargul, A. Marchant, D. Zadik, A. Rahman, R. Mills, A. Yemm, S. May, L. Williams, P. Millner, et al. Structure-Function Analysis of the Presumptive Arabidopsis Auxin Permease AUX1 PLANT CELL, November 1, 2004; 16(11): 3069 - 3083. [Abstract] [Full Text] [PDF]

				S. Trenkamp, W. Martin, and K. Tietjen Specific and differential inhibition of very-long-chain fatty acid elongases from Arabidopsis thaliana by different herbicides PNAS, August 10, 2004; 101(32): 11903 - 11908. [Abstract] [Full Text] [PDF]

				T. M. DUNN, D. V. LYNCH, L. V. MICHAELSON, and J. A. NAPIER A Post-genomic Approach to Understanding Sphingolipid Metabolism in Arabidopsis thaliana Ann. Bot., May 1, 2004; 93(5): 483 - 497. [Abstract] [Full Text] [PDF]

				T. Takagi, M. Nakamura, H. Hayashi, R. Inatsugi, R. Yano, and I. Nishida The Leaf-Order-Dependent Enhancement of Freezing Tolerance in Cold-Acclimated Arabidopsis Rosettes is not Correlated with the Transcript Levels of the Cold-Inducible Transcription Factors of CBF/DREB1 Plant Cell Physiol., September 15, 2003; 44(9): 922 - 931. [Abstract] [Full Text] [PDF]

				Z. Zheng, Q. Xia, M. Dauk, W. Shen, G. Selvaraj, and J. Zou Arabidopsis AtGPAT1, a Member of the Membrane-Bound Glycerol-3-Phosphate Acyltransferase Gene Family, Is Essential for Tapetum Differentiation and Male Fertility PLANT CELL, August 1, 2003; 15(8): 1872 - 1887. [Abstract] [Full Text] [PDF]

				K. L. Koster, N. Reisdorph, and J. L. Ramsay Changing desiccation tolerance of pea embryo protoplasts during germination J. Exp. Bot., June 1, 2003; 54(387): 1607 - 1614. [Abstract] [Full Text] [PDF]

				J.-Y. Lee and D.-H. Lee Use of Serial Analysis of Gene Expression Technology to Reveal Changes in Gene Expression in Arabidopsis Pollen Undergoing Cold Stress Plant Physiology, June 1, 2003; 132(2): 517 - 529. [Abstract] [Full Text] [PDF]

				M. Uemura, G. Warren, and P. L. Steponkus Freezing Sensitivity in the sfr4 Mutant of Arabidopsis Is Due to Low Sugar Content and Is Manifested by Loss of Osmotic Responsiveness Plant Physiology, April 1, 2003; 131(4): 1800 - 1807. [Abstract] [Full Text] [PDF]

				R. Inatsugi, M. Nakamura, and I. Nishida Phosphatidylcholine Biosynthesis at Low Temperature: Differential Expression of CTP:Phosphorylcholine Cytidylyltransferase Isogenes in Arabidopsis thaliana Plant Cell Physiol., November 15, 2002; 43(11): 1342 - 1350. [Abstract] [Full Text] [PDF]

				M. F. Quartacci, O. Glisic, B. Stevanovic, and F. Navari-Izzo Plasma membrane lipids in the resurrection plant Ramonda serbica following dehydration and rehydration J. Exp. Bot., November 1, 2002; 53(378): 2159 - 2166. [Abstract] [Full Text] [PDF]

				R. Welti, W. Li, M. Li, Y. Sang, H. Biesiada, H.-E Zhou, C. B. Rajashekar, T. D. Williams, and X. Wang Profiling Membrane Lipids in Plant Stress Responses. ROLE OF PHOSPHOLIPASE Dalpha IN FREEZING-INDUCED LIPID CHANGES IN ARABIDOPSIS J. Biol. Chem., August 23, 2002; 277(35): 31994 - 32002. [Abstract] [Full Text] [PDF]

				J. K. Pittman, T. Shigaki, N.-H. Cheng, and K. D. Hirschi Mechanism of N-terminal Autoinhibition in the Arabidopsis Ca2+/H+ Antiporter CAX1 J. Biol. Chem., July 12, 2002; 277(29): 26452 - 26459. [Abstract] [Full Text] [PDF]

				L. Xiao and K. L. Koster Desiccation tolerance of protoplasts isolated from pea embryos J. Exp. Bot., November 1, 2001; 52(364): 2105 - 2114. [Abstract] [Full Text] [PDF]

				P. V. Minorsky Plant Physiology, October 1, 2001; 127(2): 379 - 380. [Full Text] [PDF]

				N. Ukaji, C. Kuwabara, D. Takezawa, K. Arakawa, and S. Fujikawa Cold Acclimation-Induced WAP27 Localized in Endoplasmic Reticulum in Cortical Parenchyma Cells of Mulberry Tree Was Homologous to Group 3 Late-Embryogenesis Abundant Proteins Plant Physiology, August 1, 2001; 126(4): 1588 - 1597. [Abstract] [Full Text] [PDF]

				S. J. Gilmour, A. M. Sebolt, M. P. Salazar, J. D. Everard, and M. F. Thomashow Overexpression of the Arabidopsis CBF3 Transcriptional Activator Mimics Multiple Biochemical Changes Associated with Cold Acclimation Plant Physiology, December 1, 2000; 124(4): 1854 - 1865. [Abstract] [Full Text]

				H. Knight and M. R. Knight Imaging spatial and cellular characteristics of low temperature calcium signature after cold acclimation in Arabidopsis J. Exp. Bot., October 1, 2000; 51(351): 1679 - 1686. [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]

				P. L. Steponkus, M. Uemura, R. A. Joseph, S. J. Gilmour, and M. F. Thomashow Mode of action of the COR15a gene on the freezing tolerance of Arabidopsis thaliana PNAS, November 24, 1998; 95(24): 14570 - 14575. [Abstract] [Full Text] [PDF]

				T. Hamada, H. Kodama, K. Takeshita, H. Utsumi, and K. Iba Characterization of Transgenic Tobacco with an Increased alpha -Linolenic Acid Level Plant Physiology, October 1, 1998; 118(2): 591 - 598. [Abstract] [Full Text]

				Z. Xin and J. Browse eskimo1 mutants of Arabidopsis are constitutively freezing-tolerant PNAS, June 23, 1998; 95(13): 7799 - 7804. [Abstract] [Full Text] [PDF]

				J. Danyluk, A. Perron, M. Houde, A. Limin, B. Fowler, N. Benhamou, and F. Sarhan Accumulation of an Acidic Dehydrin in the Vicinity of the Plasma Membrane during Cold Acclimation of Wheat PLANT CELL, April 1, 1998; 10(4): 623 - 638. [Abstract] [Full Text]

				N. N. Artus, M. Uemura, P. L. Steponkus, S. J. Gilmour, C. Lin, and M. F. Thomashow Constitutive expression of the cold-regulated Arabidopsis thaliana COR15a gene affects both chloroplast and protoplast freezing tolerance PNAS, November 12, 1996; 93(23): 13404 - 13409. [Abstract] [Full Text] [PDF]