Abstract
Within the broader context of how lipid composition affects the cell biology and physiology of plants, the question of how membrane unsaturation affects a plant’s ability to tolerate low-temperature stresses has a long and distinguished history. A series of Arabidopsis mutants with defects in lipid metabolism has provided important examples of how membrane fatty acid composition can affect plant temperature responses, although it is not complete clear how these specialized examples relate to chilling and freezing tolerance in horticulture. In this review, we will first provide a general introduction to the lipid mutants and then consider in detail some of the studies that have demonstrated the requirements of polyunsaturated membranes for proper growth and function of plants at chilling temperatures. A specific screen for mutants that are damaged by chilling has also been undertaken and the results and prospects for this approach are discussed.
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References
Arondel V, Lemieux B, Hwang I, Gibson S, Goodman HM, Somerville CR (1992) Map-based cloning of a gene controlling omega-3 fatty acid desaturation in Arabidopsis. Science 258: 1353–1355
Botstein D, Maurer R (1982) Genetic approaches to the analysis of microbial development. Ann Rev Genet 16: 61–83
Browse J, Kunst L, Anderson S, Hugly S, Somerville CR (1989) A mutant of Arabidopsis deficient in the chlo-roplast 16:1/18:1 desaturase. Plant Physiol 90: 522–529
Browse J, Somerville C (1991) Glycerolipid synthesis: Biochemistry and regulation. Ann Rev Plant Physiol. Plant Mol Biol 42: 467–506
Browse JA, McCourt PJ, Somerville CR (1985) A mutant of Arabidopsis lacking a chloroplast-specific lipid. Science 227: 763–765
Browse JA, Warwick N, Somerville CR, Slack CR (1986) Fluxes through the prokaryotic and eukaryotic pathways of lipid synthesis in the 16:3 plant Arabidopsis thaliana. Biochem J 235: 25–31
Christiansson A, Kuypers FA, Roelofsen B, Op Den Kamp JAF, Van Deenen LLM (1985) Lipid molecular shape affects erythrocyte morphology: A study involving replacement of native phosphatidylcholine with different species followed by treatment of cells with sphingomyelinase c or phospholipase A2. J Cell Biol 101: 1455–1462
Feldmann KA (1991) T-DNA insertion mutagenesis in Arabidopsis: mutational spectrum. Plant J 1: 71–82
Gounaris K, Brain ARR, Quinn PJ, Williams WP (1984) Structural reorganisation of chloroplast thylakoid membranes in response to heat-stress. Biochim Biophys Acta 766: 198–208
Gounaris K, Mannock DD, Sen A, Brain APR, Williams WP, Quinn PJ (1983) Polyunsaturated fatty acyl residues of galactolipids are involved in the control of bilayer/nonbilayer lipid transitions in higher plant chlo-roplasts. Biochim Biophys Acta 732: 229–242
Gruner SM, Cullis PR, Hope MJ, Tilcock CPS (1985) Lipid polymorphism: The molecular basis of nonbilayer phases. Ann Rev Biophs Chem 14: 211–242
Heinz E (1993) Biosynthesis of polyunsaturated fatty acids. In TS Moore, ed, Lipid Metabolism in Plants. CRC Press, Boca Raton, FL, pp 33–89
Hugly S, Kunst L, Browse J, Somerville C (1989) Enhanced thermal tolerance and altered chloroplast ultrastructure in a mutant of Arabidopsis deficient in lipid desaturation. Plant Physiol 90: 1134–1142
Hugly S, McCourt P, Browse J, Patterson GW, Somerville C (1990) A chilling sensitive mutant of Arabidopsis with altered steryl-ester metabolism. Plant Physiol 93: 1053–1062
Hugly S, Somerville C (1992) A role for membrane lipid polyunsaturation in chloroplast biogenesis at low temperature. Plant Physiol 99: 197–202
Israelachvili JN, Marcelja S, Horn RG (1980) Physical principles of membrane organization. Quart Rev Biophys 2: 121–200
Joyard J, Block MA, Malberbe A, Marachal E, Douce R (1993) Origin and synthesis of galactolipid and sulfo-lipid headgroups. In TS Moore, Jr, ed, Lipid Metabolism in Plants. CRC Press, Boca Raton, pp 231–258
Krieg DR (1963) Ethyl methanesulfonate-induced reverison of bacteriophage T4rII mutants. Genetics 48: 561–580
Kunst L, Browse J, Somerville C (1989) A mutant of Arabidopsis deficient in desaturation of palmitic acid in leaf lipids. Plant Physiol 90: 943–947
Lindqvist Y, Huang W, Schneider G, Shanklin J (1996) Crystal structure of Æ9 stearoyl-acyl carrier protein de-saturase from castor seed and its relationship to other di-iron proteins. EMBO J 15: 4081–4092
Lyons JM (1973) chilling injury in plants. Annu Rev Plant Physiol 24: 445–466
Lyons JM, Graham D, Raison JK, eds (1979) Low Temperature Stress in Plants. Academic Press, New York
Marsh D (1990) CRC Handbook of Lipid Bilayers. CRC Press, Boca Raton, 387 pp
McCourt PJ, Kunst L, Browse J, Somerville CR (1987) The effects of reduced amounts of lipid unsaturation on chloroplast ultrastructure and photosynthesis in a mutant of Arabidopsis. Plant Physiol 84: 353–360
McEIhaney RN (1989) The influence of membrane lipid composition and physical properties of membrane structure and function in Acholeplasma laidlawii. Crit Rev Microbiol 17: 1–32
McKeon TA, Stumpf PK (1982) Purification and characterization of the stearoyl-acyl carrier protein desaturase and the acyl-acyl carrier protein thioesterase from maturing seeds of safflower. J Biol Chem 257: 12141–12147
Miquel M, Browse J (1992) Arabidopsis mutants deficient in polyunsaturated fatty acid synthesis. Biochemical and genetic characterization of a plant oleoyl-phosphatidylcholine desaturase. J Biol Chem 267: 1502–1509
Miquel M, James D, Dooner H, Browse J (1993) Arabidopsis requires polyunsaturated lipids for low temperature survival. Proc Natl Acad Sci USA 90: 6208–6212
Moir D, Botstein D (1982) Determination of the order of gene function in the yeast nuclear division pathway using cs and ts mutants. Genetics 100: 565–577
Moore TS (1982) Phospholipid biosynthesis. Ann Rev Plant Physiol 33: 235–259
Murata N (1983) Molecular species composition of phosphatidylglycerols from chilling-sensitive and chilling-resistant plants. Plant Cell Physiol 24: 81–86
Murata N, Ishizaki-Nishizawa O, Higashi S, Hayashi H, Tasaka Y, Nishida I (1992) Genetically engineered alteration in the chilling sensitivity of plants. Nature 356: 313–326
Murata N, Nishida I (1990) Lipids in relation to chilling sensitivity of plants. In CY Wang, ed, Chilling Injury of Horticultural Crops. CRC Press, Boca Raton, FL, pp 181–199
Murata N, Sato N, Takahashi N, Hamazaki Y (1982) Compositions and positional distributions of fatty acids in phospholipids from leaves of chilling-sensitive and chilling-resistant plants. Plant Cell Physiol 23: 1071–1079
Murata N, Yamaya J (1984) Temperature-dependent phase behavior of phosphatidylglycerols from chilling-sensitive and chilling-resistant plants. Plant Physiol 74: 1016–1024
Okuley J, Lightner J, Feldmann K, Yadav N, Lark E, Browse J (1994) The Arabidopsis FAD2 gene encodes the enzyme that is essential for polyunsaturated lipid synthesis. Plant Cell 6: 147–158
Patterson BD, Reid MS (1990) Genetic and environmental influences on the expression of chilling injury. In CY Wang, ed, Chilling Injury of Horticultural Crops. CRC Press, Boca Raton, pp 87–112
Patterson GW, Hugly S, Harrison D (1993) Sterols and phytyl esters of Arabidopsis thaliana under normal and chilling temperatures. Phytochemistry 33: 1381–1383
Quinn PJ, Joo F, Vigh L (1989) The role of unsaturated lipids in membrane structure and stability. Prog Biophys Mol Biol 53: 71–103
Raison JK, Orr GR (1990) Proposals for a better understanding of the molecular basis of chilling injury. In C-Y Wang, ed, Chilling Injury of Horticultural Crops. CRC Press, Boca Raton, pp 145–164
Raison JK, Wright LC (1983) Thermal phase transitions in the polar lipids of plant membranes: Their induction by disaturated phospholipids and their possible relation to chilling injury. Biochim. Biophys Acta 731: 69–74
Roughan PG, Slack CR (1982) Cellular organization of glycerolipid metabolism. Ann Rev Plant Physiol 33: 97–123
Schmidt H, Dresselhaus T, Buck F, Heinz E (1994) Purification and PCR-based cDNA cloning of a plastidial n-6 desaturase. Plant Mol. Biol. 26: 631–642
Schneider JC, Hugly S, Somerville CR (1995) Chilling sensitive mutants of Arabidopsis. Plant Mol Biol Rep 13: 11–17
Schneider JC, Nielsen E, Somerville C (1995) A chilling-sensitive mutant of Arabidopsis is deficient in chloro-plast protein accumulation at low temperature. Plant Cell Environ 18: 23–31
Shanklin J, Somerville CR (1991) The cDNA clones for stearoyl-ACP desaturase from higher plants are not homologous to yeart or mammalian genes encoding stearoyl-CoA deasturase. Proc Natl Acad Sci USA 88: 2510–2514
Shimakata T, Stumpf PK (1982) Isolation and function of spinach leaf ß-ketoacyl-[acyl-carrier-protein] syn-thases. Proc Natl Acad Sci USA 79: 5808
Singer SJ, Nicolson GL (1972) The fluid mosaic model of the structure of cell membranes. Science 175: 720–731
Slack CR, Roughan PG, Terpstra J (1976) Some properties of a microsomal oleate desaturase from leaves. Bio-chem J 155:71–80
Somerville C, Browse J (1991) Plant lipids: Metabolism mutants and membranes. Science 252: 80–87
Wang CY, ed (1990) Chilling Injury of Horticultural Crops. CRC Press, Boca Raton
Warren RC (1987) Physics and the Architecture of Cell Membranes. Adam Hilger, Bristol
Wolter FP, Schmidt R, Heinz E (1992) Chilling sensitivity of Arabidopsis thaliana with genetically engineered membrane lipids. EMBO J. 11: 4685–4692
Wu J, Browse J (1995) Elevated levels of high-melting-point phosphatidylglycerols do not induce chilling sensitivity in a mutant of Arabidopsis. The Plant Cell 7: 17–27
Wu JW, Lightner J, Warwick N, Browse J (1997) Low-temperature damage and subsequent recovery of fab 1 mutant Arabidopsis exposed to 2°C. Plant Physiol. (in press)
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Tokuhisa, J., Wu, J., Miquel, M., Xin, Z., Browse, J. (1997). Investigating the Role of Lipid Metabolism in Chilling and Freezing Tolerance. In: Li, P.H., Chen, T.H.H. (eds) Plant Cold Hardiness. Springer, Boston, MA. https://doi.org/10.1007/978-1-4899-0277-1_14
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DOI: https://doi.org/10.1007/978-1-4899-0277-1_14
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