Abstract
Membranes are prime targets of high temperature stress in plants. Thus, cell membrane stability has been used as a measure of heat tolerance in wheat. Under optimal temperature conditions, membranes are lipid bilayers that are largely in fluid phase. High temperatures or dehydration can cause phase transitions of membranes to non-bilayer phases. In order to maintain optimal fluidity and stability of membranes under high temperature conditions, wheat plants alter lipid compositions and reduce unsaturation levels in the fatty acid chains. Besides altering the fatty acid chains synthesized, the composition of chloroplast and thylakoid membranes may be adjusted by adjusting the diacylglycerol species channeled from the endoplasmic reticulum to chloroplasts under heat stress conditions.
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References
Arunga RO, Morrison WR (1971) The structural analysis of wheat flour glycerolipids. Lipids 6:768–776
Blum A, Ebercon A (1981) Cell membrane stability as a measure of drought and heat tolerance in wheat. Crop Sci 21:43–47
Browse J, Somerville C (1991) Glycerolipids synthesis: biochemistry and regulation. Annu Rev Plant Physiol Plant Mol Biol 42:467–506
Browse J, 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
Crowe JH, Hoekstra FA, Crowe LM (1989) Membrane phase transitions are responsible for imbibitional damage in dry pollen. Proc Natl Acad Sci U S A 86:520–523
Cullis PR, DeKruijff B (1979) Lipid polymorphism and the functional roles of lipids in biological membranes. Biochim Biophys Acta 559:399–420
de Vries AH, Mark AE, Marrink SJ (2004) The binary mixing behavior of phospholipids in a bilayer: amolecular dynamics study. J Phys Chem B 108:2454–2463
Djanaguiraman M, Prasad PVV, Seppanen M (2010) Selenium protects sorghum leaves from oxidative damage under high temperature stress by enhancing antioxidant defense system. Plant Physiol Biochem 48:999–1007
Djanaguiraman M, Boyle DL, Welti R, Jagadish SVK, Prasad PVV (2018) Decreased photosynthetic rate under high temperature in wheat is due to lipid desaturation, oxidation, acylation, and damage of organelles. BMC Plant Biol 18:55
Edidin M (2003) Lipids on the frontier: a century of cell-membrane bilayers. Nat Rev Mol Cell Biol 4:414–418
Farmer EE, Mueller MJ (2013) ROS-mediated lipid peroxidation and RES-activated signaling. Ann Rev Plant Biol 64:429–450
Garvey CJ, Lenné T, Koster KL, Kent B, Bryant G (2013) Phospholipid membrane protection by sugar molecules during dehydration – insights into molecular mechanisms using scattering techniques. Int J Mol Sci 14:8148–8163
Grille S, Zaslawski A, Thiele S, Plat J, Warnecke D (2010) The functions of steryl glycosides come to those who wait: recent advances in plants, fungi, bacteria and animals. Prog Lipid Res 49:262–288
Hammoudah MM, Nir S, Bentz J, Mayhew E, Stewart TP, HuiSW KRJ (1981) Interactions of La31 with phosphatidylserine vesicles binding, phase transition, leakage, 31P-NMR and fusion. Biochim Biophys Acta 645:102–114
Hansbro PM, Byard SJ, Bushby RJ, Turnbull PJ, Boden N, Saunders MR et al (1992) The conformational behaviour of phosphatidylinositol in model membranes: 2H-NMR studies. Biochim Biophys Acta 1112:187–196
Harwood J (1991) Strategies for coping with low environmental temperatures. Trends Biochem Sci 16:126–127
Heinz E, Roughan PG (1983) Similarities and differences in lipid metabolism of chloroplasts isolated from 18:3 and 16:3 plants. Plant Physiol 72:273–279
Hoekstra FA, Crowe JH, Crowe LM (1992) Germination and ion leakage are linked with phase transitions of membrane lipids during imbibition of Typha latifolia pollen. Physiol Plant 84:29–34
Holzl G, Witt S, Gaude N, Melzer M, Schottler MA, Dormann P (2009) The role of diglycosyl lipids in photosynthesis and membrane lipid homeostasis in Arabidopsis. Plant Physiol 150:1147–1159
Horvath I, Glatz A, Varvasovszki V, Torok Z, Pali T, Balogh G, Kovacs E, Nadasdi L, Benko S, Joo F, Vigh L (1998) Membrane physical state controls the signaling mechanism of the heat shock response in Synechocystis PCC 6803: identification of hsp17 as a ‘fluidity gene’. Proc Natl Acad Sci U S A 95:3513–3518
Huang B (2006) Plant-environment interactions, 3rd edn. CRC Press, Boca Raton
Iba K (2002) Acclimative response to temperature stress in higher plants: approaches of gene engineering for temperature tolerance. Ann Rev Plant Biol 53:225–245
Ibrahim AMH, Quick JS (2001) Genetic control of high temperature tolerance in wheat as measured by membrane thermal stability. Crop Sci 41:1405–1407
Jeennor S, Laoteng K, Tanticharoen M, Cheevadhanarak S (2006) Comparative fatty acid profiling of Mucor rouxii under different stress conditions. FEMS Microbiol Lett 259:60–66
Jenkins B,West JA, Koulman A (2015) A review of odd-chain fatty acid metabolism and the role of pentadecanoic acid (C15:0) and heptadecanoic acid (C17:0) in health and disease. Molecules 20:2425–2444
Jouhet J (2013) Importance of the hexagonal lipid phase in biological membrane organization. Front Plant Sci 4:494
Kunst L, Browse J, Somerville C (1988) Altered regulation of lipid biosynthesis in a mutant of Arabidopsis deficient in chloroplast glycerol-3-phosphate acyltransferase activity. Proc Natl Acad Sci U S A 85:4143–4147
Larkindale J, Huang B (2004) Changes of lipid composition and saturation level in leaves and roots for heat-stressed and heat-acclimated creeping bentgrass (Agrostis stolonifera). Environ Exp Bot 51:57–67
Li Q, Zheng Q, Shen W, Cram D, Fowler DB, Wei Y, Zou J (2015) Understanding the biochemical basis of temperature-induced lipid pathway adjustments in plants. Plant Cell 27:86–103
Martineau JR, Specht JE, Williams JH, Sullivan CY (1979) Temperature tolerance in soybeans. I. Evaluation of a technique for assessing cellular membrane thermostability. Crop Sci 19:75–78
Mene-Saffrane L, Dubugnon L, Chetelat A, Stolz S, Gouhier-Darimont C, Farmer EE (2009) Non-enzymatic oxidation of trienoic fatty acids contributes to reactive oxygen species management in Arabidopsis. J Biol Chem 284:1702–1708
Mongrand S, Bessoule J, Cabantous F, Cassagne C (1998) The C16:3/C18:3 fatty acid balance in photosynthetic tissues from 468 plant species. Phytochemistry 49:1049–1064
Murata N, Los DA (1997) Membrane fluidity and temperature perception. Plant Physiol 115:875–879
Muramatsu K, Masumizu T, Maitani Y, Hwang SH, Kohno M, Takayama K, Nagai T (2000) Electron spin resonance studies of dipalmitoylphosphatidylcholine liposomes containing soybean-derived sterylglucoside. Chem Pharm Bull 48:610–613
Narayanan S, Prasad PVV, Fritz AK, Boyle DL, Gill BS (2014) Impact of high night-time and high daytime temperature stress on winter wheat. J Agron Crop Sci 201:206–218
Narayanan S, Tamura PJ, Roth MR, Prasad PVV, Welti R (2016) Wheat leaf lipids during heat stress: I. High day and night temperatures result in major lipid alterations. Plant Cell Environ 39:787–803
Narayanan S, Prasad PVV, Welti R (2018) Alterations in wheat pollen lipidome during high day and night temperature stress. Plant Cell Environ 41:1749–1761
Ohlrogge J, Browse J (1995) Lipid biosynthesis. Plant Cell 7:957–970
Ortiz A, Killian JA, Verkleij AJ, Wilschut J (1999) Membrane fusion and the lamellar-to-inverted-hexagonal phase transition in cardiolipin vesicle systems induced by divalent cations. Biophys J 77:2003–2014
Orvar BL, Sangwan V, Omann F, Dhindsa RS (2000) Early steps in cold sensing by plant cells: the role of actin cytoskeleton and membrane fluidity. Plant J 23:785–794
Prasad PVV, Pisipati SR, Ristic Z, Bukovnik U, Fritz AK (2008) Impact of nighttime temperature on physiology and growth of spring wheat. Crop Sci 48:2372–2380
Quinn PJ (1985) A lipid-phase separation model of low-temperature damage to biological membranes. Cryobiology 22:128–146
Řezanka T, Sigler K (2009) Odd-numbered very-long-chain fatty acids from the microbial, animal and plant kingdoms. Prog Lipid Res 48:206–238
Ristic Z, Bukovnik U, Prasad PVV (2007) Correlation between heat stability of thylakoid membranes and loss of chlorophyll in winter wheat under heat stress. Crop Sci 47:2067–2073
Sairam RK, Deshmukh PS, Shukla DS (1997) Tolerance to drought and temperature stress in relation to increased antioxidant enzyme activity in wheat. J Agron Crop Sci 178:171e177
Seddon JM (1990) Structure of the inverted hexagonal (HII) phase, and non-lamellar phase transitions of lipids. Biochim Biophys Acta 1031:1–69
Shipley GG, Green JP, Nichols BW (1973) The phase behavior of monogalactosyl, digalactosyl, and sulphoquinovosyl diglycerides. Biochim Biophys Acta 311:531–544
Siegel DP, Tenchov BG (2008) Influence of the lamellar phase unbinding energy on the relative stability of lamellar and inverted cubic phases. Biophys J 94:3987–3995
Simon EW (1974) Phospholipids and plant membrane permeability. New Phytol 73:377–420
Simons K, Sampaio JL (2011) Membrane organization and lipid rafts. Cold Spring Harb Perspect Biol 3:a004697
Singer SJ, Nicolson GL (1972) The fluid mosaic model of the structure of cell membranes. Science 175:720–731
Sonnino S, Prinetti A (2013) Membrane domains and the “lipid raft” concept. Curr Med Chem 20:4–21
Sperl W, Murr C, Skladal D, Sass J, Suormala T, Baumgartner R, Wendel U (2000) Odd-numbered long-chain fatty acids in propionic acidaemia. Eur J Pediatr 159:54–58
Suss KH, Yordanov IT (1986) Biosynthetic cause of in vivo acquired thermotolerance of photosynthetic light reactions and metabolic responses of chloroplasts to heat stress. Plant Physiol 81:192–199
Sullivan CY (1972) Mechanisms of heat and drought resistance ingrain sorghum and methods of measurement. In: Raoand NGP, House LR (eds) Sorghum in the seventies. Oxford and IPH Publishing Co, New Delhi
Vikstrom S, Li L, Wieslander A (2000) The nonbilayer/bilayer lipid balance in membranes. Regulatory enzyme in Acholeplasma laidlawii is stimulated by metabolic phosphates, activator phospholipids, and double-stranded DNA. J Biol Chem 275:9296–9302
Voet D, Voet JG, Pratt CW (2008) Fundamentals of biochemistry, 3rd edn. Wiley, New York
Webb MS, Green BR (1991) Biochemical and biophysical properties of thylakoid acyl lipids. Biochim Biophys Acta 1060, 133–158.
Welti R, Rintoul DA, Goodsaid-Zalduondo F, Felder S, Silbert DF (1981) Gel phase phospholipid in the plasma membrane of sterol-depleted mouse LM cells. Analysis by fluorescence polarization and x-ray diffraction. J Biol Chem. 256(14):7528–35
Wendel U (1989) Abnormality of odd-numbered long-chain fatty acids in erythrocyte membrane lipids frompatients with disorders of propionatemetabolism. Pediatr Res 25:147–150
Williams EE (1998) Membrane lipids: what membrane physical properties are conserve during physiochemically-inducedmembrane restructuring? Am Zool 38:280–290
Zheng G, Tian B, Zhang F, Tao F, Li W (2011) Plant adaptation to frequent alterations between high and low temperatures: remodelling of membrane lipids and maintenance of unsaturation levels. Plant Cell and Environment 34:1431–1442
Acknowledgments
The author thanks Dr. Ruth Welti (Professor at Kansas State University and Director of Kansas Lipidomics Research Center) for critical review and editing of the chapter.
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Narayanan, S. (2021). Membrane Fluidity and Compositional Changes in Response to High Temperature Stress in Wheat. In: Wani, S.H., Mohan, A., Singh, G.P. (eds) Physiological, Molecular, and Genetic Perspectives of Wheat Improvement. Springer, Cham. https://doi.org/10.1007/978-3-030-59577-7_6
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