Skip to main content Accessibility help
×
Home
  • Get access
    Check if you have access via personal or institutional login
  • Cited by 24
  • Print publication year: 2010
  • Online publication date: May 2010

5 - Cell structural modifications in insects at low temperatures

from PART I - PHYSIOLOGICAL AND MOLECULAR RESPONSES

Summary

Introduction

Cells of poikilotherm organisms are subjected to a whole range of variation in environmental temperature and have evolved powerful responses to cope with daily and seasonal temperature fluctuations (Lee, 1991). This chapter deals with the acclimatory changes of the basic cell structural components, such as biological membranes, cytoskeleton, organelles (mitochondria) and large (nucleo) protein complexes, which were observed in preparation for, or in a direct response to, a decline in environmental temperature in insects. The main focus will be on biological membranes because this information is by far the most complete, and the situation in insects may be compared to knowledge on fish and other poikilotherms (Cossins and Sinensky, 1984; Cossins, 1994; Hazel, 1989; 1995; Hazel and Williams, 1990).

Considering the adaptive meaning of acclimatory responses, two broad categories can be theoretically distinguished: (i) compensation of physiological function (capacity adaptation) and (ii) preservation of biological structure (resistance adaptation) (Cossins and Bowler, 1987). Some insects inhabiting temperate zones remain fully active in buffered microhabitats throughout the cold season (Aitchison, 1979a, b), and such insects probably need a certain level of physiological compensation. Most species, however, spend winter in dormancy (Koštál et al., 2006), and those insects probably have to rely more on resistance mechanisms. Strong resistance mechanisms can be expected in those insects that undergo freezing or dehydration, sometimes reaching the cryptobiotic state (sensu Clegg, 2001).

References
Aitchison, C. W. (1979a). Winter-active subnivean invertebrates in Southern Canada. II. Coleoptera. Pedobiologia 19, 1121–128.
Aitchison, C. W. (1979b). Winter-active subnivean invertebrates in Southern Canada. IV. Diptera and Hymenoptera. Pedobiologia 19, 176–182.
Allakhverdiev, S. I., Nishiyama, Y., Suzuki, I., Tasaka, Y., and Murata, N. (1999). Genetic engineering of the unsaturation of fatty acids in membrane lipids alters the tolerance of Synechocystis to salt stress. Proceedings of National Academy of Sciences USA 96, 5862–5867.
Amos, L. A. and Amos, W. G. (1991). Molecules of Cytoskeleton. New York: Guilford Press.
Bahrndorf, S., Petersen, S. O., Loeschke, V., Overgaard, J., and Holmstrup, M. (2007). Differences in cold and drought tolerance of high arctic and sub-arctic populations of Megaphorura arctica Tullberg 1876 (Onychiuridae: Collembola). Cryobiology 55, 315–323.
Bashan, M., Akbas, H., and Yurdakoc, K. (2002). Phospholipid and triacylglycerol fatty acid composition of major life stages of sunn pest, Eurygaster integriceps (Heteroptera: Scutelleridae). Comparative Biochemistry and Physiology B 132, 375–380.
Bashan, M. and Cakmak, O. (2005). Changes in composition of phospholipid and triacylglycerol fatty acids prepared from prediapausing and diapausing individuals of Dolycoris baccarum and Piezodorus lituratus (Heteroptera: Pentatomidae). Annals of Entomological Society of America 98, 575–579.
Bayley, M., Petersen, S. O., Knigge, T., Kohler, H.-R., and Holmstrup, M. (2001). Drought acclimation confers cold tolearnce in the soil collembolan Folsomia candida. Journal of Insect Physiology 47, 1197–1204.
Behan-Martin, M. K., Jones, G. R., Bowler, K., and Cossins, A. R. (1993). A near perfect temperature adaptation of bilayer order in vertebrate brain membranes. Biochimica & Biophysica Acta 1151, 216–222.
Bennett, V. A., Pruitt, N. L., and LeeJr., R. E. Jr., R. E. (1997). Seasonal changes in fatty acid composition associated with cold-hardening in third instar larvae of Eurosta solidaginis. Journal of Comparative Physiology B 167, 249–255.
Block, W. (1996). Cold or drought – the lesser of two evils for terrestrial arthropods?European Journal of Entomology 93, 325–339.
Blomquist, G. J., Borgeson, C. E., and Vundla, M. (1991). Polyunsaturated fatty acids and eicosanoids in insects. Insect Biochemistry 21, 99–106.
Brooks, S., Clark, G. T., Wright, S. M., Trueman, R. J., Postle, A. D., Cossins, A. R., and Maclean, N. M. (2002). Electrospray ionisation mass spectrometric analysis of lipid restructuring in the carp (Cyprinus carpio L.) during cold acclimation. Journal of Experimental Biology 205, 3989–3997.
Browse, J., Miquel, M., McConn, M., and Wu, J. (1994). Arabidopsis mutants and genetic approaches to the control of lipid composition. In Temperature Adaptations of Biological Membranes, ed. Cossins, A. R. London and Chapel Hill: Portland Press, pp. 141–154.
Canavoso, L. E., Jouni, Z. E., Karnas, K. J., Pennington, J. E., and Wells, M. A. (2001). Fat metabolism in insects. Annual Review of Nutrition 21, 23–46.
Chamberlain, P. M. and Black, H. I. J. (2005). Fatty acid compositions of Collembola: unusually high proportions of c05-88635 polyunsaturated fatty acids in a terrestrial invertebrate. Comparative Biochemistry and Physiology B 140, 299–307.
Chapman, D. (1975). Phase transitions and fluidity characteristics of lipids and cell membranes. Quarterly Reviews of Biophysics 8, 185–235.
Clegg, J. S. (2001). Cryptobiosis – a peculiar state of biological organization. Comparative Biochemistry and Physiology B 128, 613–624.
Colinet, H., Nguyen, T. T. A., Cloutier, C., Michaud, D., and Hance, T. (2007). Proteomic profiling of a parasitic wasp exposed to constant and fluctuating cold exposure. Insect Biochemistry and Molecular Biology 37, 1177–1188.
Cook, H. W. and McMaster, C. R. (2002). Fatty acid desaturation and chain elongation in eukaryotes. In Biochemistry of Lipids, Lipoproteins and Membranes, ed. Vance, D. E. and Vance, J. E.. Amsterdam: Elsevier, pp. 181–204.
Cossins, A. R. (1977). Adaptations of biological membranes to temperature – the effect of temperature acclimation of goldfish upon the viscosity of synaptosomal membranes. Biochimica & Biophysica Acta 470, 395–411.
Cossins, A. R. ed. (1994). Temperature Adaptation of Biological Membranes. London and Chapel Hill: Portland Press.
Cossins, A. R. and Bowler, K. (1987). The Temperature Biology of Animals. London: Chapman and Hall.
Cossins, A. R. and Macdonald, A. G. (1989). The adaptation of biological membranes to temperature and pressure: Fish from the deep and cold. Journal of Bioenergetics and Biomembranes 21, 115–135.
Cossins, A. R., Murray, P. A. Gracey, A. Y., Logue, J., Polley, S., Caddick, M., Brooks, S., Postle, T., and Maclean, N. (2002). The role of desaturases in cold-induced lipid restructuring. Biochemical Society Transactions 30, 1082–1086.
Cossins, A. R. and Prosser, C. L. (1978). Evolutionary adaptation of membranes to temperature. Proceedings of National Academy of Sciences USA 75, 2040–2043.
Cossins, A. R. and Sinensky, M. (1984). Adaptations of membranes to temperature, pressure and exogenous lipids. In Physiology of Membrane Fluidity, 2nd edn, ed. Shinitzky, M.. Boca Raton: CRC Press, pp. 1–20.
Coyne, J. A. and Elwyn, S. (2006). Does the desaturase-2 locus in Drosophila melanogaster cause adaptation and sexual isolation?Evolution 60, 279–291.
Crockett, E. L. and Hazel, J. R. (1995). Cholesterol levels explain inverse compensation of membrane order in brush border but not homeoviscous adaptation in basolateral membranes from the intestinal epithelia of rainbow trout. Journal of Experimental Biology 198, 1105–1113.
Dallerac, R., Labeur, C., Jallon, J.-M., Knipple, D. C., Roelofs, W. L., and Wicker-Thomas, C. (2000). A Δ9 desaturase gene with a different substrate specificity is responsible for the cuticular diene hydrocarbon polymorphism in Drosophila melanogaster. Proceedings of National Academy of Sciences USA 97, 9449–9454.
Dowhan, W. (1997). Molecular basis for membrane phospholipid diversity: Why are there so many lipids?Annual Reviews of Biochemistry 66, 199–232.
Downer, R. G. H. and Kallapur, V. L. (1981). Temperature-induced changes in lipid composition and transition temperature of flight muscle mitochondria of Schistocerca gregaria. Journal of Thermal Biology 6, 189–194.
Egiersdorff, S. and Kacperska, A. (2001). Low temperature effects on growth and actin cytoskeleton organization in suspension cells of winter oilseed rape. Plant Cell and Tissue Organ Cultures 40, 17–25.
Eigenheer, A. L., Young, S., Blomquist, G. J., Borgeson, C. E., Tillman, J. A., and Tittiger, C. (2002). Isolation and molecular characterization of Musca domestica delta-9 desaturase sequences. Insect Molecular Biology 11, 533–542.
Garlick, K. M. and Robertson, R. M. (2007). Cytoskeletal stability and heat-shock mediated thermoprotection of central pattern generation in Locusta migratoria. Comparative Biochemistry and Physiology A 147, 344–348.
Gonzales, M. S. and Brenner, R. R. (1999). Fatty acid Δ9-desaturation in the Triatoma infestans fat body: Response to food and trehalose administration. Lipids 34, 1199–1205.
Greenberg, A. J., Moran, J. R., Coyne, J. A., and Wu, C.-I. (2003). Ecological adaptation during incipient speciation revealed by precise gene replacement. Science 302, 1754–1757.
Haines, T. H. (2001). Do sterols reduce proton and sodium leaks through lipid bilayers?Progress in Lipid Research 40, 299–324.
Hanson, B. J., Cummins, K. W., Cargill, A. S., and Lowry, R. R. (1985). Lipid content, fatty acid composition, and the effect of diet on fats of aquatic insects. Comparative Biochemistry and Physiology B, 80, 257–276.
Harwood, J. L., Jones, A. L., Perry, H. J., Rutter, A. J., Smith, K. L., and Williams, M. (1994). Changes in plant lipids during temperature adaptation. In Temperature Adaptation of Biological Membranes. London and Chapel Hill: Portland Press, pp. 107–118.
Hazel, J. R. (1989). Cold adaptation in ectotherms: Regulation of membrane function and cellular metabolism. Advances in Comparative and Environmental Physiology 4, 1–50.
Hazel, J. R. (1995). Thermal adaptation in biological membranes: Is homeoviscous adaptation the explanation?Annual Reviews of Physiology 57, 19–42.
Hazel, J. R. and Williams, E. E. (1990). The role of alterations in membrane lipid composition in enabling physiological adaptation of organisms to their physical environment. Progress in Lipid Research 29, 167–227.
Hayward, S. A. L., Murray, P. A., Gracey, A. Y., and Cossins, A. R. (2007). Beyond the lipid hypothesis: Mechanisms underlying phenotypic plasticity in inducible cold tolerance. In Molecular Aspects of the Stress Response: Chaperons, Membranes and Networks, ed. Csermely, P. and Vigh, L.. Austin: Landes Bioscience, pp. 132–142.
Henriques, V. and Hansen, C. (1901). Vergleichende Untersuchungen über die chemische Zusammenstzung des tierishen Fettes. Skandinawischen Archive für Physiologie 11, 151–165.
Hodková, M., Berková, P., and Zahradníčková, H. (2002). Photoperiodic regulation of the phospholipid molecular species composition in thoracic muscles and fat body of Pyrrhocoris apterus (Heteroptera) via an endocrine gland, corpus allatum. Journal of Insect Physiology 48, 1009–1019.
Hodková, M., Šimek, P., Zahradníčková, H., and Nováková, O. (1999). Seasonal changes in the phospholipid composition in thoracic muscles of a heteropteran, Pyrrhocoris apterus. Insect Biochemistry and Molecular Biology 29, 367–376.
Holmstrup, M., Hedlund, K., and Boriss, H. (2002). Drought acclimation and lipid composition in Folsomia candida: implications for cold shock, heat shock and acute desiccation stress. Journal of Insect Physiology 48, 961–970.
Huang, C.-H., Lin, H., Li, S., and Wang, G. (1997). Influence of the positions of cis double bonds in the sn-2 acyl chain of phosphatidylethanolamine on the bilayer's melting behavior. Journal of Biological Chemistry 272, 21917–21926.
Jurenka, R. A., Renobales, M., and Blomquist, G. J. (1987). De novo synthesis of polyunsaturated fatty acids in the cockroach Periplaneta americana. Archives of Biochemistry and Biophysics 255, 184–193.
Kayukawa, T., Chen, B., Hoshizaki, S., and Ishikawa, Y. (2007). Upregulation of a desaturase is associated with the enhancement of cold hardiness in the onion maggot, Delia antiqua. Insect Biochemistry and Molecular Biology 37, 1160–1167.
Kayukawa, T., Chen, B., Miyazaki, S., Itoyama, K., Shinoda, T., and Ishikawa, Y. (2005). Expression of mRNA for the t-complex polypeptide-1, a subunit of chaperonin CCT, is upregulated in association with increased cold hardiness in Delia antiqua. Cell Stress & Chaperones 10, 204–210.
Kim, M., Robich, R. M., Rinehart, J. P., and Denlinger, D. L. (2006). Upregulation of two actin genes and redistribution of actin during diapause and cold stress in the northern house mosquito, Culex pipiens. Journal of Insect Physiology 52, 1226–1233.
Kirk, G. L., Gruner, S. M., and Stein, D. L. (1984). A thermodynamic model of the lamellar to inverse hexagonal phase transition of lipid membrane-water systems. Biochemistry 23, 1093–1102.
Knipple, D. C., Rosenfield, C.-L., Nielsen, R., You, K. M., and Jeong, S. E. (2002). Evolution of the integral membrane desaturase gene family in moths and flies. Genetics 162, 1737–1752.
Koštál, V. (2006). Eco-physiological phases of insect diapause. Journal of Insect Physiology 52, 113–127.
Koštál, V., Berková, P., and Šimek, P. (2003). Remodelling of membrane phospholipids during transition to diapause and cold-acclimation in the larvae of Chymomyza costata (Drosophilidae). Comparative Biochemistry and Physiology B 135, 407–419.
Koštál, V. and Šimek, P. (1998). Changes in fatty acid composition of phospholipids and triacylglycerols after cold-acclimation of an aestivating insect prepupa. Journal of Comparative Physiology B 168, 453–460.
Koštál, V., Vambera, J., and Bastl, J. (2004). On the nature of pre-freeze mortality in insects: water balance, ion homeostasis and energy charge in the adults of Pyrrhocoris apterus. Journal of Experimental Biology 207, 1509–1521.
Kristiansen, E. and Zachariassen, K. E. (2001). Effect of freezing on the transmembrane distribution of ions in freeze-tolerant larvae of the wood fly Xylophagus cinctus (Diptera, Xylophagidae). Journal of Insect Physiology 47, 585–592.
Kukal, O., Duman, J. G., and Serianni, A. S. (1989). Cold-induced mitochondrial degradation and cryoprotectant synthesis in freeze-tolerant arctic caterpillars. Journal of Comparative Physiology B 158, 661–671.
Kukal, O. and Kevan, P. G. (1987). The influence of parasitism on the life history of a high arctic insect, Gynaephora groenlandica (Wocke) (Lepidoptera: Lymantridae). Canadian Journal of Zoology 65, 156–163.
Lee, K.-Y., Hiremath, S., and Denlinger, D. L. (1998). Expression of actin in the central nervous system is switched off during diapause in the gypsy moth, Lymantria dispar. Journal of Insect Physiology 44, 221–226.
Lee, R. E. (1991). Principles of insect low temperature tolerance. In Insects at Low Temperature, ed. Lee, R. E. and Denlinger, D. L.. New York and London: Chapman and Hall, pp. 17–46.
Lee, R. E., Chen, C. P., and Denlinger, D. L. (1987). A rapid cold-hardening process in insects. Science 238, 1415–1417.
Lee, R. E., Damoradan, K., Yi, S.-X., and Lorigan, G. A. (2006). Rapid cold-hardening increases membrane fluidity and cold tolerance of insect cells. Cryobiology 52, 459–463.
Levin, D. B., Danks, H. V., and Barber, S. A. (2003). Variations in mitochondrial DNA and gene transcription in freeze-tolerant larvae of Eurosta solidaginis (Diptera: Tephritidae) and Gynaephora groenlandica (Lepidoptera: Lymantriidae). Insect Molecular Biology 12, 281–289.
Lewis, R. N. A. H., Mannock, D. A., McElhaney, R. N., Turner, D. C., and Gruner, S. M. (1989). Effect of fatty-acyl chain length and structure on the lamellar gel to liquid-crystalline and lamellar to reverse hexagonal phase transitions of aquaeous phosphatidylethanolamine dispersions. Biochemistry 28, 541–548.
Li, A. Q., Popova-Butler, A., Dean, D. H., and Denlinger, D. L. (2007). Proteomics of the flesh fly brain reveals an abundance of upregulated heat shock proteins during pupal diapause. Journal of Insect Physiology 53, 385–391.
Li, S., Wang, G., Lin, H., and Huang, C.-H. (1998). Calorimetric studies of phosphatidylethanolamines with saturated sn-1 and dienoic sn-2 acyl chains. Journal of Biological Chemistry 273, 19009–19018.
Liang, P. and MacRae, T. H. (1997). Molecular chaperones and cytoskeleton. Journal of Cell Science 110, 1431–1440.
Liu, W., Ma, P. W. K., Marsella-Herrick, P., Rosenfield, C. L., Knipple, D. C., and Roelofs, W. (1999). Cloning and functional expression of a cDNA encoding a metabolic acyl-CoA delta 9-destaurase of the cabbage looper moth, Trichoplusia ni. Insect Biochemistry and Molecular Biology 29, 435–443.
Macartney, A., Maresca, B., and Cossins, A. R. (1994). Acyl-CoA desaturases and the adaptive regulation of membrane lipid composition. In The Temperature Biology of Animals. London: Chapman and Hall, pp. 129–139.
McElhaney, R. N. (1984). The relationship between membrane lipid fluidity and phase state and the ability of bacteria and mycoplasms to grow and survive at various temperatures. Biomembranes 12, 249–276.
McMullen, D. C. and Storey, K. B. (2008). Mitochondria of cold hardy insects: responses to cold and hypoxia assessed at enzymatic, mRNA and DNA levels. Insect Biochemistry and Molecular Biology 38, 367–373.
Michaud, M. R. and Denlinger, D. L. (2006). Oleic acid is elevated in cell membranes during rapid cold-hardening and pupal diapause in the flesh fly, Sarcophaga crassipalpis. Journal of Insect Physiology 52, 1073–1082.
Mounier, N. and Arrigo, A. P. (2002). Actin cytoskeleton and small heat shock proteins: how do they interact?Cell Stress & Chaperones 7, 167–176.
Murata, N. and Yamaya, J. (1984). Temperature-dependent phase behavior of phosphatidylglycerols from chilling sensitive and chilling-resistant plants. Plant Physiology 74, 1016–1024.
Murray, P., Hayward, S. A. L., Govan, G. G., Gracey, A. Y., and Cossins, A. R. (2007). An explicit test of the phospholipid saturation hypothesis of acquired cold tolerance in Caenorhabditis elegans. Proceedings of National Academy of Sciences USA 104, 5489–5494.
Nozawa, Y., Iida, H., Fukushima, H., Ohki, K., and Ohnishi, S. (1974). Studies on Tetrahymena membranes: temperature-induced alterations in fatty acid composition of various membrane fractions in Tetrahymena pyriformis and its effect on membrane fluidity as inferred by spin-label study. Biochemica & Biophysica Acta 367, 134–147.
Ohtsu, T., Kimura, M. T., and Katagiri, C. (1998). How Drosophila species acquire cold tolerance. Qualitative changes of phospholipids. European Journal of Biochemistry 252, 608–611.
Ohtsu, T., Katagiri, C., and Kimura, M. T. (1999). Biochemical aspects of climatic adaptations in Drosophila curviceps, D. immigrans and D. albomicans (Diptera: Drosophilidae). Environmental Entomology 28, 968–972.
Overgaard, J., Sørensen, J. G., Petersen, S. O., Loeschke, V., and Holmstrup, M. (2005). Changes in membrane lipid composition following rapid cold hardening in Drosophila melanogaster. Journal of Insect Physiology 51, 1173–1182.
Overgaard, J., Sørensen, J. G., Petersen, S. O., Loeschke, V., and Holmstrup, M. (2006). Reorganization of membrane lipids during fast and slow cold hardening in Drosophila melanogaster. Physiological Entomology 31, 328–335.
Overgaard, J., Tomčala, A., Sørensen, J. G., Holmstrup, M., Krogh, P. H., Šimek, P., and Koštál, V. (2008). Effects of acclimation temperature on thermal tolerance and membrane phosholipid composition in the fruit fly Drosophila melanogaster. Journal of Insect Physiology 54, 619–629.
Pruitt, N. L. and Lu, C. (2008). Seasonal changes in phospholipid class and class-specific fatty acid composition associated with the onset of freeze tolerance in third-instar larvae of Eurosta solidaginis. Physiological and Biochemical Zoology 81, 226–234.
Pucciarelli, S, Ballarini, P., and Miceli, C. (1997). Cold-adapted microtubules: characterization of tubulin posttranslational modifications in the Antarctic ciliate Euplotes focardii. Cell Motility and Cytoskeleton 38, 329–340.
Qin, W., Neal, S. J., Robertson, R. M., Westwood, J. T., and Walker, V. K. (2005). Cold hardening and transcriptional change in Drosophila melanogaster. Insect Molecular Biology 14, 607–613.
Ramesha, C. S. and Thompson, G. A. (1983). Cold stress induces in situ phospholipid molecular species changes in cell surface membranes. Biochimica & Biophysica Acta 731, 251–260.
Riddervold, M. H., Tittiger, C., Blomquist, G. J., and Borgeson, C. E. (2002). Biochemical and molecular characterization of house cricket (Acheta domesticus, Orthoptera: Gryllidae) delta 9 desaturase. Insect Biochemistry and Molecular Biology 32, 1731–1740.
Rinehart, J. P., Li, A. Q., Yocum, G. D., Robich, R. M., Hayward, S. A. L., and Denlinger, D. L. (2007). Up-regulation of heat shock proteins is essential for cold survival during insect diapause. Proceedings of National Academy of Sciences USA 104, 11130–11137.
Robich, R. M., Rinehart, J. P., Kitchen, L. J., and Denlinger, D. L. (2007). Diapause-specific gene expression in the northern house mosquito, Culex pipiens L., identified by suppressive subtractive hybridization. Journal of Insect Physiology 53, 235–245.
Schunke, M. and Wodtke, E. (1983). Cold-induced increase of delta-nine and delta-six desaturase activities in endoplasmic membranes of carp liver. Biochimica and Biophysica Acta 734, 70–75.
Shreve, S. M., Yi, S.-X., and Lee, R. E. (2007). Increased dietary cholesterol enhances cold tolerance in Drosophila melanogaster. Cryo-Letters 28, 33–37.
Sinensky, M. (1974). Homeoviscous adaptation – a homeostatic process that regulates viscosity of membrane lipids in Escherichia coli. Proceedings of National Academy of Sciences USA 71, 522–525.
Singer, M. (1981). Permeability of phosphatidylcholine bilayers. Chemistry and Physics of Lipids 28, 253–267.
Šlachta, M., Berková, P., Vambera, J., and Koštál, V. (2002). Physiology of cold-acclimation in non-diapausing adults of Pyrrhocoris apterus (Heteroptera). European Journal of Entomology 99, 181–187.
Sørensen, P. G. (1993). Changes of the composition of phospholipids, fatty acids and cholesterol from the erythrocyte plasma membrane from flounders (Platichthys flesus L.) which were acclimated to high and low temperatures in aquaria. Comparative Biochemistry and Physiology B 106, 907–912.
Stanley-Samuelson, D. W. and Dadd, R. H. (1983). Long-chain polyunsaturated fatty acids: patterns of occurrence in insects. Insect Biochemistry 13, 549–558.
Stanley-Samuelson, D. W., Jurenka, R. A., Cripps, C., Blomquist, G. J., and Renobales, M. (1988). Fatty acids in insects: Composition, metabolism and biological significance. Archives of Insect Biochemistry and Physiology 9, 1–33.
Storey, K. B. and Storey, J. M. (2007). Tribute to P. L. Lutz: putting life on “pause” – molecular regulation of hypometabolism. Journal of Experimental Biology 210, 1700–1714.
Suutari, M., Rintamaki, A., and Laakso, S. (1997). Membrane phospholipids in temperature adaptation of Candida utilis: alterations in fatty acid chain length and unsaturation. Journal of Lipid Research 38, 790–794.
Tasaka, Y., Gombos, Z., Nishiyama, Y., Mohanty, P., Ohba, T., Ohki, K., and Murata, N. (1996). Targeted mutagenesis of acyl-lipid desaturases in Synechocystis: evidence for the important roles of polyunsaturated membrane lipids in growth, respiration and photosynthesis. EMBO Journal 15, 6416–6425.
Thompson, S. N. (1973). A review and comparative characterization of the fatty acid composition of seven insect orders. Comparative Biochemistry and Physiology 45, 467–482.
Tiku, P. E., Gracey, A. Y., Macartney, A. I., Beynon, R. J., and Cossins, A. R. (1996). Cold-induced expression of Δ9-desaturase in carp by transcriptional and posttraslational mechanisms. Science 271, 815–818.
Tomčala, A., Tollarová, M., Overgaard, J., Šimek, P., and Koštál, V. (2006). Seasonal acquisition of chill-tolerance and restructuring of membrane glycerophospholipids in an overwintering insect: triggering by low temperature, desiccation and diapause progression. Journal of Experimental Biology 209, 4102–4114.
Wang, G., Li, S., Lin, H., Brumbaugh, E. E., and Huang, C.-H. (1999). Effects of various numbers and positions of cis double bonds in the sn-2 acyl chain of phosphatidylethanolamine on the chain-melting temperature. Journal of Biological Chemistry 274, 12289–12299.
Wicker-Thomas, C., Henriet, C., and Dallerac, R. (1997). Partial characterization of a fatty acid desaturase gene in Drosophila melanogaster. Insect Biochemistry and Molecular Biology 27, 963–972.
Wodtke, E. and Cossins, A. R. (1991). Rapid cold-induced changes of membrane order and Δ9-desaturase actitivy in endoplasmic reticulum of carp liver: A time-course study of thermal acclimation. Biochimica and Biophysica Acta 1064, 343–350.
Yi, S.-X. and Lee, R. E. (2005). Changes in gut and Malpighian tubule transport during seasonal acclimatization and freezing in the gall fly Eurosta solidaginis. Journal of Experimental Biology 208, 1895–1904.
Yocum, G. D., Kemp, W. P., Bosch, J., and Knoblett, J. M. (2005). Temporal variation in overwintering gene expression and respiration in the solitary bee Megachile rotundata. Journal of Insect Physiology 51, 621–629.
Zachariassen, K. E., Kristiansen, E., and Pedersen, S. A. (2004). Inorganic ions in cold-hardiness. Cryobiology 48, 126–133.