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5 - Cell structural modifications in insects at low temperatures

from PART I - PHYSIOLOGICAL AND MOLECULAR RESPONSES

Published online by Cambridge University Press:  04 May 2010

By
Vladimír Koštál
Edited by
David L. Denlinger  and
Richard E. Lee, Jr
David L. Denlinger
Affiliation:
Ohio State University
Richard E. Lee, Jr
Affiliation:
Miami University
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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).

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Low Temperature Biology of Insects , pp. 116 - 140
Publisher: Cambridge University Press
Print publication year: 2010

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References

Aitchison, C. W. (1979a). Winter-active subnivean invertebrates in Southern Canada. II. Coleoptera. Pedobiologia 19, 1121–128.Google Scholar
Aitchison, C. W. (1979b). Winter-active subnivean invertebrates in Southern Canada. IV. Diptera and Hymenoptera. Pedobiologia 19, 176–182.Google Scholar
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.CrossRefGoogle ScholarPubMed
Amos, L. A. and Amos, W. G. (1991). Molecules of Cytoskeleton. New York: Guilford Press.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
Block, W. (1996). Cold or drought – the lesser of two evils for terrestrial arthropods?European Journal of Entomology 93, 325–339.Google Scholar
Blomquist, G. J., Borgeson, C. E., and Vundla, M. (1991). Polyunsaturated fatty acids and eicosanoids in insects. Insect Biochemistry 21, 99–106.CrossRefGoogle Scholar
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.Google ScholarPubMed
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.Google Scholar
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
Chapman, D. (1975). Phase transitions and fluidity characteristics of lipids and cell membranes. Quarterly Reviews of Biophysics 8, 185–235.CrossRefGoogle ScholarPubMed
Clegg, J. S. (2001). Cryptobiosis – a peculiar state of biological organization. Comparative Biochemistry and Physiology B 128, 613–624.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
Cossins, A. R. and Prosser, C. L. (1978). Evolutionary adaptation of membranes to temperature. Proceedings of National Academy of Sciences USA 75, 2040–2043.CrossRefGoogle Scholar
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.Google Scholar
Coyne, J. A. and Elwyn, S. (2006). Does the desaturase-2 locus in Drosophila melanogaster cause adaptation and sexual isolation?Evolution 60, 279–291.CrossRefGoogle ScholarPubMed
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.Google Scholar
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.CrossRefGoogle ScholarPubMed
Dowhan, W. (1997). Molecular basis for membrane phospholipid diversity: Why are there so many lipids?Annual Reviews of Biochemistry 66, 199–232.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
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.Google Scholar
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
Haines, T. H. (2001). Do sterols reduce proton and sodium leaks through lipid bilayers?Progress in Lipid Research 40, 299–324.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
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.Google Scholar
Hazel, J. R. (1989). Cold adaptation in ectotherms: Regulation of membrane function and cellular metabolism. Advances in Comparative and Environmental Physiology 4, 1–50.CrossRefGoogle Scholar
Hazel, J. R. (1995). Thermal adaptation in biological membranes: Is homeoviscous adaptation the explanation?Annual Reviews of Physiology 57, 19–42.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
Henriques, V. and Hansen, C. (1901). Vergleichende Untersuchungen über die chemische Zusammenstzung des tierishen Fettes. Skandinawischen Archive für Physiologie 11, 151–165.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
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.Google ScholarPubMed
Koštál, V. (2006). Eco-physiological phases of insect diapause. Journal of Insect Physiology 52, 113–127.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
Lee, R. E., Chen, C. P., and Denlinger, D. L. (1987). A rapid cold-hardening process in insects. Science 238, 1415–1417.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Liang, P. and MacRae, T. H. (1997). Molecular chaperones and cytoskeleton. Journal of Cell Science 110, 1431–1440.Google ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.Google Scholar
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.Google Scholar
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Mounier, N. and Arrigo, A. P. (2002). Actin cytoskeleton and small heat shock proteins: how do they interact?Cell Stress & Chaperones 7, 167–176.2.0.CO;2>CrossRefGoogle ScholarPubMed
Murata, N. and Yamaya, J. (1984). Temperature-dependent phase behavior of phosphatidylglycerols from chilling sensitive and chilling-resistant plants. Plant Physiology 74, 1016–1024.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
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, 329–340.3.0.CO;2-Z>CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
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.Google ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Singer, M. (1981). Permeability of phosphatidylcholine bilayers. Chemistry and Physics of Lipids 28, 253–267.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
Stanley-Samuelson, D. W. and Dadd, R. H. (1983). Long-chain polyunsaturated fatty acids: patterns of occurrence in insects. Insect Biochemistry 13, 549–558.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
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.Google ScholarPubMed
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.Google ScholarPubMed
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.Google Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Zachariassen, K. E., Kristiansen, E., and Pedersen, S. A. (2004). Inorganic ions in cold-hardiness. Cryobiology 48, 126–133.CrossRefGoogle ScholarPubMed

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