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2 - Rapid cold-hardening: Ecological significance and underpinning mechanisms

from PART I - PHYSIOLOGICAL AND MOLECULAR RESPONSES

Published online by Cambridge University Press:  04 May 2010

David L. Denlinger
Affiliation:
Ohio State University
Richard E. Lee, Jr
Affiliation:
Miami University
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Summary

Introduction

Insects are constantly subjected to changes in environmental temperature. Most studies of insect acclimation to low temperature concern seasonal changes that occur over weeks or months in preparation for winter, and, accordingly, most chapters in this volume focus on seasonal cold-hardening. In contrast, during the past 10 years considerable attention has been paid to rapid acclimatory responses to both high (i.e. induction of heat shock or stress proteins (Feder et al., 2002) and low temperature. This chapter summarizes our current understanding of the rapid cold-hardening (RCH) response. When our previous book (Lee and Denlinger, 1991) was being written, the RCH response had only just been described and merited only a few scattered paragraphs. Indeed, at that time it was unclear whether this response was merely a laboratory artifact or a previously unrecognized type of rapid acclimation. Since then, the RCH response has emerged as a highly conserved trait, allowing diverse insect groups to swiftly adjust their physiological state and organismal performance to match even modest changes in environmental temperature. In this chapter, we summarize evidence supporting the ecological relevance and emerging physiological underpinnings of the RCH response.

The RCH response protects against a form of non-freezing injury known as cold-shock or direct-chilling injury. Cold-shock injury is well known among microbes, plants and animals, and represents a major obstacle for the successful cryopreservation of many types of cells and tissues (Grout, 1987). Injury is not associated with internal ice formation.

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Publisher: Cambridge University Press
Print publication year: 2010

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References

Bahrndorff, S., Loeschcke, V., Pertoldi, C., Beier, C., and Holmstrup, M. (2009). The rapid cold hardening response of Collembola is influenced by thermal variability of the habitat. Functional Ecology 23, 340–347CrossRefGoogle Scholar
Bale, J. S. (2002). Insects and low temperatures: from molecular biology to distributions and abundance. Philosophical Transactions of the Royal Society of London Series B-Biological Sciences 357, 849–861.CrossRefGoogle ScholarPubMed
Baust, J. M., Buskirk, R., and Baust, J. G. (2002). Gene activation of the apoptotic caspase cascade following cryogenic storage. Cell Preservation Technology 1, 63–80.CrossRefGoogle Scholar
Broufas, G. D. and Koveos, D. S. (2001). Rapid cold hardening in the predatory mite Euseius (Amblyseius) finlandicus (Acari: Phytoseiidae). Journal of Insect Physiology 47, 699–708.CrossRefGoogle Scholar
Burks, C. S. and Hagstrum, D. W. (1999). Rapid cold hardening capacity in five species of coleopteran pests of stored grain. Journal of Stored Products Research 35, 65–75.CrossRefGoogle Scholar
Burton, V., Mitchell, H. K., Young, P., and Petersen, N. S. (1988). Heat shock protection against cold stress of Drosophila melanogaster. Molecular and Cellular Biology 8, 3550–3552.CrossRefGoogle ScholarPubMed
Chen, C.-P. and Walker, V. K. (1994). Cold-shock and chilling tolerance in Drosophila. Journal of Insect Physiology 40, 661–669.CrossRefGoogle Scholar
Chen, C. P., Denlinger, D. L., and Lee, R. E. (1987). Cold-shock injury and rapid cold hardening in the flesh fly Sarcophaga crassipalpis. Physiological Zoology 60, 297–304.CrossRefGoogle Scholar
Chown, S. L. and Terblanche, J. S. (2007). Physiological diversity in insects: ecological and evolutionary contexts. Advances in Insect Physiology 33, 50–152.CrossRefGoogle Scholar
Coulson, S. J. and Bale, J. S. (1990). Characterization and limitations of the rapid cold-hardening response in the house fly Musca domestica (Diptera: Muscidae). Journal of Insect Physiology 36, 207–211.CrossRefGoogle Scholar
Coulson, S. J. and Bale, J. S. (1991). Anoxia induces rapid cold hardening in the house fly Musca domestica (Diptera: Muscidae). Journal of Insect Physiology 37, 497–501.CrossRefGoogle Scholar
Coulson, S. C. and Bale, J. S. (1992). Effect of rapid cold hardening on reproduction and survival of offspring in the house fly Musca domestica. Journal of Insect Physiology 38, 421–424.CrossRefGoogle Scholar
Coulson, S. J., Fisher, J., and Bale, J. S. (1992). A 31P NMR investigation of the energy charge of the house fly Musca domestica (Diptera: Muscidae) during rapid cold hardening and cold shock. CryoLetters 13, 183–192.Google Scholar
Crockett, E. L. (1998). Cholesterol function in plasma membranes from ectotherms: membrane-specific roles in adaptation to temperatures. American Zoologist 38, 291–304.CrossRefGoogle Scholar
Czajka, M. C. and Lee, R. E. (1990). A rapid cold-hardening response protecting against cold shock injury in Drosophila melanogaster. Journal of Experimental Biology 148, 245–254.Google ScholarPubMed
David, J. R., Gibert, P., Moreteau, B., Gilchrist, G. W., and Huey, R. B. (2003). The fly that came in from the cold: geographic variation of recovery time from low-temperature exposure in Drosophila subobscura. Functional Ecology 17, 425–430.CrossRefGoogle Scholar
David, R. J., Gibert, P., Pla, E., Petavy, G., Karan, D., and Moreteau, B. (1998). Cold stress tolerance in Drosophila: analysis of chill coma recovery in D. melanogaster. Journal of Thermal Biology 23, 291–299.CrossRefGoogle Scholar
Denlinger, D. L., Joplin, K. H., Chen, C. P., and Lee, R. E. (1991). Cold shock and heat shock. In Insects at Low Temperature, ed. Lee, R. E., and Denlinger, D. L.. New York: Chapman and Hall, pp. 131–148.CrossRefGoogle Scholar
Drobnis, E. Z., Crowe, L. M., Berger, T., Anchordoguy, T. J., Overstreet, J. W., and Crowe, J. H. (1993). Cold shock damage is due to lipid phase transitions in cell membranes: a demonstration using sperm as a model. Journal of Experimental Zoology 265, 432–437.CrossRefGoogle Scholar
Elnitsky, M. A., Hayward, S. A. L., Rinehart, J. P., Denlinger, D. L., and Lee, R. E. (2008). Cryoprotective dehydration and the resistance to inoculative freezing in the Antarctic midge, Belgica antarctica. Journal of Experimental Biology 211, 524–530.CrossRefGoogle ScholarPubMed
Feder, M. E., Bedford, T. C., Albright, D. R., and Michalak, P. (2002). Evolvability of Hsp70 expression under artificial selection for inducible thermotolerance in independent populations of Drosophila melanogaster. Physiological and Biochemical Zoology 75, 325–334.CrossRefGoogle ScholarPubMed
Fuchs, B. C. and Bode, B. P. (2006). Stressing out over survival: glutamine as an apoptotic modulator. Journal of Surgical Research 131, 26–40.CrossRefGoogle ScholarPubMed
Fujiwara, Y. and Denlinger, D. L. (2007). p38 MAP kinase is a likely component of the signal transduction pathway triggering rapid cold hardening in the flesh fly, Sarcophaga crassipalpis. Journal of Experimental Biology 210: 3295–3300.CrossRefGoogle Scholar
Grout, B. W. (1987). Direct chilling injury. In The Effects of Low Temperatures on Biological Systems, ed. Grout, B. W.. and Morris, G. J.. London: Edward Arnold, pp. 120–146.Google Scholar
Hazel, J. R. (1995). Thermal adaptation in biological membranes: is homeoviscous adaptation the explanation?Annual Review of Physiology 57, 19–42.CrossRefGoogle ScholarPubMed
Jagdale, G. B., Parwinder, S. G., and Salmnen, S. O. (2005). Both heat-shock and cold-shock influence trehalose metabolism in an entomopathogenic nematode. Journal of Parasitology 91, 988–994.CrossRefGoogle Scholar
Joplin, K. H. and Denlinger, D. L. (1990). Developmental and tissue specific control of the heat shock induced 70kDa related proteins in the flesh fly, Sarcophaga crassipalpis. Journal of Insect Physiology 36, 239–249.CrossRefGoogle Scholar
Kelty, J. (2007). Rapid cold-hardening of Drosophila melanogaster in a field setting. Physiological Entomology 32, 343–350.CrossRefGoogle Scholar
Kelty, J. D., Killian, K. A., and Lee, R. E. (1996). Cold shock and rapid cold-hardening of pharate adult flesh flies (Sarcophaga crassipalpis): effects on behaviour and neuromuscular function following eclosion. Physiological Entomology 21, 283–288.CrossRefGoogle Scholar
Kelty, J. D. and Lee, R. E. (1999). Induction of rapid cold-hardening by cooling at ecologically relevant rates in Drosophila melanogaster. Journal of Insect Physiology 45, 719–726.CrossRefGoogle ScholarPubMed
Kelty, J. D. and Lee, R. E. (2001). Rapid cold-hardening of Drosophila melanogaster (Diptera: Drosophilidae) during ecologically based thermoperiodic cycles. Journal of Experimental Biology 204, 1659–1666.Google ScholarPubMed
Kim, Y. and Kim, N. (1997). Cold hardiness in Spodoptera exigua (Lepidoptera: Noctuidae). Environmental Entomology 26, 1117–1123.CrossRefGoogle Scholar
Kim, Y.-S., Denlinger, D. L., and Smith, B. (2005). Spatial conditioning in the flesh fly, Sarcophaga crassipalpis: disruption of learning by cold shock and protection by rapid cold hardening. Journal of Asia-Pacific Entomology 8, 345–351.CrossRefGoogle Scholar
Klok, C. J., Chown, S. L., and Gaston, K. J. (2003). The geographical range structure of the holly leaf-miner. III. Cold-hardiness physiology. Functional Ecology 17, 858–868.CrossRefGoogle Scholar
Koveos, D. S. (2001). Rapid cold hardening in the olive fruit fly Bactrocera oleae under laboratory and field conditions. Entomologia Experimentalis et Applicata 101, 257–263.CrossRefGoogle Scholar
Larsen, K. J. and Lee, R. E. (1994). Cold tolerance including rapid cold-hardening and inoculative freezing in migrant monarch butterflies in Ohio. Journal of Insect Physiology 40, 859–864.CrossRefGoogle Scholar
Larsen, K. J., Lee, R. E., and Nault, L. R. (1993). Influence of developmental conditions on cold-hardiness of adult Dalbulus leafhoppers – implications for overwintering. Entomologia Experimentalis et Applicata 67, 99–108.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. and Denlinger, D. L. (1991). Insects at Low Temperature. New York: Chapman and Hall.CrossRefGoogle Scholar
Lee, R. E., Damodaran, 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
Leopold, R. A. (1998). Cold storage of insects for integrated pest management. In Temperature Sensitivity in Insects and Application in Integrated Pest Management, ed. Hallman, G. J. and Denlinger, D. L.. Boulder: Westview Press, pp. 235–267.Google Scholar
Li, A. and Denlinger, D. L. (2008). Rapid cold hardening elicits changes in brain protein profiles of the flesh fly, Sarcophaga crassipalpis. Insect Molecular Biology 17, 565–572.CrossRefGoogle ScholarPubMed
Li, Y., Gong, H., and Park, H. Y. (1999). Characterization of rapid cold-hardiness response in the overwintering mature larvae of pine needle gall midge, Thecodiplosis japonensis. CryoLetters 20, 383–392.Google Scholar
Mangan, R. L. and Hallman, G. J. (1998). Temperature treatments for quarantine security: new approaches for fresh commodities. In Temperature Sensitivity in Insects and Application in Integrated Pest Management, ed. Hallman, G. J. and Denlinger, D. L.. Boulder: Westview Press, pp. 201–234.Google Scholar
Massip, A., Leibo, S. P., and Blesbios, E. (2004). Cryobiology of gametes and the breeding of domestic animals. In Life in the Frozen State, ed. Fuller, B. J., Lane, N. and Benson, E. E.. Boca Raton: CRC Press, pp. 371–392.CrossRefGoogle Scholar
McDonald, J. R., Bale, J. S., and Walters, K. A. (1997). Rapid cold hardening in the western flower thrips Frankliniella occidentalis. Journal of Insect Physiology 43, 759–766.CrossRefGoogle Scholar
McElhaney, R. N. (1974). The effect of alterations in the physical state of the membrane lipids on the ability of Acholeplasma laidlawii B to grow at various temperatures. Journal of Molecular Biology 84, 145–157.CrossRefGoogle Scholar
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
Michaud, M. R. and Denlinger, D. L. (2007). Shifts in carbohydrate, polyol, and amino acid pools during rapid cold hardening and diapause-associated cold hardening in flesh flies (Sarcophaga crassipalpis): a metabolomic comparison. Journal of Comparative Physiology B 177, 753–763.CrossRefGoogle ScholarPubMed
Monroy, A. F. and Dhindsa, R. S. (1995). Low-temperature signal transduction: induction of cold acclimation-specific genes of alfalfa by calcium at 25°C. Plant Cell 7, 321–331.Google ScholarPubMed
Murakami, M., Kondo, T., Sato, S., Li, Y., and Chan, P. H. (1997). Occurrence of apoptosis following cold injury-induced brain edema in mice. Neuroscience 81, 231–237.CrossRefGoogle ScholarPubMed
Murata, N. and Los, D. A. (1997). Membrane fluidity and temperature perception. Plant Physiology 115, 875–879.CrossRefGoogle ScholarPubMed
Nunamaker, R. A. (1993). Rapid cold-hardening in Culicoides variipennis sonorensis (Diptera: Ceratopogonidae). Journal of Medical Entomology 30, 913–917.CrossRefGoogle Scholar
Orvar, B. L., Sangwan, V., Omann, F., and Dhindsa, R. S. (2000). Early steps in cold sensing by plant cells: the role of actin cytoskeleton and membrane fluidity. Plant Journal 23, 785–794.CrossRefGoogle ScholarPubMed
Overgaard, J., Malmendal, A., Sørenson, J. G., Bundy, J. G., Loeschcke, V., Nielsen, N. C., and Holmstrup, M. (2007). Metabolomic profiling of rapid cold hardening and cold shock in Drosophila melanogaster. Journal of Insect Physiology 53, 1218–1232.CrossRefGoogle ScholarPubMed
Overgaard, J., Sørensen, J. G., Petersen, S. O., Loeschcke, 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. and Sørensen, J. G. (2008). Rapid thermal adaptation during field temperature variations in Drosophila melanogaster. Cryobiology 56, 159–162.CrossRefGoogle ScholarPubMed
Phanvijhitsiri, K., Musch, M. W., Ropeleski, M. J., and Chang, E. B. (2005). Molecular mechanisms of L-glutamine modulation of heat stimulated Hsp25 production. FASEB Journal 19, A1496–A1497.Google Scholar
Powell, S. J. and Bale, J. S. (2004). Cold shock injury and ecological costs of rapid cold hardening in the grain aphid Sitobion avenae (Hemiptera: Aphididae). Journal of Insect Physiology 50, 277–284.CrossRefGoogle Scholar
Powell, S. J. and Bale, J. S. (2005). Low temperature acclimated populations of the grain aphid Sitobion avenae retain ability to rapidly cold harden with enhanced fitness. Journal of Experimental Biology 208, 2615–2620.CrossRefGoogle ScholarPubMed
Powell, S. J. and Bale, J. S. (2006). Effect of long-term and rapid cold-hardening on the cold torpor temperature of an aphid. Physiological Entomology 31, 348–352.CrossRefGoogle Scholar
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
Rako, L. and Hoffman, A. A. (2006). Complexity of the cold acclimation response in Drosophila melanogaster. Journal of Insect Physiology 52, 94–104.CrossRefGoogle ScholarPubMed
Rinehart, J. P., Yocum, G. D., and Denlinger, D. L. (2000). Thermotolerance and rapid cold hardening ameliorate the negative effects of brief exposures to high or low temperatures on fecundity in the flesh fly, Sarcophaga crassipalpis. Physiological Entomology 25, 330–336.CrossRefGoogle Scholar
Rosales, A. L., Krafsur, E. S., and Kim, Y. (1994). Cryobiology of the face fly and house fly (Diptera: Muscidae). Journal of Medical Entomology 31, 671–680.CrossRefGoogle Scholar
Shintani, Y. and Ishikawa, Y. (2007). Relationship between rapid cold-hardening and cold acclimation in the eggs of the yellow-spotted longicorn beetle, Psacothea hilaris. Journal of Insect Physiology 53, 1055–1062.CrossRefGoogle ScholarPubMed
Shreve, S. M., Kelty, J. D., and Lee, R. E. (2004). Preservation of reproductive behaviors during modest cooling: rapid cold-hardening fine-tunes organismal response. Journal of Experimental Biology 207, 1797–1802.CrossRefGoogle ScholarPubMed
Shreve, S. M., Yi, S.-X., and Lee, R. E. (2007) Increased dietary cholesterol enhances cold tolerance in Drosophila melanogaster. CryoLetters 28, 33–37.Google ScholarPubMed
Sinclair, B. J. and Chown, S. L. (2006). Rapid cold-hardening in a Karoo beetle, Afrinus sp. Physiological Entomology 31, 98–101.CrossRefGoogle Scholar
Sinclair, B. J., Klok, C. J., Scott, M. B., Terblanche, J. S., and Chown, S. L. (2003). Diurnal variation in supercooling points of three species of Collembola from Cape Hallett, Antarctica. Journal of Insect Physiology 49, 1049–1061.CrossRefGoogle ScholarPubMed
Smallwood, M. and Bowles, D. J. (2002). Plants in a cold climate. Philosophical Transactions of the Royal Society of London Series B-Biological Sciences 357, 831–846.CrossRefGoogle Scholar
Teets, N. M., Elnitsky, M. A., Benoit, J. B., Lopez-Martinez, G., Denlinger, D. L., and Lee, R. E. (2008). Rapid cold-hardening in larvae of the Antarctic midge, Belgica antarctica: Cellular cold-sensing and a role for calcium. American Journal of Physiology 294, R1938–R1946.Google Scholar
Terblanche, J. S., Clusella-Trullas, S., Deere, J. A., and Chown, S. L. (2008). Thermal tolerance in a south-east African population of the tsetse fly Glossina pallidipes (Diptera, Glossinidae): implications for forecasting climate change impacts. Journal of Insect Physiology 54, 114–127.CrossRefGoogle Scholar
Terblanche, J. S., Marais, E., and Chown, S. L. (2007). Stage-related variation in rapid cold hardening as a test of the environmental predictability hypothesis. Journal of Insect Physiology 53, 455–462.CrossRefGoogle ScholarPubMed
ThompsonJr., G. A. Jr., G. A. (1983). Mechanisms of homeoviscous adaptation in membranes. In Cellular Acclimatisation to Environmental Change, ed. Cossins, A. R. and Sheterline, P.. Cambridge: Cambridge University Press, pp. 33–54.Google Scholar
Wang, X. and Kang, L. (2003). Rapid cold hardening in young hoppers of the migratory locust Locusta migratoria L. (Orthoptera: Acridiidae). CryoLetters 24, 331–340.Google Scholar
Watanabe, M., Kikawada, T., Minagawa, N., Yukuhiro, F., and Okuda, T. (2002). Mechanism allowing an insect to survive complete dehydration and extreme temperatures. Journal of Experimental Biology 205, 2799–2802.Google ScholarPubMed
Worland, M. R. and Convey, P. (2001). Rapid cold hardening in Antarctic microarthropods. Functional Ecology 15, 515–524.CrossRefGoogle Scholar
Worland, M. R., Convey, P., and Lukešovà, A. (2000). Rapid cold hardening: a gut feeling. CryoLetters 21, 315–324.Google ScholarPubMed
Worland, M. R., Hawes, T. C., and Bale, J. S. (2007). Temporal resolution of cold acclimation and de-acclimation in the Antarctic collembolan, Cryptopygus antarcticus. Physiological Entomology 32, 233–239.CrossRefGoogle Scholar
Yi, S.-X. and Lee, R. E. (2004). In vivo and in vitro rapid cold hardening protects cells from cold-shock injury in the flesh fly. Journal of Comparative Physiology B 174, 611–615.CrossRefGoogle ScholarPubMed
Yi, S.-X., Yin, C. M., and Nordin, J. H. (1987). The in vitro biosynthesis and secretion of glycerol by larval fat bodies of chilled Ostrinia nubilalis. Journal of Insect Physiology 33, 523–528.CrossRefGoogle Scholar
Yi, S.-X., Moore, C. W., and Lee, R. E. (2007). Rapid cold-hardening protects Drosophila melanogaster from cold-induced apoptosis. Apoptosis 12, 1183–1193.CrossRefGoogle ScholarPubMed
Yocum, G. D. and Denlinger, D. L. 1994. Anoxia blocks thermotolerance and the induction of rapid cold hardening in the flesh fly, Sarcophaga crassipalpis. Physiological Entomology 19, 152–158.CrossRefGoogle Scholar
Yoder, J., Benoit, J. B., Denlinger, D. L., and Rivers, D. B. (2006). Stress-induced accumulation of glycerol in the flesh fly, Sarcophaga bullata: Evidence indicating anti-desiccant and cryoprotectant functions of this polyol and a role for the brain in coordinating the response. Journal of Insect Physiology 52, 202–214.CrossRefGoogle Scholar

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