Abstract
Insects vary considerably in their ability to survive low temperatures. The tractability of these organisms to experimentation has lead to considerable physiology-based work investigating both the variability between species and the actual mechanisms themselves. This has highlighted a range of strategies including freeze tolerance, freeze avoidance, protective dehydration and rapid cold hardening, which are often associated with the production of specific chemicals such as antifreezes and polyol cryoprotectants. But we are still far from identifying the critical elements behind over-wintering success and how some species can regularly survive temperatures below −20°C. Molecular biology is the most recent tool to be added to the insect physiologist’s armoury. With the public availability of the genome sequence of model insects such as Drosophila and the production of custom-made molecular resources, such as EST libraries and microarrays, we are now in a position to start dissecting the molecular mechanisms behind some of these well-characterised physiological responses. This review aims to provide a state-of-the-art snapshot of the molecular work currently being conducted into insect cold tolerance and the very interesting preliminary results from such studies, which provide great promise for the future.
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References
Adams MD, Celniker SE, Holt RA, Evans CA, Gocayne JD, Amanatides PG, Scherer SE, Li PW, Hoskins RA, Galle RF et al (2000) The genome sequence of Drosophila melanogaster. Science 287:2185–2195
Agre P, Preston GM, Smith BL, Jung JS, Raina S, Moon c, Guggino WB, Nielson S (1993) Aquaporin chip—the archetypal molecular water channel. Am J Sci 265:F463–F476
Andorfer CA, Duman JG (2000) Isolation and characterization of cDNA clones encoding antifreeze proteins of the pyrochroid beetle Dendroides canadensis. J Insect Physiol 46:365–372
Arber S, Halder G, Caroni P (1994) Muscle LIM protein, a novel regulator of myogenesis, promotes myogenic differentiation. Cell 79:221–231
Bale JS (1993) Classes of insect cold hardiness. Funct Ecol 7:751–753
Bale JS (2002) Insects and low temperatures: from molecular biology to distributions and abundance. Philos Trans R Soc B 357:849–861
Bayley M, Peterson SO, Knigge T, Kohler HR, Holmstrup M (2001) Drought acclimation confers cold tolerance in the soil collembolan Folsomia candida. J Insect Physiol 47:1197–1204
Bennett VA, Pruitt NL, Lee RE (1997) Seasonal changes in fatty acid composition associated with cold-hardening in third instar larvae of Eurosta solidaginis. J Comp Physiol B 167:249–255
Bennett VA, Lee RE, Nauman JS, Kukal O (2003) Selection of overwintering microhabitats used by the Arctic woolybear caterpillar, Gynaephora groenlandica. Cryoletters 24:191–200
Bilgen T, English TE, McMullen DC, Storey KB (2001) EsMlp, a muscle-LIM protein gene, is up-regulated during cold exposure in the freeze-avoiding larvae of Epiblema scudderiana. Cryobiology 3:11–20
Cannon RJC, Block W (1988) Cold tolerance of microarthropods. Biol Rev 63:23–77
Chen CP, Denlinger DL (1992) Reduction of cold injury in flies using an intermittent pulse of high-temperature. Cryobiology 29:138–143
Chen CP, Denlinger DL, Lee RE (1987) Cold-shock injury and rapid cold hardening in the flesh fly, Sarcophaga crassipalpis. Physiol Zool 60:297–304
Chen LB, DeVries AL, Cheng CHC (1997) Convergent evolution of antifreeze glycoproteins in Antarctic notothenioid fish and Arctic cod. Proc Natl Acad Sci USA 94:3817–3822
Chen B, Kayukawa T, Monteiro A, Ishikawa Y (2005) The expression of the HSP90 gene in response to winter and summer diapauses and thermal-stress in the onion maggot, Delia antiqua. Insect Mol Biol 14:697–702
Chino CP (1957) Conversion of glycogen to sorbitol and glycerol in the diapause egg of the Bombyx silkworm. Nature 180:606–607
Chown SL, Terblanche JS (2007) Physiological diversity in insects: ecological and evolutionary contexts. Adv Insect Physiol 33:50–152
Clark MS, Fraser KPPF, Peck LS (2008) Antarctic marine molluscs do have an HSP70 heat shock response. Cell Stress Chaperone 13. doi: 10.1007/s12192-008-0014-8
Clark MS, Thorne MAS, Purać J, Grubor-Lajšić G, Kube M, Reinhardt R, Worland MR (2007) Surviving extreme polar winters by desiccation: clues from Arctic springtail (Onychiurus arcticus) EST libraries. BMC Genomics doi:10.1186/1471-2164-8-475
Cohet Y, Vouidibio J, David JR (1980) Thermal tolerance and geographical-distribution: a comparison of cosmopolitan and tropical endemic Drosophila species. J Therm Biol 5:69–74
Colinet H, Nguyen TTA, Cloutier C, Michaud D, Hance T (2007) Proteomic profiling of a parasitic wasp exposed to constant and fluctuating cold exposure. Insect Biochem Mol 37:1177–1188
Convey P (1996) The influence of environmental characteristics on life history attributes of Antarctic terrestrial biota. Biol Rev 71:191–225
Convey P (2000) How does cold constrain life cycles of terrestrial plants and animals? Cryoletters 21:73–82
Cossins AR (ed) (1994) Temperature adaptations of biological membranes. Portland Press, London
Crowe JH, Hoekstra FA, Crowe LM (1992) Anhydrobiosis. Annu Rev Physiol 54:579–599
Czajka MC, Lee RE (1990) A rapid cold-hardening response protecting against cold shock injury in Drosophila melanogaster. J Exp Biol 148:245–254
Dallerac R, Labeur C, Jallon JM, Knippie DC, Roelofs WL, Wicker-Thomas C (2000) A Delta 9 desaturase gene with a different substrate specificity is responsible for the cuticular diene hydrocarbon polymorphism in Drosophila melanogaster. Proc Natl Acad Sci USA 97:9449–9454
Danks HV (2005) Key themes in the study of seasonal adaptations in insects I. Patterns of cold hardiness. Appl Entomol Zool 40:199–211
Denlinger DL (2002) Regulation of diapause. Annu Rev Entomol 47:93–122
DeVries AL (1971) Glycoproteins as biological antifreeze agents in Antarctic fishes. Science 172:1152
Diabo S, Kimura MT, Goto SG (2001) Upregulation of genes belonging to the drosomycin family in diapausing adults of Drosophila triauraria. Gene 278:177–184
Doucet D, Tyshenko MG, Davies PL, Walker VK (2002) A family of expressed antifreeze protein genes from the moth, Choristoneura fumiferana. Eur J Biochem 269:38–46
Drobnis EZ, Crowe LM, Berger T, Anchordoguy TJ, Overstreet JW, Crowe JH (1993) Cold shock damage is due to lipid phase-transition in cell membranes—a demonstration using sperm as a model. J Exp Zool 265:432–437
Duman JG (1977) Role of macromolecular antifreeze in the darkling beetle Meracantha contracta. J Comp Physiol 115:279–286
Duman JG (2001) Antifreeze and ice nucleator proteins in terrestrial arthropods. Annu Rev Physiol 63:327–357
Duman JG, Bennett T, Sformo T, Hochstrasser R, Barnes BM (2004) Antifreeze proteins in Alaskan insects and spiders. J Insect Physiol 50:259–266
Duman JG, DeVries AL (1974) Effects of temperature and photoperiod on antifreeze production in cold water fishes. J Exp Biol 190:89–97
Duman JG, Li N, Verleye D, Goetz FW, Wu DW, Andorfer CA, Benjamin T, Parmelee DC (1998) Molecular characterization and sequencing of antifreeze proteins from larvae of the beetle Dendroides canadensis. J Comp Physiol B 168:225–232
Eigenheer AL, Young S, Blomquist GJ, Borgeson CE, Tillman JA, Tittiger C (2002) Isolation and molecular characterization of Musca domestica delta-9 desaturase sequences. Insect Mol Biol 11:533–542
Ellers J, Marien J, Driessen G, Van Straalen N (2008) Temperature induced gene expression associated with different thermal reaction norms and growth rate. J Exp Zool (Mol Dev Evol) 310B:137–147
Feder ME, Hofmann GE (1999) Heat-shock proteins, molecular chaperones, and stress response: evolutionary and ecological physiology. Annu Rev Physiol 61:243–282
Fink AL (1999) Chaperone-mediated protein folding. Physiol Rev 79:425–449
Forge TA, MacGuidwin AE (1992) Effects of water potential and temperature on survival of the nematode Meloidogyne hapla in frozen soil. Can J Zool 70:1553–1560
Frenot Y, Chown SL, Whinam J, Selkirk PM, Convey P, Skotnicki M, Bergstrom DM (2005) Biological invasions in the Antarctic: extent, impacts and implications. Biol Rev 80:45–72
Fujiwara Y, Denlinger DL (2007) p38 MAPK is a likely component of the signal transduction pathway triggering rapid cold hardening in the flesh fly Sarcophaga crassipalpis. J Exp Biol 210:3295–3300
Fujiwara Y, Shindome C, Takeda M, Shiomi K (2006) The roles of ERK and p38 MAPK signalling cascades on embryonic diapause initiation and termination of the silkworm, Bombyx mori. Insect Biochem Mol Biol 36:47–53
Gaston KJ, Chown SL, Evans KL (2008) Ecogeographical rules: elements of a synthesis. J Biogeogr 35:483–500
Godlewski J, Kudkiewicz B, Grzelak K, Cymborowski B (2001) Expression of larval hemolymph proteins (lhp) genes and protein synthesis in the fat body of the greater wax moth (Galleria mellonella) larvae during diapause. J Insect Physiol 47:759–766
Goto SG (2000) Expression of Drosophila homologue of senescence marker protein-30 during cold acclimation. J Insect Physiol 46:1111–1120
Goto SG (2001) A novel gene that is upregulated during recovery from cold shock in Drosophila melanogaster. Gene 270:259–264
Goto SG, Kimura MT (1998) Heat and cold-shock responses and temperature adaptations in subtropical and temperate species of Drosophila. J Insect Physiol 44:1233–1239
Goto SG, Kimura MT (2004) Heat shock responsive gene are not involved in the adult diapause of Drosophila triauraria. Gene 326:117–122
Goto SG, Yoshida KM, Kimura MT (1998) Accumulation of Hsp70 mRNA under environmental stress in diapausing and nondiapausing adults of Drosophila triauraria. J Insect Physiol 44:1009–1015
Graham LA, Davies PL (2005) Glycine-rich antifreeze proteins from snow fleas. Science 310:461
Graham LA, Bendena WG, Walker VK (1996) Juvenile hormone regulation and developmental expression of a Tenebrio desiccation stress protein gene. Dev Genet 18:296–305
Graham LA, Liou YC, Walker VK, Davies PL (1997) Hyperactive antifreeze protein from beetles. Nature 388:727–728
Grewal PS, Bornstein-Forest S, Burnell AM, Glazer I, Jagdale GB (2006) Physiological, genetic, and molecular mechanisms of chemoreception, thermobiosis, and anhydrobiosis in entomopathogenic nematodes. Biol Control 38:54–65
Hayakawa Y (1985) Activation of insect fat-body phosphorylase by cold-phosphorylase-kinase, phosphatase and ATP level. Insect Biochem 15:123–128
Hayward SAL, Rinehart JP, Denlinger DL (2004) Desiccation and rehydration elicit distinct heat shock protein transcript response in flesh fly. J Exp Biol 207:963–971
Hayward SAL, Pavlides SC, Tammariello SP, Rinehart JP, Denlinger DL (2005) Temporal expression patterns of diapause-associated genes in flesh fly pupae from the onset of diapause through post-diapause quiescence. J Insect Physiol 51:631–640
Hayward SAL, Rinehart JP, Sandro LH, Lee RE, Denlinger DL (2007) Slow dehydration promotes desiccation and freeze tolerance in the Antarctic midge Belgica antarctica. J Exp Biol 210:836–844
Hartl FU (1996) Molecular chaperones in cellular protein folding. Nature 381:571–580
Hengherr S, Heyer AG, Kohler HR, Schill RO (2007) Trehalose and anhydrobiosis in tardigrades—evidence for divergence in response to dehydration. FEBS J doi: 10.1111/j.1742-4658.2007.06198.x
Hoffmann AA (1990) Acclimation for desiccation resistance in Drosophila melanogaster and the association between acclimation response and genetic-variation. J Insect Physiol 36:885–891
Hofmann GE (2005) Patterns of Hsp gene expression in exothermic marine organisms on small to large biogeographic scales. Integr Comp Biol 45:247–255
Hoffmann AA, Parsons PA (1993) Selection for adult desiccation resistance in Drosophila melanogaster—fitness components, larval resistance and stress tolerance. Biol J Linn Soc 48:43–54
Hoffmann AA, Sørensen JG, Loeschoke V (2003) Adaptation of Drosophila to temperature extremes: bringing together quantitative and molecular approaches. J Therm Biol 28:175–213
Holmstrup M, Hedlund K, Boriss H (2002) Drought acclimation and lipid composition in Folsomia candida: implications for cold shock, heat shock and acute desiccation stress. J Insect Physiol 48:961–970
Holt RA, Subramanian GM, Halpern A, Sutton GG, Charlab R, Nusskern DR, Wincker P, Clark AG, Ribeiro JMC, Wides R et al (2002) The genome sequence of the malaria mosquito Anopheles gambiae. Science 298:129. doi:10.1126/science.1076181
Hosier JS, Burns JE, Esch HE (2000) Flight muscle resting potential and species-specific differences in chill coma. J Insect Physiol 46:621–627
Huang LH, Kang L (2007) Cloning and interspecific altered expression of heat shock protein genes in two leafminer species in response to thermal stress. Insect Mol Biol 16:491–500
Huang T, Nicodemus J, Zarka DG, Thomashow MF, Wisniewski M, Duman JG (2002) Expression of an insect (Dendroides canadensis) antifreeze protein in Arabidopsis thaliana results in a decrease in plant freezing temperature. Plant Mol Biol 50:333–344
Joanisse DR, Storey KB (1994a) Enzyme-activity profiles in and overwintering population of freeze-avoiding gall moth larvae, Epiblema scudderiana. Can J Zool 72:1079–1086
Joanisse DR, Storey KB (1994b) Enzyme-activity profiles in and overwintering population of freeze-tolerant larvae of the gall fly, Eurosta solidaginis. J Comp Physiol B 164:247–255
Joplin KH, Denlinger DL (1990) Development and tissue specific control of the heat-shock induced 70 kDa related proteins in the flesh fly Sarcophaga crassipalpis. J Insect Physiol 36:239–249
Kayukawa T, Chen B, Miyazaki S, Itoyama K, Shinoda T, Ishikawa Y (2005) Expression of the 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 Chaperone 10:204–210
Kayukawa T, Chen B, Hoshizaki S, Ishikawa Y (2007a) Upregulation of a desaturase is associated with enhancement of cold hardiness in the onion maggot Delia antiqua. Insect Biochem Mol Biol 37:1160–1167
Kayukawa T, Chen B, Hoshizaki S, Ishikawa Y (2007b) Upregulation of a desaturase is associated with the enhancement of cold hardiness in the onion maggot, Delia antiqua. Insect Biochem Mol Biol 37:1160–1167
Kelty JD, Lee RE (1999) Induction of rapid cold hardening by cooling at ecologically relevant rates in Drosophila melanogaster. J Insect Physiol 45:719–726
Kelty JD, Lee RE (2001) Rapid cold-hardening of Drosophila melanogaster (Diptera: Drosophilidae) during ecologically based thermoperiodic cycles. J Exp Biol 204:1659–1666
Kidokoro K, Iwata K-I, Takeda M, Fujiwara Y (2006) Involvement of ERK/MAPK in regulation of diapuase intensity in the false melon beetle, Atrachya menetriesi. J Insect Physiol 52:1189–1193
Kikawada T, Nakahara Y, Kanamori Y, Iwata K-I, Watanabe M, McGee B, Tunnacliffe A, Okuda T (2006) Dehydration-induced expression of LEA proteins in an anhydrobiotic chironomid. Biochem Bioph Res Co 348:56–61
Kim M, Robich RM, Rinehart JP, Denlinger DL (2006) Upregulation of two actin genes and redistribution of actin during dipause and cold stress in the northern house mosquito, Culex pipiens. J Insect Physiol 52:1226–1233
Knight CA, Duman JG (1986) Inhibition of recrystallization by insect thermal hysteresis proteins—a possible cryoprotective role. Cryobiol 23:256–262
Koštál V, Berková P, Šimek P (2003) Remodelling of membrane phospholipids during transition to diapause and cold-acclimation in the larvae of Chymomyza costata (Drosophila). Comp Biochem Physiol B 135:407–419
Koštál V, Vambera J, 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. J Exp Biol 207:1509–1521
Koštál V, Renault D, Mehrabianová A, Bastl J (2007) Insect cold tolerance and repair of chill-injury at fluctuating thermal regimes: role of homeostasis. Comp Biochem Physiol A 147:231–238
Kruse E, Uehlein N, Kaldenhoff R (2006) The aquaporins. Genome Biol 7:206. doi:10.1186/gb-2006-7-2-206
Kukal O (1991) Behavioral and physiological adaptations to cold in a freeze-tolerant arctic insect. In: Lee RE, Denlinger DL (eds) Insects at low temperature. Chapman and Hall, London, pp 276–300
Kukal O, Duman JG, Serianni AS (1989) Cold-induced mitochondrial degradation and cryoprotectants synthesis in freeze-tolerant Arctic caterpillars. J Comp Physiol B 158:661–671
Lalouette L, Kostal V, Colinet H, Gagneul D, Renault D (2007) Cold exposure and associated metabolic changes in adult tropical beetles exposed to fluctuating thermal regimes. FEBS J 274:1759–1767
Lee RE, Denlinger DL (1991) Insects at low temperature. Chapman and Hall, London
Lee RE, Chen CP, Meacham MH, Denlinger DL (1987) Ontogenic patterns of cold-hardiness and glycerol production in Sarcophaga crassipalpis. J Insect Physiol 33:587–592
Lee RE, Strong-Gunderson JM, Lee MR, Grove KS, Riga TJ (1991) Isolation of ice nucleating active bacteria from insects. J Exp Zool 257:124–127
Levin DB, Danks HV, Barber SA (2003) Variation in mitochondrial DNA and gene transcription in freezing-tolerant larvae of Eurosta solidaginis (Diptera: Tephritidae) and Gynaephora groenlandica (Lepidoptera: Lymantriidae). Insect Mol Biol 12:281–289
Lewis DK, Spurgeon D, Sappington TW, Keeley LL (2002) A hexamerin protein AgSP-1 is associated with diapause in the boll weevil. J Insect Physiol 48:887–901
Li AQ, Popova-Butler A, Dean DH, Denlinger DL (2007) Proteomics of the flesh fly brain reveals an abundance of upregulated heat shock proteins during pupal diapause. J Insect Physiol 53:385–391
Liu W, Ma PWK, Marsella-Herrick P, Rosenfield CL, Knipple DC, Roelofs T (1999) Cloning and functional expression of a cDNA encoding a metabolic acyl-CoA Delta 9-desaturase of the cabbage looper moth, Trichoplusia ni. Insect Biochem Mol Biol 29:435–443
Michaud MR, Denlinger DL (2004) Molecular modalities of insect cold survival: current understanding and future trends. Int Congress Ser 1275:32–46
Michaud MR, Denlinger DL (2006) Oleic acid is elevated in cell membranes during rapid cold-hardening and pupal diapause in the flesh fly, Sarcophaga crassipalpis. J Insect Physiol 52:1073–1082
Michaud MR, Denlinger DL (2007) Shifts in the carbohydrate, polyol and amino acid pools during rapid cold-hardening and diapause-associated cold-hardening in flesh flies (Sarcophaga crassipalpis): a metabolomic comparison. J Comp Physiol B 177:753–763
Morimoto RI (1998) Regulation of the heat shock transcriptional response: cross talk between a family of heat shock factors, molecular chaperones, and negative regulators. Gene Dev 12:3788–3796
P Morin Jr, McMullen DC, Storey KB (2005) HIF-1α involvement in low temperature and anoxia survival by a freeze tolerant insect. Mol Cell Biochem 280:99–106
Nene V, Wortman JR, Lawson D, Haas B, Kodira C, Tu Z, Loftus B, Xi Z, Megy K, Grabherr M (2007) Genome sequence of Aedes aegypti, a major arbovirus vector. Science 316:1718. doi:10.1126/science.1138878
Nenev LG, Duman JG, Low MG, Sehl LC, Castellino FJ (1989) Purification and characterization of an insect hemolymph lipoprotein ice nucleator: evidence for the importance of phosphatidylinositol and apolipoprotein in the ice nucleator activity. Cryobiology 27:416–422
Nicodemus J, O’Tousa JE, Duman JG (2006) Expression of a beetle, Dendroides canadensis, antifreeze protein in Drosophila melanogaster. J Insect Physiol 52:888–896
Nielsen MM, Overgaard J, Sørensen JG, Holmstrup M, Justesen J, Loeschcke V (2005) Role of HSF activation for resistance to heat, cold and high-temperature knock-down. J Insect Physiol 51:1320–1329
Nordin JH, Cui Z, Yin C-M (1984) Cold-induced glycerol accumulation by Ostrinia nubilalis larvae is developmentally regulated. J Insect Physiol 30:563–566
Norry FM, Gomez FH, Loeschcke V (2007) Knockdown resistance to heat stress and slow recovery from chill coma are genetically associated in a quantitative trait locus region of chromosome 2 in Drosophila melanogaster. Mol Ecol 16:3274–3284
Nunamaker RA, Dean VC, Murphy KE, Lockwood JA (1996) Stress proteins elicited by cold shock in the midge Culicoides variipennis sonorensis Wirth and Jones. Comp Biochem Physiol B 113:73–77
Ohtsu T, Kimura MT, Katagiri C (1998) How Drosophila species acquire cold tolerance—qualitative changes of phospholipids. Eur J Biochem 252:608–611
Overgaard J, Malmendal A, Sorensen JG, Bundy JG, Loeschcke V, Nielson NC, Holmstrop M (2007) Metabolomic profiling of rapid cold hardening and cold shock in Drosophila melanogaster. J Insect Physiol 12:1218–1232
Parsell DA, Lindquist S (1993) The function of heat-shock proteins in stress tolerance, degradation and reactivation of damaged proteins. Ann Rev Genet 27:437–496
Pfister TD, Storey KB (2002) Protein kinase A: purification and characterization of the enzyme from two cold-hardy goldenrod gall insects. Insect Biochem Mol Biol 32:505–515
Pfister TD, Storey KB (2006) Insect freeze tolerance: roles of protein phosphatases and protein kinase A. Insect Biochem Mol Biol 36:18–24
Pietrantonio PV, Gibson GE, Strey AA, Petzel D, Hayes TK (2000) Characterization of a leucokinin binding protein in Aedes aegypti (Diptera : Culicidae) Malpighian tubule. Insect Biochem Mol Biol 30:1147–1159
Place SP, Zippay ML, Hofmann GE (2004) Constitutive roles for inducible genes: evidence for the alteration in expression of the inducible hsp70 gene in Antarctic notothenioid fish. Am J Physiol Reg I 287:R429–R436
Privalov PL (1990) Cold denaturation of proteins. Crit Rev Biochem Mol Biol 25:281–305
Qin W, Neal SJ, Robertson RM, Westwood JT, Walker VK (2005) Cold hardening and transcriptional change in Drosophila melanogaster. Insect Mol Biol 14:607–613
Qin W, Doucet D, Tyshenko MG, Walker VK (2007) Transcription of antifreeze protein genes in Choristoneura fumiferana. Insect Mol Biol 16:423–434
Rako L, Blacket MJ, McKechnie SW, Stephen W, Hoffmann AA, Ary A (2007) Candidate genes and thermal phenotypes: identifying ecologically important genetic variation for thermotolerance in the Australian Drosophila melanogaster cline. Mol Biol 16:2948–2957
Raymond JA, DeVries AL (1977) Adsorption inhibition as a mechanism of freezing resistance in polar fishes. Proc Natl Acad Sci USA 74:2589–2593
Rinehart JP, Denlinger DL (2000) Heat-shock protein 90 is down regulated during pupal diapause in the flesh fly, Sarcophagus crassipalpis, but remains responsive to thermal stress. Insect Mol Biol 9:641–645
Rinehart JP, Yocum GD, Denlinger DL (2000) Developmental upregulation of inducible hsp70 transcripts, but not the cognate form, during pupal diapause in the flesh fly, Sarcophagus crassipalpis. Insect Biochem Mol Biol 30:515–521
Rinehart JP, Hayward SAL, Elnitsky MA, Sandro LH, Lee RE (2006a) Continuous up-regulation of heat shock proteins in larvae, but not adults, in a polar insect. Proc Natl Acad Sci USA 103:14225–14227
Rinehart JP, Robich RM, Denlinger DL (2006b) Enhanced cold and desiccation tolerance in diapausing adults of Culex pipiens and a role for HSP70 in response to cold shock but not as a component of the diapause program. J Med Entomol 43:713–722
Rinehart JP, Li A, Yocum GD, Robich RM, Hayward SAL, Denlinger DL (2007) Up-regulation of heat shock proteins is essential for cold survival during insect dipause. Proc Natl Acad Sci USA 104:11130–11137
Ring RA, Riegert PW (1991) A tribute to R.W. Salt. In: Lee RE, Denlinger DL (eds) Insects at low temperature. Chapman and Hall, London, pp 3–16
Ring RA, Danks HV (1994) Desiccation and cryoprotection—overlapping adaptations. Cryoletters 15:181–190
Russell NJ (1997) Psychrophilic bacteria—molecular adaptations of membrane lipids. Comp Biochem Physiol A 118:489–493
Sakamoto T, Bryant DA (1997) Temperature-regulated mRNA accumulation and stabilization for fatty acid desaturase genes in the cyanobacterium Synechococcus sp. strain PCC 7002. Mol Microbiol 23:1281–1292
Salt RW (1957) Natural occurrence of glycerol in insects and its relation to their ability to survive freezing. Can Entomol 89:491–494
Salt RW (1959) Role of glycerol in the cold-hardening of Bracon cephi (Gahan). Can J Zool 37:59–69
Salt RW (1961) Principles of insect cold hardiness. Annu Rev Entomol 6:55–74
Salt RW (1966) Factors influencing nucleation in supercooled insects. Can J Zool 44:117–133
Salvucci ME, Strecher DS, Henneberry TJ (2000) Heat shock proteins in whiteflies, an insect that accumulates sorbitol in response to heat stress. J Thermal Biol 25:363–371
Scotter AJ, Marshall CB, Graham LA, Gilbert JA, Garnham CP, Davies PL (2006) The basis for hyperactivity of antifreeze proteins. Cryobiology 53:229–239
Sinclair BJ, Stevens MI (2006) Terrestrial microarthropods of Victoria Land and Queen Maud Mountains, Antarctica: implications of climate change. Soil Biol Biochem 38:3158–3170
Sinclair BJ, Gibbs AG, Roberts SP (2007) Gene transcription during exposure to, and recovery from, cold and desiccation stress in Drosophila melanogaster. Insect Mol Biol 16:435–443
Slachta M, Berkova P, Vambera J, Koštál V (2002) Physiology of cold-acclimation in non-diapausing adults of Pyrrhocoris apterus (Heteroptera). Eur J Entomol 99:181–187
Sømme L (1982) Supercooling and winter survival in terrestrial arthropods. Comp Biochem Physiol A 73:519–543
Sømme L (1999) The physiology of cold hardiness in terrestrial arthropods. Eur J Entomol 96:1–10
Sømme L, Block W (1982) Cold hardiness of Collembola at Signy Island, maritime Antarctic. Oikos 38:68–176
Sonoda S, Fukumoto K, Izumi Y, Ashfaq M, Yoshida H, Tsumuki H (2006a) Methionine-rich storage protein gene in the rice stem borer, Chilo suppressalis, is expressed during diapause in response to cold acclimation. Insect Mol Biol 15:853–859
Sonoda S, Fukumoto K, Izumi Y, Yoshida H, Tsumuki H (2006b) Cloning of heat shock protein genes (hsp90 and hsc70) and their expression during larval diapause and cold tolerance acquisition in the rice stem borer, Chilo suppressalis Walker. Arch Insect Biochem Physiol 63:36–47
Storey JM, Storey KB (1981) Biochemical strategies of overwintering in the gall fly larva, Eurosta solidaginis—effect of low-temperature acclimation on the activities of enzymes of intermediary metabolism. J Comp Physiol 144:191–199
Storey JM, Storey KB (1986) Winter survival of the gall fly larvae, Eurosta solidaginis: profiles of fuel reserves and cryoprotectants in a natural population. J Insect Physiol 32:549–556
Storey KB (1997) Organic solutes if freeze tolerance. Comp Biochem Physiol A 117:319–326
Storey KB, Storey JM (1991) Glucose-6-phosphate-dehydrogenase in cold hardy insects—kinetic-properties, freezing stabilization, and control of hexose-monophosphate shunt activity. Insect Biochem 21:157–164
Storey KB, Storey JM (1996) Natural freezing survival in animals. Ann Rev Ecol Syst 27:365–386
Stronach BE, Siegrist SE, Beckerle MC (1996) Two muscle-specific LIM proteins in Drosophila. J Cell Biol 134:1179–1195
Tachibana SI, Numata H, Goto SG (2005) Gene expression of the heat shock proteins (Hsp23, Hsp70 and Hsp90) during and after larval diapause in the blow fly Lucilia sericata. J Insect Physiol 51:641–647
Tammariello SP, Rinehart JP, Denlinger DL (1999) Desiccation elicits heat shock protein transcription in the flesh fly Sarcophaga crassipalpis, but does not enhance tolerance to high or low temperatures. J Insect Physiol 45:933–938
The C. elegans Sequencing Consortium (1998) The genome sequence of the nematode C. elegans: a platform for investigating biology. Science 282:2012–2018
Thibaud JM (1968) Cycle de tube digestif lors de l’intermue chez les Hypogastruridae (Collemboles) épigés et cavernicoles. Rev Ecol Biol Sol 4:647–655
Tiku PE, Gracey AY, Macartney AI, Beynon RJ, Cossins AR (1996) Cold-induced expression of Delta(9)-desaturase in carp by transcriptional and posttranslational mechanisms. Science 271:815–818
Timmermans MJTN, Ellers J, Van Straalen NM (2007) Allelic diversity of metallothionein in Orchesella cincta (L): traces of natural selection by environmental pollution. Heredity 98:311–319
Tomanek L, Somero GN (1999) Evolutionary and acclimation-induced variation in the heat-shock responses of congeneric marine snails (genus Tegula) from different thermal habitats: implications for limits of thermotolerance and biogeography. J Exp Biol 202:2925–2936
Tomcala A, Tollarova M, Overgaard J, Simek P, 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. J Exp Biol 209:4102–4114
Tursman D, Duman JG, Knight CA (1994) Freeze tolerance adaptations in the centipede, Lithobius forficatus. J Exp Zool 268:347–353
Tyshenko MG, Doucet D, Walker VK (2005) Analysis of antifreeze proteins within spruce budworm sister species. Insect Mol Biol 14:319–326
Tyshenko MG, Walker VK (2004) Hyperactive spruce budworm antifreeze expression in transgenic Drosophila does not confer cold shock tolerance. Cryobiology 49:28–36
Vega SE, del Rio AH, Bamberg JB, Palta JP (2004) Evidence for the up-regulation of stearoyl-ACP (A9) desaturase gene expression during cold acclimation. Am J Potato Res 81:125–135
Whyard S, Wyatt GR, Walker VK (1986) The heat shock response in Locusta migratoria. J Comp Physiol B 156:813–817
Worland MR (2005) Factors that influence freezing in the sub-Antarctic springtail Tullbergia antarctica. J Insect Physiol 51:881–894
Worland MR, Lukešovà A (2000) The effect of feeding on specific soil algae on the cold hardiness of two Antarctic micro-arthropods (Alaskozetes antarcticus and Cryptopygus antarcticus). Polar Biol 23:766–774
Worland MR, Convey P (2001) Rapid cold hardening in Antarctic microarthropods. Funct Ecol 15:515–524
Worland MR, Grubor-Lajsic G, Montiel PO (1998) Partial desiccation induced by sub-zero temperatures as a component of the survival strategy of the Arctic collembolan Onychiurus arcticus (Tullberg). J Insect Physiol 44:211–219
Worland MR, Leinaas HP, Chown SL (2006) Supercooling point frequency distributions in Collembola are affected by moulting. Funct Ecol 20:323–329
Wu DW, Duman JG (1991) Activation of antifreeze proteins from larvae of the beetle Dendroides canadensis. J Com Physiol B 161:279–283
Wyatt GR (1963) The biochemistry of insect hemolymph. Annu Rev Entomol 6:75–102
Xu WH, Denlinger DL (2003) Molecular characterization of prothoracicotropic hormone and diapause hormone in Heliothis virescens during diapause, and a new role for diapause hormone. Insect Mol Biol 12:509–516
Yamashita O (1996) Diapause hormone of the silk moth Bombyx mori, structure, gene expression and function. J Insect Physiol 42:669–679
Yocum GD (2001) Differentiual expression of two HSP70 transcripts in response to cold shock, thermoperiod, and adult diapause in the Colorado potato beetle. J Insect Physiol 47:1139–1145
Yocum GD, Joplin KH, Denlinger DL (1998) Expression of heat-shock proteins in response to high and low temperature extremes in diapausing pharate larvae of the gypsy moth, Lymantria dispar. Arch Insect Biochem Physiol 18:239–249
Yocum GD, Kemp WP, Bosch J, Knoblett JN (2005) Temporal variation in overwintering gene expression and respiration in the solitary bee Megachile rotundata. J Insect Physiol 51:621–629
Yoshiga T, Okano K, Mita K, Shimada T, Matsumoto S (2000) cDNA cloning of acyl-CoA desaturase homologs in the silkworm, Bombyx mori. Gene 246:339–345
Zachariassen KE (1991) The water relations of overwintering insects. In: Lee RE, Denlinger DL (eds) Insects at low temperature. Chapman and Hall, London, pp 47–63
Zachariassen KE, Hammel HT (1976) Nucleating agents in the haemolymph of insects tolerant to freezing. Nature 262:285–287
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This paper was produced within the BAS BIOREACH/BIOFLAME core programmes and also contributes to the SCAR EBA programme. The authors would like to thank Peter Convey for critical reading of the manuscript.
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Communicated by I.D. Hume.
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Clark, M.S., Worland, M.R. How insects survive the cold: molecular mechanisms—a review. J Comp Physiol B 178, 917–933 (2008). https://doi.org/10.1007/s00360-008-0286-4
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DOI: https://doi.org/10.1007/s00360-008-0286-4