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Cold-induced mitochondrial degradation and cryoprotectant synthesis in freeze-tolerant arctic caterpillars

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Summary

The larvae ofGynaephora groenlandica, a long-lived moth endemic to the high arctic, are perennially freeze-tolerant and able to increase their freeze-tolerance by synthesizing glycerol. Cold-induced mitochondrial changes were correlated (using electron microscopy, DNA staining, cytochrome c assay, and oxygen uptake) with glycerol production (using NMR spectroscopy) in larvae under different acclimations and in the field. Hypometabolism in summer- or warm-acclimated larvae led to glycerol accumulation. Extended exposure to near-zero or freezing temperatures caused mitochondrial degradation and glycerol accumulation. Rapid freezing of warm-acclimated larvae did not result in mitochondrial breakdown. Mitochondrial reconstitution upon warm-acclimation occurred much more rapidly (<1 week) than did degradation (>2 months). Concomitant with mitochondrial breakdown was reduced oxidative metabolism, but the cytochrome c concentration remained independent of acclimation temperature. The adaptive response to cold by mitochondrial degradation and glycerol accumulation byG. groenlandica may be linked to diapause in other species of ectotherms.

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References

  • Asahina E (1969) Frost resistance in insects. Adv Insect Physiol 6:1–45

    Google Scholar 

  • Ballantyne J, Storey KB (1984) Characterization of mitochondria isolated from the freezing-tolerant larvae of the goldenrod gall fly (Eurosta solidaginis): substrate preference, salt effects, and pH effects on warm- and cold-acclimated animals. Can J Zool 63:373–379

    Google Scholar 

  • Chen C-P, Denlinger DL, Lee RE (1987) Cold-shock injury and rapid cold-hardening in the flesh flySarcophaga crassipalpis. Physiol Zool 60:297–304

    Google Scholar 

  • Chino H (1957a) Carbohydrate metabolism in diapause egg of the silkworm,Bombyx mori I. Diapause and the change in glycogen content. Embryologia 3:295–316

    Google Scholar 

  • Chino H (1957b) Conversion of glycogen to sorbitol and glycerol in the diapause egg of theBombyx silkworm. Nature 180:606–607

    Google Scholar 

  • Chino H (1958) Carbohydrate metabolism in diapause eggs of the silkworm,Bombyx mori. II. Conversion of glycogen into sorbitol and glycerol during diapause. J Insect Physiol 2:1–12

    Google Scholar 

  • Chino H (1960) Enzymatic pathways in the formation of sorbitol and glycerol in the diapausing eggs of the silkwormBombyx mori. I. On the polyol dehydrogenases. J Insect Physiol 5:1–15

    Google Scholar 

  • Clarke KU, Baldwin RW (1960) The effect of insect hormones and of 2,4-dinitrophenol on the mitochondria ofLocusta migratoria L. J Insect Physiol 5:37

    Google Scholar 

  • Colowick SP, Kaplan NO (1955) Methods in enzymology. Academic Press, New York, p 143

    Google Scholar 

  • Conradi-Larsen E, Somme L (1973) The overwintering ofPelophila borealis Payk. II. Aerobic and anaerobic metabolism. Norsk Ent Tidsskr 20:325–332

    Google Scholar 

  • Denlinger DL, Willis JH, Fraenkel G (1972) Rates and cycles of oxygen consumption during pupal diapause inSarcophaga flesh flies. J Insect Physiol 18:871–882

    Google Scholar 

  • Harvey WR, Williams CM (1958) Physiology of insect diapause XII. The mechanisms of carbon monoxide sensitivity and insensitivity during the pupal diapause of the Cecropia silkworm. Biol Bull (Woods Hole, Mass) 114:36–53

    Google Scholar 

  • Hayakawa Y (1985) Activation mechanism of insect fat body phosphorylase by cold. Insect Biochem 15:123–128

    Google Scholar 

  • Hayakawa Y, Chino H (1982) Phosphofructokinase as a possible key enzyme regulating glycerol or trehalose accumulation in diapausing insects. Insect Biochem 12:639–642

    Google Scholar 

  • Herbert D, Phipps RJ, Strange RE (1971) Chemical analysis of microbial cells. Methods Microbiol 5B:209–344

    Google Scholar 

  • Hochachka PW, Somero GN (1985) Biochemical adaptation. Princeton University Press, Princeton

    Google Scholar 

  • Ingrisch S (1987) Oxygen consumption by developing and diapausing eggs ofEupholidoptera smyrnensis (Orthoptera: Tetigoniidae). J Insect Physiol 33:861–865

    Google Scholar 

  • Kageyama T (1976) Pathways of carbohydrate metabolism in the eggs of the silkworm,Bombyx mori. Insect Biochem 6:507–511

    Google Scholar 

  • Keeley LL (1973) Characterization of insect fat body mitochondria isolated by a rapid procedure. Comp Biochem Physiol 46 B:147–151

    Google Scholar 

  • Keeley LL (1981) Neuroendocrine regulation of mitochondrial development and function in the insect fat body. In: Downer RGH (ed) Energy metabolism in insects. Plenum Press, New York, pp 207–239

    Google Scholar 

  • Keister M, Buck J (1964) Respiration. In: Rockstein M (ed) The physiology of Insecta. Academic Press, New York, pp 627–658

    Google Scholar 

  • Kukal O, Kevan PG (1987) The influence of parasitism on the life history of a high arctic insect,Gynaephora groenlandica (Wocke) (Lepidoptera: Lymantriidae). Can J Zool 65:156–163

    Google Scholar 

  • Kukal O, Dawson TE (in press) Temperature and food quality influences feeding behavior, assimilation efficiency and growth rate of arctic woolly-bear caterpillars. Oecologia

  • Kukal O, Serianni AS, Duman JG (1988a) Glycerol metabolism in a freeze-tolerant arctic insect: an in vivo13C NMR study. J Comp Physiol B 158:175–183

    Google Scholar 

  • Kukal O, Heinrich B, Duman JG (1988b) Behavioural thermoregulation in the freeze tolerant arctic caterpillar,Gynaephora groenlandica. J Exp Biol 138:181–193

    Google Scholar 

  • Kurland CG, Schneidermann HA, Smith RD (1958) Oxygen debts in diapausing insects. Anat Rec 132:465–466

    Google Scholar 

  • Lee AD (1955) The physiology of diapause in arthropods. Cambridge University Press, London

    Google Scholar 

  • Lee RE, Chen C-P, Meacham MH, Denlinger DL (1987) Ontogenic patterns of cold-hardiness and glycerol production inSarcophaga crassipalpis. J Insect Physiol 33:587–592

    Google Scholar 

  • Mansingh A, Smallman BN (1972) Variation in polyhydric alcohol in relation to diapause and coldhardiness in the larvae ofIsia isabella. J Insect Physiol 18:1565–1571

    Google Scholar 

  • Mazur P (1984) Freezing of living cells: mechanisms and implications. Am J Physiol 247:125–142

    Google Scholar 

  • Meyer SGE (1978) Effects of heat, cold, anaerobiosis and inhibitors on metabolite concentrations in larvae ofCallitroga macellaria. Insect Biochem 6:471–47

    Google Scholar 

  • Meyer SGE (1980) Studies on anaerobic glucose and glutamate metabolism in larvae ofCallitroga macellaria. Insect Biochem 10:449–455

    Google Scholar 

  • Minks AK (1967) Biochemical aspects of juvenile hormone action in the adultLocusta migratoria. Arch Neerl Zool 17:175

    Google Scholar 

  • Nordin JH, Cui Z, Yin C (1984) Cold-induced glycerol accumulation byostrinia nubilalis larvae is developmentally regulated. J Insect Physiol 30:563–566

    Google Scholar 

  • Plaxton W, Storey KB (1986) Glycolytic enzyme binding and metabolic control in anaerobiosis. J Comp Physiol B 156:635–640

    Google Scholar 

  • Rojas RR, Lee RE, Luu T, Baust JG (1983) Temperature dependence-independence of antifreeze turnover inEurosta solidaginis (Fitch). J Insect Physiol 29:865–869

    Google Scholar 

  • Salt RW (1958) Role of glycerol in producing abnormally low supercooling and freezing points in an insect,Bracon cephi (Gahan). Nature 181:1281

    Google Scholar 

  • Schneiderman HA, Williams CM (1953) The physiology of insect diapause VII. The physiology of the Cecropia silkworm during diapause and during development. Biol Bull (Woods Hole, Mass) 105:320–334

    Google Scholar 

  • Schneiderman HA, Williams CM (1954) Physiology of insect diapause. VIII. Qualitative changes in the metabolism of the Cecropia silkworm during diapause and development. Biol Bull (Woods Hole, Mass) 106:200–210

    Google Scholar 

  • Scholander PF, Flagg W, Hoch RJ, Irving L (1963) Climatic adaptation in arctic and tropical poikilotherms. Physiol Zool 26:67–92

    Google Scholar 

  • Scholander PF, Flagg W, Hoch RJ, Irving L (1954) Studies on the physiology of frozen plants and animals in the arctic. J Cell Comp Physiol 49:1–56

    Google Scholar 

  • Selwyn MJ (1987) Holes in mitochondrial membranes. Nature 330:424–425

    Google Scholar 

  • Shappirio DG, Williams CM (1957a) The cytochrome system of the Cecropia silkworms. I. Spectroscopic studies of individual tissues. Proc R Soc London B 147:218–232

    Google Scholar 

  • Shappirio DG, Williams CM (1957b) The cytochrome system of the Cecropia silkworm II. Spectrophotometric studies of oxidative enzyme systems in the wing epithelium. Proc R Soc London B 147:233–246

    Google Scholar 

  • Siegert KJ (1986) The effects of chilling and integumentary injury on carbohydrate and lipid metabolism in diapause and non-diapause pupae ofManduca sexta. Comp Biochem Physiol 85A:257–262

    Google Scholar 

  • Siegert KJ (1987) Carbohydrate metabolism in starved first instar larvae ofMaduca sexta. Arch Insect Biochem Physiol 4:151–160

    Google Scholar 

  • Siegert KJ, Ziegler R (1983) A hormone from the corpora cardiaca controls fat body glycogen phosphorylase during starvation in tobacco hornworm larvae. Nature 301:526–527

    Google Scholar 

  • Somme L (1974) Anaerobiosis in some alpine Coleoptera. Norsk Ent Tidsskr 21:155–158

    Google Scholar 

  • Storey KB, Storey JM (1983) Biochemistry of freeze tolerance in terrestrial insects. Trends Biochem Sci 8:242–245

    Google Scholar 

  • Takehara I (1966) Natural occurrence of glycerol in the slug caterpillarMonema flavescens. Low Temp Sci B 14:1–34

    Google Scholar 

  • Tauber MJ, Tauber CA, Masaki S (1986) Seasonal adaptations of insects. Oxford University Press. New York

    Google Scholar 

  • Tsumuki H, Rojas RR, Storey KB, Baust JG (1986) The fate of [14C]glucose during cold-hardening inEurosta solidaginis (Fitch). Insect Biochem 17:347–352

    Google Scholar 

  • Wilhelm RC, Schneiderman HA, Daniel LJ (1961) The effects of anaerobiosis on the giant silkwormsHyalophora cecropia andSamia cynthia with special reference to the accumulation of glycerol and lactic acid. J Insect Physiol 7:273–288

    Google Scholar 

  • Williams JN Jr (1964) A method of the simultaneous quantitative estimation of cytochromes a, b, c1 and c in mitochondria. Arch Biochem Biophys 107:537–543

    Google Scholar 

  • Williamson DH, Fennell DJ (1975) The use of fluorescent DNA-binding agent for detecting and separating yeast mitochondrial DNA. In: Prescott DM (ed) Methods in cell biology, vol 12. Academic Press, pp 335–351

  • Wittekind D (1972) Fluorescence properties of the monoaminoacridines and some 2-aminoacridine derivatives. In: Thaer AA, Sernetz M (eds) Fluorescence techniques in biology. Springer, Berlin Heidelberg New York, pp 95–105

    Google Scholar 

  • Wood FE, Nordin JH (1980) Activation of hexose monophosphate shunt during cold-induced glycerol accumulation byProtophormia terranovae. Insect Biochem 10:87–93

    Google Scholar 

  • Wyatt GR (1960) Phosphorus compounds in insect development. Proc 4th Int Congr Biochem 12:161–178

    Google Scholar 

  • Wyatt GR, Meyer WL (1959) The chemistry of insect hemolymph III. Glycerol. J Gen Physiol 42:1005–1011

    Google Scholar 

  • Wyatt GR, Kalf GF (1958) Organic components of insect hemolymph. Proc 10th Int Congr Ent 2:333

    Google Scholar 

  • Yancey PH, Clark ME, Hank SC, Bowlus RD, Somero GN (1982) Living with water stress: evolution of osmolyte systems. Science 217:1214–1222

    Google Scholar 

  • Yi S, Yin C, Nordin JH (1987) The chilling-induced biosynthesis and secretion of glycerol byOstrinia nubilalis larval fat bodies in vitro. J Insect Physiol 33:523–528

    Google Scholar 

  • Zachariassen KE (1985) Physiology of cold tolerance in insects. Physiol Rev 65:799–832

    Google Scholar 

  • Zebe EC, McShan WH (1957) Lactic and α-glycerophosphate dehydrogenases in insects. J Gen Physiol 40:779–790

    Google Scholar 

  • Ziegler R, Wyatt GR (1975) Phosphorylase and glycerol production activated by cold in diapausing silkworm pupae. Nature 254:622–625

    Google Scholar 

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  1. Olga Kukal

    Present address: Entomology Department, Ohio State University, 43210, Columbus, Ohio, USA

Authors and Affiliations

  1. Department of Biological Sciences, University of Notre Dame, 46556, Notre Dame, Indiana, USA

    Olga Kukal & John G. Duman

  2. Department of Chemistry, University of Notre Dame, 46556, Notre Dame, Indiana, USA

    Anthony S. Serianni

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  2. John G. Duman
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Kukal, O., Duman, J.G. & Serianni, A.S. Cold-induced mitochondrial degradation and cryoprotectant synthesis in freeze-tolerant arctic caterpillars. J Comp Physiol B 158, 661–671 (1989). https://doi.org/10.1007/BF00693004

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