Seasonal changes of free amino acids and thermal hysteresis in overwintering heteropteran insect, Pyrrhocoris apterus

Comparative Biochemistry and Physiology - A Molecular and Integrative Physiology

Volumn 160, Issue 2, 2011, Pages 245-251

  Koštál, Vladimír ^a,b   Renault, David ^c   Rozsypal, Jan ^a,b  

^a INSTITUTE OF ENTOMOLOGY   (Czech Republic)

^b UNIVERSITY OF SOUTH BOHEMIA   (Czech Republic)

^c UNIVERSITÉ DE RENNES 1   (France)

Author keywords

Antifreeze; Cold tolerance; Cryoprotectants; Diapause; Ice nucleation; Osmolytes

Indexed keywords

4 AMINOBUTYRIC ACID; ALANINE; AMINO ACID; ARGININE; ASPARAGINE; ASPARTIC ACID; BETA ALANINE; BIOLOGICAL MARKER; GLUTAMIC ACID; GLUTAMINE; ISOLEUCINE; LEUCINE; MECYSTEINE; PROLINE; THERMAL HYSTERESIS FACTOR; THREONINE; TYROSINE; UNCLASSIFIED DRUG; VALINE;

AMINO ACID ANALYSIS; ARTICLE; AUTUMN; BODY TEMPERATURE; COLD TOLERANCE; CONTROLLED STUDY; DIAPAUSE; FEMALE; FLUID BALANCE; HEMOLYMPH; HETEROPTERA; HYSTERESIS; MALE; NONHUMAN; OSMOLALITY; OVERWINTERING; PROTEIN DEGRADATION; PYRRHOCORIS APTERUS; SEASONAL VARIATION; SPRING; WINTER;

HETEROPTERA; HEXAPODA; PYRRHOCORIS APTERUS;

EID: 79960698165     PISSN: 10956433     EISSN: 15314332     Source Type: Journal    
DOI: 10.1016/j.cbpa.2011.06.017     Document Type: Article

References (77)

1. Arakawa T., Timasheff S.N. The stabilization of proteins by osmolytes. Biophys. J. 1985, 47:411-414.
2. Arakawa T., Timasheff S.N. Preferential interactions of proteins with solvent components in aquaeous amino acid solutions. Arch. Biochem. Biophys. 1983, 224:169-177.
3. Bennett V.A., Sformo T., Walters K., Toien O., Jeannet K., Hochstrasser R., Pan Q.F., Serianni A.S., Barnes B.M., Duman J.G. Comparative overwintering physiology of Alaska and Indiana populations of the beetle Cucujus clavipes (Fabricius): roles of antifreeze proteins, polyols, dehydration and diapause. J. Exp. Biol. 2005, 208:4467-4477.
4. Block W. Differential scanning calorimetry in ecophysiological research. Acta Oecol. 1994, 15:13-22.
5. Chen P.S. Amino acid and protein metabolism. Comprehensive Insect Physiology, Biochemistry and Pharmacology 1985, 10:177-199. Pergamon Press, Oxford.
6. Colinet H., Hance T., Vernon P., Bouchereau A., Renault D. Does fluctuating thermal regime trigger free amino acid production in the parasitic wasp Aphidius colemani (Hymenoptera: Aphidiinae)?. Comp. Biochem. Physiol. A 2007, 147:484-492.
7. Danks H.V. The wider integration of studies on insect cold-hardiness. Eur. J. Entomol. 1996, 93:383-403.
8. Danks H.V. The range of insect dormancy responses. Eur. J. Entomol. 2002, 99:127-142.
9. Low Temperature Biology of Insects 2010, Cambridge University Press, Cambridge, 390 p. D.L. Denlinger, R.E. Lee (Eds.).
10. Dittami S.M., Gravot A., Renault D., Goulitquer S., Eggert A., Bouchereau A., Boyen C., Tonon T. Integrative analysis of metabolite and transcript abundance during the short-term response to abiotic stress in the brown alga Ectocarpus siliculosus. Plant Cell Environ. 2011, 10.1111/j.1365-3040.2010.02268.x.
11. Ditrich, T, Koštál, V., 2011. Comparative analysis of overwintering physiology in nine species of semiaquatic bugs (Heteroptera: Gerromorpha). Physiol. Entomol., in press.
12. Duman J.G. Thermal hysteresis factors in overwintering insects. J. Insect Physiol. 1979, 25:805-810.
13. Duman J.G. Antifreeze and ice nuclator proteins in terrestrial arthropods. Annu. Rev. Physiol. 2001, 63:327-357.
14. Duman J.G., Bennett V., Sformo T., Hochstrasser R., Barnes B.M. Antifreeze proteins in Alaskan insects and spiders. J. Insect Physiol. 2004, 50:259-266.
15. Fields P.G., Fleurat-Lessard F., Lavenseau L., Febvay G., Peypelut L., Bonnot G. The effect of cold acclimation and deacclimation on cold tolerance, trehalose and free amino acid levels in Sitophilus granarius and Cryptolestes ferrugineus (Coleoptera). J. Insect Physiol. 1998, 44:955-965.
16. Florkin M., Jeuniaux C. Hemolymph: Composition. The Physiology of Insecta 1974, V:291-297. Academic Press, New York.
17. Francois J. Caracterisation biochimique et biophysique du collagene de l'insecte Tenebrio molitor L. (Coleoptera, Tenebrionidae). Biochimie 1985, 67:1035-1042.
18. Gehrken U. Inoculative freezing and thermal hysteresis in the adult beetles Ips acuminatus and Rhagium inquisitor. J. Insect Physiol. 1992, 38:519-524.
19. Gordon M.K., Hahn R.A. Collagens. Cell Tissue Res. 2010, 339:247-257.
20. Gorres K.L., Raines R.T. Prolyl 4-hydroxylase. Crit. Rev. Biochem. Mol. Biol. 2010, 45:106-124.
21. Hadley N.F. Water relations of terrestrial arthropods 1994, Academic Press, San Diego, 356 p.
22. Hahn D.A., Denlinger D.L. Energetics of insect diapause. Annu. Rev. Entomol. 2011, 56:103-121.
23. Hanec W., Beck S.D. Cold-hardiness in the European corn borer, Pyrausta nubilalis (Hübn.). J. Insect Physiol. 1960, 5:169-180.
24. Hanzal R., Jegorov A. Changes in free amino acid composition in haemolymph of larvae of the wax moth, Galleria mellonela L., during cold acclimation. Comp. Biochem. Physiol. 1991, A 100:957-962.
25. Hodek I. Diapause in females of Pyrrhocoris apterus L. (Heteroptera). Acta Entomol Bohemoslov. 1968, 65:422-435.
26. Hodek I. Role of environmental factors and endogenous mechanisms in the seasonality of reproduction in insects diapausing as adults. Diapause and Life Cycle Strategies in Insects 1983, 9-33. Dr. W. Junk Publishers, The Hague, Boston, London. V.K. Brown, I. Hodek (Eds.).
27. Hodková M. Nervous inhibition of corpora allata by photoperiod in Pyrrhocoris apterus. Nature 1976, 263:521-523.
28. Hodková M. Hormonal and nervous inhibition of reproduction by brain in diapausing females of Pyrrhocoris apterus L. (Hemiptera). Zool. J Physiol. 1979, 83:126-136.
29. Hodková M. Regulation of diapause and reproduction in Pyrrhocoris apterus (L.) (Heteroptera) - Neuroendocrine outputs (mini-review). Entomol. Sci. 1999, 2:563-566.
30. Hodková M., Berková P., Zahradníčková H. Photoperiodic regulation of the phospholipid molecular species composition in thoracic muscles and fat body of Pyrrhocoris apterus (Heteroptera) via an endocrine gland, corpus allatum. J. Insect Physiol. 2002, 48:1009-1019.
31. Hodková M., Hodek I. Control of diapause and supercooling by the retrocerebral complex in Pyrrhocoris apterus. Entomol. Exp. Appl. 1994, 7:237-245.
32. Hodková M., Hodek I. Temperature regulation of supercooling and gut nucleation in relation to diapause of Pyrrhocoris apterus (L.) (Heteroptera). Cryobiology 1997, 34:70-79.
33. Hodková M., Šimek P., Zahradníčková H., Nováková O. Seasonal changes in the phospholipid composition in thoracic muscles of a heteropteran, Pyrrhocoris apterus. Insect Biochem. Mol. Biol. 1999, 29:367-376.
34. Hodková M., Syrová Z., Doležel D., Šauman I. Period gene expression in relation to seasonality and circadian rhythms in the linden bug, Pyrrhocoris apterus (Heteroptera). Eur. J. Entomol. 2003, 100:267-273.
35. Hodková M., Okuda T., Wagner R.M. Regulation of corpora allata in females of Pyrrhocoris apterus (Heteroptera) (a mini-review). In Vitro Cell. Dev. Biol. - Animal 2001, 37:560-563.
36. Issartel J., Renault D., Voituron Y., Bouchereau A., Vernon P., Hervant F. Metabolic responses to cold in subterranean crustaceans. J. Exp. Biol. 2005, 208:2923-2929.
37. Koštál V., Berková P., Šimek P. Remodelling of membrane phospholipids during transition to diapause and cold-acclimation in the larvae of Chymomyza costata (Drosophilidae). Comp. Biochem. Physiol. B 2003, 135:407-419.
38. Koštál, V., Doležal, P., Rozsypal, J., Moravcová, M., Zahradnicková, H., Šimek, P., 2011. Physiological and biochemical analysis of overwintering and cold tolerance in two Central European populations of the spruce bark beetle, Ips typographus. J. Insect Physiol, in press.
39. Koštál V., Renault D., Mehrabianová A., Bastl J. Insect cold tolerance and repair of chill-injury at fluctuating thermal regimes: role of ion homeostasis. Comp. Biochem. Physiol. A 2007, 147:231-238.
40. Koštál V., Šimek P. Overwintering strategy in Pyrrhocoris apterus (Heteroptera): the relations between life-cycle, chill tolerance and physiological adjustments. J. Insect Physiol. 2000, 46:1321-1329.
41. Koštál V., Šlachta M. Variation in cold acclimation during overwintering of Pyrrhocoris apterus (Insecta: Heteroptera). Acta Soc. Zool. Bohem. 2001, 65:239-245.
42. Koštál V., Šlachta M., Šimek P. Cryoprotective role of polyols independent of the increase in supercooling capacity in diapausing adults of Pyrrhocoris apterus (Heteroptera: Insecta). Comp. Biochem. Physiol. B 2001, 130:365-374.
43. Koštál V., Tamura M., Tollarová M., Zahradníčková H. Enzymatic capacity for accumulation of polyol cryoprotectants changes during the diapause development in the adult red firebug, Pyrrhocoris apterus. Physiol. Entomol. 2004, 29:344-355.
44. Koštál V., Tollarová-Borovanská M. The 70kDa Heat shock protein assists during the reparation of chilling injury in the insect, Pyrrhocoris apterus. PLoS One 2009, e4546:1-9.
45. Koštál V., Tollarová M., Doležel D. Dynamism in physiology and gene transcription during reproductive diapause in a heteropteran bug, Pyrrhocoris apterus. J. Insect Physiol. 2008, 54:77-88.
46. Koštál V., Tollarová M., Šula J. Adjustments of the enzymatic complement for polyol biosynthesis and accumulation in diapausing cold-acclimated adults of Pyrrhocoris apterus. J. Insect Physiol. 2004, 50:303-313.
47. Koštál V., Vambera J., Bastl J. 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. 2004, 207:1509-1521.
48. Lalouette L., Koštál V., Colinet H., Gagneul D., Renault D. Cold exposure and associated metabolic changes in adult tropical beetles exposed to fluctuating thermal regimes. FEBS J. 2007, 274:1759-1767.
49. Leather S.R., Walters K.F.A., Bale J.S. The Ecology of Insect Overwintering 1994, Cambridge University Press, Cambridge, 255 p.
50. Insects at Low Temperature 1991, Chapman and Hall, New York and London, 513 p. R.E. Lee, D.L. Denlinger (Eds.).
51. Lefevere K.S., Koopmanschap A.B., De Kort C.A.D. Changes in the concentrations of metabolites in haemolymph during and after diapause in female Colorado potato beetle, Leptinotarsa decemlineata. J. Insect Physiol. 1989, 35:121-128.
52. MacMillan H.A., Sinclair B.J. The role of the gut in insect chilling injury: cold-induced disruption of osmoregulation in the field cricket, Gryllus pennsylvanicus. J. Exp. Biol. 2011, 214:726-734.
53. Mansingh A. Changes in the free amino acids of the haemolymph of Antheraea pernyi during induction and termination of diapause. J. Insect Physiol. 1967, 13:1645-1655.
54. Michaud M.R., Benoit J.B., Lopez-Martinez G., Elnitsky M.A., Lee J.R., Denlinger D.L. Metabolomics reveals unique and shared metabolic changes in response to heat shock, freezing and desiccation in the Antarctic midge, Belgica anatarctica. J. Insect Physiol. 2008, 54:645-655.
55. Michaud M.R., Denlinger D.L. 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 2007, 177:753-763.
56. Morgan T.D., Chippendale G.M. Free amino acids of the haemolymph of the Southwestern corn borer and the European corn borer in relation to their diapause. J. Insect Physiol. 1983, 29:735-740.
57. Nation J.L. Insect Physiology and Biochemistry 2002, CRC Press, Boca Raton, 485 p.
58. Olsen T.M., Sass S.J., Li N., Duman J.G. Factors contributing to seasonal increases in inoculative freezing resistance in overwintering fire-colored beetle larvae Dendroides canadensis (Pyrrochroidae). J. Exp. Biol. 1998, 201:1585-1594.
59. Patterson J.L., Kelly T.J., Duman J.G. Purification and composition of a thermal hysteresis producing protein from the milkweed bug, Oncopeltus fasciatus. J. Comp. Physiol. B 1981, 142:539-542.
60. Raymond J.A., DeVries A.L. Adsorption inhibition as a mechanism of freezing resistance in polar fishes. Proc. Natl. Acad. Sci. USA 1977, 74:2589-2593.
61. Renault D., Bouchereau A., Delettre Y.R., Hervant F., Vernon P. Changes in free amino acids in Alphitobius diaperinus (Coleoptera: Tenebrionidae) during thermal and food stress. Comp. Biochem. Physiol. A 2006, 143:279-285.
62. Renault H., Roussel V., Amrani A.E., Arzel M., Renault D., Bouchereau A., Deleu C. The Arabidopsis pop2-1 mutant reveals the involvement of GABA transaminase (POP2) in salt stress tolerance. BMC Plant Biol. 2010, 10:20. 10.1186/1471-2229-10-20.
63. Ring R.A., Danks H.V. Dessication and cryoprotection: overlapping adaptations. CryoLett. 1994, 15:181-190.
64. Salt R.W. Principles of insect cold hardiness. Annu. Rev. Entomol. 1961, 6:55-64.
65. Sformo T., Walters K., Jeannet K., Wowk B., Fahy G.M., Barnes B.M., Duman J.G. Deep supercooling, vitrification and limited survival to-100 degrees C in the Alaskan beetle Cucujus clavipes puniceus (Coleoptera: Cucujidae) larvae. J. Exp. Biol. 2010, 213:502-509.
66. Sláma K. Hormonal control of respiratory metabolism during growth, reproduction and diapause in female adults of Pyrrhocoris apterus L. (Hemiptera). J. Insect Physiol. 1964, 10:283-303.
67. Socha R. Pyrrhocoris apterus (Heteroptera) - an experimental model species: a review. Eur. J. Entomol. 1993, 90:241-286.
68. Storey K.B., Baust J.G., Storey J.M. Intermediary metabolism during low temperature acclimation in the overwintering gall fly larva, Eurosta solidaginis. J. Comp. Physiol 1981, 144 B:183-190.
69. Storey K.B., Storey J.M. Biochemistry of cryoprotectants. Insects at Low Temperature 1991, 64-93. Chapman and Hall, New York and London. R.E. Lee, D.L. Denlinger (Eds.).
70. Šula J., Socha R., Zemek R. Wing morph-related physiological differences in adults of temperate population of Pyrrhocoris apterus (L.) (Heteroptera: Pyrrhocoridae). Comp. Biochem. Physiol. 1998, A 121:365-373.
71. Suzuki K., Hosaka M., Miya K. The amino acid pool of Bombyx mori eggs during diapause. Insect Biochem. 1984, 14:557-561.
72. Tomčala A., Tollarová M., Overgaard J., Šimek P., Koštál V. 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. 2006, 209:4102-4114.
73. Van der Laak S. Physiological adaptations to low temperature in freezing-tolerant Phyllodecta laticollis beetles. Comp. Biochem. Physiol. A 1982, 73:613-620.
74. Walters K.R., Serriannni A., Sformo T., Barnes B.M., Duman J.G. A nonprotein thermal hysteresis-producing antifreeze in the freeze-tolerant Alaskan beetle Upis ceramboides. Proc. Natl. Acad. Sci. USA 2009, 106:20210-20215.
75. Zachariassen K.E. Physiology of cold tolerance in insects. Physiol. Rev. 1985, 65:799-832.
76. Zachariassen K.E., Husby J.A. Antifreeze effect of thermal hysteresis agents protects highly supercooled insects. Nature 1982, 298:865-867.
77. Zachariassen K.E., Kristiansen E. Ice nucleation and antinucleation in nature. Cryobiol. 2000, 41:257-279.