Cell Stress and Chaperones

, Volume 14, Issue 2, pp 219–226 | Cite as

Extreme thermotolerance and behavioral induction of 70-kDa heat shock proteins and their encoding genes in honey bees

Short Communication


Foraging honey bees frequently leave the hive to gather pollen and nectar for the colony. This period of their lives is marked by periodic extremes of body temperature, metabolic expenditure, and flight muscle activity. Following ecologically relevant episodes of hyperthermia between 33°C and 50°C, heat shock protein 70 (Hsp70) expression and hsp70/hsc70-4 activity in brains of nonflying laboratory-held bees increased by only two to three times baseline at temperatures 46–50°C. Induction was undetectable in thoracic–flight muscles. Yet, thorax hsp70 mRNA (but not hsc70-4 mRNA) levels were up to ten times higher in flight-capable hive bees and foraging bees compared to 1-day-old, flight-incapable bees, while brain hsp70/hsc70-4 mRNA levels were low and varied little among behavioral groups. These data suggest honey bee tissues, especially flight muscles, are extremely thermotolerant. Furthermore, Hsp70 expression in the thoraces of flight-capable bees is probably flight-induced by oxidative and mechanical damage to flight muscle proteins rather than temperature.


Brain Honey bee Hsp70 Muscle Thermotolerance 


  1. Alamillo J, Almoguera C, Bartels D, Jordano J (1995) Constitutive expression of small heat shock proteins in vegetative tissues of the resurrection plant Craterostigma plantagineum. Plant Molec Biol 29:1093–1099 doi:10.1007/BF00014981 CrossRefGoogle Scholar
  2. Ben Shahar Y, Robichon A, Sokolowski MB, Robinson GE (2002) Influence of gene action across different time scales on behavior. Science 296:741–744 doi:10.1126/science.1069911 PubMedCrossRefGoogle Scholar
  3. Ben Shahar Y, Leung HT, Pak WL, Sokolowski MB, Robinson GE (2003) cGMP-dependent changes in phototaxis: a possible role for the foraging gene in honey bee division of labor. J Exp Biol 206:2507–2515 doi:10.1242/jeb.00442 PubMedCrossRefGoogle Scholar
  4. Bronk P, Wenniger JJ, Dawson-Scully K, Guo X, Hong S, Atwood HL, Zinsmaier KE (2001) Drosophila Hsc70-4 is critical for neurotransmitter exocytosis in vivo. Neuron 30:475–488 doi:10.1016/S0896-6273(01)00292-6 PubMedCrossRefGoogle Scholar
  5. Buckley BA, Hofmann GE (2004) Magnitude and duration of thermal stress determine kinetics of hsp gene regulation in the goby Gillichthys mirabilis. Physiol Biochem Zool 77:570–581 doi:10.1086/420944 PubMedCrossRefGoogle Scholar
  6. Burke JJ, Hatfield JL, Klein RP, Mullet JE (1985) Accumulation of heat shock proteins in field-grown cotton. Plant Physiol 78:394–398PubMedCrossRefGoogle Scholar
  7. Chacon-Almeida VML, Simões ZLP, Bitondi MMG (2000) Induction of heat shock proteins in the larval fat body of Apis mellifera L. bees. Apidologie 31:487–501 doi:10.1051/apido:2000141 CrossRefGoogle Scholar
  8. Chen B, Zhong D, Monteiro A (2006) Comparative genomics and evolution of the HSP90 family of genes across all kingdoms of organisms. BMC Genomics 7:156 doi:10.1186/1471-2164-7-156 PubMedCrossRefGoogle Scholar
  9. Colombo SJ, Timmer VR, Colclough ML, Blumwald E (1995) Diurnal variation in heat tolerance and heat shock protein expression in black spruce (Picea mariana). Can J Forest Res 25:369–375 doi:10.1139/x95-041 CrossRefGoogle Scholar
  10. Daborn P, Yen JL, Bogwitz MR, Le Goff G, Feil E, Jeffers S, Tijet N, Perry T, Heckel D, Batterham P, Feyereisen R, Wilson TG, French-Constant RH (2002) A single p450 allele associated with insecticide resistance in Drosophila. Science 297:2253–2256 doi:10.1126/science.1074170 PubMedCrossRefGoogle Scholar
  11. Denlinger DL (2002) Regulation of diapause. Annu Rev Entomol 47:93–122 doi:10.1146/annurev.ento.47.091201.145137 PubMedCrossRefGoogle Scholar
  12. Elekonich MM, Roberts SP (2005) Genetic and physiological underpinnings of age-related and environmentally-mediated phenotypic plasticity in honey bees. Comp Biochem Physiol A 141:362–371 doi:10.1016/j.cbpb.2005.04.014 CrossRefGoogle Scholar
  13. Feder ME (1997) Necrotic fruit: a novel model system for thermal ecologists. J Therm Biol 22:1–9 doi:10.1016/S0306-4565(96)00028-9 CrossRefGoogle Scholar
  14. Feder ME, Hofmann GE (1999) Heat shock proteins, molecular chaperones and the stress response: evolutionary and ecological physiology. Ann Rev Physiol 61:243–282 doi:10.1146/annurev.physiol.61.1.243 CrossRefGoogle Scholar
  15. Feder ME, Blair N, Figueras H (1997) Natural thermal stress and heat-shock protein expression in Drosophila larvae and pupae. Funct Ecol 11:90–100 doi:10.1046/j.1365-2435.1997.00060.x CrossRefGoogle Scholar
  16. Feder ME, Roberts SP, Bordelon AC (2000) Molecular thermal telemetry of free-ranging adult Drosophila melanogaster. Oecologia 123:460–465 doi:10.1007/s004420000334 CrossRefGoogle Scholar
  17. Gehring WJ, Wehner R (1995) Heat shock protein synthesis and thermotolerance in Cataglyphis, an ant from the Sahara desert. PNAS 92:2994–2998 doi:10.1073/pnas.92.7.2994 PubMedCrossRefGoogle Scholar
  18. Gregorc A, Bowen ID (1999) In situ localization of heat-shock and histone proteins in honey bee (Apis mellifera L.) larvae infected with Paenibacillus larvae. Cell Biol Int 23:211–218 doi:10.1006/cbir.1999.0344 PubMedCrossRefGoogle Scholar
  19. Grozinger CM, Hassig CA, Schreiber SL (1999) Three proteins define a class of human histone deacetylases related to yeast Hdalp. PNAS 96:4468–4473 doi:10.1073/pnas.96.9.4868 CrossRefGoogle Scholar
  20. Hamilton EW, Heckathorn SA, Downs CA, Schwarz TE, Coleman JS, Hallberg RL (1996) Heat shock proteins are produced by field grown naturally occurring plants in the summer in the temperate northeast. US Bull Ecol Soc Am 77(Suppl Part 2):180Google Scholar
  21. Harrison JM, Fewell JH, Roberts SP, Hall HG (1996) Achievement of thermal stability by varying metabolic heat production in flying honeybees. Science 274:88–90 doi:10.1126/science.274.5284.88 PubMedCrossRefGoogle Scholar
  22. Heinrich B (1980) Mechanisms of body temperature regulation in honeybees, Apis mellifera. II. Regulation of thoracic temperature at high air temperatures. J Exp Biol 85:73–87Google Scholar
  23. Helmuth BST, Hofmann GE (2001) Microhabitats, thermal heterogeneity, and patterns of physiological stress in the rocky intertidal zone. Biol Bull 201:374–384 doi:10.2307/1543615 PubMedCrossRefGoogle Scholar
  24. Hendershot KL, Weng J, Nguyen HT (1992) Induction temperature of heat shock protein synthesis in wheat. Crop Sci 32:256–261Google Scholar
  25. Hernandez LD, Vierling E (1993) Expression of low molecular weight heat shock proteins under field conditions. Plant Physiol 101:1209–1216PubMedGoogle Scholar
  26. Hofmann GE, Somero GN (1996) Protein ubiquitination and stress protein synthesis in Mytilus trossulus occurs during recovery from tidal emersion. Mol Mar Biol Biotechnol 5:175–184Google Scholar
  27. Honey Bee Genome Sequencing Consortium (2006) Insights into social insects from the genome of the honey bee Apis mellifera. Nature 433:931–949Google Scholar
  28. Huey RB, Bennett AF (1990) Physiological adjustments to fluctuating thermal environments: an ecological and evolutionary perspective. In: Morimoto RI, Tissieres A, Georgopoulos C (eds) Stress proteins in biology and medicine. Cold Spring Harbor Lab Press, Cold Spring Harbor, pp 37–59Google Scholar
  29. Joplin KH, Denlinger DL (1990) Developmental 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 doi:10.1016/0022-1910(90)90108-R CrossRefGoogle Scholar
  30. Kimpel JA, Key JL (1985) Presence of heat shock mRNAs in field grown soybeans. Plant Physiol 79:672–678PubMedCrossRefGoogle Scholar
  31. Krebs RA, Feder ME (1997) Tissue-specific variation in Hsp70 expression and thermal damage in Drosophila melanogaster larvae. J Exp Biol 200:2007–2015PubMedGoogle Scholar
  32. Neukirch A (1982) Dependence of the life-span of the honeybee (Apis mellifera) upon flight performance and energy consumption. J Comp Phys B 146:35–40CrossRefGoogle Scholar
  33. Nguyen HT, Joshi CP, Klueva N, Weng J, Hendershot KL, Blum A (1994) The heat-shock response and expression of heat-shock proteins in wheat under diurnal heat stress and field conditions. Aust J Plant Physiol 21:857–67CrossRefGoogle Scholar
  34. Palter KB, Watanabe M, Stinson L, Mahowald AP, Craig EA (1986) Expression and localization of Drosophila melanogaster hsp70 cognate proteins. Mol Cell Biol 6:1187–1203PubMedGoogle Scholar
  35. Roberts SP, Harrison JF (1999) Mechanisms of thermal stability during flight in the honeybee Apis mellifera. J Exp Biol 202:1523–1533PubMedGoogle Scholar
  36. Roberts SP, Elekonich MM (2005) Commentary: behavioral development and the ontogeny of flight capacity in honey bees. J Exp Biol 208:4193–4198 doi:10.1242/jeb.01862 PubMedCrossRefGoogle Scholar
  37. Schulz DJ, Elekonich MM, Robinson GE (2003) Biogenic amines in the antennal lobes and the initiation and maintenance of foraging behavior in honey bees. J Neurobiol 54:406–416 doi:10.1002/neu.10138 PubMedCrossRefGoogle Scholar
  38. Severson DW, Erickson EH Jr, Williamson JL, Aiken JM (1990) Heat stress induced enhancement of heat shock protein gene activity in the honey bee (Apis mellifera). Experientia 46:737–739 doi:10.1007/BF01939951 PubMedCrossRefGoogle Scholar
  39. Singh AK, Lakhotia SC (2000) Tissue-specific variations in the induction of Hsp70 and Hs64 by heat shock in insects. Cell Stress Chaperones 5:90–97 doi:10.1379/1466-1268(2000)005<0090:TSVITI>2.0.CO;2 PubMedCrossRefGoogle Scholar
  40. Thellin O, Zorzi W, Lakaye B, De Borman B, Coumans B, Hennen G, Grisar T, Igout A, Heinen E (1999) Housekeeping genes as internal standards: use and limits. J Biotechnology 75:291–295 doi:10.1016/S0168-1656(99)00163-7 CrossRefGoogle Scholar
  41. Tomanek L, Somero GN (1997) The effect of temperature on protein synthesis in snails of the genus Tegula from the sub-and intertidal zone. Am Zool 37:188AGoogle Scholar
  42. Velazquez JM, Sonoda S, Bugaisky G, Lindquist S (1983) Is the major Drosophila heat shock protein present in cells that have not been heat shocked? J Cell Biol 96:286–290 doi:10.1083/jcb.96.1.286 PubMedCrossRefGoogle Scholar
  43. Whitfield CW, Cziko AM, Robinson GE (2003) Gene expression profiles in the brain predict behavior in individual honey bees. Science 302:296–299 doi:10.1126/science.1086807 PubMedCrossRefGoogle Scholar
  44. Wilkinson L, Blank G, Gruber C (1996) Desktop data analysis with systat. Upper Saddle River, N.J.: Prentice HallGoogle Scholar
  45. Williams JB, Roberts SP, Elekonich MM (2008) Age and natural metabolically-intensive behavior affect oxidative stress and antioxidant mechanisms. Exp Gerontol 43:538–549 doi:10.1016/j.exger.2008.02.001 PubMedCrossRefGoogle Scholar
  46. Winston ML (1987) The biology of the honeybee. Harvard University Press, CambridgeGoogle Scholar

Copyright information

© Cell Stress Society International 2008

Authors and Affiliations

  1. 1.School of Life SciencesUniversity of Nevada Las VegasLas VegasUSA

Personalised recommendations