Expression of hSP90 gene and its relationship with ambient temperature and foraging rate in apis mellifera meda

Document Type : Research Paper

Authors

1 Department of Animal Science, Faculty of Agricultural and Natural Resources, Persian Gulf ,University, Bushehr, Iran

2 Department of Plant Protection, Faculty of Agricultural and Natural Resources, Persian Gulf University, Bushehr, Iran.

Abstract

Objective
HSP90 is a member of heat shock proteins (HSPs) family which produces in response to environmental stress factors and has different roles in cells. In this study, the differential expression of HSP90 gene during the day and its relationship with ambient temperature and foraging rate of worker bees were investigated.
 
Material and methods
The worker bees’ commuting in front of hive and ambient temperature in five different times of day (at 7:00, 9:30, 12:00, 14:30 and 17:00) were recorded for three days. The relative transcription level of HSP90 gene was measured in those times using real-time PCR method. The effects of day and different times in a day were subjected to the model as random and fixed effects, respectively, for analyzing worker bees’ commuting and ambient temperature. The regression between these traits was also run.
 
Results
Results showed that time of day has significant effect on ambient temperature, worker bees’ commuting and relative expression of HSP90 (P < 0.01). The highest and lowest ambient temperature were recorded at 12:00 pm and 7:00 am, respectively. The highest and least worker bees’ commuting were obtained at 17:00 and 12:00 pm, respectively. In addition, the highest and lowest HSP90 gene transcription level were recorded at 12:00 pm and 7:00 am o’clock, respectively. The regression analysis revealed that worker bees’ commuting and relative expression of HSP90 gene were increased with increasing of ambient temperature; the commuting of bees was reduced in temperature above 39 ̊ C. Furthermore, the worker bees’ commuting was increased with increasing of HSP90 expression to three-fold, which was decreased with more relative expression level.
 
Conclusion
In general, the trend of worker bees’ commuting, ambient temperature, and relative expression of HSP90 gene were clear during the day. When the ambient temperature was increased, the relative transcription level of HSP90 gene was increased in response to heat stress, while the number of commuter bees was decreased. The management of heat shock can be recommended to improve nectar gathering by commuter bees.
 
 

Keywords


 
بهادر یاسر ، محمدآبادی محمدرضا ، خضری امین ، اسدی مهدیه ، مدحتی لیلا (1395) مطالعه تنوع ژنتیکی جمعیتهای زنبور عسل استان کرمان با استفاده از نشانگرهای  ISSR. پژوهش‌های تولیدات دامی 13، 192-186.
توحیدی نژاد فاطمه، محمدآبادی محمدرضا، اسمعیلی زاده کشکوئیه علی، نجمی نوری عذرا (1393) مقایسه سطوح مختلف بیان ژنRheb  در بافت‌های مختلف بز کرکی راینی. مجله بیوتکنولوژی کشاورزی 6، 50-35. 
محمدآبادی محمدرضا (1398) بیان ژن کالپاستاتین در بز کرکی راینی با استفاده از Real Time PCR. مجله بیوتکنولوژی کشاورزی 11، 235-219. 
محمودی مریم ، آیت اللهی احمد ، محمدآبادی محمدرضا (1396). بررسی اگزون چهارم ژن کاپاکازئین گوسفند کرمانی با تکنیک PCR-RFLP. مجله بیوتکنولوژی کشاورزی 9، 119-128.
مرمضی سالم، مسعودی علی اکبر، واعظ ترشیزی رسول، پاکدل عباس (1393). تمایز بیان ژن انتقال دهنده نوع 1 گلوکز (GLUT1) در زمان‌های متفاوت فیزیولوژیکی در غدد پستانی بزهای عدنی ایران. مجله بیوتکنولوژی کشاورزی 6، 159-173.
References
Aamodt RM (2008) The caste-and age-specific expression signature of honeybee heat shock genes shows an alternative splicing-dependent regulation of Hsp90. Mech Ageing Dev 129, 632–637.
Ali MAM (2011) Comparative study for evaluating two honey bee races, Apis mellifera jementica (indigenous race) and Apis mellifera carnica (carniolan race) in brood production, population development and foraging activity under the environmental conditions of the central region of the Kingdom of Saudi Arabia. Ann Agric Sci 56, 127–134.
Alqarni AS (2006) Tolerance of summer temperature in imported and indigenous honeybee Apis mellifera L. races in central Saudi Arabia. Saudi J Biol Sci 13, 123–127.
Alves LHS, Cassino PCR, Prezoto F (2015) Effects of abiotic factors on the foraging activity of Apis mellifera Linnaeus, 1758 in inflorescences of Vernonia polyanthes Less (Asteraceae). Acta Sci Anim Sci 37, 405–409.
Bahador Y, Mohammadabadi M, Khezri A et al. (2016) Study of genetic diversity in honey bee populations in kerman province using ISSR markers. Res Anim Prod 7, 186–192 (In Persian).
Beekman M, Sumpter DJT, Seraphides N et al. (2004) Comparing foraging behaviour of small and large honey‐bee colonies by decoding waggle dances made by foragers. Funct Ecol 18, 829–835.
Boorstein WR, Ziegelhoffer T, Craig EA (1994) Molecular evolution of the HSP70 multigene family. J Mol Evol 38, 1–17.
Blazyte-Cereskiene L, Vaitkeviciene G, Venskutonyte S et al. (2010) Honey bee foraging in spring oilseed rape crops under high ambient temperature conditions. Zemdirb (Agric) 97, 61–70.
Brunt SA, Silver JC (1991) Molecular cloning and characterization of two distinct hsp 85 sequences from the steroid responsive fungus Achlya ambisexualis. Curr Genet 19, 383–388.
Corbet SA, Fussell M, Ake R et al. (1993) Temperature and the pollinating activity of social bees. Ecol Entomol 18, 17–30.
Elekonich MM (2009) Extreme thermotolerance and behavioral induction of 70-kDa heat shock proteins and their encoding genes in honey bees. Cell Stress Chaperones 14, 219–226.
Elsik CG, Worley KC, Bennett AK et al. (2014) Finding the missing honey bee genes: lessons learned from a genome upgrade. BMC Genomics 15, 86.
Feder ME, Hofmann GE (1999) Heat-shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology. Annu Rev Physiol 61, 243–282.
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.
Gvozdenov Z, Bendix LD, Kolhe J et al. (2019) The Hsp90 Molecular Chaperone Regulates the Transcription Factor Network Controlling Chromatin Accessibility. J Mol Biol 431, 4993–5003.
Hartl FU, Hayer-Hartl M (2002) Molecular chaperones in the cytosol: from nascent chain to folded protein. J Sci 295, 1852–1858.
Hilario SD, Imperatriz-Fonseca VL, Kleinert A (2000) Flight activity and colony strength in the stingless bee Melipona bicolor bicolor (Apidae, Meliponinae). Rev Bras Biol 60, 299–306.
Human H, Brodschneider R, Dietemann V et al. (2013) Miscellaneous standard methods for Apis mellifera research. J Apic Res 52, 1–53.
Isaacs JS, Jung Y-J, Mimnaugh EG et al. (2002) Hsp90 regulates a von Hippel Lindau-independent hypoxia-inducible factor-1α-degradative pathway. J Biol Chem 277, 29936–29944.
King AM, MacRae TH (2015) Insect heat shock proteins during stress and diapause. Annu Rev Entomol 60, 59–75.
Koo J, Son T-G, Kim S-Y et al. (2015) Differential responses of Apis mellifera heat shock protein genes to heat shock, flower-thinning formulations, and imidacloprid. J Asia Pac Entomol 18, 583–589.
Kregel KC (2002) Invited review: heat shock proteins: modifying factors in physiological stress responses and acquired thermotolerance. J Appl Physiol 92, 2177–2186.
Lindquist S, Craig EA (1988) The heat-shock proteins. Annu Rev Genet 22, 631–677.
Lourenço AP, Mackert A, dos Santos Cristino A et al (2008) Validation of reference genes for gene expression studies in the honey bee, Apis mellifera, by quantitative real-time RT-PCR. Apidologie 39, 372–385.
Mahmoodi M, Ayatollahi A, Mohammadabadi MR (2018) Studying exon 4 of kappa-casein gene in Kermani sheep using PCR-RFLP. Agric Biotec J 9, 119–128 (In Persian).
Medrzycki P, Giffard H, Aupinel P et al. (2013) Standard methods for toxicology research in Apis mellifera. J Apic Res 52, 1–60.
Mohammadabadi MR (2019) Expression of calpastatin gene in Raini Cashmere goat using Real Time PCR. Agric Biotec J 11, 219–235 (In persian).
Mohammadabadi MR (2017) Role of clostridium perfringens in pathogenicity of some domestic animals. J Adv Agric 7, 1117–1121.
Morammazi S, Masoudi AA, Vaez Torshizi R et al. (2015) Differential Gene Expression of Glucose Transporter 1 (GLUT1) in Different Physiological Times in Mammary Glands of Iranian Adani Goats 6, 159-173 (In Persian).
Nadeau K, Das A, Walsh CT (1993) Hsp90 chaperonins possess ATPase activity and bind heat shock transcription factors and peptidyl prolyl isomerases. J Biol Chem 268, 1479–1487.
Pernal SF, Currie RW (2001) The influence of pollen quality on foraging behavior in honeybees (Apis mellifera L.). Behav Ecol Sociobiol 51, 53–68.
Polatto LP, Chaud-Netto J, Alves-Junior V V (2014) Influence of abiotic factors and floral resource availability on daily foraging activity of bees. J Insect Behav 27, 593–612.
Pratt WB, Toft DO (2003) Regulation of signaling protein function and trafficking by the hsp90/hsp70-based chaperone machinery. Exp Biol Med 228, 111–133.
Richter K, Haslbeck M, Buchner J (2010) The heat shock response: life on the verge of death. Mol Cell 40, 253–266.
Rinehart JP, Li A, Yocum GD et al. (2007) Up-regulation of heat shock proteins is essential for cold survival during insect diapause. Proc Natl Acad Sci 104, 11130–11137.
Rueppell O, Bachelier C, Fondrk MK et al. (2007) Regulation of life history determines lifespan of worker honey bees (Apis mellifera L.). Exp Gerontol 42, 1020–1032.
Rutherford S, Knapp JR, Csermely P (2007) Hsp90 and developmental networks. In: Molecular aspects of the stress Response: Chaperones, membranes and networks. Springer, pp 190–197.
Sangster TA, Lindquist S, Queitsch C (2004) Under cover: causes, effects and implications of Hsp90 mediated genetic capacitance. Bioessays 26, 348–362.
Sawarkar R, Sievers C, Paro R (2012) Hsp90 globally targets paused RNA polymerase to regulate gene expression in response to environmental stimuli. Cell 149, 807–818.
Scharlaken B, de Graaf DC, Goossens K et al. (2008). Reference gene selection for insect expression studies using quantitative real-time PCR: The head of the honeybee, Apis mellifera, after a bacterial challenge. J Insect Sci. 8, 33.
Severson DW, Erickson EH, Williamson JL et al. (1990) Heat stress induced enhancement of heat shock protein gene activity in the honey bee (Apis mellifera). Experientia 46, 737–739.
Sonoda S, Ashfaq M, Tsumuki H (2007) A comparison of heat shock protein genes from cultured cells of the cabbage armyworm, Mamestra brassicae, in response to heavy metals. Arch Insect Biochem Physiol Publ Collab with Entomol Soc Am 65, 210–222.
Tedeschi JN, Kennington WJ, Berry O et al. (2015). Increased expression of Hsp70 and Hsp90 mRNA as biomarkers of thermal stress in loggerhead turtle embryos (Caretta caretta). J Therm Biol, 47, 42-50.
Tohidinejad F, Mohammadabadi MR, Esmailizadeh AK et al. (2015) Comparison of different levels of Rheb gene expression in different tissues of Raini Cashmir goat. Agric Biotechnol J 6, 35–50 (In Persian).
Wang MN, Liu LX, Deng YT et al. (2020) Regulatory mechanism of heat shock protein 90 on autophagy-related transcription factor EB in human hepatocellular carcinoma cells. Acta Physiol Sin 72, 157–166.
Weinstock GM, Robinson GE, Gibbs RA et al. (2006) Insights into social insects from the genome of the honeybee Apis mellifera. Nature 443, 931–949.
Xu H-J, Xue J, Lu B et al. (2015) Two insulin receptors determine alternative wing morphs in planthoppers. Nature 519, 464.
Xu PJ, Xiao JH, Xia QY et al. (2010) Apis mellifera has two isoforms of cytoplasmic HSP90. Insect Mol Biol 19, 593–597.
Zhao R, Houry WA (2007) Molecular interaction network of the Hsp90 chaperone system. Adv Exp Med Biol 594, 27–36.
Zou J, Guo Y, Guettouche T et al. (1998) Repression of heat shock transcription factor HSF1 activation by HSP90 (HSP90 complex) that forms a stress-sensitive complex with HSF1. Cell 94, 471–480.