Eur. J. Entomol. 120: 161-169, 2023 | DOI: 10.14411/eje.2023.021

Plant essential oils induce expression of heat shock proteins and antioxidant enzyme activity in carob moth, Ectomyelois ceratoniae (Lepidoptera: Pyralidae)Original article

Saeed FARAHANI ORCID..., Ali R. BANDANI ORCID...*
Plant Protection Department, College of Agriculture and Natural Resources, University of Tehran, Iran; e-mails: farahanisaeed@ut.ac.ir, abandani@ut.ac.ir

Rising concerns about the negative effects of chemical compounds in pest control have made it increasingly necessary to find new environmentally friendly compounds to combat insect pests. In recent years, the use of plant derivatives, such as, essential oils have proved very promising. Despite the many studies on essential oils, there are very few studies on the effect of these oils on induction of Heat shock proteins (HSPs) and antioxidant enzymes. Therefore, it was hypothesized that the exposure of insects to essential oils induce stress, which it is likely induces the production of heat shock proteins and antioxidant enzymes. Thus, Ectomyelois ceratoniae Clark (Lepidoptera: Pyralidae) was used as a model insect to study the lethal and sublethal effect of the fumigant toxicity of the essential oils extracted from the plants Thymus daenensis Celak and Satureja khuzistanica Jamzad. Gas Chromatography/Mass Spectrometry indicated that thymol and carvacrol were the major component of T. daenensis and S. khuzistanica extracts, respectively. Exposing E. ceratoniae to sublethal doses of the essential oils (LC30) and using RT-qPCR indicated that the expression levels of HSP70 and HSP90 were significantly increased. Activities of antioxidant enzymes including SOD, CA, POX, GST and the concentration of MDA increased following exposure to sublethal doses of both essential oils. These findings clearly show that in addition to the reported effects of essential oils, oxidative stress and induction of free radical production could be another mode of the action of essential oils on insects.

Keywords: Thymus daenensis, Satureja khuzistanica, Integrated Pest Management, IPM, HSPs

Received: October 9, 2022; Revised: April 4, 2023; Accepted: April 4, 2023; Published online: May 22, 2023  Show citation

ACS AIP APA ASA Harvard Chicago Chicago Notes IEEE ISO690 MLA NLM Turabian Vancouver
FARAHANI, S., & BANDANI, A.R. (2023). Plant essential oils induce expression of heat shock proteins and antioxidant enzyme activity in carob moth, Ectomyelois ceratoniae (Lepidoptera: Pyralidae). EJE, 120, Article 161-169. https://doi.org/10.14411/eje.2023.021
Share...
Download citation
  • BibTeX (.bib)
  • Bookends (.ris)
  • EasyBib (.ris)
  • EndNote (.enw)
  • EndNote 8 (.xml)
  • ISI WoS (.isi)
  • Medlars (.medlars)
  • Mendeley (.ris)
  • MODS (.xml)
  • Papers (.ris)
  • RefWorks (.txt)
  • RefManager (.ris)
  • RIS (.ris)
  • MS Word (.xml)
  • Zotero (.ris)
    • Open full article

    References

    1. Abid I., Laghfiri M., Bouamri R., Aleya L. & Bourioug M. 2021: Integrated pest management (IPM) for Ectomyelois ceratoniae on date palm. - Curr. Opin. Environ. Sci. Health 19: 100219, 12 pp.. Go to original source...
    2. Asada K. 1984: Chloroplasts: Formation of active oxygen and its scavenging. - Meth. Enzymol. 105: 422-429. Go to original source...
    3. Ayvaz A., Sagdic O., Karaborklu S. & Ozturk I. 2010: Insecticidal activity of the essential oils from different plants against three stored-product insects. - J. Insect Sci. 10: 21, 13 pp. Go to original source...
    4. Bar-Or D., Rael L.T., Lau E.P., Rao N.K., Thomas G.W., Winkler J.V., Richard L., Yukl R. & Curtis C.G. 2001: An analog of the human albumin N-terminus (Asp-Ala-His-Lys) prevents formation of copper-induced reactive oxygen species - Biochem. Biophys. Res. Commun. 284: 856-862. Go to original source...
    5. Beauchamp C. & Fridovich I. 1971: Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. - Anal. Biochem. 44: 276-287. Go to original source...
    6. Bloomquist J.R. 1996: Ion channels as targets for insecticides. - Annu. Rev. Entomol. 41: 163-190. Go to original source...
    7. Boutjagualt I., Hmimid F., Errami A., Bouharroud R., Qessaoui R., Etahiri S. & Benba J. 2022: Chemical composition and insecticidal effects of brown algae (Fucus spiralis) essential oil against Ceratitis capitata Wiedemann (Diptera: Tephritidae) pupae and adults. - Biocatal. Agric. Biotechnol. 40: 102308, 9 pp. Go to original source...
    8. Bradford M.M. 1976: A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. - Anal. Biochem. 72: 248-254. Go to original source...
    9. Bulgarini G., Bortolini S. & Maistrello L. 2021: Repellent activity of essential oils on adults of Halyomorpha halys (Heteroptera: Pentatomidae) in different physiological-behavioural phases. - J. Appl. Entomol. 145: 575-586. Go to original source...
    10. Chohan T., Chohan T., Zhou L., Yang Q., Min L. & Cao H. 2018: Repellency, toxicity, gene expression profiling and in silico studies to explore insecticidal potential of Melaleuca alternifolia essential oil against Myzus persicae. - Toxins 10(11): 425, 15 pp. Go to original source...
    11. Dambolena J.S., Zunino M.P., Herrera J.M., Pizzolitto R.P., Areco V.A. & Zygadlo J.A. 2016: Terpenes: Natural products for controlling insects of importance to human health - A structure-activity relationship study. - Psyche 2016: 4595823, 17 pp. Go to original source...
    12. De Medeiros M.D.G.F., Da Silva A.C., Citó A.M.D.G.L., Borges A.R., De Lima S.G., Lopes J.A.D. & Figueiredo R.C.B.Q. 2011: In vitro antileishmanial activity and cytotoxicity of essential oil from Lippia sidoides Cham. - Parasitol. Int. 60: 237-241. Go to original source...
    13. Doganlar O. & Doganlar Z.B. 2015: Responses of antioxidant enzymes and heat shock proteins in Drosophila to treatment with a pesticide mixture. - Arch. Biol. Sci. (Belgrade) 67: 869-876. Go to original source...
    14. Dutta M., Rajak P., Khatun S. & Roy S. 2017: Toxicity assessment of sodium fluoride in Drosophila melanogaster after chronic sub-lethal exposure. - Chemosphere 166: 255-266. Go to original source...
    15. Enan E. 2001: Insecticidal activity of essential oils: octopaminergic sites of action. - Comp. Biochem. Physiol. (C) 130: 325-337. Go to original source...
    16. Enan E.E. 2005a: Molecular and pharmacological analysis of an octopamine receptor from american cockroach and fruit fly in response to plant essential oils. - Arch. Insect Biochem. Physiol. 59: 161-171. Go to original source...
    17. Enan E.E. 2005b: Molecular response of Drosophila melanogaster tyramine receptor cascade to plant essential oils. - Insect Biochem. Mol. Biol. 35: 309-321. Go to original source...
    18. Fang S.M., Zhang Q., Zhang Y.L., Zhang G.Z., Zhang Z. & Yu Q.Y. 2021: Heat shock protein 70 family in response to multiple abiotic stresses in the silkworm. - Insects 12(10): 928, 13 pp. Go to original source...
    19. Farahani S., Bandani A.R., Alizadeh H., Goldansaz S.H. & Whyard S. 2020a: Differential expression of heat shock proteins and antioxidant enzymes in response to temperature, starvation, and parasitism in the Carob moth larvae, Ectomyelois ceratoniae (Lepidoptera: Pyralidae). - PLoS ONE 15(1): e0228104, 18 pp. Go to original source...
    20. Farahani S., Bandani A.R. & Amiri A. 2020b: Toxicity and repellency effects of three essential oils on two populations of Tetranychus urticae (Acari: Tetranychidae). - Persian J. Acarol. 9: 67-81.
    21. Felton G.W. & Summers C.B. 1995: Antioxidant systems in insects. - Arch. Insect Biochem. Physiol. 29: 187-197. Go to original source...
    22. Fridovich I. 1995: Superoxide radical and superoxide dismutases. - Annu. Rev. Biochem. 64: 97-112. Go to original source...
    23. Garcia D.A., Bujons J., Vale C. & Suñol C. 2006: Allosteric positive interaction of thymol with the GABAA receptor in primary cultures of mouse cortical neurons. - Neuropharmacology 50: 25-35. Go to original source...
    24. George D.G.M. & Gatehouse A.M.R. 2013: Oxidative stress enzymes in Busseola fusca. - Int. J. Curr. Microbiol. Appl. Sci. 2: 485-495.
    25. Gothilf S. 1984: Biology of Spectrobates ceratoniae on almonds in Israel. - Phytoparasitica 12: 77-87. Go to original source...
    26. Grieshop M.J., Flinn P.W. & Nechols J.R. 2006: Biological control of Indian meal moth (Lepidoptera: Pyralidae) on finished stored products using egg and larval parasitoids. - J. Econ. Entomol. 99: 1080-1084. Go to original source...
    27. Guleria S. & Tiku A.K. 2009: Botanicals in pest management: current status and future perspectives. In Peshin R. & Dhawan A.K. (eds): Integrated Pest Management, Innovation-Development Process. Springer, Dordrecht, pp. 317-329. Go to original source...
    28. Gupta S.C., Sharma A., Mishra M., Mishra R.K. & Chowdhuri D.K. 2010: Heat shock proteins in toxicology: how close and how far? - Life Sci. 86: 377-384. Go to original source...
    29. Guru P.N., Mridula D., Dukare A.S., Ghodki B.M., Paschapur A.U., Samal I., Nikhil Raj M., Padala V.K., Rajashekhar M & Subbanna A.R.N.S. 2022: A comprehensive review on advances in storage pest management: Current scenario and future prospects. - Front. Sustain. Food Syst. 6: 993341, 21 pp. Go to original source...
    30. Habig W., Pabst M.J. & Jakoby W.B. 1974: Glutathione-S-transferase. The first enzymatic step in mercapturic acid formation. - J. Biol. Chem. 249: 7130-7139. Go to original source...
    31. Halaouli S., Asther M., Sigoillot J.C., Hamdi M. & Lomascolo A. 2006: Fungal tyrosinases: new prospects in molecular characteristics, bioengineering and biotechnological applications. - J. Appl. Microbiol. 100: 219-232. Go to original source...
    32. Isman M.B. 2006: Botanical insecticides, deterrents, and repellents in modern agriculture and an increasingly regulated world. - Annu. Rev. Entomol. 51: 45-66. Go to original source...
    33. Izadi H., Mohammadzadeh M. & Mehrabian M. 2019: Changes in biochemical contents and survival rates of two stored product moths under different thermal regimes. - J. Therm. Biol. 80: 7-15. Go to original source...
    34. Jankowska M., Rogalska J., Wyszkowska J. & Stankiewicz M. 2017: Molecular targets for components of essential oils in the insect nervous system - a review. - Molecules 23: 34, 20 pp. Go to original source...
    35. Jena K., Kar P.K., Kausar Z. & Babu C.S. 2013: Effects of temperature on modulation of oxidative stress and antioxidant defenses in testes of tropical tasar silkworm Antheraea mylitta. - J. Therm. Biol. 38: 199-204. Go to original source...
    36. Jindal V., Dhaliwal G.S. & Koul O. 2013: Pest management in 21st century: Roadmap for future. - Biopestic. Int. 9: 1-22.
    37. Khatun S., Rajak P., Dutta M. & Roy S. 2017: Sodium fluoride adversely affects ovarian development and reproduction in Drosophila melanogaster. - Chemosphere 186: 51-61. Go to original source...
    38. Kostyukovsky M., Rafaeli A., Gileadi C., Demchenko N. & Shaaya E. 2002: Activation of octopaminergic receptors by essential oil constituents isolated from aromatic plants: possible mode of action against insect pests. - Pest Manag. Sci. 58: 1101-1106. Go to original source...
    39. Koul O., Walia S. & Dhaliwal G.S. 2008: Essential oils as green pesticides: potential and constraints. - Biopestic. Int. 4: 63-84.
    40. Krishnan N., Kodrķk D., K³udkiewicz B. & Sehnal F. 2009: Glutathione-ascorbic acid redox cycle and thioredoxin reductase activity in the digestive tract of Leptinotarsa decemlineata (Say). - Insect Biochem. Mol. Biol. 39: 180-188. Go to original source...
    41. Kumar K.B. & Khan P.A. 1982: Peroxidase and polyphenol oxidase in excised ragi (Eleusine corocana cv PR 202) leaves during senescence. - Indian J. Exp. Biol. 20: 412-416.
    42. Lazarevię J., Jevremovię S., Kostię I., Kostię M., Vuleta A., Manita¹evię Jovanovię S. & ©e¹lija Jovanovię D. 2020: Toxic, oviposition deterrent and oxidative stress effects of Thymus vulgaris essential oil against Acanthoscelides obtectus. - Insects 11: 563, 19 pp. Go to original source...
    43. Lee S., Tsao R., Peterson C. & Coats J.R. 1997: Insecticidal activity of monoterpenoids to western corn rootworm (Coleoptera: Chrysomelidae), twospotted spider mite (Acari: Tetranychidae), and house fly (Diptera: Muscidae). - J. Econ. Entomol. 90: 883-892. Go to original source...
    44. LeOra Software 1994: POLO-PC: A User's Guide to Probit or Logit Analysis. Leora Software, Berkeley, CA, 28 pp.
    45. Liao M., Xiao J.J., Zhou L.J., Yao X., Tang F., Hua R.M. & Cao H.Q. 2017: Chemical composition, insecticidal and biochemical effects of Melaleuca alternifolia essential oil on the Helicoverpa armigera. - J. Appl. Entomol. 141: 721-728. Go to original source...
    46. Livak K.J. & Schmittgen T.D. 2001: Analysis of relative gene expression data using real-time quantitative PCR and the 2- ΔΔCT method. - Methods 25: 402-408. Go to original source...
    47. Lukasik I., Golawska S., Wojcicka A. & Golawski A. 2011: Effect of host plants on antioxidant system of pea aphid Acyrthosiphon pisum. - Bull. Insectol. 64: 153-158.
    48. Mansour S.A., Messeha S.S. & El-Gengaihi S.E. 2000: Botanical biocides. 4. Mosquitocidal activity of certain Thymus capitatus constituents. - J. Nat. Toxins 9: 49-62.
    49. Mayer A.M. 1986: Polyphenol oxidases in plants-recent progress. - Phytochemistry 26: 11-20. Go to original source...
    50. Mediouni J. & Dhouibi M.H. 2007: Mass-rearing and field performance of irradiated carob moth Ectomyelois ceratoniae in Tunisia. In Vreysen M.J.B., Robinson A.S. & Hendrichs J. (eds): Area-Wide Control of Insect Pests. Springer, Dordrecht, pp. 265- 273. Go to original source...
    51. Miresmailli S., Bradbury R. & Isman M.B. 2006: Comparative toxicity of Rosmarinus officinalis L. essential oil and blends of its major constituents against Tetranychus urticae Koch (Acari: Tetranychidae) on two different host plants. - Pest Manag. Sci. 62: 366-371. Go to original source...
    52. Mohammadi B., Haeseler G., Leuwer M., Dengler R., Krampfl K. & Bufler J. 2001: Structural requirements of phenol derivatives for direct activation of chloride currents via GABAA receptors. - Eur. J. Pharmacol. 421: 85-91. Go to original source...
    53. Mohapatra D., Kar A. & Giri S.K. 2015: Insect pest management in stored pulses: an overview. - Food Bioprocess Technol. 8: 239-265. Go to original source...
    54. Moura E.D.S., Faroni L.R.D.A., Zanuncio J.C., Heleno F.F. & Prates L.H.F. 2019: Insecticidal activity of Vanillosmopsis arborea essential oil and of its major constituent α-bisabolol against Callosobruchus maculatus (Coleoptera: Chrysomelidae). - Sci. Rep. 9: 3723, 8 pp. Go to original source...
    55. Nay J.E. 2006: Biology, Ecology, and Management of the Carob Moth, Ectomyelois ceratoniae (Zeller) (Lepidoptera: Pyralidae), a Pest of Dates, Phoenix dactylifera L., in Southern California. University of California, Riverside, 556 pp.
    56. Ndomo A.F., Tapondjou L.A., Ngamo L.T. & Hance T. 2010: Insecticidal activities of essential oil of Callistemon viminalis applied as fumigant and powder against two bruchids. - J. Appl. Entomol. 134: 333-341. Go to original source...
    57. Papachristos D.P. & Stamopoulos D.C. 2004: Fumigant toxicity of three essential oils on the eggs of Acanthoscelides obtectus (Say) (Coleoptera: Bruchidae). - J. Stored Prod. Res. 40: 517-525. Go to original source...
    58. Pavela R. & Benelli G. 2016: Essential oils as ecofriendly biopesticides? Challenges and constraints. - Trends Plant Sci. 21: 1000-1007. Go to original source...
    59. Piner P. & Üner N. 2012: Oxidative and apoptotic effects of lambda-cyhalothrin modulated by piperonyl butoxide in the liver of Oreochromis niloticus. - Environ. Toxicol. Pharmacol. 33: 414-420. Go to original source...
    60. Pinho A.I., Wallau G.L., Nunes M.E.M., Leite N.F., Tintino S.R., da Cruz L.C., da Cunha F.A.B., da Costa J.G., Melo Coutinho D.H., Posser T. & Franco J.L. 2014: Fumigant activity of the Psidium guajava var. pomifera (Myrtaceae) essential oil in Drosophila melanogaster by means of oxidative stress. - Oxid. Med. Cell. Longev. 2014: 696785, 8 pp. Go to original source...
    61. Priestley C.M., Williamson E.M., Wafford K.A. & Sattelle D.B. 2003: Thymol, a constituent of thyme essential oil, is a positive allosteric modulator of human GABAA receptors and a homo-oligomeric GABA receptor from Drosophila melanogaster. - Br. J. Pharmacol. 140: 1363-1372. Go to original source...
    62. Rahimi V., Hajizadeh J., Zibaee A. & Jalali Sendi J. 2018: Effect of Polygonum persicaria (Polygonales: Polygonaceae) extracted agglutinin on life table and antioxidant responses in Helicoverpa armigera (Lepidoptera: Noctuidae) larvae. - J. Econ. Entomol. 111: 662-671. Go to original source...
    63. Rana V.S., Das M. & Blazquez M.A. 2016: Essential oil yield, chemical composition, and total citral content of nine cultivars of Cymbopogon species from Western India. - J. Herbs Spices Med. Plants 22: 289-299. Go to original source...
    64. Ryan M.F. & Byrne O. 1988: Plant-insect coevolution and inhibition of acetylcholinesterase. - J. Chem. Ecol. 14: 1965-1975. Go to original source...
    65. Sahebzadeh N. & Lau W.H. 2017: Expression of heat-shock protein genes in Apis mellifera meda (Hymenoptera: Apidae) after exposure to monoterpenoids and infestation by Varroa destructor mites (Acari: Varroidae). - Eur. J. Entomol. 114: 195-202. Go to original source...
    66. Sarkar S., Podder S. & Roy S. 2015: Flubendiamide-induced HSP70 expression in transgenic Drosophila melanogaster (hsp70-lacZ). - Curr. Sci. 10: 2044-2050.
    67. Schulte P.M. 2014: What is environmental stress? Insights from fish living in a variable environment. - J. Exp. Biol. 217: 23-34. Go to original source...
    68. Shahriari M., Zibaee A., Sahebzadeh N. & Shamakhi L. 2018: Effects of α-pinene, trans-anethole, and thymol as the essential oil constituents on antioxidant system and acetylcholine esterase of Ephestia kuehniella Zeller (Lepidoptera: Pyralidae). - Pestic. Biochem. Physiol. 150: 40-47. Go to original source...
    69. Simmonds M.S.J., Manlove J.D., Blaney W.M. & Khambay B.P.S. 2002: Effects of selected botanical insecticides on the behaviour and mortality of the glasshouse whitefly Trialeurodes vaporariorum and the parasitoid Encarsia formosa. - Entomol. Exp. Appl. 102: 39-47. Go to original source...
    70. Stejskal V. 2015: Pest prevention during storage, transportation and handling of stored products. - Integ. Prot. Stored Prod. 111: 171-176.
    71. Tong F., Gross A.D., Dolan M.C. & Coats J.R. 2013: The phenolic monoterpenoid carvacrol inhibits the binding of nicotine to the housefly nicotinic acetylcholine receptor. - Pest Manag. Sci. 69: 775-780. Go to original source...
    72. Wang Y., Oberley L.W. & Murhammer D.W. 2001: Evidence of oxidative stress following the viral infection of two lepidopteran insect cell lines. - Free Radic. Biol. Med. 31: 1448-1455. Go to original source...
    73. Warner R.L., Barnes M.M., Laird E.F. & Lanham M.D. 1990: Chemical control of carob moth, Ectomyelois ceratoniae (Lepidoptera: Pyralidae), and various nitidulid beetles (Coleoptera) on 'Deglet Noor' dates in California. - J. Econ. Entomol. 83: 2357-2361. Go to original source...
    74. Yu Q.Y., Fang S.M., Zuo W.D., Dai F.Y., Zhang Z. & Lu C. 2011: Effect of organophosphate phoxim exposure on certain oxidative stress biomarkers in the silkworm. - J. Econ. Entomol. 104: 101-106. Go to original source...
    75. Zhao L. & Jones W.A. 2012: Expression of heat shock protein genes in insect stress responses. - Invertebr. Surviv. J. 9: 93-101.
    76. Ziaee M., Moharramipour S. & Mohsenifar A. 2014: Toxicity of Carum copticum essential oil-loaded nanogel against Sitophilus granarius and Tribolium confusum. - J. Appl. Entomol. 138: 763-771. Go to original source...
    77. Zribi I., Bleton J., Moussa F. & Abderrabba M. 2019: GC-MS analysis of the volatile profile and the essential oil compositions of Tunisian Borago officinalis L.: Regional locality and organ dependency. - Ind. Crops Prod. 129: 290-292. Go to original source...

    This is an open access article distributed under the terms of the Creative Commons Attribution 4.0 International License (CC BY 4.0), which permits use, distribution, and reproduction in any medium, provided the original publication is properly cited. No use, distribution or reproduction is permitted which does not comply with these terms.


    Return to the content