Oxidative effects of boric acid on different developmental stages of Drosophila melanogaster Meigen, 1830 (Diptera: Drosophilidae)

Abstract

Synthetic organic insecticides are widely used to combat agricultural pests. Boric acid has a great importance in pest management because it has less toxic effect on non-target organisms compared to other organic chemical insecticides. For this purpose, the fruit fly Drosophila melanogaster Meigen, 1830 (Diptera: Drosophilidae) was reared from first stage larvae on an artificial diet containing boric acid at 10, 100, 200 or 300 mg/L to adult stage. The effect of boric acid on important oxidative stress indicators such as lipid peroxidation product of malondialdehyde contents (MDA) and protein oxidation products of protein carbonyl contents (PCO) and detoxification enzyme activity of glutathione S-transferase (GST) in the third stage larvae, pupae, adults and eggs of D. melanogaster were investigated. All boric acid concentrations significantly increased MDA content in third stage larva. When the adults from the larvae reared on 300 mg/L of dietary BA were also fed with high BA concentration for a 10-day period, MDA and PCO contents of male and female adults were considerably went up in comparison to control. MDA and PCO content in the eggs of these females were hugely increased. The rise in PCO content of the eggs was 31-fold relative to control. Our results indicate that BA feeding at high concentrations in all developmental stages of D. melanogaster is more effective on oxidative stress indicators and detoxification enzyme.

Keywords

• Boric acid,Drosophila melanogaster,oxidative stress

Drosophila melanogaster Meigen, 1830 (Diptera: Drosophilidae)’in farklı gelişme dönemleri üzerine Borik asitin oksidatif etkileri

Öz

Tarımsal zararlılar ile mücadelede sentetik organik insektisitler yoğun olarak kullanılmaktadır. Borik asit organik kimyasal insektisitlere göre hedef olmayan organizmalara karşı daha düşük toksisiteye sahip olması nedeniyle önem taşımaktadır. Bu amaçla çalışmamızda meyve sineği Drosophila melanogaster Meigen,1830 (Diptera: Drosophilidae)'in birinci dönem larvaları borik asitin farklı konsantrasyonlarını (10, 100, 200 ve 300 mg/L) içeren yapay besinler ile yetiştirilmiştir. Drosophila melanogaster' in üçüncü dönem larva, pupa, ergin dönemleri ve yumurtalarında oksidatif stresin önemli indikatörleri olan lipid peroksidasyonu ürünü malondialdehid (MDA) ve protein oksidasyon ürünü protein karbonil miktarları (PCO) ile detoksifikasyon enzimi glutatyon-S-transferaz (GST) aktivitesi üzerine etkisi incelenmiştir. Borik asitin denenen konsantrasyonlarını içeren yapay besinler ile yetiştirilen D. melanogaster’ in üçüncü dönem larvalarının MDA miktarı önemli derecede artmıştır. Yüksek borik asit ile yetiştirilen erginlerin 10 gün süreyle 300 mg/L borik asit içeren besin ile beslenilmesi sonucunda kontrol besinine göre dişi ve erkek bireylerde MDA ve PCO miktarları önemli derecede artmıştır. Bu dişilerin yumurtalarındaki MDA, PCO miktarları ve GST aktivitesi önemli derecede artarken, PCO miktarındaki artış yaklaşık 31 katı oranında olmuştur. Sonuçlarımız, borik asitin yüksek konsantrasyonlarıyla beslenen D. melanogaster’in tüm gelişme dönemlerindeki oksidatif stres indikatörleri ve detoksifikasyon enzimi üzerine oldukça etkili olduğunu göstermiştir.

Anahtar Kelimeler

• Borik asit,Drosophila melanogaster,oksidatif stres

References

1. Ahmad, S., 1995. Oxidative stress from environmental pollutants. Archives of Insect Biochemistry and Physiology, 29: 135-157.
2. Ali, A., R. D. Xue & D. R. Barnard, 2006. Effects of sublethal exposure to boric acid sugar bait on adult survival, host-seeking, blood feeding behavior, and reproduction of Stegomyia albopicta. Journal of the American Mosquito Control, 22: 464-468.
3. Anonymous, 2004. Avrupa Perakendecileri Ürün Çalışma Grubu’nun İyi Tarım Teknikleri Uygulamaları (EUREPGAP). Akdeniz Yaş Meyve Sebze İhracatçıları Birliği, ARGE Dış İlişkileri Şube Müdürlüğü, 36 s.
4. Ay, R. & S. Yorulmaz, 2008. "The evaluation of the esterase and glutathion s-transferase enzymes in two-spotted spider mite Tetranychus urticae Koch (Acarina: Tetranychidae) selected with bifenthrin, 419-424". Integrative Acarology Proceedings on the 6th European Association of Acarologists Congress (21-25 July, France) Proceedings, 491 pp.
5. Barbehenn, R. V. & J. Stannard, 2004. Antioxidant defense of the midgut epithelium by the peritrophic envelope in caterpillars. Journal of Insect Physiology, 50: 783-790.
6. Büyükgüzel, K. & E. İçen, 2004. Effects of gyrase inhibitors on the total protein content of Pimpla turionellae L. reared on an artificial diet. Journal of Entomological Science, 39 (1): 108-116.
7. Büyükgüzel, K., 2006. Malathion-induced oxidative stress in a parasitoid wasp: Effect on adult emergence, longevity, fecundity, oxidative and antioxidative response of the Pimpla turionellae. Journal of Economic Entomology, 99: 1225-1234.
8. Büyükgüzel, E. & Y. Kalender, 2007. Penicillin-induced oxidative stress: effects on antioxidative response of midgut tissues in larval instars of G. mellonella. Journal of Economic Entomology, 100: 1533-1541.

9. Büyükgüzel, E., 2013. Protein oksidasyonun biyokimyasal ve moleküler mekanizması. Karaelmas Fen ve Mühendislik Dergisi, 3 (1): 40-51.
10. Büyükgüzel, E., K. Büyükgüzel, E. Erdem, Z. Adamski, P. Marciniak, K. Ziemnicki, E. Ventrella, L. Scrano & S.A. Bufo, 2013. The influence of dietary α-solanine on the waxmoth Galleria mellonella L. Archives of Insect Biochemistry and Physiology, 89 (4):1-10.
11. Büyükgüzel, E. & R. Akın, 2014. Redoksa duyarlı sinyal iletiminde reaktif oksijen türlerinin (ROT) rolü. Karaelmas Fen ve Mühendislik Dergisi, 4 (2): 70-81.
12. Büyükgüzel, E. & S. Kayaoğlu, 2014. Niklozamidin Galleria mellonella L. (Lepidoptera: Pyralidae)’nın bazı biyolojik ve fizyolojik özelliklerine etkisi. Türkiye Entomoloji Dergisi, 38 (1): 83-99.
13. Cisneros, J., J. A. Perez, D.I. Penagos, D. Goulson, Caballero, D. R. Cave & T. Wiliams, 2002. Formulation of a nucleopolyhedrovirus with boric acid for control of Spodoptera frugiperda in maize. Biological Control, 23: 87-95.
14. Cochran, D. G., 1995. Toxic effects of boric acid on the German cockroach. Experientia, 51: 561-563.
15. Cohen, A. C. & P. Crittenden, 2004. Deliberately added and “cryptic” antioxidants in three artificial diets for insects. Journal of Economic Entomology, 97: 265- 272.
16. Damien, C., V. H. Chantal, S. Pirouz, F. H. Zerimech, J. Laurence & M. H. Jean, 2004. Cellular impact of metal trace elements in terricolous lichen Diploschistes muscorum (Scop.) R. Sant-identification of oxidative stress biomarkers. Water Air Soil Pollution, 152: 55-69.
17. Dandapat, J., G. B. N. Chainy & K. J. Rao, 2003. Improved post-larval production in giant prawn, Macrobrachium rosenbergii through modulation of antioxidant defense system by dietary vitamin-E. Indian Journal of Biotechnology, 2 (2): 195-202.
18. De Man, W., A. De Loof, T. Bries & R. Huybrecths, 1981. Effect of absisic acid on vitellogenesis in Sarcophoga bulata. Entomologia Experimentalis et Applicata, 29: 259-267.
19. Durmuş, Y. & K. Büyükgüzel, 2008. Biological and immune response of Galleria mellonella L. (Lepidoptera: Pyralidae) to sodium tetraborate. Journal of Economic Entomology, 101: 777-783.
20. EFSA, 2004. Opinion of the scientific panel on dietetic products, nutrition and allergies on a request from the commission related to the tolerable upper intake level of boron (sodium borate and boric acid) (Request N_ EFSAQ- 2003-018). European Food Safety Authority Journal, 80: 1-22.
21. Erdem, M., C. Küçük, E. Büyükgüzel & K. Büyükgüzel, 2013. "The effect of gemifloxacin on hemoplymph oxidative and antioxıdative response of Galleria mellonella L. (Lepidoptera: Pyralidae), 168". Drug Discovery and Therapy World Congress (3-6 June, USA) Proceedings, 226 pp.
22. Erdem, M. & E. Büyükgüzel, 2015. The effects of xanthotoxin on the biology and biochemistry of Galleria mellonella L. (Lepidoptera: Pyralidae). Archives of Insect Biochemistry and Physiology, 89 (4): 193-203.
23. Espinoza-Navarro, O., H. Rodrignez, M. Rodrignez, E. Silva & A. Luque, 2009. Alteraton of the reproductive patternsin Drosophila melanogaster by Effect of high concentrations of Boron on in vitro cultured medium. International Journal of Morphology, 27 (3): 765-770.
24. Evans, P., L. Lyras & B. Halliwel, 1999. Measurement of protein carbonyls in human brain tissue. Methods in Enzymology, 300: 145-156.
25. Fışkın, K., S. Kandemir, D. Hamamcı, E. Yeşilada & A. N. Bozcuk, 1994. Age-related changes in catalase, glutathione reductase activities, the amount of glutathione in total body of Oregon and vestigial Drosophila melanogaster. Archives of Gerontology and Geriatrics, 4: 85-90.
26. Ford, D. J., T. L. Propst, E. L. Stover, P. L. Strong & F. J. Murray,1998. Adverse reproductive and developmental effects in xenopus from insufficient boron. Biological Trace Element Research, 66: 237-259.
27. Gelbič, I. & J. Šula, 1990. Ovicidal and biochemical effects of hempa and a nucleoside analogue on Pyrrhocoris apterus (L.) (Het., Pyrrhocoridae). Journal Applied Entomology and Zoology,109: 401-409.
28. Giordano, G., Z. Afsharinejad, M. Guizzetti, A. Vitalone, T. J. Kavanagh & L. G. Costa, 2007. Organophosphorus insecticides chlorpyrifos and diazinon and oxidative stress in neuronal cells in a genetic model of glutathione deficiency. Toxicology and Applied Pharmacology, 219:181-189.
29. Gore, J. C., L. Zurek, R. G. Santangelo, S. M. Stringham, D. W. Watson & C. Schal, 2004. Water solutions of boric acid and sugar for management of German cocroach populations in livestock production system. Journal of Economic Entomology, 97: 715-720.
30. Gülbahar, Ö., 2007. Protein oksidasyonun mekanizması, önemi ve yaşlılıkla ilgisi. Turkish Journal of Geriatrics, 10: 43-48.
31. Habes, D., S. Morakchi, N. Aribi, J. P. Farine & N. Soltani, 2006. Boric acid toxicity to the German cockroach, Blattella germanica: Alterations in midgut structure, and acetylcholinestrease and glutathione S-transferase activity. Pesticide Biochemistry and Physiology, 84: 17-24.
32. Habig, W. H., M. J. Pabst & W. B. Jakoby, 1974. Glutathione-s-transferases: the first enzymatic step in mercapturic acid formation. Journal of Biological Chemistry, 249: 7130-7139.
33. Hadim, N., 2008. Pamuk Yaprak Kurdu Spodoptera littoralis (Boisduval) (Lepidoptera: Noctuidae)’te İnsektisitlere Karşı Oluşan Direncin Biyokimyasal ve Moleküler Karakterizasyonu. Ankara Üniversitesi Biyoteknoloji Enstitüsü, (Basılmamış) Doktora Tezi, Ankara, 146 s.
34. Hermes-Lima, M. & T. Zenteno-Savín, 2002. Animal response to drastic changes in oxygen availability and physiological oxidative stress. Comparative Biochemistry and Physiology Part C: Toxicology, 133: 537-56.
35. Hyršl, P., E. Büyükgüzel & K. Büyükgüzel, 2007. The effects of boric acid-induced oxidative stress on antioxidant enzymes and survivorship in Galleria mellonella. Archives of Insect Biochemistry and Physiology, 66: 23-31.
36. Jain, S. K. & S. N. Levine, 1995. Elevated lipid peroxidation and Vitamin E quinine levels in heart ventricles of streptozoticin-treated diabetic rats. Free Radical Biology and Medicine, 18: 337-341.
37. Jordens, R. G., M. D. Berry, C. Gillott & A. A. Boulton, 1999. Prolongation of life in an experimental model of ageing in Drosophila melanogaster. Neurochemical Research, 24 (2): 227-233.
38. Jolly, W. L., 1991. Modern Inorganic Chemistry. 2nd Ed, McGraw-Hill, New York, 655 pp.
39. Kaya, B., H. Çetin, S. Kocaoğlu & E. Demir, 2009. Farklı Oranlardaki Sentetik Pyretroit ve Piperonyl Butoxide (PBO) Karışımlarının Drosophila melanogaster Üzerindeki İnsektisidal ve Genotoksik Etkilerinin Araştırılması. Tübitak, TBAG, 107T189, 49 s.
40. Keser, D., 2010. Aspirin ve Asetaldehitin Drosophila melanogaster’in Bazı Gelişimsel Özellikleri Üzerine Etkileri. Kocaeli Üniversitesi Fen Bilimleri Enstitüsü Biyoloji Anabilim Dalı, (Basılmamış) Yüksek Lisans Tezi, Kocaeli, 68 s.
41. Kilani-Morakchi, S., N. Aribi, J. P. Farine, C. Everaerts & N. Soltani, 2005. Effets de l’acide borique sur les profiles d’hydrocarbures cuticulaires chez un insecte à intérêt médical, Blattella germanica (Dictyoptera: Blattellidae). Journal of the Algerian Chemical Society, 15 (2): 225-231.
42. Krishnan, N. & D. Kodrik, 2006. Antioxidant enzymes in Spodoptera littoralis (Boisduval): Are they enhanced to protect gut tissues during oxidative stress? Journal of Insect Physiology, 52: 11-20.
43. Lagadic, L., A. Cuany, J. B. Bergé & M. Echaubard, 1993. Purification and Partial Characterization of Glutathione S-transferase from insecticide-resistant and lindane-inducced susceptible Spodoptera littoralis (Boisd.) larvae. Insect Biochemistry and Molecular Biology, 23 (4): 467-474.
44. Le Bourg, E., N. Minois, P. Bullens & P. Baret, 2000. A mild stress due to hypergravity exposure at young age increases longevity in Drosophila melanogaster males. Biogerontology, 1 (2): 145-155.
45. Lesch, C., A. Goto, M. Lindgren, G. Bidla, M. S. Dushay & U. Theopold, 2007. A role for Hemolectin in coagulation and immunity in Drosophila melanogaster. Developmental and Comparative Immunology, 31: 1255-1263.
46. Levine, R. L., J. A. Williams, E. R. Stadtman & E. Shacter, 1994. Carbonyl assays for determination of oxidatively modified proteins. Methods in Enzymology, 233: 346-357.
47. Li, Y. M., H. Y. E. Chan, X. Q. Yao, Y. Huang, & Z. Y. Chen, 2008. Green tea catechins and broccoli reduve fat-induced mortality in Drosophila melanogaster. Journal of Nutritional Biochemistry, 19: 376-383.
48. Lowry, O. H., N. I. Rosebroug, A. L. Farr & R. J. Randall, 1951. Protein measurement with the Folin phenol reagent. Journal of Biological Chemistry, 19: 265.
49. Lozinsky, O. V., 2013. Aconitase and developmental end points as early indicators of cellular toxicity induced by xenobiotics in Drosophila melanogaster. Iranian Journal of Toxicology, 8 (24): 998-1003.
50. Lozinsky, O. V., O. V. Lushchak, N. I. Kryshchuk, N. Y. Shchypanska, A. H. Riabkina, S. V. Skarbek, I. V. Maksymiv, J. M. Storey, K. B. Storey & V. I. Lushchak, 2012. S-Nitrosoglutathione-induced toxicity in Drosophila melanogaster: Delayed pupation and induced mild oxidative/nitrosative stress in eclosed flies. Comparative Biochemistry and Physiology Part A: Molecular and Integrative Physiology, 64 (80): 162- 70.
51. Maistrello, L., G. Henderson & R. A. Laine, 2002. Comparative effects of vetiver oil, nootkatone and disodium octaborate tetrahydrate on Coptotermes formosanus and its symbiotic fauna. Pest Management Science, 59: 58-68.
52. Massie, H., 1994. Effect of dietary boron on the aging process. Environmental Health Perspectives, 102 (7): 45-48.
53. Missirlis, F., S. Rahlfs, N. Dimopoulos, H. Bauer, K. Becker, A. Hilliker & J. P. Phillips, 2003. A putative glutathione peroxidase of Drosophila encodes thioredoxin peroxidase that provides resistance against oxidative stress but fails to complement a lack of catalase activity. Journal of Biological Chemistry, 384 (3): 463-472.
54. Otitoju, O. & I. N. E. Onwurah, 2007. Glutathione S-transferase (GST) activity as a biomarker in ecological risk assessment of pesticide contaminated environment. African Journal of Biotechnology, 6: 1455-1459.
55. Özata, L., 2006. Bazı Tekstil Boyalarının Drosophila melanogaster Üzerine Toksik Ve Genotoksik Etkilerinin Araştırılması. İnönü Üniversitesi Fen Bilimleri Enstitüsü, (Basılmamış) Doktora Tezi, Malatya, 87 s.
56. Park, M., Q. Li, N. Shcheynikov, W. Zeng & S. Muallern, 2004. NaBC1 is a ubiquitous electrogenic Na1-coupled borate transporter essential for cellular boron homeostasis and cell growth and proliferation. Molecular Cell,16: 331-341.
57. Partridge, L., A. Hoffman & S. Jones, 1987. Male size and mating success in Drosophila melanogaster and Drosophila pseudoobscura under field conditions. Animal Behaviour, 35: 468-476.
58. Peric-Mataruga, V., D. Blagojevic, M. B. Spasic, J. Ivanovic & M. Jankovic-Hladni, 1997. Effect of the host plant on the antioxidative defence in the midgut of Lymantria dispar L. caterpillars of different population origins. Journal of Insect Physiology, 43: 101-106.
59. Rakotondravelo, M. L., T. D. Anderson, R. E. Charlton & K. Y. Zhu, 2006. Sublethal Effects of Three Pesticides on Activities of Selected Target and Detoxification Enzymes in the Aquatic Midge, Chironomus tentans (Diptera: Chironomidae). Archives of Environmental Contamination and Toxicology, 51: 360-366.
60. Rowe, R. I., C. Bouzan, S. Nabili & C. D. Eckart, 1998. The response of trout and zebrafish embryos to low and high boron concentrations is u-shaped. Biological Trace Element Research, 66: 261-270.
61. Sarıkaya, R., K. Erciyas, A. F. Erciyas, S. Ay, M. İ. Kara & U. Sezer, 2012. Antioksidanların (Bor ve Thymoqinone) Antigenotoksik Etkilerinin Drosophila Somatik Mutasyon ve Rekombinasyon Testi ile Araştırılması. Tübitak, Araştırma Projesi, 210T159, 38 s.
62. Scott, J. G., D. G. Cochran & B. D. Siegfried, 1990. Insecticide toxicity, synergism and resistance in the German cockroach (Dictyoptera: Blattellidae). Journal of Economic Entomology, 83: 1698-1703.
63. SPSS, 1997. User’s Manual, Version 10. SPSS Inc., Chicago, IL.
64. Taşkın, V., K. Küçükakyüz, T. Arslan, B. Çöl & B. Taşkın Göçmen, 2007. The biochemical basis of insecticide resistance and determination of esterase enzyme patterns by using PAGE in field collected populations of Drosophila melanogaster from Muğla province of Turkey. Journal of Cell and Molecular Biology, 6 (1): 31-40.
65. Toba, G. & T. Aigaki, 2000. Disruption of the microsomal glutathione S-transferase-like gene reduces life span of Drosophila melanogaster. Gene, 253 (2): 179-187.
66. Uysal, H. & T. Şişman, 2003. Genetik Laboratuvar Kılavuzu. Atatürk Üniversitesi Fen Fakültesi, Biyoloji Bölümü Yayını, Erzurum.
67. Vasseur, P. & C. Leguille, 2004. Defense systems of benthic invertebrates in response to environmental stressors. Environmental Toxicology, 19: 433-436.
68. Vontas, J. G., A. A. Enayati, G. J. Small & J. Hemingway, 2000. A simple biochemical assay for glutathione s-transferase activity and its possible field application for screening glutathione s-transferase- based insecticide resistance. Pesticide Biochemistry and Physiology, 68: 184-192.
69. Vontas, J. G., G. J. Small & J. Hemingway, 2001. Glutathione S-transferases as antioxidant defence agents confer pyrethroid resistance in Nilaparvata lugens. Biochemical Journal, 357: 65-72.
70. Vuran, E., M. Erdem, E. Büyükgüzel & K. Büyükgüzel, 2013. "The effect of Ornidazole on biological and biochemical parameters of Galleria mellonella L., 153". Drug Discovery and Therapy World Congress (3-6 June, USA) Proceedings, 226 pp.
71. Wang, Y., L. W. Oberley & D. W. Murhammer, 2001. Evidence of oxidative stres following the viral infection of two lepidopteran insect cell lines. Free Radical Biology and Medicine, 31: 1448-1455.
72. Wu, G. & T. Miyata, 2005. Susceptibilities to methamidophos and enzymatic characteristics in 18 species of pest insects and their natural enemies in crucifer vegetable crops. Pesticide Biochemistry and Physiology, 82: 79-93.
73. Xue, R. D. & D. R. Barnard, 2003. Boric acid bait kills adult mosquitoes (Diptera: Culicidae). Journal of Economic Entomology, 96:1559-1562.
74. Xue, R. D., D. L. Kline, A. Ali & D. R. Branard, 2006. Application of boric acid baits to plant foliage for adult mosquito control. Journal of the American Mosquito Control, 22: 497-500.
75. Yang, L. K., H. N. Nigg, S. Fraser, E. Burns & S. E. Simpson, 2000. Midgut proteinase types and sodium tetraborate effects on midgut proteinase activities of female Anastrepha suspensa (Diptera: Tephritidae). Annals of the Entomological Society of America, 93: 602-609.
76. Yeşilada, E. & A. N. Bozcuk, 1995. The effects of ABA and kinetin on the fecundity of Drosophila melanogaster. Turkish Journal of Biology, 19: 37-44.
77. Yüzüak, H., 2008. Yaşlanma Sürecinde Pankreas Dokusunda NOX, MDA, GSH Düzeyleri ve Melatoninin Etkisi. Gazi Üniversitesi Sağlık Bilimleri Enstitüsü Fizyoloji Anabilim Dalı, (Basılmamış) Yüksek Lisans Tezi, Ankara, 95 s.