Hyphantria cunea granulovirus tarafından enfekte edilen Hyphantria cunea (Drury,1773) (Lepidoptera: Arctiidae) larvalarının hemosit konsantrasyonu ve antioksidan enzim aktivitelerine bitki fenolik bileşiklerinin etkisi

Öz

Bu çalışmanın amacı, dört bitkide (elma, dut, erik ve ceviz) bulunan fenolik maddelerin Hyphantria cunea granulovirus ile enfekte ve enfekte olmamış Hyphantria cunea (Drury, 1773) (Lepidoptera: Arctiidae) larvalarının hemosit konsantrasyonları ve antioksidan enzim aktivitesine olan etkilerini belirlemekti. Bu çalışmada kullanılan bitkiler Bafra, Samsun, Türkiye’de 2019 yılında toplandı. Bu bitkilerin yapraklarının fenolik konsantrasyonları belirlendi. Daha sonra, bu fenoliğin enfekte ve enfekte olmayan larvaların hemosit konsantrasyonlarına ve antioksidan enzim aktivitesine olan etkisi belirlendi. Tüm grupların hemosit konsantrasyonlarının virüs enfeksiyonu ile arttığı belirlendi. Viral enfeksiyon sonucu tüm gruplarda malondialdehit konsantrasyonu azaldı. Hem enfekte hem de enfekte olmayan larvalar arasında en yüksek süperoksit dismutaz ve katalaz aktiviteleri klorojenik asit konsantrasyonunun en yüksek olduğu erik gruplarında iken, en düşük glutatyon peroksidaz aktivitesi de bu gruplardaydı. Bütün bunlar, konukçu bitkilerin farklı fenolik konsantrasyonlarının H. cunea larvalarının hemosit konsantrasyonlarını ve antioksidan enzim aktivitesini etkilediğini göstermiştir.

Anahtar Kelimeler

• Antioksidan aktivite
• granulovirüs
• hemosit
• Hyphantria cunea
• fenolik bileşikler

Effect of plant phenolic compounds on the hemocyte concentration and antioxidant enzyme activity in Hyphantria cunea (Drury, 1773) (Lepidoptera: Arctiidae) larvae infected by Hyphantria cunea granulovirus

Abstract

The aim of this study was to determine the effects of phenolic substances in different plants (mulberry, apple, walnut and plum) on hemocyte counts and antioxidant enzyme activities of Hyphantria cunea larvae infected with Hyphantria cunea granulovirus (HycuGV) and uninfected. In the study, the phenolic contents of plant materials were firstly determined. Then, the effects of these ingredients on hemocyte counts and antioxidant enzyme activities of infected and uninfected larvae were determined. As a result of the study, the hemocyte counts of all groups increased with the infection was determined. In enzyme activity, the phenoloxidase (PO) activities of larvae fed on apple leaves and plum leaves containing rosmarinic acid and protocatechuic acid increased with infection was determined. The amounts of malondialdehyde (MDA) decreased in all groups as a result of viral infection. While the highest superoxide dismutase (SOD) and catalase (CAT) activities among both infected and uninfected larvae were in the plum groups with the highest amount of chlorogenic acid, the lowest glutathione peroxidase (GSH-Px) activities were also in these groups. All this showed that different phenolic contents of host plants affected the hemocyte counts and antioxidant enzyme activities of H. cunea larvae.

Keywords

• Antioxidant activity
• granulovirus
• hemocyte
• Hyphantria cunea
• phenolic compounds

References

1. Abdelsalam, S. A., A. M. A. Awad, M. A. A. Abdelrahman, M. A. K. Nasser & N. M. R. Abdelhamid, 2016. Antioxidant defense response of the green peach aphid, Myzus persicae against secondary metabolites of the host plants cumin, anise, and coriander. Journal of Agricultural Science and Technology, 18 (6): 1583-1592.
2. Adomako-Bonsu, A. G., S. L. Chan, M. Pratten & J. R. Fry, 2017. Antioxidant activity of rosmarinic acid and its principal metabolites in chemical and cellular systems: Importance of physico-chemical characteristics. Toxicology in Vitro, 40: 248-255.
3. Akita, N. & M. Hoshi, 1995. Hemocytes release phenoloxidase upon contact reaction, an allogeneic interaction, in the ascidian Halocynthia roretzi. Cell Structure and Function, 20 (1): 81-87.
4. Alon, M., M. Elbaz, M. M. Ben-Zvi, E. Feldmesser, A. Vainstein & S. Morin, 2012. Insights into the transcriptomics of polyphagy: Bemisia tabaci adaptability to phenylpropanoids involves coordinated expression of defense and metabolic genes. Insect Biochemistry and Molecular Biology, 42 (4): 251-263.
5. Ashida, M. & K. Söderhäll, 1984. The prophenoloxidase activating system in crayfish. Comparative Biochemistry and Physiology-Part B- Biochemistry and Molecular Biology, 77 (1): 21-26.
6. Barthel, A., H. Vogel, Y. Pauchet, G. Pauls, G. Kunert, A. T. Groot, W. Boland, D. G. Heckel & H. M. Heidel-Fischer, 2016. Immune modulation enables a specialist insect to benefit from antibacterial withanolides in its host plant. Nature Communications, 7: 12530 (1-11).
7. Bate-Smith, E. C., 1977. Astringent tannins of Acer species. Phytochemistry, 16 (9): 2331-2336.
8. Baud, O., A. E. Greene, J. Li, H. Wang, J. J. Volpe & P. A. Rosenberg, 2004. Glutathione peroxidase-catalase cooperativity is required for resistance to hydrogen peroxide by mature rat oligodendrocytes. Journal of Neuroscience, 24 (7): 1531-1540.

9. Bayramoglu, Z., R. Nalcacıoglu, Z. Demirbag & I. Demir, 2018. Characterization of a Betabaculovirus from the fall webworm, Hyphantria cunea Drury (Lepidoptera: Erebidae), in Turkey. Biocontrol Science and Technology, 28 (12): 1178-1190.
10. Brigelius-Flohé, R. & M. Maiorino, 2013. Glutathione peroxidases. Biochimica et Biophysica Acta, 1830 (5): 3289-3303.
11. Dampc, J., M. Kula-Maximenko, M. Molon & R. Durak, 2020. Enzymatic defense response of apple aphid Aphis pomi to increased temperature. Insects, 11 (7): 436.
12. Draper, H. H. & M. Hadley, 1990. Malondialdehyde determination as index of lipid peroxidation. Methods in Enzymology, 186: 421-431.
13. Dudzic, J. P., S. Kondo, R. Ueda, C. M. Bergman & B. Lemaitre, 2015. Drosophila innate immunity: regional and functional specialization of prophenoloxidases. BMC Biology, 13: 81 (1-16).
14. Durak, R., W. Bednarski, M. Formela-Luboińska, A. Woźniak, B. Borowiak-Sobkowiak, T. Durak, R. Dembczyński & I. Morkunas, 2018. Defense responses of Thuja orientalis to infestation of anholocyclic species aphid Cinara tujafilina. Journal of Plant Physiology, 232: 160-170.
15. Ebrahimi, M. & M. Ajamhassani, 2020. Investigating the effect of starvation and various nutritional types on the hemocytic profile and phenoloxidase activity in the Indian meal moth Plodia interpunctella (Hübner) (Lepidoptera: Pyralidae). Invertebrate Survival Journal, 17 (1): 175-185.
16. Farrar, R. R. & R. L. Ridgway, 2000. Host plant effects on the activity of selected nuclear polyhedrosis viruses against the corn earworm and beet armyworm (Lepidoptera: Noctuidae). Environmental Entomology, 29 (1): 108-115.
17. Fitts, J. E. & D. Laird, 2004. “Direct Microscopic Methods for Bacteria of Somatic Cells, 269-280”. In: Standard Methods for the Examination of Dairy Products (Eds. H. M. Wekl & J. F. Frank). American Public Health Association, Washington, USA, 412 pp.
18. Flohé, L. & F. Ötting, 1984. Superoxide dismutase assays. Methods in Enzymology, 105: 93-104.
19. Gencer, D., Z. Bayramoglu, R. Nalcacıoglu, Z. Demirbag & I. Demir, 2020. Genome sequence analysis and organization of the Hyphantria cunea granulovirus (HycuGV-Hc1) from Turkey. Genomics, 112 (1): 459-466.
20. Gencer, D., Z. Bayramoglu, R. Nalcacıoglu, R. G. Kleespies, Z. Demirbag & I. Demir, 2018. Characterisation of three alphabaculovirus isolates from the gypsy moth, Lymantria dispar dispar (Lepidoptera: Erebidae), in Turkey. Biocontrol Science and Technology, 28 (2): 107-121.
21. Gencer, D., O. Yanar, A. Yeşilyurt, R. Nalcacıoglu & I. Demir, 2019. Characterization of a novel baculovirus isolate from Malacosoma neustria (Linnaeus, 1758) (Lepidoptera: Lasiocampidae) in Samsun and its pathogenicity in different hosts. Turkish Journal of Entomology, 43 (4): 429-440.
22. Ghosh, S., A. K. Prasad & A. Mukhopadhyay, 2018. Effects of feeding regimes on hemocyte counts in two congeners of Hyposidra (Lepidoptera: Geometridae). Entomologia Generalis, 38 (1): 73-82.
23. Giannenas, I., C. P. Papaneophytou, E. Tsalie, I. Pappas, E. Triantafillou, D. Tontis & G. A. Kontopidis, 2014. Dietary supplementation of benzoic acid and essential oil compounds affects buffering capacity of the feeds, performance of Turkey poults and their antioxidant status, pH in the digestive tract, intestinal microbiota and morphology. Asian-Australasian Journal of Animal Science, 27 (2): 225-236.
24. Girsang, E., I. N. E. Lister, C. N. Ginting, M. Bethasari, A. Amalia & W. Widowati, 2020. Comparison of antiaging and antioxidant activities of protocatechuic and ferulic acids. Molecular and Cellular Biomedical Sciences, 4 (2): 68-75.
25. Gowler, C. D., K. E. Leon, M. D. Hunter & J. C. de Roode, 2015. Secondary defense chemicals in milkweed reduce parasite infection in Monarch butterflies, Danaus plexippus. Journal of Chemical Ecology, 41 (6): 520-523.
26. Hafeez, M., S. Liu, S. Jan, A. Gulzar, G. M. Fernández-Grandon, M. Qasim, K. A. Khan, B. Ali, S. J. Kedir, M. Fahad & M. Wang, 2019. Enhanced effects of dietary tannic acid with chlorantraniliprole on life table parameters and nutritional physiology of Spodoptera exigua (Hübner). Pesticide Biochemistry and Physiology, 155: 108-118.
27. Huang, X., S. Lv, Z. Zhang & B. H. Chang, 2020. Phenotypic and transcriptomic response of the grasshopper Oedaleus asiaticus (Orthoptera: Acrididae) to toxic rutin. Frontiers in Physiology, 11: 52.
28. Iacopini, P., M. Baldi, P. Storchi & L. Sebastiani, 2008. Catechin, epicatechin, quercetin, rutin and resveratrol in red grape: content, in vitro antioxidant activity and interactions. Journal of Food Composition and Analysis, 21 (8): 589-598.
29. Ikeda, M., H. Yamada, R. Hamajima & M. Kobayashi, 2013. Baculovirus genes modulating intracellular innate antiviral immunity of lepidopteran insect cells. Virology, 435 (1): 1-13.
30. Janssen-Heininger, Y. M., B. T. Mossman, N. H. Heintz, H. J. Forman, B. Kalyanaraman, T. Finkel, J. S. Stamler, S. G. Rhee & A. van der Vliet, 2008. Redox-based regulation of signal transduction: principles, pitfalls, and promises. Free Radical Biology and Medicine, 45 (1): 1-17.
31. Jiang, H., A. Vilcinskas & M. R. Kanost, 2010. “Immunity in lepidopteran insects, 181-204”. In: Invertebrate Immunity. Advances in Experimental Medicine and Biology (Ed. K. Söderhäll). Springer, Boston, USA, 708 pp.
32. Kamalakkannan, N. & P. S. M. Prince, 2006. Antihyperglycaemic and antioxidant effect of rutin, a polyphenolic flavonoid, in streptozotocin-induced diabetic wistar rats. Basic and Clinical Pharmacology and Toxicology, 98 (1): 97-103.
33. Kaushal, J., S. Mehandia, G. Singh, A. Raina & S. K. Arya, 2018. Catalase enzyme: Application in bioremediation and food industry. Biocatalysis and Agricultural Biotechnology, 16: 192-199.
34. Kim, H., J. H. Pan, S. H. Kim, J. H. Lee & J. W. Park, 2018. Chlorogenic acid ameliorates alcohol-induced liver injuries through scavenging reactive oxygen species. Biochimie, 150: 131-138.
35. Kobayashi, Y., Y. Nojima, T. Sakamoto, K. Iwabuchi, T. Nakazato, H. Bono, A. Toyoda, A. Fujiyama, M. R. Kanost & H. Tabunoki, 2019. Comparative analysis of seven types of superoxide dismutases for their ability to respond to oxidative stress in Bombyx mori. Scientific Reports, 9: 2170 (1-12).
36. Lawrence, R. A. & R. F. Burk, 1976. Glutathione peroxidase activity in selenium deficient rat liver. Biochemical and Biophysical Research Communications, 71 (4): 952-958.
37. Li, Z. Q., X. H. Song, M. Wang, S. Wang & G. H. Huang, 2021. Melanization induced by Heliothis virescens ascovirus 3h promotes viral replication. Insect Science, 28 (2): 472-484.
38. Lowry, O. H., N. T. Rosebrough, A. L. Farr & R. J. Randall, 1951. Protein measurement with the folin phenol reagent. Journal of Biological Chemistry, 193 (1): 265-275.
39. Luck, H., 1963. “Catalase, 885-894”. In: Methods of Enzymatic Analysis (Ed. H. U. Bergmeyer). Weinheim and Academic Press, New York, USA, 1064 pp.
40. Lukasik, I., 2007. Changes in activity of superoxide dismutase and catalase within cereal aphids in response to plant o-dihydroxyphenols. Journal of Applied Entomology, 131 (3): 209-214.
41. Mahmoud, D. M. & D. E. Soliman, 2015. Haemocytes and protein changes in Schistocerca gregaria after infection with nucleopolyhedrovirus. Journal of Entomology and Nematology, 7 (5): 39-45.
42. McCord, J. M. & I. Fridovich, 1969. Superoxide dismutase. An enzymic function for erithrocuprein (Hemocuprein). Journal of Biological Chemistry, 244 (22): 6049-6055.
43. Millanta, F., S. Sagona, M. Mazzei, M. Forzan, A. Poli & A. Felicioli, 2019. Phenoloxidase activity and haemolymph cytology in honeybees challenged with a virus suspension (deformed wings virus DWV) or phosphate buffered suspension (PBS). Ciência Rural, 49 (2): e20180726.
44. Muller, K., F. Vogelweith, D. Thiery, Y. Moret & J. Moreau, 2015. Immune benefits from alternative host plants could maintain polyphagy in a phytophagous insect. Oecologia, 177 (2): 467-475.
45. Nakhleh, J., L. El-Moussawi & M. A. Osta, 2017. “The melanization response in insect immunity, 83-109”. In: Advances in Insect Physiology (Ed. P. Ligoxygakis). Academic Press, Cambridge, UK, 248 pp.
46. Naveed, M., V. Hejazi, M. Abbas, A. A. Kamboh, G. J. Khan, M. Shumzaid, F. Ahmad, D. Babazadeh, X. FangFang, F. Modarresi-Ghazani, L. WenHua & Z. XiaoHui, 2018. Chlorogenic acid (CGA): A pharmacological review and call for further research. Biomedicine & Pharmacotherapy, 97: 67-74.
47. Oboh, G., A. O. Ademosun, P. O. Ayeni, O. S. Omojokun & F. Bello, 2015. Comparative effect of quercetin and rutin on α-amylase, α-glucosidase, and some pro-oxidant-induced lipid peroxidation in rat pancreas. Comparative Clinical Pathology, 24 (5): 1103-1110.
48. Pandey, S., J. P. Pandey & R. K. Tiwari, 2012. Effect of some botanicals on hemocytes and molting of Papilio demoleus larvae. Journal of Entomology, 9 (1): 23-31.
49. Payab, M., M. J. Chaichi, O. L. Nazari & F. Y. Maleki, 2019. Tannin extraction from oak gall and evaluation of anti-oxidant activity and tannin iron chelation compared with deferoxamine drug. Journal of Drug Design and Medicinal Chemistry, 5 (2): 18-25.
50. Perić-Mataruga, V., M. Vlahović, M. Mrdaković, D. Todorović, D. Matić, A. Gavrilović & L. Ilijin, 2014. Prothoracicotropic hormone producing neurosecretory neurons and antioxidative defense in midgut of Lymantria dispar in trophic stress. Turkish Journal of Biology, 38 (3): 403-411.
51. Povey, S., S. C. Cotter, S. J. Simpson & K. Wilson, 2013. Dynamics of macronutrient self-medication and illness-induced anorexia in virally infected insects. Journal of Animal Ecology, 83 (1): 245-255.
52. Rao, X. J., E. J. Ling & X. Q. Yu, 2010. The role of lysozyme in the prophenoloxidase activation system of Manduca sexta: an in vitro approach. Developmental and Comparative Immunology, 34 (3): 264-271.
53. Sayed, W. A. A., H. El-Bendary & A. M. A. El-Helaly, 2020. Increasing the efficacy of the cotton leaf worm Spodoptera littoralis nucleopolyhedrosis virus using certain essential oils. Egyptian Journal of Biological Pest Control, 30: 8 (1-7).
54. Schuessel, K., C. Frey, C. Jourdan, U. Keil, C. C. Weber, F. Muller-Spahn, W. E. Muller & A. Eckert, 2006. Aging sensitizes toward ROS formation and lipid peroxidation in PS1M146L transgenic mice. Free Radical Biology & Medicine, 40 (5): 850-862.
55. Simmonds, M. J., P. C. Stevenson & F. E. Hanson, 2019. Rosmarinic acid in Canna generalis activates the medial deterrent chemosensory neurone and deters feeding in the tobacco hornworm Manduca sexta. Physiological Entomology, 44 (2): 140-147.
56. Smilanich, A. M., T. C. Langus, L. Doan, L. A. Dyer, J. G. Harrison, J. Hsueh & M. B. Teglas, 2018. Host plant associated enhancement of immunity and survival in virus infected caterpillars. Journal of Invertebrate Pathology, 151: 102-112.
57. Sun, L., J. Yin, H. Du, P. Liu & C. Cao, 2020. Characterisation of GST genes from the Hyphantria cunea and their response to the oxidative stress caused by the infection of Hyphantria cunea nucleopolyhedrovirus (HcNPV). Pesticide Biochemistry and Physiology, 163: 254-262.
58. Trowbridge, A. M., M. D. Bowers & R. K. Monson, 2016. Conifer monoterpene chemistry during an outbreak enhances consumption and immune response of an eruptive folivore. Journal of Chemical Ecology, 42 (12): 1281-1292.
59. Türkan, F., P. Taslimi & F. Z. Saltan, 2019. Tannic acid as a natural antioxidant compound: discovery of a potent metabolic enzyme inhibitor for a new therapeutic approach in diabetes and Alzheimer’s disease. Journal of Biochemical and Molecular Toxicology, 33 (8): e22340.
60. Velika, B. & I. Kron, 2012. Antioxidant properties of benzoic acid derivatives against superoxide radical. Free Radicals and Antioxidants, 2 (4): 62-67.
61. Wan, N. F., X. Li, L. Guo, X. Y. Ji, H. Zhang, Y. J. Chen & J. X. Jiang, 2018. Phytochemical variation mediates the susceptibility of insect herbivores to entomoviruses. Journal of Applied Entomology, 142 (7): 705-715.
62. Wang, Y., L. W. Oberley & D. W. Murhammer, 2001. Evidence of oxidative stress following the viral infection of two Lepidopteran insect cell lines. Free Radical Biology and Medicine, 31 (11): 1448-1455.
63. Wang, J. Y., H. Zhang, E. Siemann, N. N. Fan, X. Y. Ji, Y. J. Chen, J. X. Jiang & N. F. Wan, 2021. Plants impact cellular immunity of caterpillars to an entomovirus. Pest Management Science, 77 (5): 2415-2424.
64. Wang, J. Y., H. Zhang, E. Siemann, X. Y. Ji, Y. J. Chen, Y. Wang, J. X. Jiang & N. F. Wan, 2020. Immunity of an insect herbivore to an entomovirus is affected by different host plants. Pest Management Science, 76 (3): 1004-1010.
65. Woestmann, L., M. Gibbs, H. Hesketh & M. Saastamoinen, 2018. Viral exposure effects on life-history, flight-related traits, and wing melanisation in the Glanville fritillary butterfly. Journal of Insect Physiology, 107: 136-143.
66. Yuan, C., L. Xing, M. Wang, X. Wang, M. Yin, Q. Wang, Z. Hu & Z. Zou, 2017. Inhibition of melanization by serpin-5 and serpin-9 promotes baculovirus infection in cotton bollworm Helicoverpa armigera. PLoS Pathogens, 13 (9): e1006645.
67. Zhu, K., X. Zeng, F. Tan, W. Li, C. Li, Y. Song & X. Zhao, 2019. Effect of insect tea on D-galactose-induced oxidation in mice and its mechanisms. Food Science and Nutrition, 7 (12): 4105-4115.