Changes in the Antioxidant Enzyme Activities and Physiological Responses of Sea Buckthorn (Elaeagnus rhamnoides L.) Infested with the Lackey Moth (Malacosoma neustria L.)

Abstract

Herbivorous insect infestations are a serious problem that threatens the plants. To cope with this issue, plants utilize various defense mechanisms. Malacosoma neustria L. (the lackey moth) (Lepidoptera: Lasiocampidae), which causes significant damage by feeding on many shrub-like and woody plants during its larval stage, is a worldwide pest. Sea buckthorn, Elaeagnus rhamnoides L. (Rosales: Elaeagnaceae), which has economic, ecological, and medicinal importance, is one of the plants most preferred by this insect. The changes in the amounts of secondary compounds, fresh and dry weights, the levels of chlorophyll a, chlorophyll b, and total chlorophyll, the contents of total protein, the contents of malondialdehyde (MDA), the activities of ascorbate peroxidase (APX), superoxide dismutase (SOD), and catalase (CAT) in leaves of the M. neustria-infested and non-infested E. rhamnoides were compared in this study. The leaves of E. rhamnoides were collected from the Kızılırmak Delta in Samsun Province, Turkey. The moth-infested and non-infested leaves constituted experimental groups. As a result, it was determined that the fresh weight and the content of protein in the lackey moth-infested leaves decreased. In contrast, the levels of total chlorophyll, chlorophyll a, and chlorophyll b, the content of MDA, the activities of SOD, CAT, and APX increased. Additionally, it was found that both the amount and composition of secondary compounds differ between the moth-infested and non-infested leaves. In conclusion, our findings indicate that E. rhamnoides defends itself against M. neustria infestation, which is a biotic stress factor, through both ROS-scavenging enzymes and its secondary compounds..

Keywords

• Antioxidant defense system
• Chlorophyll
• Herbivore
• Malacosoma Neustria
• Sea buckthorn

Lackey Moth (Malacosoma neustria L.) ile İstila edilen Deniz Topalak (Elaeagnus rhamnoides L.)'ın Antioksidan Enzim Aktiviteleri ve Fizyolojik Tepkilerindeki Değişiklikler

Abstract

Herbivor böcek istilaları, bitkileri tehdit eden ciddi bir sorundur. Bitkiler bu sorunla başa çıkmak için çeşitli savunma mekanizmaları kullanır. Larva döneminde birçok çalı benzeri ve odunsu bitkiyle beslenerek önemli hasara neden olan Malacosoma neustria L. (uşak güvesi) (Lepidoptera: Lasiocampidae), dünya çapında bir zararlıdır. Ekonomik, ekolojik ve tıbbi öneme sahip olan deniz iğdesi Elaeagnus rhamnoides L. (Rosales: Elaeagnaceae), bu böceğin en çok tercih ettiği bitkilerden biridir. Bu çalışmada, M. neustria ile istila ve istila olmayan E. rhamnoides yapraklarında sekonder bileşik miktarları, yaş ve kuru ağırlıklar, klorofil a, klorofil b ve toplam klorofil düzeyleri, toplam protein içeriği, malondialdehit (MDA) içeriği, askorbat peroksidaz (APX), süperoksit dismutaz (SOD) ve katalaz (CAT) aktivitelerinin değişimleri karşılaştırılmıştır. E. rhamnoides yaprakları, Türkiye'nin Samsun ilindeki Kızılırmak Deltası'ndan toplanmıştır. Güve istilalı ve istilalı olmayan yapraklar deneme gruplarını oluşturmuştur. Sonuç olarak, güve istilasına uğramış yapraklarda yaş ağırlık ve protein içeriğinin azaldığı tespit edilmiştir. Aksine, toplam klorofil, klorofil a ve klorofil b seviyelerinin, MDA içeriğinin, SOD, CAT ve APX aktivitelerinin ise arttığı tespit edilmiştir. Ayrıca, güve istilasına uğramış ve uğramamış yapraklarda sekonder bileşiklerin hem miktarı hem de bileşiminin farklılık gösterdiği bulunmuştur. Sonuç olarak, bulgularımız E. rhamnoides'in biyotik bir stres faktörü olan M. neustria istilasına karşı hem ROS-süpürücü enzimler hem de sekonder bileşikleri aracılığıyla kendini savunduğunu göstermektedir.

Keywords

• Malacosoma neustria
• Antioksidan enzimler
• Klorofil
• Herbivor
• Malacosoma neustria
• Deniz topalak

References

1. Abbate, C., Toscano, S., Arcidiacono, R., Romano, D., Russo, A. & Mazzeo, G. (2018). Induced responses of Bougainvillea glabra Choisy (Nyctaginaceae) against Phenacoccus peruvianus Granara de Willink (Hemiptera: Pseudococcidae) attack: Preliminary results. Arthropod-Plant Interactions, 12, 41-48.
2. Afroz, M., Rahman, M. & Amin, R. (2021). Insect plant interaction with reference to secondary metabolites: A review. Agricultural Reviews, 42(4), 427-433.
3. Arnon, D. L. (1949). Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. Plant Physiology, 24(1), 549-557.
4. Awasthi, J., Saha, B., Chowardhara, B., Devi, S. S., Borgohain, P. & Panda, S. K. (2018). Qualitative analysis of lipid peroxidation in plants under multiple stress through schiff’s reagent: A histochemical approach. Bio-protocol, 8(8), e2807.
5. Baker, A., Lin, C. C., Lett, C., Karpinska, B., Wright, M. H. & Foyer, C. H. (2023). Catalase: A critical node in the regulation of cell fate. Free Radical Biology and Medicine, 199, 56-66.
6. Bhattacharjee, S. (2014). Membrane lipid peroxidation and its conflict of interest: The two faces of oxidative stress. Current Science, 107, 1811-1823.
7. Bradford, M. M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry, 72(1-2), 248-254.
8. Cervilla, L. M., Blasco, B., Rios, J. J., Romero, L. & Ruiz, J. M. (2007). Oxidative stress and antioxidants in tomato (Solanum lycopersicum) plants subjected to boron toxicity. Annals of Botany, 100(4), 747-756.

9. Chen, Z. Y., Peng, Z. S., Yang, J., Chen, W. Y. & Ou Yang, Z. M. (2011). A mathematical model for describing light-response curves in Nicotiana tabacum L. Photosynthetica, 49(3), 467-471.
10. Chen, C. Y., Huang P. H., Yeh K. W. & Wang S. J. (2022). Colonization of Piriformospora indica enhances insect herbivore resistance of rice plants through jasmonic acid- and antioxidant-mediated defense mechanisms. Journal of Plant Interactions, 17(1), 9-18.
11. Chovanová, K., Böhmer, M., Poljovka, A., Budiš, J., Harichová, J., Szemeš, T. & Zámocký, M. (2020). Parallel molecular evolution of catalases and superoxide dismutases-focus on thermophilic fungal genomes. Antioxidants, 9(11), 1047.
12. Costa, E. N., Martins, L. O., Reis, L. C., Fernandes, M. G. & de Paula Quintão Scalon, S. (2020). Resistance of cowpea genotypes to Spodoptera frugiperda (Lepidoptera: Noctuidae) and its relationship to resistance-related enzymes. Journal of Economic Entomology, 113, 2521-2529.
13. Croft, H., & Chen, J. (2017). Leaf pigment content. In S. Liang, (Ed.), Comprehensive Remote Sensing, (pp. 1-26) Amsterdam: Elsevier.
14. Divekar, P. A., Narayana, S., Divekar, B. A., Kumar, R., Gadratagi, B. G., Ray, A., Singh, A. K., Rani, V., Singh, V., Singh, A. K., Kumar, A., Singh, R. P., Meena, R. S. & Behera, T. K. (2022). Plant secondary metabolites as defense tools against herbivores for sustainable crop protection. International Journal of Molecular Sciences, 23, 2690.
15. Donbaloglu Bozca, F. & Leblebici, S. (2022). Interactive effect of boric acid and temperature stress on phenological characteristics and antioxidant system in Helianthus annuus L. South African Journal of Botany, 147(2022), 391-399.
16. Foyer, C. H. & Noctor, G. (2011). Ascorbate and glutathione: The heart of the redox hub. Plant Physiology, 155(1), 2-18.
17. Gallon, M. E. & Smilanich, A. M. (2023). Effects of host plants on development and immunity of a generalist insect herbivore. Journal of Chemical Ecology, 49(3-4), 142-154.
18. Golan, K., Jurado, I. G., Kot, I., Górska-Drabik, E., Kmieć, K., Łagowska, B., Skwaryło-Bednarz, B., Kopacki, M. & Jamiołkowska, A. (2021). Defense responses in the interactions between medicinal plants from Lamiaceae family and the two-spotted spider mite Tetranychus urticae Koch (Acari: Tetranychidae). Agronomy, 11, 438.
19. Gomes, M. P., Kitamura, R. S. A., Marques, R. Z., Barbato, M. L. & Zámocký, M. (2022). The role of H2O2-scavenging enzymes (ascorbate peroxidase and catalase) in the tolerance of Lemna minor to antibiotics: Implications for phytoremediation. Antioxidants, 11(1), 151.
20. Gull, A., Lone, A. A. & Wani, N. U. I. (2019). Biotic and abiotic stresses in plants. IntechOpen, 2019, 85832.
21. Gulsen, O., Eickhoff, T., Heng-Moss, T., Shearman, R., Baxendale, F., Sarath, G. & Lee, D. (2010). Characterization of peroxidase changes in resistant and susceptible warm season turf grasses challenged by Blissus occiduus. Arthropod-Plant Interactions, 4, 45-55.
22. Havugimana, S., Kiseleva, I. S. & Nsengumuremyi, D. (2023). Lipid peroxidation within different amaranth cultivars. Brazilian Journal of Science, 2(3), 1-5.
23. Hörtensteiner, S. & Kräutler, B. (2011). Chlorophyll breakdown in higher plants. Biochimica et Biophysica Acta-Bioenergetics, 1807(8), 977-988.
24. Huihui, Z., Xin, L., Zisong, X., Yue, W., Zhiyuan, T., Meijun, A., Yuehui Z., Wenxu, Z., Nan, X. & Guangyu, S. (2020). Toxic effects of heavy metals Pb and Cd on mulberry (Morus alba L.) seedling leaves: Photosynthetic function and reactive oxygen species (ROS) metabolism responses. Ecotoxicology and Environmental Safety, 195, 110469.
25. Huo, C., He, L., Yu, T., Ji, X., Li, R., Zhu, S., Zhang F., Xie, H. & Liu, W. (2022). The superoxide dismutase gene family in Nicotiana tabacum: Genome-wide identification, characterization, expression profiling and functional analysis in response to heavy metal stress. Frontiers in Plant Science, 13, 904105.
26. Iqbal, Z., Iqbal, M. S., Hashem, A., Abd_Allah, E. F. & Ansari, M. I. (2021). Plant defense responses to biotic stress and its interplay with fluctuating dark/light conditions. Frontiers in Plant Science, 12, 631810.
27. Jan, R., Asaf, S., Numan, M., Lubna & Kim, K. M. (2021). Plant secondary metabolite biosynthesis and transcriptional regulation in response to biotic and abiotic stress conditions. Agronomy, 11, 968.
28. Jood, S. & Kapoor, A. C. (1993). Protein and uric acid contents of cereal grains as affected by insect infestation. Food Chemistry, 46, 143-146.
29. Kabay, T. & Şensoy, S. (2017). Enzyme, chlorophyll and ion changes in some common bean genotypes by high temperature stress. Ege Üniversitesi Ziraat Fakültesi Dergisi, 54(4), 429-437.
30. Kaur, R., Guptaa, A. K. & Taggar, G. K. (2015). Induced resistance by oxidative shifts in pigeon pea (Cajanus cajan L.) following Helicoverpa armigera (Hübner) herbivory. Pest Management Science, 71, 770-782.
31. Kerchev, P. I., Fenton, B., Foyer, C. H. & Hancock, R. D. (2012). Infestation of potato (Solanum tuberosum L.) by the peach-potato aphid (Myzus persicae Sulzer) alters cellular redox status and is influenced by ascorbate. Plant, Cell & Environment, 35, 430-440.
32. Khattab, H. (2007). The defense mechanism of cabbage plant against phloem-sucking aphid (Brevicoryne brassicae L.). Australian Journal of Basic and Applied Sciences, 1, 56-62.
33. Kmieć, K., Rubinowska, K. & Golan, K. (2018). Tetraneura ulmi (Hemiptera: Eriosomatinae) induces oxidative stress and alters antioxidant enzyme activities in elm leaves. Environmental Entomology, 47, 840-847.
34. Kot, I. & Kmieć, K. (2020). Poplar tree response to feeding by the petiole gall aphid Pemphigus spyrothecae Pass. Insects, 11(5), 282.
35. Kovalikova, Z., Kubes, J., Skalicky, M., Kuchtickova, N., Maskova, L., Tuma, J., Vachova, P. & Hejnak, V. (2019). Changes in content of polyphenols and ascorbic acid in leaves of white cabbage after pest infestation. Molecules, 24, 2622.
36. Leblebici, S., Donbaloğlu Bozca, F., Topkara, E. F. & Yanar, O. (2023). Comparison of physiological responses in some Pinus species attacked by pine processionary moth. Russian Journal of Plant Physiology, 70, 143.
37. Li, S. (2023). Novel insight into functions of ascorbate peroxidase in higher plants: More than a simple antioxidant enzyme. Redox Biology, 64, 102789.
38. Maffei, M. E., Mithofer, A. & Boland, W. (2007a). Insect feeding on plants: Rapid signals and responses preceding the induction of phytochemical release. Phytochemistry, 68, 2946-2959.
39. Maffei, M. E., Mithöfer, A. & Boland, W. (2007b). Before gene expression: Early events in plant-insect interaction. Trends in Plant Science, 12, 310-316.
40. Mai, V. C., Tran, N. T. & Nguyen, D. S. (2016). The involvement of peroxidases in soybean seedlings’ defense against infestation of cowpea aphid. Arthropod-Plant Interactions, 10, 283-292.
41. Mir, R. A. & Khah, M. A. (2024). Recent progress in enzymatic antioxidant defense system in plants against different environmental stresses. In M. A. Ahanger, J. A. Bhat, P. Ahmad, R. John (Eds.), Improving Stress Resilience in Plants: Physiological and Biochemical Basis and Utilization in Breeding, (pp. 203-224). Cambridge: Academic Press.
42. Moser, S., Erhart, T., Neuhauser, S. & Kräutler, B. (2020). Phyllobilins from senescence-associated chlorophyll breakdown in the leaves of basil (Ocimum basilicum) show increased abundance upon herbivore attack. Journal of Agricultural and Food Chemistry, 68(27), 7132-7142.
43. Muthuswami, M., Subramanian, S., Krishnan, R., Thangamalar, A. & Indumathi, P. (2010). Quantitative and qualitative damage caused in mulberry varieties due to infestation of thrips Pseudodentrothrips mori Niwa. Karnataka Journal of Agricultural Sciences, 23, 146-148.
44. Nadarajah, K. K. (2020). ROS homeostasis in abiotic stress tolerance in plants. International Journal of Molecular Sciences, 21, 5208.
45. Nta, A. I., Mofunanya, A. A. J., Ogar, V. B., Omara-Achong, T. E. & Azuike, P. A. (2019). Comparative effect of Acanthoscelides obtectus (Say) infestation on nutrients of Phaseolus vulgaris (Linn.) and Phaseolus acutifolius (Gray). Pakistan Journal of Biological Sciences, 22, 494-501.
46. Özbek, H. & Çoruh, S. (2010). Egg parasitoids of Malacosoma neustria (L.) Lepidoptera: Lasiocampidae) in Erzurum province of Turkey. Turkish Journal of Entomology, 34(4), 551-560.
47. Pan, Y., Zhao, S., Wang, Z., Wang, X., Zhang, X., Lee, Y. & Xi, J. (2020). Quantitative proteomics suggests changes in the carbohydrate metabolism of maize in response to larvae of the belowground herbivore Holotrichia parallela. PeerJ, 8, e9819.
48. Pichersky, E. & Lewinsohn, E. (2011). Convergent evolution in plant specialized metabolism. Annual Review of Plant Biology, 62, 549-566.
49. Rahdari, P. & Hoseini, S. M. (2012). Drought stress: A review. International Journal of Agronomy and Plant Production, 3(10), 443-446.
50. Ramírez-Gómez, X. S., Jiménez-García, S. N., Campos, V. B. & Campos, M. L. G. (2020). Plant metabolites in plant defense against pathogens. London: IntechOpen.
51. Rodríguez, J., Novoa, A., Sotes, G., Pauchard, A. & González, L. (2023). Variation in defensive traits against herbivores of native and invasive populations of Carpobrotus edulis. Biological Invasions, 25(4), 1149-1164.
52. Roitto, M., Markkola, A., Julkunen-Tiitto, R., Sarjala, T., Rautio, P., Kuikka, K. & Tuomi, J. (2003). Defoliation-induced responses in peroxidases, phenolics, and polyamines in Scots pine (Pinus sylvestris L.) needles. Journal of Chemical Ecology, 29(6), 1905-1918.
53. Ruan, C. & Li, D. (2002). Community characteristics of Hippophae rhamnoides forest and water and nutrient condition of the woodland in Loess Hilly Region. Journal of Applied Ecology, 13(9), 1061-1064.
54. Sairam, R. K. & Saxena, D. C. (2000). Oxidative stress and antioxidants in wheat genotypes: possible mechanism of water stress tolerance. Journal of Agronomy and Crop Science, 184(1), 55-61.
55. Salam, U., Ullah, S., Tang, Z. H., Elateeq, A. A., Khan, Y., Khan, J., Khan, A. & Ali, S. (2023). Plant metabolomics: An overview of the role of primary and secondary metabolites against different environmental stress factors. Life, 13(3), 706.
56. Santamaria, M. E., Arnaiz, A., Velasco-Arroyo, B., Grbic, V., Diaz, I. & Martinez, M. (2018). Arabidopsis response to the spider mite Tetranychus urticae depends on the regulation of reactive oxygen species homeostasis. Scientific Reports, 8, 9432.
57. Sau, A. K., Dhillon, M. K. & Trivedi, N. (2022). Activation of antioxidant defense in maize in response to attack by Sesamia inferens (Walker). Phytoparasitica, 50, 1043-1058.
58. Singh, H., Grewal, S. K., Singh, R. & Bhardwaj, R. D. (2023). Induced defense responses in cultivated and wild chickpea genotypes against Helicoverpa armigera infestation. Biologia Futura, 74, 231-246.
59. Skórzyńska-Polit, E. (2007). Lipid peorxidation in plant cells, its physiological role and changes under heavy metal stress. Acta Societatis Botanicorum Poloniae, 76, 49-54.
60. Skwarek, M., Patykowski, J. & Witczak, A. (2017). Changes in antioxidant enzyme activities in Pinus sylvestris and Larix decidua seedlings after Melolontha melolontha attack. Leśne Prace Badawcze, 78(2), 159-164.
61. Somegowda, M., Raghavendra, S., Sridhara, S., Rajeshwara, A. N., Pramod, S. N., Shivashankar, S., Lin, F., Zin El-Abedin, T. K., Wani, S. H. & Elansary, H. O. (2021). Defensive mechanisms in cucurbits against melon fly (Bactrocera cucurbitae) infestation through excessive production of defensive enzymes and antioxidants. Molecules, 26, 6345.
62. Stathas, I. G., Sakellaridis, A. C., Papadelli, M., Kapolos, J., Papadimitriou, K. & Stathas, G. J. (2023). The effects of insect infestation on stored agricultural products and the quality of food. Foods, 12, 2046.
63. Stobdan, T., Targais, K., Lamo, D. & Srivastava, R. (2013). Judicious use of natural resources: A case study of traditional uses of seabuckthorn (Hippophae rhamnoides L.) in trans-himalayan ladakh, India. National Academy Science Letters, 36, 609-613.
64. Suma, R. (2001). Enzymatic studies in the thrips infested mulberry leaves (Ph.D. Thesis). Bangalore University, Bangalore.
65. Sülüs, S. & Leblebici, S. (2022). Effect of boric acid application on antioxidant enzymes activity and gene expression in safflower (Carthamus tinctorius L.) cultivars. Biological and Applied Sciences, 65, e22200702.
66. Sytykiewicz, H., Łukasik, I., Goławska, S. & Chrzanowski, G. (2019). Aphid-triggered changes in oxidative damage markers of nucleic acids, proteins, and lipids in maize (Zea mays L.) seedlings. International Journal of Molecular Sciences, 20, 3742.
67. Teklić, T., Parađiković, N., Špoljarević, M., Zeljković, S., Lončarić, Z., & Lisjak, M. (2021). Linking abiotic stress, plant metabolites, biostimulants and functional food. Annals of Applied Biology, 178, 169-191.
68. Tepe, M. & Aydemir, T. (2011). Antioxidant responses of lentil and barley plants to boron toxicity under different nitrogen sources. African Journal of Biotechnology, 10, 53.
69. Trajković, A. & Žikić, V. (2023). Stuck in the caterpillars’ web: A half-century of biocontrol research and application on gregarious lepidopteran pests in Europe. Sustainability, 15, 2881. https://doi.org/10.3390/su15042881
70. Tripathi, D. K., Mishra, R. K., Singh, S., Singh, S., Singh, V. P., Singh, P. K. & Pandey, A. C. (2017). Nitric oxide ameliorates zinc oxide nanoparticles phytotoxicity in wheat seedlings: Implication of the ascorbate-glutathione cycle. Frontiers in Plant Science, 8, 1.
71. Tyagi, S., Shah, A., Karthik, K., Rathinam, M., Rai, V., Chaudhary, N. & Sreevathsa R. (2022). Reactive oxygen species in plants: An invincible fulcrum for biotic stress mitigation. Applied Microbiology and Biotechnology, 106(18), 5945-5955.
72. Usha Rani, P. & Jyothsna, Y. (2010). Biochemical and enzymatic changes in rice as a mechanism of defense. Acta Physiologiae Plantarum, 32, 695-701.
73. Wang, Z., Zhao, F., Wei, P., Chai, X., Hou, G. & Meng, Q. (2022). Phytochemistry, health benefits, and food applications of sea buckthorn (Hippophae rhamnoides L.): A comprehensive review. Frontiers in Nutrition, 9, 1036295.
74. Yang, J., Ma, C., Jia, R., Zhang, H., Zhao, Y., Yue, H., Li, H. & Jiang, X. (2023). Different responses of two maize cultivars to Spodoptera frugiperda (Lepidoptera: Noctuidae) larvae infestation provide insights into their differences in resistance. Frontiers in Plant Science, 14, 1065891.
75. Yarsi, G. (2023). Effects of mycorrhiza, seaweed and bionutrient applied to reduce the salt stress on nutrient content, plant growth, malondialdehyde (MDA) and proline in pepper. Journal of Elementology, 28, 3.
76. Zhang, Q., Zhou, M. & Wang, J. (2022). Increasing the activities of protective enzymes is an important strategy to improve resistance in cucumber to powdery mildew disease and melon aphid under different infection/infestation patterns. Frontiers in Plant Science, 13, 950538.
77. Zoufan, P., Zare Bavani, M.R., Tousi, S. & Rahnama, A. (2023). Effect of exogenous melatonin on improvement of chlorophyll content and photochemical efficiency of PSII in mallow plants (Malva parviflora L.) treated with cadmium. Physiology and Molecular Biology of Plants, 29(1), 145-157.
78. Züst, T. & Agrawal, A. A. (2016). Mechanisms and evolution of plant resistance to aphids. Nature Plants, 2, 15206.