The influence of Cameraria ohridella (Lepidoptera, Gracillariidae) on the activity of the enzymatic antioxidant system of protection of the assimilating organs of Aesculus hippocastanum in an urbogenic environment


  • L. V. Shupranova Oles Honchar Dnipro National University http://orcid.org/0000-0002-6174-2580
  • K. K. Holoborodko Oles Honchar Dnipro National University
  • O. V. Seliutina Oles Honchar Dnipro National University
  • O. Y. Pakhomov Oles Honchar Dnipro National University http://orcid.org/0000-0002-5192-6140
Keywords: benzidine-peroxidase; peroxidase isoenzymes; guajacol-peroxidase; catalase.

Abstract

In the last two decades, the horse chestnut (Aesculus hippocastanum L.), introduced into the steppe zone of Ukraine, has been severely affected by the horse chestnut leaf miner Camereraria ohridella Deschka & Dimič, 1986, which results in damage to the assimilating organs, premature leaf defoliation and, as a consequence, a significant reduction in the reserve substances required for normal life of the plant. In recent studies, the main focus has been placed on the study of the pest’s effects on the non-enzymatic antioxidant protection system of the representatives of the genus Aesculus, while the enzymatic system of horse chestnut protection from the active forms of oxygen under stress is still poorly understood. The purpose of this study was to evaluate the reaction of catalase and two peroxidases of A. hippocastanum leaves, which differ in the level of damage by C. ohridella. The intensity of damage to A. hippocastanum leaves by the horse chestnut leaf miner in the park zones and botanical gardens of Dnipro city was determined, the activity and isoenzyme composition of benzidine-peroxidase, activity of guaiacol-peroxidase and catalase were measured. The lowest average benzidine-peroxidase activity was found in the group of trees with low level of leaf blight and the highest activity – in the group with high level. The opposite dependence was shown by catalase, the activity of which significantly decreases with increasing level of damage inflicted by the phytophage on the chestnut’s assimilating organs. Based on the determination of the variation coefficients, it has been shown that benzidine-peroxidase activity has a higher level of variability than that of catalase and guaiacol-peroxidase. It is established that under the influence of the leaf miner, activity of guaiacol-peroxidase was significantly higher by 87.1% and 75.6%, respectively, for medium and high levels of damage caused to the leaf by this phytophage as compared to that for low levels of damage. The increased level of leaf damage caused by the phytophage is reflected in the change in the isozyme profile of benzidine-peroxidase. The high activity of benzidine-peroxidase in the leaves of A. hippocastanum is due to the presence of several molecular forms that exhibit maximum activity in the narrow pH range (4.15–4.69). Quantitative redistribution of activity between the different molecular forms of benzidine peroxidase can be considered as the main regularity of changes in the expression of benzidine-peroxidase caused by different levels of leaf damage. The results showed that only one benzidine-peroxidase isoform with an isoelectric point of 4.15 shows a significant increase in activity (on average by 2.1 times) in A. hippocastanum leaves with medium and high levels of damage by C. ohridella. Significant reduction in activity is reported for dominant isoperoxidase with an isoelectric point of 4.25 revealing medium pest damage, and for high damage only a decreasing tendency is shown. The data obtained show that horse chestnut trees can specifically respond to mechanical damage by C. ohridella to leaves due to the changes in the activity of individual molecular forms of peroxidase. Further studies of oxidative metabolism are needed to understand the formation of resistance of representatives of the Aesculus genus to damage caused by this moth species based on a wider range of redox enzymes.

References

Allison, S. D., & Schultz, S. C. (2004). Differential activity of peroxidase isozymes in response to wounding, gypsy moth, and plant hormones in northern red oak (Quercus rubra L.). Journal Chemical Ecology, 30(7), 1363–1379.


Apers, S., Naessens, T., Pieters, L., & Vlietinck, A. (2006). Densitometric thin-layer chromatographic determination of aescin in a herbal medicinal product containing Aesculus and Vitis dry extracts. Journal of Chromatography A, 1112, 165–170.


Augustin, S., Guichard, S., Heitland, W., Freise, J., Svatoš, A., & Gilbert, M. (2008). Monitoring and dispersal of the invading Gracillariidae Cameraria ohridella. Journal of Applied Entomology, 133(1), 58–66.


Bagnoli, F., Capuana, M., & Racchi, M. L. (1998). Developmental changes of catalase and superoxide dismutase isoenzyme, in zygotic and somatic embryos of horse chestnut. Australian Journal of Plant Physiology, 25(8), 909–913.


Baraniak, E., Walczak, U., & Zduniak, P. (2005). Appearance and migration of the horse-chestnut leafminer Cameraria ohridella in relation to city size and leaf-raking, using the example of two cities in Western Poland, Journal Pest Science, 78, 145–149.


Baranovski, B., Khromykh, N., Karmyzova, L., Ivanko, I., & Lykholat, Y. (2016). Anyalysis of the alien flora of Dnipropetrovsk province. Biological Bulletin of Bogdan Chmelnitskiy Melitopol State Pedagogical University, 6(3), 419–429.


Bede, J. C., McNeil, J. N., & Tobe, S. S. (2006). The role of neuropeptides in ca­terpillar nutritional ecology. Peptides, 28, 185–196.


Bradford, M. M. (1976). A rapid and sensitive method for quantitation of microgram quantities of protein utilizing the principle of protein dye binding. Analytical Biochemistry, 72, 248–254.


Ćalić-Dragosavac, D., Zdravković-Korać, S., Šavikin-Fodulović, K., Radojevič, C., & Vinterhalter, B. (2010). Determination of aescin content in androgenic embryos and hairy root culture of Aesculus hippocastanum. Pharmaceutical Biology, 48(5), 563–567.


Chen, Z., Silva, H., & Klessing, D. F. (1993). Active oxygen species in the induction of plant systemic acquired resistance by salicylic acid. Science, 262(12), 1883–1886.


De Prins, J., De Prins, W., & De Coninck, E. (2003). The pupal morphology of Cameraria ohridella compared with that of the genus Phyllonorycter (Lepidoptera: Gracillariidae). Anzeiger für Schädlingskunde, 76(6), 145.


Didur, O. O., Kulbachko, Y. L., & Pakhomov, O. Y. (2018). Species structure of oribatid mite population (Acari, Oribatea) in the forest floor litter in the reclaimed territories (Ukraine). Vestnik Zoologii, 52(4), 331–340.


Dowd, D., Lagrimini, L. M., & Hermіs, D. A. (1999). Tobacco anionic peroxidase often increases resistance to insects in different dicotyledonous species. Pesticide Science, 55, 633–634.


Dowd, P. F., Hermis, D. A., Berhow, M. A., & Lagrimini, L. M. (2000). Mechanism of insect resistance in transgenic plants (over) expressing a tobacco anionic peroxidase. Plant Peroxidase Newsletter, 14, 93–101.


Dаbrowska, G., Kata, A., Goc, A., Szechynska-Hebda, M., & Skrzypek, E. (2007). Characteristics of the plant ascorbate peroxidase family. Acta Biologica Cracoviensia: Series Botanica, 49(1), 7–17.


Filho, O. G. (2006). Coffee leaf miner resistance. Brazilian Journal of Plant Physiology, 18(1), 109–117.


Gilbert, M., Gregoire, J. C., Freise, J. F., & Heitland, W. (2004). Long-distance dispersal and human population density allow the prediction of invasive patterns in the horse chestnut leafminer Cameraria ohridella. Journal of Animal Ecology, 73, 459–468.


Goth, L. (1991). A simple method for determination of serum catalase activity and revision of reference range. Clinica Chimica Acta, 196, 143–152.


Grabenweger, G., Kehrli, P., Schlick-Steiner, B., Steiner, F., Stolz, M., & Bacher, S. (2005). Predator complex of the horse chestnut leafminer Cameraria ohridella: Identification and impact assessment. Journal of Applied Entomology, 129(7), 353.


Gregory, R. P. F. (1966). A rapid assay for peroxidase activity. Biochemical Journal, 101(3), 582–583.


Hiraga, S., Sasaki, K., Ito, H., Ohashi, Y., & Matsui H. (2001). A large family of class III plant peroxidases. Plant Cell Physiology, 42(5), 462–468.


Holoborodko, K. K., Marenkov, O. M., Gorban, V. A., & Voronkova, Y. S. (2016). The problem of assessing the viability of invasive species in the conditions of the steppe zone of Ukraine. Visnyk of Dnipropetrovsk University, Biology, Ecology, 24(2), 466–472.


Holoborodko, K. K., Ryabka, K. O., Zaiceva, I. A., & Kondrat’eva, K. V. (2009). Poshyrennya ta suchasnyy stan kashtanovoyi minuyuchoyi moli (Cameraria ohridella Deschka & Dimič, 1986) u m. Dnipropetrovs’k [Distribution and current state of horse-chestnut leaf miner (Cameraria ohridella Deschka & Dimič, 1986) in Dnipropetrovsk]. Problems of Bioindications and Ecology, 14(2), 163–168 (in Ukrainian).


Hryhoryuk, I. P., & Luk’yanenko, T. L. (2015). Fiziolohichni i molekulyarni os­novy stiykosti vydiv roslyn rodu Aesculus L. proty kashtanovoyi minuyuchoyi moli [Physiological and molecular bases of resistance of species of plants of the genus Aesculus L. against horse-chestnut leaf miner]. Komprynt, Kyiv (in Ukrainian).


Jagiełło, R., Baraniak, E., Karolewski, P., Łakomy, P., Behnke-Borowczyk, J., Walczak, U., & Giertych, M. J. (2017). Ecophysiological aspects of the interaction between Cameraria ohridella and Guignardia aesculi on Aesculus hippocastanum. Dendrobiology, 78, 146–156.


Jagillo, E., Baraniak, E., Guzicka, M., Karolewsk, P., Ukowski, A., & Giertych, M. J. (2019). One step closer to understanding the ecology of Cameraria ohridella (Lepidoptera: Gracillariidae): The effects of light conditions. European Journal of Entomology, 116, 42–51.


Kharytonov, M. M., Kroik, A. A., Shupranova, L. V., & Vinnichenko, O. M. (2008). Air pollution assessment related with large industrial city activities. NATO RW: Simulation and assessment of chemical processes in a multiphase environment. Alushta, Ukraine. Pp. 385–393.


Kulbachko, Y. L., Didur, O. O., Loza, I. M., Pakhomov, O. E., & Bezrodnova, O. V. (2015). Environmental aspects of the effect of earthworm (Lumbricidae, Oligochaeta) tropho-metabolic activity on the pH buffering capacity of remediated soil (steppe zone, Ukraine). Biology Bulletin, 42(10), 899–904.


Lees, D. C., Lack, H. W., Rougerie, R., Hernandez-Lopez, A., Raus, T., Avtzis, N. D., Augustin, S., & Lopez-Vaamonde, C. (2011). Tracking origins of invasive herbivores through herbaria and archival DNA: The case of the horse-chestnut leaf miner. Frontiers in Ecology and the Environment, 9, 322–328.


Lev-Yadun, S., & Gould, K. S. (2009). Role of anthocyanins in plant defence. In: Gould, K., Davies, K., & Winefield, C. (Eds.). Anthocyanins, biosynthesis, functions, and applications. Springer, New-York. Pp. 21–48.


Low, P. S., & Merida, J. R. (1996). The oxidative burst in plant defence: Function and signal transduction. Physiologia Plantarum, 96, 533–542.


Loza, I. M., Pakhomov, O. Y., & Chorna, V. I. (2018). Evaluation of remediation ef­ficiency of manganese quarry lands after open-cut mining: Ecosystem appro­ach. Naukovyi Visnyk Natsionalnoho Hirnychoho Universytetu, (4), 122–128.


Lykholat, Y., Khromykh, N., Didur, O., Alexeyeva, A., Lykholat, T., & Davydov, V. (2018). Modeling the invasiveness of Ulmus pumila in urban ecosystems under climate change. Regulatory Mechanisms in Biosystems, 9(2), 161–166.


Mierziak, J., Kostyn, K., & Kulma, A. (2014). Flavonoids as important molecules of plant interactions with the environment. Molecules, 19, 16240–16265.


Mithofer, A., & Boland, W. (2012). Plant defense against herbivores: Chemical aspects. Annual Review of Plant Biology, 63, 431–450.


Oszmianski, J., Kalisz, S., & Wojdyło, A. (2014). The content of phenolic compounds in leaf tissues of white (Aesculus hippocastanum L.) and red horse chestnut (Aesculus carnea H.) colonized by the horse chestnut leaf miner (Cameraria ohridella Deschka & Dimic). Molecules, 19, 14625–14636.


Oszmianski, J., Kolniak-Ostek, J., & Biernat, A. (2015). The content of phenolic compounds in leaf tissues of Aesculus glabra and Aesculus parviflora Walt. Molecules, 20, 2176–2189.


Pasichnyy, H. V., & Serdyuk, S. M. (2002). Dynamika vazhkykh metaliv v hruntovomu pokryvi u zv’yazku z tekhnohennym zabrudnennyam otochuyuchoho seredovyshcha (na prykladi m. Dnipropetrovska) [Dynamics of heavy metals in the soil cover due to anthropogenic pollution of the environment (for example, Dnipropetrovsk)]. Ecology and Nature Management, 4, 111–117 (in Ukrainian).


Penteliuk, O., Likhanov, A., & Hrygoriuk, I. (2016). Dynamika vmistu polifenoliv u lystkakh roslyn hirkokashtana zvychaynoho (Aesculus hippocastanum L.) za umov mekhanichnykh poshkodzhen’ [Dynamics of polyphenols in the leaves of horse-chestnut (Aesculus hippocastanum L.) plants in the condition of mechanical damage]. Bioresursy i Pryrodokorystuvannya, 8, 5–12 (in Ukrainian).


Ranieri, A., Castagna, A., Baldam, B., & Soldatini, G. F. (2001). Iron deficiency differently affects peroxidase isoforms in sunflower. Journal of Experimental Botany, 52(354), 25–35.


Shupranova, L. V., Kharytonov, M. M., & Khlopova, V. M. (2014). Air pollution assessment in the Dnepropetrovsk industrial megapolice of ukraine. In: Proceedings of the 32nd NATO/SPS International Technical Meeting on Air Pollution Modeling and its Application. Utrecht, The Netherlands. 7–11 May, 2012. Springer Science+Business Media, Dordtrecht. Pp. 101–104.


Štajner, D., Popović, B. M., Ćalić, D., & Štajner, M. (2014). Comparative study of antioxidant status in androgenic embryos of Aesculus hippocastanum and Aesculus flava. The Scientific World Journal, 2014, 18–25.


Stygar, D., Dolezych, B., Nakonieczny, M., & Zaak, M. (2010). Digestive enzymes activity in larvae of Cameraria ohridella (Lepidoptera: Gracillariidae). Comptes Rendus Biologies, 333, 725–735.


Weryszko-Chmielewska, E., & Haratym, W. (2011). Changes in leaf tissues of common horse chestnut (Aesculus hippocastanum L.) colonised by the horse-chestnut leaf miner (Cameraria ohridella Deschka & Dimić). Acta Agrobotanica, 64, 11–22.


Zerova, M. D., Nikitenko, G. N., Narolsky, N. B., Gershenson, Z. S., Sviridov, S. V., Lukash, O. V., & Babidoritsh, M. M. (2007). Kashtanovaya mynyruyushchaya mol na Ukrayne [Horse-chesttnut leaf miner, Cameraria ohri­della, in Ukraine]. Veles, Kiev (in Russian).


Adams, R. P. (1995). Identification of essential oil components by gas chromato­graphy/mass spectroscopy. Allured Publishing Corporation, Carol Stream.


Anonymous (2011). European Pharmacopoeia, 7th ed. Council of Europe, Strasbourg.


Asghari, B., Salehi, P., Sonboli, A., & Nejad-Ebrahimi, S. (2015). Flavonoids from Salvia chloroleuca with α-amylsae and α-glucosidase inhibitory effect. Iranian Journal of Pharmaceutical Research, 14(2), 609–615.


Dudareva, N., Klempien, A., Muhlemann, J. K., & Kaplan, I. (2013). Biosynthesis, function and metabolic engineering of plant volatile organic compounds. New Phytologist, 198, 16–32.


Govaert, L., Pantel, J. H., & De Meester, L. (2016). Eco-evolutionary partitioning metrics: Assessing the importance of ecological and evolutionary contributions to population and community change. Ecological Letters, 19, 839–853.


Jamzad, Z. (2012). Flora of Iran. Vol. 76. Lamiaceae. Research Institute of Forest and Rangelands, Tehran.


Lima, M. E. L., Cordeiro, I., Young, M. C. M., Sobra, M. E. G., & Moreno, P. R. H. (2006). Antimicrobial activity of the essential oil from two specimens of Pimenta pseudocaryophyllus (Gomes) L. R. Landrum (Myrtaceae) native from São Paulo State-Brazil. Pharmacology Online, 3, 589–593.


Maffei, M. E., Gertsch, J., & Appendino, G. (2011). Plant volatiles: Production, function and pharmacology. Natural Product Reports, 28, 1359–1380.


Mozaffarian, V. (1996). A dictionary of Iranian plant names. Farhang Moaser, Tehran, Iran.


Palkovacs, E. P., & Post, D. M. (2009). Experimental evidence that phenotypic diver­gence in predators drives community divergence in prey. Ecology, 90, 300–305.


Paula, J. A. M., Ferri, P. H., Bara, M. T. F., Tresvenzol, L. M. F., Sá, F. A. S., & Paula, J. R. (2011). Infraspecific chemical variability in the essential oils of Pimenta pseudocaryophyllus (Gomes) L. R. Landrum (Myrtaceae). Biochemical Systematics and Ecology, 39, 643–650.


Potzernheim, M. C. L., Bizzo, H. R., & Vieira, R. F. (2006). Análise dos oleos essenciais de três espécies de Piper coletadas na região do Distrito Federal (Cerrado) e comparação com oleos de plantas procedentes da região de Paraty, RJ (Mata Atlântica). Revista Brasileira de Farmacognosia, 16, 246–251.


Rustaiyan, A., Masoudi, S., Monfared, A., & Komeilizadeh, H. (1999). Volatile constituents of three Salvia species grown wild in Iran. Flavour Fragrance Journal, 14, 276–278.


Stace, C. A. (1989). Plant taxonomy and biosystematics. Edward Arnold.


Talebi, S. M., Atri, M., Sheidai, M., Sharifnia, F., & Noormohammadi, Z. (2014). Infraspecific variations in Linum album based on the determination of special stations approach in Iran. Phytologia Balcanica, 20(1), 9–22.


Talebi, S. M., Nohooji, M. G., & Yarmohammadi, M. (2017a). Infraspecific va­riations in essential oil compositions of Nepeta fissa from Iran. Nusantara Bioscience, 9(3), 318–321.


Talebi, S. M., Nohooji, M. G., Yarmohammadi, M., Khani, M., & Matsyura, A. (2019). Effect of altitude on essential oil composition and on glandular trichome density in three Nepeta species (N. sessilifolia, N. heliotropifolia and N. fissa). Mediterranean Botany, 40(1), 81–93.


Talebi, S. M., Rezakhanlou, A., & Matsyura, A. (2017b). Do we have infraspecific taxa of Salvia multicaulis Vahl (Lamiaceae) in Iran? Ukrainian Journal of Ecology, 7(4), 432–439.


Talebi, S. M., Salahi Isfahani, G., & Azizi, N. (2014). Inter and intrapopulation variations in Stachys inflate Benth. based on phenotype plasticity (an ecological and phytogeographical review). International Research Journal of Biological Sciences, 3(2), 9–20.


Talebi, S. M., Yadegari, P., Behzadpour, S., & Matsyura, A. (2019). Infraspecific morphological variations of Salvia limbata in Iran. Acta Biologica Sibirica, 5(1), 113–121.


Tayarani-Najarana, Z., Asili, J., Aioubi, E., & Emami, S. A. (2013). Growth inhibition and apoptosis induction of Salvia chloroleuca on MCF-7 breast cancer cell line. Iranian Journal of Pharmaceutical Research, 12(4), 789–799.


Topcu, G. (2006). Bioactive triterpenoids from Salvia species. Journal of Natural Products, 69, 482–487.


Tzakou, O., Pitarokili, B., Chinou, L. B., & Harvala, C. (2001). Composition and antimicrobial activity of the essential oil of Salvia vingens. Planta Medica, 67, 81–83.


Ulubelen, A., Tan, N., & Topcu, G. (1997). Terpenoid from Salvia candidissima subsp. candidissima. Phytochemistry, 45, 1221–1223.


Violle, C., Enquist, B. J., McGill, B. J., Jiang, L., Albert, C. H., Hulshof, C., Jung, V., & Messier, J. (2012). The return of the variance: Intraspecific variability in community ecology. Trends in Ecology and Evolution, 27(4), 244–252.


Yadollahi, A., Firouznia, A., & Rajab Zadeh, G. (2013). Chemical composition and antibacterial properties of the essential oil of Salvia chloroleuca Rech. F. & Allen in North Khorasan Province. Journal of North Khorasan University of Medical Sciences, 4(5), 69–76.


Yarmoohammadi, M., Talebi, S. M., & Nohooji, M. G. (2017). Infraspecific vari­ations in essential oil and glandular trichomes in Nepeta heliotropifolia. Biodiversitas, 18, 964–970.


Yousefzadi, M., Sonboli, A., Nejad-Ebrahimi, S., & Hashemi, S. H. (2008). Anti­microbial activity of essential oil and major constituents of Salvia chloroleuca. Zeitschrift für Naturforschung C, Journal of Biosciences, 63, 337–340.


Zohary, M. (1973). Geobotanical Foundations of the Middle East. Vol. 2. Gustav Fisher Verlag, Stuttgart.

Published
2019-08-13
Section
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