Determination of secondary metabolite in galls of some cynipid wasps (Hymenoptera: Cynipidae) and characterization of the phenolic compound

Year 2023, Volume: 10 Issue: 4, 555 - 569, 01.12.2023

Musa Tataroğlu Özge Kılınçarslan Aksoy Yusuf Katılmış Ramazan Mammadov

https://doi.org/10.21448/ijsm.1300763

Abstract

The galls of cynipid species (Hymenoptera: Cynipidae) have been used since ancient times as an important source of bioactive compounds. Many researchers have evaluated the medicinal potential of some cynipid galls and found that these galls have numerous ethnomedical uses. The aim of this study was to determine the total bioactive (phenolic, flavonoid and tannin) compound amounts of gall extracts, to reveal the phenolic compound contents by HPLC method and to set ground for future pharmaceutical studies. The galls of cynipid wasps (totally 24 taxa) on host plants were collected from the Eastern Black Sea Region of Türkiye. Acetone, ethanol, methanol, and water extracts of these galls were prepared for quantity analysis and HPLC. The phenolic compound amounts (phenolic, flavonoid and tannin) of the cynipid gall extracts were determined, and their phenolic compound contents were also revealed. Some phenolic compounds in ethanol gall extracts were analyzed using HPLC, and some of these compounds were detected for the first time in the cynipid galls. 2,5-dihydroxybenzoic acid, caffeic acid, epicatechin, and ellagic acid are the most abundant in the ethanolic gall extracts. Total phenolic, flavonoid and tannin amounts of the cynipid gall extracts showed high variation. All these studies on quantification and characterization of phenolic compound are the first detailed studies on these taxa of cynipid galls and show that these cynipid galls might pharmaceutically be an important source for human and animal health.

Keywords

Cynipid, Gall, Phenolic, Tannin, Flavonoid

Project Number

117Z096

References

• Abrahamson, W.G., McCrea, K.D., Whitwell, A.J., & Vernieri, L.A. (1991). The role of phenolics in goldenrod ball gall resistance. Biochemical Systematics and Ecology, 19(8), 615-622. https://doi.org/10.1016/0305-1978(91)90077-D
• Achakzai, A.K.K., Achakzai, P., Masood, A., Kayani, S.A., & Tareen, R.B. (2009). Response of plant parts and age on the distribution of secondary metabolites on plants found in Quetta. Pakistan Journal of Botany, 41(5), 2129-2135.
• Arvouet-Grand, A., Vennat, B., Pourrat, A., & Legret, P. (1994). Standardisation d'un extrait de propolis et identification des principaux constituants [Standardization of propolis extract and identification of principal constituents]. Journal de pharmacie de Belgique, 49(6), 462-468.
• Asif, M., Ansari, S.H., Haquea, Md.R., & Kalam, N. (2012). Estimation of total phenolic, flavonoid contents and antioxidant activity in the nut galls of Quercus infectoria Olivier. Journal of Pharmacy Research, 5(7), 3855-3857.
• Azmaz, M., & Katılmış, Y. (2017). Updated species list of Cynipidae (Hymenoptera) from Turkey. Zootaxa, 4303(3), 361-378. https://doi.org/10.11646/zootaxa.4303.3.3
• Azmaz, M., & Katılmış, Y. (2020a). A new species of herb gall wasp (Cynipidae, Aulacideini, Aulacidea) from Turkey. Zootaxa, 4747(2), 378 390. https://doi.org/10.11646/zootaxa.4747.2.9
• Azmaz, M., & Katılmış, Y. (2020b). A new species of Cynips (Cynipidae: Cynipini) from Turkey. Zoology in the Middle East, 66(3), 232 239. https://doi.org/10.1080/09397140.2020.1782579
• Azmaz, M., & Katılmış, Y. (2021a). Three new species of herb gall wasps (Hymenoptera: Cynipidae) from Turkey. European Journal of Taxonomy, 757(1), 152 168. https://doi.org/10.5852/ejt.2021.757.1421
• Azmaz, M., & Katılmış, Y. (2021b). Two new oak gall wasp species (Hymenoptera: Cynipidae, Cynipini) from Quercus pontica (Fagaceae) in Turkey. Zootaxa, 5016(3), 382-394. https://doi.org/10.11646/zootaxa.5016.3.4
• Azmaz, M., Kılınçarslan Aksoy, Ö., Katılmış, Y., & Mammadov, R. (2020). Investigation of the antioxidant activity and phenolic compounds of Andricus quercustozae gall and host plant (Quercus infectoria). International Journal of Secondary Metabolite, 7(2), 77-87. https://doi.org/10.21448/ijsm.674930
• Azmaz, M. (2021). Quercus infectoria Oliv. (Mazı Meşesi) köklerinde oluşan mazılar (Hymenoptera: Cynipidae): İki yeni kayıt [Cynipid Galls (Hymenoptera: Cynipidae) on Roots of Quercus infectoria Oliv.: Two new records from Turkey]. Turkish Journal of Forestry, 22(2), 91-96. https://doi.org/10.18182/tjf.908162
• Barton, K.E., & Koricheva, J. (2010). The ontogeny of plant defense and herbivory: characterizing general patterns using meta‑analysis. The American Naturalist, 175(4), 481-493. https://doi.org/10.1086/650722
• Bayrak, S., & Avcı, M. (2019). Gall forming Cynipini (Hymenoptera: Cynipidae) species in Isparta oak forests. Munis Entomology & Zoology, 14(2), 552-564.
• Bekir, J., Mars, M., Souchard., J.P., & Bouajila, J. (2013). Assessment of antioxidant, antiinflammatory, anti-cholinesterase and cytotoxic activities of pomegranate (Punica granatum) leaves. Food and Chemical Toxicology, 55, 470 475. https://doi.org/10.1016/j.fct.2013.01.036
• Bhattacharya, A., Sood, P., & Citovsky, V. (2010). The roles of plant phenolics in defence and communication during Agrobacterium and Rhizobium infection. Molecular Plant Pathology, 11(5), 705-719. https://doi.org/10.1111/j.1364-3703.2010.00625.x
• Bragança, G.P., Oliveira, D.C., & Isaias, R.M.S. (2017). Compartmentalization of metabolites and enzymatic mediation in nutritive cells of Cecidomyiidae galls on Piper arboreum Aubl. (Piperaceae). Journal of Plant Studies, 6(1), 11-22. https://doi.org/10.5539/jps.v6n1p11
• Bronner, R. (1992). Biology of insect-induced galls: The role of nutritive cells in the nutrition of cynipids and cecidomyiids. Oxford University Press.
• Buffington, M.L., Forshage, M., Liljeblad, J., Tang, C-T., & van Noort, S. (2020). World Cynipoidea (Hymenoptera): A Key to Higher-Level Groups. Insect Systematics and Diversity, 4(4), 1-69. https://doi.org/10.1093/isd/ixaa003
• Caponio, F., Alloggio, V., & Gomes, T. (1999). Phenolic compounds of virgin olive oil: influence of pastepreperation techniques. Food Chemistry, 64(2), 203-209. https://doi.org/10.1016/S0308-8146(98)00146-0
• Chikezie, P.C., Ibegbulem, C.O., & Mbagwu, F.N. (2015). Bioactive principles from medicinal plants. Research Journal of Phytochemistry, 9(3), 88 115. https://doi.org/10.3923/rjphyto.2015.88.115
• Chomel, M., Guittonny‑Larcheveque, M., Fernandez, C., Gallet, C., DesRochers, A., Paré, D., Jackson, B.G., & Baldy, V. (2016). Plant secondary metabolites: a key driver of litter decomposition and soil nutrient cycling. Journal of Ecology, 104(6), 1527-1541. https://doi.org/10.1111/1365-2745.12644
• Cornell, H.V., & Hawkins, B.A. (2003). Herbivore responses to plant secondary compounds: a test of phytochemical coevolution theory. The American Naturalist, 161(4), 507-522. https://doi.org/10.1086/368346
• Cuevas-Reyes, P., Quesada, M., Hanson, P., Dirzo, R., & Oyama, K. (2004). Diversity of gall-inducing insects in a Mexican tropical dry forest: the importance of plant species richness, life forms, host plant age and plant density. Journal of Ecology, 92(4), 707-716. https://doi.org/10.1111/j.0022-0477.2004.00896.x
• Del Rio, D., Rodriguez-Mateos, A., Spencer, J.P.E., Tognolini, M., Borges, G., & Crozier, A. (2013). Dietary (Poly)phenolics in human health: structures, bioavailability, and evidence of protective effects against chronic diseases. Antioxidants & Redox Signaling, 18(14), 1818-1892. https://doi.org/10.1089/ars.2012.4581
• Demirel, M., Azmaz, M., & Katılmış, Y. (2022). A new species of oak gall wasp (Hymenoptera: Cynipidae, Cynipini) from Turkey. Zootaxa, 5087(4), 583 590. https://doi.org/10.11646/zootaxa.5087.4.6
• Demirel, M., Tataroğlu, M., & Katılmış, Y. (2023). Cynipidae (Hymenoptera, Cynipoidea) fauna of Burdur province (Türkiye). Zootaxa, 5296(3), 362 380. https://doi.org/10.11646/zootaxa.5296.3.3
• Detoni, M., Vasconcelos, E.G., Scio, E., Aguiar, J.A.K., Isaias, R.M.S., & Soares, G.L.G. (2010). Differential biochemical responses of Calliandra brevipes (Fabaceae, Mimosoidae) to galling behaviour by Tanaostigmodes ringueleti and T. mecanga (Hymenoptera, Tanaostigmatidae). Australian Journal of Botany, 58(4), 280 285. https://doi.org/10.1071/BT09213
• Elham, A., Arken, M., Kalimanjan, G., Arkin, A., & Iminjan, M. (2021). A review of the phytochemical, pharmacological, pharmacokinetic, and toxicological evaluation of Quercus infectoria galls. Journal of Ethnopharmacology, 273, 113592. https://doi.org/10.1016/j.jep.2020.113592
• Eyüpoğlu, F. (1999). Türkiye Topraklarının Verimlilik Durumu [The Fertility Status of Turkish Agricultural Soils]. T.C. Başbakanlık Köy Hizmetleri Genel Müdürlüğü, Toprak ve Gübre Araştırma Enstitüsü Yayınları, Genel Yayın No: 220.
• Fatih, B., & Gençer, L. (2022). New Record of Inquiline Wasp of The Genus Synergus Hartig, 1840 From Sivas, Turkey. ISPEC Journal of Agr. Sciences, 6(3), 591-596. https://doi.org/10.5281/zenodo.7038169
• Ferreira, B.G., Avritzer, S.C., & Isaias, R.M.S. (2017). Totipotent nutritive cells and indeterminate growth in galls of Ditylenchus gallaeformans (Nematoda) on reproductive apices of Miconia. Flora, 227, 36-45. https://doi.org/10.1016/j.flora.2016.12.008
• Fürstenberg-Hägg, J., Zagrobelny, M., & Bak, S. (2013). Plant defense against insect herbivores. International Journal of Molecular Sciences, 14(5), 10242-10297. https://doi.org/10.3390/ijms140510242
• Galla, B.P. (1911). Galls. The British Pharmaceutical Codex. Council of the Pharmaceutical Society of Great Britain.
• Gao, J., Yang, X., Yin, W., & Li, M. (2018). Gallnuts: A Potential Treasure in Anticancer Drug Discovery. Evidence-Based Complementary and Alternative Medicine, 4930371. https://doi.org/10.1155/2018/4930371
• Giron, D., Huguet, E., Stone, G.N., & Body, M. (2016). Insect-induced effects on plants and possible effectors used by galling and leaf-mining insects to manipulate their host-plant. Journal of Insect Physiology, 84, 70-89. https://doi.org/10.1016/j.jinsphys.2015.12.009
• Hartley, S.E. (1998). The chemical composition of plant galls: are levels of nutrients and secondary compounds controlled by the gall-former? Oecologia, 113, 492-501. https://doi.org/10.1007/s004420050401
• Hu, J., Gao, J., Zhao, Z., Yang, X., & Chen, L. (2020). Extraction Optimization of Galla Turcica Polysaccharides and Determination of Its Antioxidant Activities In Vitro. Natural Product Communications, 15(3), 1-9. https://doi.org/10.1177/1934578X20911764
• Hussein, R.A., & El-Anssary, A.A. (2019). Plants Secondary Metabolites: The Key Drivers of the Pharmacological Actions of Medicinal Plants. Intech Open. https://doi.org/10.5772/intechopen.76139
• Iminjan, M., Amat, N., Li, X.H., Upur, H., Ahmat, D., & He, B. (2014). Investigation into the Toxicity of traditional Uyghur medicine Quercus infectoria galls water extract. PLoS One, 9, e90756. https://doi.org/10.1371/journal.pone.0090756
• Imtiyaz, S., Ali, S.J., Tariq, M., Chaudhary, S.S., & Aslam, M. (2013). Oak Galls: The Medicinal Balls. Journal of Pharmaceutical and Scientific Innovation, 2(1), 18-21.
• Isaias, R.M.D.S., Carneiro, R.G.S., Oliveira, D.C., & Santos, J.C. (2013). Illustrated and annotated checklist of Brazilian gall morphotypes. Neotropical Entomology, 42(3), 230-239. https://doi.org/10.1007/s13744-013-0115-7
• Isaias, R.M.S., Soares, G.L.G., Christiano, J.C.S., Gonçalves, S.J.M.R. (2000). Análise comparativa entre as defesas mecânicas e químicas de Aspidosperma australe Müell. Arg. E Aspidosperma cylindrocarpon Müell. Arg. (Apocynaceae) contra herbivoria [Comparative analysis between mechanical and chemical defenses in Aspidospema australe Müell. Arg. and Aspidosperma cylindrocarpon Müell. Arg. (Apocynaceae) against herbivory]. Floresta e Ambiente, 7(1), 19-30.
• Iylia Arina, M.Z., & Harisun, Y. (2019). Effect of extraction temperatures on tannin content and antioxidant activity of Quercus infectoria (Manjakani). Biocatalysis and Agricultural Biotechnology, 19, 101104. https://doi.org/10.1016/j.bcab.2019.101104
• Kariñho-Betancourt, E., Hernández-Soto, P., Rendón-Anaya, M., Calderón-Cortés, N., & Oyama, K. (2019). Differential expression of genes associated with phenolic compounds in galls of Quercus castanea induced by Amphibolips michoacaensis. Journal of Plant Interactions, 14(1), 177-186. https://doi.org/10.1080/17429145.2019.1603404
• Kılınçarslan Aksoy, Ö., Mammadov, R., & Seçme, M. (2020). Antioxidant activity, phytochemical composition of Andricus tomentosus and its antiproliferative effect on Mia-Paca2 cell line. Molecular Biology Reports, 47, 7633-7641. https://doi.org/10.1007/s11033-020-05833-5
• Kot, I., Sempruch, C., Rubinowska, K., & Michalek, W. (2019). Effect of Neuroterus quercusbaccarum (L.) galls on physiological and biochemical response of Quercus robur leaves. Bulletin of Entomological Research, 110(1), 34 43. https://doi.org/10.1017/S0007485319000221
• Kuster, V.C., Rezende, U.C., Cardoso, J.C.F., Isaias, R.M.S., & Oliveira, D.C. (2020). Co-Evolution of Secondary Metabolites: How Galling Organisms Manipulate the Secondary Metabolites in the Host Plant Tissues? A Histochemical Overview in Neotropical Gall Systems. Springer International Publishing. https://doi.org/10.1007/978-3-319-96397-6_29
• Larew, H.G. (1987). Oak galls preserved by the eruption of Mount Vesuvius in AD 79, and their probable use. Economic Botany, 41, 33-40. https://doi.org/10.1007/BF02859343
• Lattanzio, V. (2013). Natural Products: Phenolic Compounds: Introduction. Berlin, Heidelberg: Springer. https://doi.org/10.1007/978-3-642-22144-6_57
• Mammadov, R., Ili, P., Ertem Vaizoğullar, H., & Afacan Makascı, A. (2011). Antioxidant Activity and Total Phenolic Content of Gagea fibrosa and Romulea ramiflora. Iranian Journal of Chemistry and Chemical Engineering, 30(3), 57 62. https://doi.org/10.30492/IJCCE.2011.6218
• Mammadov, R. (2014). Tohumlu Bitkilerde Sekonder Metabolitler [Secondary Metabolites in Seed Plants]. Nobel Akademik Yayıncılık.
• Mani, M.S. (1964). Ecology of plant galls. Dr. W. Junk Publish, Hague.
• Mutun, S., Dinç, S., & Melika, G. (2020). Two new species of oak gall wasps from Turkey (Hymenoptera: Cynipidae, Cynipini). Zootaxa, 4890(3), 428 438. https://doi.org/10.11646/zootaxa.4890.3.9
• Noori, M., Talebi, M., & Ahmadi, T. (2015). Comparative Studies of Leaf, Gall and Bark Flavonoids in Collected Quercus brantii Lindl. (Fagaceae) from Lorestan Province, Iran. International Journal of Plant Research, 5(2), 42-49.
• Oefele, F. (1933). Geschichte der Cecidologie: Vorgeschichte zur Cecidologie der klassischen Schriftsteller. Teil 1, Arthur Nemayer, Mittenwald.
• Oliveira, D.C., Isaias, R.M.S., Fernandes, G.W., Ferreira, B.G., Carneiro, R.G.S, & Fuzaro, L. (2016). Manipulation of host plant cells and tissues by gall-inducing insects and adaptive strategies used by different feeding guilds. Journal of Insect Physiology, 84, 103-113. https://doi.org/10.1016/j.jinsphys.2015.11.012
• Oliveira, D.C., Moreira, A.S.F.P., & Isaias, R.M.S. (2014). Neotropical insect galls: Functional gradients in insect gall tissues, studies on neotropical host plants. Springer Netherlands.
• Özyazıcı, M.A., Aydoğan, M., Bayraklı, B., & Dengiz, O. (2013). Basic Characteristic Properties and Fertility Conditions of The Red-Yellow Podzolic Soils in Eastern Black Sea Region. Anadolu Journal of Agricultural Sciences, 28(1), 24 32. https://doi.org/10.7161/anajas.2013.281.24
• Price, P.W., Waring, G.L., & Fernandes, G.W. (1986). Hypotheses on the adaptive nature of galls. Proceedings of the Entomological Society of Washington, 88(2), 361-363.
• Price, P.W., Fernandes, G.W., & Waring, G.L. (1987). Adaptive nature of insect galls. Environmental Entomology, 16(1), 15-24. https://doi.org/10.1093/ee/16.1.15
• Rokas, A., Atkinson, R.J., Webster, L.M.I., Csóka, G., & Stone, G.N. (2003). Out of Anatolia: longitudinal gradients in genetic diversity support an eastern origin for a Circum-Mediterranean oak gall wasp Andricus quercustozae. Molecular Ecology, 12, 2153-2174. https://doi.org/10.1046/j.1365-294X.2003.01894.x
• Ronquist, F., Nieves-Aldrey, J.L., Buffington, M.L., Liu, Zh., Liljeblad, J., & Nylander, J.A.A. (2015). Phylogeny, Evolution and Classification of Gall Wasps: The Plot Thickens. PLoS ONE, 10(5), 1-40. https://doi.org/10.1371/journal.pone.0123301
• Schimitschek, E. (1953). Forestry insects of Turkey and its surrounding. İstanbul University Publications.
• Slinkard, K., & Singleton, V.L. (1977). Total phenol analyses: Automation and comparison with manual methods. American Journal of Enology and Viticulture, 28, 49-55. https://doi.org/10.5344/ajev.1977.28.1.49
• Stone, G.N., & Schönrogge, K. (2003). The adaptive significance of insect gall morphology. Trends in Ecology & Evolution, 18(10), 512-522. https://doi.org/10.1016/S0169-5347(03)00247-7
• Sukor, N.F., Jusoh, R., & Kamarudin, N.S. (2020). Focused–type ultrasound extraction of phenolic acids from Q. infectoria galls: Process modelling and sequential optimization. Chemical Engineering and Processing - Process Intensification, 154, 108004. https://doi.org/10.1016/j.cep.2020.108004
• Taper, M.L., & Case, T.J. (1987). Interactions between oak tannins and parasite community structure: Unexpected benefits of tannins to cynipid gall-wasps. Oecologia, 71, 254-261. https://doi.org/10.1007/BF00377292
• Tataroğlu, M., & Katılmış, Y. (2022). First record of Barbotinia oraniensis (Barbotin, 1964) (Hymenoptera: Cynipidae) from Turkey. Turkish Journal of Forestry, 23(2), 103-105. https://doi.org/10.18182/tjf.1126406
• Vuolo, M.M., Lima, V.S., & Junior, M.R.M. (2019). Bioactive compounds: health benefits and potential applications. phenolic compounds: structure, classification, and antioxidant Power. Woodhead Publishing. https://doi.org/10.1016/B978-0-12-814774-0.00002-5
• Yılmaz Sarıözlü, N., & Kıvanç, M. (2011). Nuts and Seeds in Health and Disease Prevention: Gallnuts (Quercus infectoria Oliv. and Rhus chinensis Mill.) and Their Usage in Health. Academic Press. https://doi.org/10.1016/B978-0-12-375688-6.10060-X
• Yusof, W.N.S.W., & Abdullah, H. (2020). Phytochemicals and Cytotoxicity of Quercus infectoria Ethyl Acetate Extracts on Human Cancer Cells. Tropical Life Sciences Research, 31(1), 69-84. https://doi.org/10.21315/tlsr2020.31.1.5
• Zhang, Y., Wu, S., Qin, Y., Liu, J., Liu, J., Wang, Q., Ren, F., & Zhang, H. (2018). Interaction of phenolic acids and their derivatives with human serum albumin: structure affinity relationships and effects on antioxidant activity. Food Chemistry, 240, 1072-1080. https://doi.org/10.1016/j.foodchem.2017.07.100