Effect on Total Phenolic, Total Flavonoid, and Antioxidant Activity in Hazelnut Kernels Damaged by Brown Marmorated Stink Bug [Halyomorpha halys Stal (Hemiptera: Pentatomidae)]

Yıl 2024, Cilt: 7 Sayı: 6, 1321 - 1326, 15.11.2024

Orhan Karakaya , İsmail Oğuz Özdemir , Umut Ateş , Burhan Öztürk , Mansur Uluca , Celal Tuncer

https://doi.org/10.34248/bsengineering.1555222

Öz

This study was carried out to determine the changes in bioactive compounds in necrotic kernels of Palaz hazelnut (Corylus avellana L.) cultivar damaged by brown marmorated stink bug (BMSB), Halyomorpha halys (Hemiptera: Pentatomidae). For this purpose, total phenolics, total flavonoids and antioxidant activity were determined in healthy kernel (HK) (control), whole of damaged kernel (WDK), healthy part of damaged kernel (HPDK) and necrotic part of damaged kernel (NPDK). The total phenolics, total flavonoids and antioxidant activity of the hazelnut kernel injured by BMSB increased as compared with the HK. The highest total phenolics was determined in NPDK (1781.3 mg 100 g-1), while the lowest in HPDK and HK (130.1 and 275.4 mg 100 g-1, respectively). The highest total flavonoids were determined in NPDK (679.0 mg 100 g-1) compared to the HK (64.5 mg 100 g-1). According to DPPH and FRAP assays, the highest antioxidant activity was determined in NPDK (7.20 and 49.10 mmol kg-1, respectively), and the lowest in HK (1.48 and 18.55 mmol kg-1, respectively). As a conclusion, the increase in phenolics, flavonoids, and antioxidants in the injured kernel can be due to the plant's natural defense mechanism against biotic stress because of the insect.

Anahtar Kelimeler

Bioactive compounds, Brown marmorated stink bug, Insect damage, Invasive, Necrotic kernel

Etik Beyan

-

Destekleyen Kurum

-

Proje Numarası

-

Teşekkür

-

Kahverengi Kokarca, Halyomorpha halys Stal (Hemiptera: Pentatomidae)’nın İç Fındıktaki Zararının Toplam Fenolik, Toplam Flavonoid ve Antioksidan Aktivite Üzerine Etkisi

Öz

Bu çalışma, kahverengi kokarca, Halyomorpha halys (Hemiptera: Pentatomidae)’nın Palaz fındık (Corylus avellana L.) çeşidinde beslenmesi sonucu ortaya çıkan lekeli iç fındıklardaki biyoaktif bileşiklerin değişimini belirlemek amacıyla yürütülmüştür. Bu amaçla sağlıklı iç (Sİ) (kontrol), lekeli iç fındığın tamamı (LİT), lekeli iç fındığın sağlıklı kısmı (LİS) ve lekeli iç fındığın nekrotik (LİN) kısımlarındaki toplam fenolik, toplam flavonoid ve antioksidan aktivite belirlenmiştir. Sİ meyvelerine kıyasla zarar gören meyvelerde toplam fenolik, toplam flavonoid ve antioksidan aktivite artmıştır. En yüksek toplam fenolik LİN meyvelerinde (1781.3 mg 100 g-1) belirlenirken, en düşük Sİ ve LİS meyvelerinde (sırasıyla 130.1 ve 275.4 mg 100 g-1) tespit edilmiştir. Sİ (64.5 mg 100 g-1) meyvelerine kıyasla en yüksek toplam flavonoid LİN meyvelerinde (679.0 mg 100 g-1) belirlenmiştir. DPPH ve FRAP testlerine göre en yüksek antioksidan aktivite LİN meyvelerinde (sırasıyla 7.20 ve 49.10 mmol kg-1) tespit edilmiştir. En düşük antioksidan aktivite ise Sİ meyvelerinde (sırasıyla 1.48 ve 18.55 mmol kg-1) belirlenmiştir. Sonuç olarak, zarar gören fındık meyvelerindeki fenolikler, flavonoidler ve antioksidanlardaki artışın böcek kaynaklı biyotik strese karşı bitkinin doğal savunma mekanizmasından kaynaklandığı söylenebilir.

Anahtar Kelimeler

Biyoaktif bileşikler, Böcek zararı, İstilacı, Kahverengi kokarca, Lekeli iç

Etik Beyan

-

Destekleyen Kurum

-

Proje Numarası

-

Teşekkür

-

Kaynakça

• Adjei-Fremah S, Jackai LE, Schimmel K, Worku M. 2018. Microarray analysis of the effect of Cowpea (Vigna unguiculata) phenolic extract in bovine peripheral blood. J Appl Anim Res, 46(1): 100-106.
• Ak K, Tuncer C, Baltacı A, Eser Ü, Saruhan İ. 2018. Incidence and severity of stink bugs damage on kernels in Turkish hazelnut orchards. Acta Hortic, 1226: 379–384.
• Ak K, Uluca M, Aydin Ö, Gokturk T. 2019. Important invasive species and its pest status in Turkey: Halyomorpha halys (Stål) (Heteroptera: Pentatomidae). J Plant Dis Prot, 126(5): 401-408
• Ak K, Uluca M, Tunçer C. 2023. Distribution and population density of Halyomorpha halys (Stål, 1855) (Hemiptera: Pentatomidae) in Black Sea Region of Türkiye. Turk J Zool, 47(2): 120-129.
• Arshiya S. 2013. The antioxidant effect of certain fruits. Int J Pharm Sci Res, 5(12): 265-268.
• Balta MF, Yarılgaç T, Aşkın MA, Kuçuk M, Balta F, Özrenk K. 2006. Determination of fatty acid compositions, oil contents and some quality traits of hazelnut genetic resources grown in eastern Anatolia of Turkey. J Food Compos Anal, 19(6-7): 681-686.
• Benzie IF, Strain JJ. 1996. The ferric reducing ability of plasma (FRAP) as a measure of “antioxidant power”: the FRAP assay. Anal Biochem, 239(1): 70-76.
• Blois MS. 1958. Antioxidant determinations by the use of a stable free radical. Nature, 181: 1199-1200.
• Bosco L, Moraglio ST, Tavella L. 2018. Halyomorpha halys, a serious threat for hazelnut in newly invaded areas. J Pest Sci, 91(2): 661-670.
• Buchanan BB, Gruissem W, Jones RL. 2015. Biochemistry and Molecular Biology of Plants. John Wiley & Sons, London, UK, 2nd ed., pp: 1132.
• Chang CC, Yang MH, Wen HM, Chern JC. 2002. Estimation of total flavonoid content in propolis by two complementary colorimetric methods. J Food Drug Anal, 10(3): 165.
• EPPO, 2024. European and Mediterranean Plant Protection Organization. Halyomorpha halys (HALYHA): URL: https://gd.eppo.int/taxon/HALYHA/distribution (accessed date: May 27, 2024).
• FAO, 2022. Food and agriculture organization statistics. Hazelnut production statistics. Retrieved March 7, 2023 from: 〈https://www.fao.org/faostat/en/#data/QCL (accessed date: May 27, 2024).
• Grazia J, Panizzi AR, Greve C, Schwertner CF, Campos LA, de A. Garbelotto T, Fernandes JAM. 2015. Stink bugs (Pentatomidae): True bugs (Heteroptera) of the neotropics. Entomology in Focus, vol 2. Springer, Dordrecht, New York, USA, pp: 681-756.
• Hamilton GC, Ahn JJ, Bu W, Leskey TC, Nielsen AL, Park YL, Rabitsch W, Hoelmer KA. 2018. Halyomorpha halys (Stål). McPherson, J. E. (ed.): in: Invasive Stink Bugs and Related Species (Pentatomoidea) (s. 243-293): Boca Raton, Florida, USA, pp: 165.
• Hedstrom CS, Shearer PW, Miller JC, Walton VM. 2014. The effects of kernel feeding by Halyomorpha halys (Hemiptera: Pentatomidae) on commercial hazelnuts. J Econ Entomol, 107(5): 1858-1865.
• Ivancic T, Grohar MC, Jakopic J, Veberic R, Hudina M. 2022. Effect of brown marmorated stink bug (Halyomorpha halys Stål.) infestation on the phenolic response and quality of olive fruits (Olea europaea L.). Agronomy, 12(9): 2200.
• Karakaya O, Yaman İ, Kırkaya H, Uzun S, Kaya T, Balta MF. 2023. Effect of Cluster Drop Intensity on Nut Traits, Biochemical Properties, and Fatty Acids Composition in the ‘Çakıldak’ Hazelnut Cultivar. Erwerbs-Obstbau, 65(4): 785-793.
• Karakaya O. 2023. The intensity of cluster drop affects bioactive compounds and fatty acids composition in hazelnut. Grasas y Aceites, 74(1): e487.
• Kaur H, Salh PK, Singh B. 2017. Role of defense enzymes and phenolics in resistance of wheat crop (Triticum aestivum L.) towards aphid complex. J Plant Interact, 12(1): 304-311.
• Khavari M, Fatahi R, Zamani Z. 2021. Salicylic acid and kaolin effects on pomological, physiological, and phytochemical characters of hazelnut (Corylus avellana) at warm summer condition. Sci Rep, 11(1): 4568.
• Kistner EJ. 2017. Climate change impacts on the potential distribution and abundance of the brown marmorated stink bug (Hemiptera: Pentatomidae) with special reference to North America and Europe. Environ Entomol, 46(6): 1212-1224.
• Lattanzio V, Cardinali A, Linsalata V. 2012. Plant phenolics: a biochemical and physiological perspective. Recent Adv Polyphenol Res, 3: 1-39.
• Li X, Xiu D, Huang J, Yu B, Jia S, Song L. 2023. Nutshell Physicochemical Characteristics of Different Hazel Cultivars and Their Defensive Activity toward Curculio nucum (Coleoptera: Curculionidae). Forests, 14(2): 319.
• Lucini T, Panizzi AR. 2018a. Electropenetrography (EPG): a breakthrough tool unveiling stink bug (Pentatomidae) feeding on plants. Neo Entomol, 47(1): 6-18.
• Lucini T, Panizzi AR. 2018b. Electropenetrography monitoring of the neotropical brown-stink bug (Hemiptera: Pentatomidae) on soybean pods: an electrical penetration graph-histology analysis. J Insect Sci, 18(6): 5.
• Memoli A, Albanese D, Esti M, Lombardelli C, Crescitelli A, Di Matteo M, Benucci I. 2017. Effect of bug damage and mold contamination on fatty acids and sterols of hazelnut oil. Eur Food Res Technol, 243: 651-658.
• Mierziak J, Kostyn K, Kulma A. 2014. Flavonoids as important molecules of plant interactions with the environment. Molecules, 19(10): 16240-16265.
• Moraglio ST, Bosco L, Tavella L. 2018. Halyomorpha halys invasion: a new issue for hazelnut crop in northwestern Italy and western Georgia? Acta Hortic, (1226): 379-384.
• Murvanidze M, Krawczyk G, Inasaridze N, Dekanoidze L, Samsonadze N, Macharashvili M, Khutsıshvılı S, Shengelaia S. 2018. Preliminary data on the biology of brown marmorated stink bug Halyomorpha halys (Hemiptera, Pentatomidae) in Georgia. Turk J Zool, 42(6): 617-624.
• Özdemir İO, Tuncer C. 2021. Türkiye'de yeni bir istilacı polifag zararlı, kahverengi kokarca [Halyomorpha halys (stål, 1855) (Hemiptera: Pentatomidae)]: tanımı, benzer türler ve mevcut durum. BSJ Eng Sci, 4(2): 58-67.
• Özdemir IO, Tuncer C, Solmaz FG, Ozturk B. 2023a. The impact of green shield bug (Palomena prasina [Hemiptera: Pentatomidae]) infestation on antioxidant enzyme activities in hazelnut (Corylus avellana L. cvs.‘Tombul,’‘Palaz’and ‘Çakıldak’): Erwerbs-Obstbau, 2023: 1-7.
• Özdemir IO, Karakaya O, Ates U, Ozturk B, Uluca M, Tuncer C. 2023b. Characterization of hazelnut kernel responses to brown marmorated stink bug [Halyomorpha halys Stal (Hemiptera: Pentatomidae)] infestations: Changes in bioactive compounds and fatty acid composition. J Food Compos Anal, 124: 105696.
• Panizzi AR, McPherson JE, James DG, Javahery M, McPherson RM. 2000. Stink bugs (Pentatomidae): In Heteroptera of Economic Importance, CRC Press: Boca Raton, FL, USA, 1st ed., pp: 421–474.
• Panizzi AR, Lucini T. 2017. Host plant-stink bug (Pentatomidae) relationships. In Stinkbugs, CRC Press, New York, USA, pp: 31-58.
• Peiffer M, Felton GW. 2014. Insights into the saliva of the brown marmorated stink bug Halyomorpha halys (Hemiptera: Pentatomidae): PloS one, 9(2): e88483.
• Reyes LF, Villarreal JE, Cisneros-Zevallos L. 2007. The increase in antioxidant capacity after wounding depends on the type of fruit or vegetable tissue. Food Chem, 101(3): 1254-1262.
• Rice KB, Bergh CJ, Bergmann EJ, Biddinger DJ, Dieckhoff C, Dively G, Fraser H, Gariepy T, Hamilton G, Haye T, Herbert A, Hoelmer K, Hooks CR, Jones A, Krawczyk G, Kuhar T, Martinson H, Mitchell W, Nielsen AL, Pfeiffer DG, Raupp MJ, Rodriguez-Saona C, Shearer P, Shrewsbury P, Venugopal PD, Whalen J, Wiman NG, Leskey TC, Tooker, J. F. 2014. Biology, ecology, and management of brown marmorated stink bug (Hemiptera: Pentatomidae). J Integr Pest Manag, 5(3): A1-A13.
• Soriano IR, Asenstorfer RE, Schmidt O, Riley IT. 2004. Inducible flavone in oats (Avena sativa) is a novel defense against plant-parasitic nematodes. Phytopathology, 94(11): 1207-1214.
• Tonkaz T, Şahin S, Bostan SZ, Korkmaz K. 2019. Effect of supplementary irrigation on total antioxidant capacity and phenolic content of hazelnut. AZD, 8(Özel Sayı): 79-84.
• Tuncer C, Saruhan I, Akca I. 2005. The insect pest problem affecting hazelnut kernel quality in Turkey. Acta Hortic, (686): 367–375.
• Turan A. 2021. Effect of the damages caused by the green shield bug (Palomena prasina L.) on the qualitative traits of hazelnuts. Grasas y Aceites, 72(1): e391.
• War AR, Paulraj MG, Ahmad T, Buhroo AA, Hussain B, Ignacimuthu S, Sharma HC. 2012. Mechanisms of plant defense against insect herbivores. Plant Signal Behav, 7(10): 1306-1320.
• Weber NC, Razinger J, Jakopič J, Schmitzer V, Hudina M, Slatnar A, Veberič R, Štampar F, Zamljen, T. 2021. Brown Marmorated Stink Bug (Halyomorpha halys Stål.) Attack Induces a Metabolic Response in Strawberry (Fragaria× ananassa Duch.) Fruit. Horticulturae, 7(12): 561.
• Yactayo-Chang JP, Tang HV, Mendoza J, Christensen SA, Block AK. 2020. Plant defense chemicals against insect pests. Agronomy, 10(8): 1156.
• Yılmaz M, Karakaya O, Balta MF, Balta F, Yaman İ. 2019 Change of biochemical characteristics depending on kernel size in Çakıldak hazelnut cultivar. AZD, 8: 61-70.
• Zamljen T, Veberic R, Hudina M, Slatnar A. 2021. The brown marmorated stink bug (Halyomorpha halys Stål.) influences pungent and non-pungent Capsicum cultivars’ pre-and post-harvest quality. Agronomy, 11(11): 2252.
• Zhou Y, Giusti MM, Parker J, Salamanca J, Rodriguez-Saona C. 2016. Frugivory by brown marmorated stink bug (Hemiptera: Pentatomidae) alters blueberry fruit chemistry and preference by conspecifics. Environ Entomol, 45(5): 1227-1234.