TY  - JOUR
T1  - Gall wasps change the biochemical composition of Eucalyptus leaves
TT  - Gal arıları Eucalyptus yapraklarının biyokimyasal kompozisyonunu değiştirir
AU  - Keleş, Yüksel
AU  - Aytar, Fatih
PY  - 2025
DA  - August
Y2  - 2025
DO  - 10.30616/ajb.1701359
JF  - Anatolian Journal of Botany
JO  - Ant J Bot
PB  - Abdullah KAYA
WT  - DergiPark
SN  - 2602-2818
SP  - 141
EP  - 149
VL  - 9
IS  - 2
LA  - en
AB  - Determining the effects of gall wasps on leaf biochemistry may contribute to the understanding of damage mechanisms. The study was carried out in eucalyptus plantations in the coastal regions of the Northeastern Mediterranean (Tarsus/Mersin/Turkey). Biochemical analyses were performed on Eucalyptus camaldulensis leaves infested and uninfested with two different gall wasps (Leptocybe invasa and Ophelimus maskelli) and the data were compared. The flavonoid content of the leaves reduced 16.5% in leaves infested with L. invasa and 33.7% with O. maskelli. Total antioxidant capacity decreased with O. maskelli infestation but did not change with L. invasa infestation. Copper ion reduction capacity increased significantly with both pest infestations. Ascorbic acid increased by 87% in L. invasa infestation and 120% in O. maskelli infestation compared to control. Superoxide generation rates of noninfested and infested leaves from the infested trees were found to be higher than those of the control samples. Differences in the biochemical composition of infested and non-infested leaves of infested plants were determined. The invasion of gall wasps triggers oxidative stress by increasing the rate of superoxide production in eucalyptus leaves.
KW  - antioxidant
KW  - insect pest
KW  - Leptocybe invasa
KW  - Ophelimus maskelli
KW  - Photosynthetic pigments
N2  - Gal arılarının yaprak biyokimyası üzerindeki etkilerinin belirlenmesi, zarar mekanizmalarının anlaşılmasına katkı sağlayabilir. Çalışma Kuzey Doğu Akdeniz (Tarsus/Mersin/Turkiye) sahil bölgelerindeki okaliptus plantasyonlarında gerçekleştirildi. İki farklı gal arısı (Leptocybe invasa ve Ophelimus maskelli), ile istila edilmiş ve edilmemiş Eucalyptus camaldulensis yapraklarında biyokimyasal analizler yapıldı ve veriler karşılaştırıldı. Yaprakların flavonoid içeriğinde L. invasa  istilasında %16,5, O. maskelli istilasında %33,7 azalma belirlendi. Toplam antioksidan kapasite, O. maskelli istilasıyla azaldı ancak L. invasa istilasıyla değişmedi. Bakır iyonu indirgeme kapasitesi, her iki pest istilasında da önemli ölçüde arttı. Askorbik asit, L. invasa istilasında kontrole göre %87 ve O. maskelli istilasında %120 arttı. İstila edilmiş ağaçlardan istila edilmemiş ve istila edilmiş yaprakların süperoksit üretim oranlarının kontrol örneklerinden daha yüksek olduğu bulundu. İstila edilmiş bitkilerin istila edilmiş ve edilmemiş yapraklarının biyokimyasal kompozisyonunda farklılıklar belirlendi. Gal arılarının istilası, okaliptüs yapraklarında süperoksit üretim oranını artırarak oksidatif stresi tetiklemektedir.
CR  - Adel-Sellami M, Sellami M, Benrima A (2025). Variations in Ophelimus maskelli (Hymenoptera: Eulophidae) population density and infestation on Eucalyptus and the impact of its parasitoid Closterocerus chamaeleon (Hymenoptera: Eulophidae) in Algeria. Acta Phytopathologica et Entomologica Hungarica 59(2): 121-132. https://doi.org/10.1556/038.2024.00214
CR  - Ali S, Bashir BA, Kamili AN, Bhat AA, Mir ZA, Bhat JA, Tyagi A, Islam ST, Mushtaq M, Yadav P, Rawat S, Grover A (2018). Pathogenesis-related proteins and peptides as promising tools for engineering plants with multiple stress tolerance. Microbiological Research 212-213: 29-37. https://doi.org/10.1016/j.micres.2018.04.008
CR  - Apak R, Güçlü K, Ozyurek M, Kandemir SE (2004). Novel total antioxidant capacity index for dietary polyphenols and vitamins C and E, using their cupric ion reducing capability in the presence of neocuproine: cuprac method. Journal of Agricultual and Food Chemistry 52: 7970-7981.  https://doi.org/10.1021/jf048741x
CR  - Badmin J (2008). Spread of Ophelimus maskelli Ashmead (Hymenoptera: Eulophidae) in south-east England. British Journal of Entomology and Natural History 21(3): 147.
CR  - Bari R, Jones JD (2009). Role of plant hormones in plant defence responses. Plant Molecular Biology 69(4): 473-88. https://doi.org/10.1007/s11103-008-9435-0
CR  - Beyer WF, Fridovich I (1987). Assaying for superoxide dismutase activity: some large consequences of minor changes in conditions. Analitic Biochemistry 161: 559-566. https://doi.org/10.1016/0003-2697(87)90489-1
CR  - Bates LS, Walderen RD, Taere ID (1973). Rapid determination of free proline for water stress studies. Plant and Soil 39: 205-207. https://doi.org/10.1007/BF00018060
CR  - Billings RF (2011). Guide to Potential Insects, Diseases, and Other Damaging Agents of Eucalyptus in the Southeastern United States. California: Advanced Forest Protection Inc.
CR  - Branco M, Battisti A, Mendel Z (2016). Foliage feeding invasive insects: Defoliators and gall makers. In: Paine TD, Lieutier F (edts). Insects and Diseases of Mediterranean Forest Systems. Switzerland: Springer International Publishing, pp. 211-238.  https://doi.org/10.1007/978-3-319-24744-1_8
CR  - Chen Y-M, Lucas PW, Wellburn AR (1991). Relationship between foliar injury and changes in antioxidant levels in red and norway spruce exposed to acid mists. Environmental Pollution 69: 1-5. https://doi.org/10.1016/0269-7491(91)90159-T
CR  - Chen Z, Kolb TE, Clancy KM (2002). The role of monoterpenes in resistance of douglas fir to western spruce budworm defoliation.  Journal of Chemical Ecologie 28: 897-920. https:// doi.org/10.1023/A:1015297315104
CR  - de Souza Tavares W, Sinulingga NGHB, Saha MA, Sunardi K, Sihombing IFL, Tarigan M, Kkadan SK, Duran A (2023). Leptocybe invasa (Hymenoptera: Eulophidae) galls parasitized by Megastigmus sp. (Hymenoptera: Torymidae): First record in Indonesia on a new host plant, Eucalyptus brassiana (Myrtaceae). Journal of Plant Diseases and Protection 130(4): 1149-1153. https://doi.org/10.1007/s41348-023-00742-8
CR  - Dittrich-Schröder G, Wingfield MJ, Hurley BP, Slippers B (2012). Diversity in Eucalyptus susceptibility to the gall-forming wasp Leptocybe invasa. Agricultural and Forest Entomology 14: 419-427. https://doi.org/10.1111/j.1461-9563.2012.0058 3.x
CR  - Elansary HO, Salem MZM,  Ashmawy NA, Yessoufou K, El-Settawy AAA (2017). In vitro antibacterial, antifungal and antioxidant activities of Eucalyptus spp. leaf extracts related to phenolic composition. Natural Product Resarch 31: 2927-2930. https://doi.org/10.1080/14786419.2017.1303698
CR  - Eyles A, Bonello P, Ganley R, Mohammed C (2010). Induced resistance to pests and pathogens in trees. New Phytologist 185: 893-908. https://doi.org/ 10.1111/j.1469-137.2009.03127 .x
CR  - Ferraris L, Gentile IA, Matta A (1987). Variations of phenols concentration as a consequence of stresses that induce resistance to fusarium wilt of tomato / Veränderungen der phenolkonzentration als folge von streß-situationen, die resistenz gegen fusarium-welke in tomaten induzieren. Zeitschrift Für Pflanzenkrankheiten Und Pflanzenschutz 94(6): 624-629.  http://www.jstor.org/stable/43385627
CR  - Floris I,  Cocco A, Buffa F, Mannu R, Satta A  (2018). Insect pests of Eucalyptus plantations in Sardinia (Italy). Redia 101: 61-71. http://dx.doi.org/10.19263/REDIA-101.18.09
CR  - Franceschi V, Krokene P, Christiansen E, Krekling T (2005). Anatomical and chemical defenses of conifer bark against bark beetles and other pests. New phytologist 167: 353-375. https://doi.org/10.1111/j.1469-8137.2005.0143 6.x.
CR  - Glazebrook J (2005). Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens.  Annual Review of Phytopathology 43: 205-227. https://doi.org/10.1146/annurev.phyto.43.040204.135923
CR  - Gossett DR, Millhollon EP, Lucas MC (1994). Antioxidant response to NaCl stress in salt - tolerant and salt - sensitive cultivars of cotton. Crop Science 34: 706-714. https://doi.org/10.2135/cropsci1994.0011183X003400030020x
CR  - Halhoul MN, Kleinberg I (1972). Differential determination of glucose and fructose yielding substances with anthrone. Analitic Biochemistry 50: 337-343.  https://doi.org/10.1016/0003-2697(72)90042-5
CR  - Hakiman M, Maziah M (2009). Non enzymatic and enzymatic antioxidant activities in aqueous extract of different Ficus deltoidea accessions. Journal of Medicinal Plants Research  3(3):  120-131.  https://doi.org/10.5897/JMPR.9000931
CR  - Hinchee M, Zhang C, Chang S, Cunningham M, Hammond W, Nehra N (2011). Biotech Eucalyptus can sustainably address society’s tolerant  need for wood: the example of freeze Eucalyptus in the southeastern U.S. BMC Proceedings  5 (Suppl 7): I24. https://doi.org/10.1186/1753-6561-5-S7-I24
CR  - Mendel Z, Protasov A, Fisher N, LaSalle J (2004). Taxonomy and biology of Leptocybe invasa gen. & sp. n. (Hymenoptera: Eulophidae), an invasive gall inducer on Eucalyptus. Australian Journal of Entomology 43: 101-13. https://doi.org/10.1111/j.1440-6055.2003.00393 .x
CR  - Mhoswa L, O’Neill MM, Mphahlele MM, Oates CN, Pa KG, Slippers B, Myburg AA, Naidoo S (2020). A genome-wide association study for resistance to the insect pest Leptocybe invasa in Eucalyptus grandis reveals genomic regions and positional candidate defense genes. Plant Cell Physiology 61(7): 1285-1296.  https://doi.org/10.1093/pcp/pcaa057
CR  - Mithöfer A, Boland W (2008). Recognition of herbivory-associated molecular patterns. Plant Physiology 146: 825-831. PMC2259064 https://doi.org/10.1104/pp.107.113118
CR  - Moore TC (1974) Thin-layer chromatography of chloroplast pigments and determination of pigment absorption spectra. In: Moore TC (edt.). Research Experiences in Plant Physiology. Berlin: Springer, pp 51-65. https://doi.org/10.1007/978-3-642-96168-7_5
CR  - Mortensen A, Skibsted LH, Truscotn TG (2001). The interaction of dietary carotenoids with radical species. Archives of Biochemistry and Biophysics 385(1):13-19. https://doi.org/10.1006/abbi. 2000.2172
CR  - Naidoo S, Külheim C, Zwart L, Mangwanda R, Oates CN, Visser EA, Wilken FE, Mamni TB, Myburg AA (2014). Uncovering the defence responses of Eucalyptus to pests and pathogens in the genomics age. Tree Physiology 34: 931-943. https://doi.org/10.1093/treephys/tpu075
CR  - Oates CN, Külheim C, Myburg AA, Slippers B, Naidoo S (2015). The transcriptome and terpene profile of Eucalyptus grandis reveals mechanisms of defense against the insect pest, Leptocybe invasa. Plant Cell Physiology 56(7): 1418-1428. https://doi.org/10.1093/pcp/pcv064
CR  - Orozco-Cárdenas ML, Narváez-Vásquez  J, Ryan CA (2001). Hydrogen peroxide acts as a second messenger for the induction of defense genes in tomato plants in response to wounding, systemin, and methyl jasmonate. The Plant Cell 13(1): 179-191.  https://doi.org/10.2307/3871162
CR  - Paine TD, Steinbauer MJ, Lawson SA (2011). Native and exotic pests of Eucalyptus: A worldwide perspective. Annual Review of Entomology 56: 181-201. https://doi.org/10.1146/annurev-ento-120709-144817
CR  - Passardi F, Penel C, Dunand C (2004). Performing the paradoxical: how plant peroxidases modify the cell wall. Trends in Plant Science 9: 534-540. https://doi.org/10.1016/j.tplants.2004.09.002
CR  - Pekal A, Pyrzynska K (2014). Evaluation of aluminium complexation reaction for flavonoid content assay. Food Analitical Methods 7: 1776-1782.  https://doi.org/10.1007/s12161-014-9814-x
CR  - Pisoschi AM, Pop A, Cimpeanu C, Predoi G (2016). Antioxidant capacity determination in Plants and plant-derived products: A Review. Hindawi Publishing Corporation Oxidative Medicine and Cellular Longevity: 9130976.  http://dx.doi.org/10.1155/2016/9130976
CR  - Porra RJ,  Thompson RA, Kriedemann PE (1989). Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvent verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. Biochimica et Biophysica acta Bioenergetics 975: 384-394.  https://doi.org/10.1016/S0005-2728(89)80347-0
CR  - Prieto P, Pineda M, Aguilar M (1999). Spectrophotometric quantitation of antioxidant capacity through the formation of a phosphomolybdenum complex: specific application to the determination of vitamin E. Analytical Biochemistry 269 (2): 337-341. https://doi.org/10.1006/abio.1999.4019
CR  - Protasov A, La Salle J, Blumberg D, Brand D, Saphir N, Assael F, Fisher N, Mendel Z (2007). Biology, revised taxonomy and impact on host plants of Ophelimus maskelli, an invasive gall inducer on Eucalyptus spp. in the Mediterranean Area. Phytoparasitica 35: 50-76. https://doi.org/10.1007/BF02981061
CR  - Schöner S, Heinrich Krause G (1990). Protective systems against active oxygen species in spinach: response to cold acclimation in excess light. Planta 180: 383-389.  https://doi.org/10.1007/BF00198790
CR  - Sahin Basak S, Candan F (2010). Chemical composition and In vitro antioxidant and antidiabetic activities of  Eucalyptus camaldulensis Dehnh. essential oil.  Journal Iran Chemical Society 7: 216-226.  https://doi.org/10.1007/BF03245882
CR  - Singh R, Singh S, Parihar P, Mishra RK, Tripathi DK, Singh VP, Chauhan DK, Prasad SM (2016). Reactive oxygen species (ROS): Beneficial companions of plants' developmental processes. Frontiers in Plant Science 27(7): 1299.  https://doi.org/10.3389/fpls.2016.01299
CR  - Tian J, Jiang F, Wu Z (2015). The apoplastic oxidative burst as a key factor of hyperhydricity in garlic plantlet in vitro. Plant Cell Tissue and Organ Culture 120: 571-584. https://doi.org/10.1007/s11240-014-0623-0
CR  - Wingfield MJ, Slippers B, Hurley BP, Coutinho TA, Wingfield BD, Roux J (2008). Eucalypt pests and diseases: growing threats to plantation productivity. Southern Forest 70: 139-144. https://doi.org/10.2989/SOUTH.FOR.2008.70.2.9.537
CR  - Wingfield MJ, Roux J, Slippers B, Hurley BP, Garnas J, Myburg AA, Wingfield BD (2013). Established and new technologies reduce increasing pest and pathogen threats to eucalypt plantations. Forest Ecology and Management 301: 35-42. https://doi.org/10.1016/j.foreco.2012.09.002
CR  - van Loon LC (2009). Advances in botanical research-plant innate immunity. Oxford: Elsevier. eBook ISBN: 9780080888798
CR  - Vastrad S, Ramanagouda H (2014). Invasive gall wasp (Leptocybe invasa) in Eucalypt and its management. In: Bhojvaid PP, Kaushik S, Singh YP, Kumar D, Thapliyal M, Barthwal S (edts.). Eucalypts in India, 1st edition: I. Dehradun: Envis Centre on Forestry, pp. 346-380. https://doi.org/10.13140/RG.2.1.1561.7449.
CR  - Zhang H, Song J, Zhao H, Li M, Han W (2021). Predicting the distribution of the invasive species Leptocybe invasa: Combining MaxEnt and geodetector models. Insects 12(2): 92.  https://doi.org/10.3390/insects12020092.
UR  - https://doi.org/10.30616/ajb.1701359
L1  - https://dergipark.org.tr/en/download/article-file/4879233
ER  -