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Effect of Neuroterus quercusbaccarum (L.) galls on physiological and biochemical response of Quercus robur leaves

  • I. Kot (a1), C. Sempruch (a2), K. Rubinowska (a3) and W. Michałek (a3)


Gall formation is associated with multiple changes in plant cells, which still requires a better understanding. In this study, galls caused by sexual generation (♀♂) of Neuroterus quercusbaccarum (L.) (Hymenoptera: Cynipidae) on pedunculate oak trees (Quercus robur L.) were used as a model. Cytoplasmic membrane condition, concentration of hydrogen peroxide (H2O2), the activity of antioxidant enzymes and amino acid decarboxylase as well as chlorophyll fluorescence parameters were determined. Changes in physiological and biochemical parameters were analyzed in foliar tissues with galls and gall tissues themselves and compared to control. The presence of galls on oak leaves caused an increase of lipid peroxidation level. A significant decline in H2O2 and TBARS content with the reduction of guaiacol peroxidase (GPX) and ascorbate peroxidase (APX) activity were observed in gall tissues. The activity amino acid decarboxylase, i.e., LDC, ODC and TyDC varied between samples, which may affect the content of amino acids. The presence of N. quercusbaccarum galls caused an insignificant increase of the chlorophylls, carotenoids and anthocyanin contents, while the content of pigments and their ratios in gall tissues was extremely low. Moreover, photosynthetic parameters (F0, Fm, Fv/Fm, Y, qP) were significantly decreased. Data generated in this study indicate that the development of N. quercusbaccarum galls on pedunculate oak leaves has a negative effect on host plant related to the disruption of cell membrane integrity, disturbance of photosynthesis and reduction of the antioxidant potential of the host plant.


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Aldea, M., Hamilton, J.G., Resti, J.P., Zangerl, A.R., Berenbaum, M.R., Frank, T.D. & DeLucia, E.H. (2006) Comparison of photosynthetic damage from arthropod herbivory and pathogen infection in understory hardwood saplings. Oecologia 149, 221232.
Ashraf, M. & Harris, P.J.C. (2013) Photosynthesis under stressful environments: an overview. Photosynthetica 51(2), 163190
Barry, K.M. & Newnham, G.J. (2012) Quantification of chlorophyll and carotenoid pigments in eucalyptus foliage with the radiative transfer model PROSPECT 5 is affected by anthocyanin and epicuticular waxes. pp. 1–7 in Proceedings of the Geospatial Science Research Symposium, RMIT University, Melbourne, Victoria.
Bela, K., Horvátha, E., Galléa, Á., Szabadosb, L., Tari, I. & Csiszára, J. (2015) Plant glutathione peroxidases: emerging role of the antioxidant enzymes in plant development and stress responses. Journal of Plant Physiology 176, 192201.
Bi, J.L. & Felton, G.W. (1995) Foliar oxidative stress and insect herbivory: primary compounds, secondary metabolites, and reactive oxygen species as components of induced resistance. Journal of Chemical Ecology 21, 15111527.
Bi, J.L., Murphy, J.B. & Felton, G.W. (1997) Antinutritive and oxidatitive components as mechanisms of induced resistance in cotton to Helicoverpa zea. Journal of Chemical Ecology 23(1), 97117.
Carneiro, R.G.S., Castro, A.C. & Isaias, R.M.S. (2014) Unique histochemical gradients in a photosynthesis-deficient plant gall. South African Journal of Botany 92, 97104.
Caverzan, A., Passaia, G., Rosa, S.B., Ribeiro, C.W., Lazzarotto, F. & Margis-Pinheiro, M. (2012) Plant responses to stresses: role of ascorbate peroxidase in the antioxidant protection. Genetics and Molecular Biology 35(4), 10111019.
Collins, R.M., Afzal, M., Ward, D., Prescott, M.C., Sait, S.M., Rees, H.H. & Tomsett, A.B. (2010) Different proteomic analysis of Arabidopsis thaliana genotypes exhibiting resistance or susceptibility to the insect herbivore, Plutella xylostella. PLoS ONE 5(4), e10103.
Dorchin, N., Cramer, M.D. & Hoffman, J.H. (2006) Photosynthesis and sink activity of wasp-induced galls in Acacia pycnantha. Ecology 87, 17811791.
Florencio-Ortiz, V., Sellés-Marchart, S., Zubcoff-Vallejo, J., Jander, G. & Casas, J.L. (2018) Changes in the free amino acids composition of Capsicum annuum (pepper) leaves in response to Myzus persicae (green peach aphid) infestation. A comparison with water stress. PloS ONE 13(6), e0198093,
Golan, K., Rubinowska, K., Kmieć, K., Kot, I., Górska-Drabik, E., Łagowska, B. & Michałek, W. (2015) Impact of scale insect infestation on the content of photosynthetic pigments and chlorophyll fluorescence in two host plant species. Arthropod-Plant Interactions. 9, 5565.
Gill, S. S. & Tuteja, N. (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiology and Biochemistry 48, 909930.
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, 7089.
Guidi, L. & Degl'Innocenti, E. (2012) Chlorophyll a fluorescence in abiotic stress pp. 359399 in Venkateswarlu, B., Shanker, A., Shanker, C., Maheswari, M. (Ed.) Crop Stress and its Management: Perspectives and Strategies. Dordrecht, the Netherlands, Springer.
Gutsche, A.R., Heng-Moss, T.M., Higley, L.G., Sarath, G. & Mornhinweg, D.W. (2009) Physiological responses of resistant and susceptible barley, Hordeum vulgare to the Russian wheat aphid, Diuraphis noxia (Mordvilko). Arthropod-Plant Interactions 3, 233240.
Haiden, S.A., Hoffmann, J.H. & Cramer, M.D. (2012) Benefits of photosynthesis for insects in galls. Oecologia 170, 987997.
Hartley, S.E. (1998). The chemical composition of plant galls: are levels of nutrients and secondary compounds controlled by the gall-former? Oecologia 113, 492501.
Heath, R.L. & Packer, L. (1968) Effect of light on lipid peroxidation in chloroplasts. Biochemical and Biophysical Research Communications 19, 716720.
Huang, J., Zhang, P.J., Zhang, J., Lu, Y.B., Huang, F. & Li, M.J. (2013) Chlorophyll content and chlorophyll fluorescence in tomato leaves infested with an invasive mealybug, Phenacoccus solenopsis (Hemiptera: Pseudococcidae). Environmental Entomology 42(5), 973979.
Huang, M.Y., Chou, H.M., Chang, Y.T. & Yang, C.M. (2014 a) The number of cecidomyiid insect galls affects the photosynthesis of Machilus thunbergii host leaves. Journal of Asia-Pacific Entomology 17, 151154.
Huang, M.Y., Huang, W.D., Chou, H.M., Lin, K.H., Chen, C.C., Chen, P.J., Chang, Y.T. & Yang, C.M. (2014 b) Leaf-derived cecidomyiid galls are sinks in Machilus thunbergii (Lauraceae) leaves. Physiologia Plantarum 152(3), 475485.
Isaias, R.M.S. & Oliveira, D. C. (2012) Gall phenotypes – product of plant cells defensive responses to the inducers attack 12, pp. 273290 in: Mérillon, J.M., Ramawat, K.G. (Ed) Plant Defense: Biology. Control. Progress in Biological Control. Dordrecht, Netherlands, Springer Science+Business Media B.V., doi: 10.1007/978-94-007-1933-0_11.
Jena, S. & Choudhuri, M.A. (1981) Glycolate metabolism of three submerged aquatic angiosperms during aging. Aquatic Botany 12, 345354.
Jiang, Y., Veromann-Jürgenson, L-L., Ye, J. & Niinemets, Ü. (2018) Oak gall wasp infections of Quercus robur leaves lead to profound modifications in foliage photosynthetic and volatile emission characteristics. Plant, Cell & Environment 41, 160175.
Juneau, P., Green, B.R. & Harrison, P.J. (2005) Simulation of Pulse-Amplitude-Modulated (PAM) fluorescence: limitations of some PAM-parameters in studying environmental stress effects. Photosynthetica 43(1), 7583.
Kalaji, H.M., Carpentier, R., Allakherdiev, S.I. & Bosa, K. (2012) Fluorescence parameters as early indicators of light stress in barley. Journal of Photochemistry and Phytobiology B: Biology 112, 16.
Kampichler, C. & Teschner, M. (2002) The spatial distribution of leaf galls of Mikola fagi (Diptera: Cecidomyiidae) and Neuroterus quercusbaccarum (Hymenoptera: Cynipidae) in the canopy of a Central European mixed forest. European Journal Entomology 99, 7984.
Khattab, H. (2007) The defense mechanism of cabbage plant against phloem-sucking aphid (Brevicoryne brassicae L.). Australian Journal of Basic and Applied Sciences 1, 5662.
Kierych, E. (1979) Galasówkowate (Cynipoidea) p. 103 in Catalogus faunae Poloniae. Warsaw, PWN.
Kmieć, K., Kot, I., Golan, K., Górska-Drabik, E., Łagowska, B., Rubinowska, K. & Michałek, W. (2016) Physiological response of orchids to mealybugs (Hemiptera: Pseudococcidae) infestation. Journal of Economic Entomology 109(6), 24892494.
Kmieć, K., Rubinowska, K. & Golan, K. (2018) Tetraneura ulmi (Hemiptera: Eriosomatinae) induces oxidative stress and alters antioxidative enzyme activities in elm leaves. Environmental Entomology 47(4), 840847. doi: 10.1093/ee/nvy055
Kościelniak, J. (1993) Wpływ następczy temperatur w termoperiodyzmie dobowym na produktywność fotosyntetyczną kukurydzy (Zea mays L.)/Successive effect of temperature daily thermoperiodism in the photosynthetic productivity of maize (Zea mays L.). PhD dissertation 174, University of Agriculture, Cracow.
Kot, I. & Rubinowska, K. (2018) Physiological response of pedunculated oak trees to gall-inducing Cynipidae. Environmental Entomology 47(3), 669675
Kot, I., Jakubczyk, A., Karaś, M. & Złotek, U. (2018 a) Biochemical responses induced in galls of three Cynipidae species in oak trees. Bulletin of Entomological Research 108(4), 494500
Kot, I., Rubinowska, K. & Michałek, W. (2018 b) Changes in chlorophyll a fluorescence and pigments composition in oak leaves with galls of two cynipid species (Hymenoptera, Cynipidae). Acta Scientarum Polonorum, Hortorum Cultus 17(6), 147157.
Kovácsné-Koncz, N., Szabó, L.J., Máthe, C., Jámbrik, K. & M-Hamvas, M. (2011) Histological study of quercus galls of Neuroterus quercusbaccarum (L.) (Hymenoptera: Cynipidae). Acta Biologica Szegediensis 55(2), 247253.
Lichtenthaler, H.K. & Wellburn, A.R. (1983) Determination of total carotenoids and chlorophyll a and b of leaf extract in different solvents. Biochemical Society Transactions 11, 591592.
Lowry, J.O.H., Rosebrough, N.J., Farr, A.L. & Randal, R.J. (1951) Protein measurement with the Folin phenol reagent. Journal of Biological Chemistry 193, 256277.
Łukasik, I., Goławska, S. & Wójcicka, A. (2012) Effect of cereal aphid infestation on ascorbate content and ascorbate peroxidase activity in triticale. Polish Journal of Environmental Studies 6, 19371941.
Maffei, M.E., Mithöfer, A. & Boland, W. (2007) Insects feeding on plants: rapid signals and responses preceding the induction of phytochemical release. Phytochemistry 68, 29462959.
Małolepsza, A., Urbanek, H. & Polit, J. (1994) Some biochemical of strawberry plants to infection with Botrytis cinerea and salicylic acid treatment. Acta Agrobotanica 47, 7381.
Miller-Fleming, L., Olin-Sandoval, V., Campbell, K. & Ralser, M. (2015) Remaining mysteries of molecular biology: the role of polyamines in the cell. Journal of Molecular Biology 427, 33893406.
Muneer, S., Jeong, H.K., Park, Y.G. & Jeong, B.R. (2018) Proteomic analysis of aphid-resistant and –sensitive rose (Rosa hybrid) cultivars at two developmental stages. Proteomes 6(25). doi: 10.3390/proteomes6020025.
Nabity, P.D., Zavala, J.A. & DeLucia, E.H. (2009) Indirect suppression of photosynthesis on individual leaves by arthropod herbivory. Annals of Botany 103(4), 655663.
Nabity, P.D., Hillstrom, M.L., Lindroth, R.L. & DeLucia, E.H. (2012) Elevated CO2 interacts with herbivory to alter chlorophyll fluorescence and leaf temperature in Betula papyrifera and Populus tremuloides. Oecologia 169, 905913.
Nakano, Y. & Asada, K. (1981) Hydrogen peroxide is scavenged by ascorbate specific peroxidase in spinach chloroplasts. Plant and Cell Physiology 22, 867880.
Ngo, T.T., Brillhart, K.L., Davis, R.H., Wong, R.C., Bovaird, J.H., Digangi, J.J., Risov, J.L., Marsh, J.L., Phan, A.P.H. & Lenhoff, H.M. (1987) Spectrophotometric assay for ornithine decarboxylase. Analytical Biochemistry 160, 290293.
Oliveira, D.C., Isaias, R.M.S., Moreira, A.S.F.P., Magalhães, T.A. & Lemos-Filho, J.P. (2011) Is the oxidative stress caused by Aspidosperma spp. Galls capable of altering leaf photosynthesis? Plant Science 180, 489495.
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, 103113.
Pandey, S., Fartyal, D., Agarwal, A., Shukla, T., James, D., Kaul, T., Negi, Y.K., Arora, S. & Reddy, M.K. (2017) Abiotic stress tolerance in plants: myriad roles of ascorbate peroxidase. Frontiers in Plant Sciences 8, 581.
Patra, B., Bera, S. & Mehltreter, K. (2010) Structure, biochemistry and ecology of entomogenous galls in Selaginella Pal. Beauv. (Selaginellaceae) from India. Journal of Plant Interactions 5(1), 2936.
Phan, A.P.H., Ngo, T.T. & Lenhoff, H.M. (1982) Spectrophotometric assay for lysine decarboxylase. Analytical Biochemistry 120, 193197.
Phan, A.P.H., Ngo, T.T. & Lenhoff, H.M. (1983) Tyrosine decarboxylase. Spectrophotometric assay and application determining pyridoxal-5′-phosphate. Applied Biochemistry and Biotechnology 8, 127133.
Quan, L.J., Shang, B., Shi, W.W. & Li, H.Y. (2008) Hydrogen peroxide in plants: a versatile molecule of the reactive oxygen species network. Journal of Integrative Plant Biology 50, 218.
Rabino, I. & Mancinelli, A. (1986). Light, temperature and anthocyanin production. Plant Physiology 81, 922924.
Ramakrishna, A. & Ravishankar, G.A. (2011) Influence of abiotic stress signals on secondary metabolites in plants. Plant Signaling & Behavior 6(11), 17201731.
Retuerto, R., Fernandez-Lema, B., Rodriguez, R. & Obeso, J.R. (2004) Increased photosynthetic performance in holly trees infested by scale insects. Functional Ecology 18, 664669.
StatSoft Inc. (2016) Statistica (data analysis software system), version v. 13.1,
Samsone, I., Andersone, U. & Ievinsh, G. (2012) Variable effect of arthropod-induced galls on photochemistry of photosynthesis, oxidative enzyme activity and ethylene production in tree leaf tissues. Environmental and Experimental Biology 10, 1526.
Schreiber, U. (2004) Pulse amplitude modulation (PAM) fluorometry and saturation pulse method: an overview pp. 279319 in Papageorgiou, G.C. (Ed.) Chlorophyll A Fluorescence: A Signature of Photosynthesis. Dordrecht, Kluwer Academic.
Sempruch, C., Horbowicz, M., Kosson, R. & Leszczyński, B. (2012 a) Biochemical interactions between triticale (Triticosecale; Poaceae) amines and bird cherry-oat aphid (Rhopalosiphum padi; Aphididae). Biochemical Systematics and Ecology 40, 162168.
Sempruch, C., Leszczyński, B., Protasiuk, M. & Zarzecka, K. (2012 b) Effects of Sitobion avenae (Fabricius 1775) versus Oulema melanopus (Linnaeus 1758) and Leptinotarsa decemlineata (Say 1824) on selected amino acid decarboxylases activity within host plant tissues. Aphids and Other Hemipterous Insects 18, 8391.
Sempruch, C., Marczuk, W., Leszczyński, B., Kozak, A., Zawadzka, W., Klewek, A. & Jankowska, J. (2013) Effect of pea aphid infestation on activity of amino acid decarboxylases in pea tissues. Acta Biologica Cracoviensia, Series Botanica 55(2), 4550.
Sempruch, C., Golan, K., Górska-Drabik, E., Kmieć, K., Kot, I. & Łagowska, B. (2014) The effect of a mealybug infestation on the activity of amino acid decarboxylases in orchid leaves. Journal of Plant Interactions 9(1), 825831.
Sempruch, C., Goławska, S., Osiński, P., Leszczyński, B., Czerniewicz, P., Sytykiewicz, H. & Matok, H. (2016) Influence of selected plant amines on probing and feeding behaviour of bird cherry-oat aphid (Rhopalosiphum padi L.). Bulletin of Entomological Research 106, 368377.
Stone, G.N., Schönrogge, K., Atkinson, R.J., Bellido, D. & Pujade-Villar, J. (2002) The population biology of oak gall wasps (Hymenoptera: Cynipidae). Annual Review of Entomology 47, 633668.
Subramanyam, S., Sardesai, N., Minocha, S.C., Zheng, C., Shulke, R.H. & Williams, C.E. (2015) Hessian fly larvae feeding triggers enhanced polyamine levels in susceptible but not resistant wheat. BMC Plant Biology 15(3). doi: 10.1186/s12870-014-0396-y.
Sytykiewicz, H. (2014) Differential expression of superoxide dismutase genes in aphid-stressed maize (Zea mays L.) seedlings. PloS ONE 9(4), e94847.
Sytykiewicz, H. (2016 a) Expression patterns of genes involved in ascorbate-glutathione cycle in aphid-infested maize (Zea mays L.) seedlings. International Journal of Molecular Sciences 17(268). doi: 10.3390/ijms17030268.
Sytykiewicz, H. (2016 b) Transcriptional reprogramming of genes related to ascorbate and glutathione biosynthesis, turnover and translocation in aphid-challenged maize seedlings. Biochemical Systematics and Ecology 69, 236251.
Sytykiewicz, H., Chrzanowski, G., Czerniewicz, P., Sprawka, I., Łukasik, I., Goławska, S. & Sempruch, C. (2014) Expression profiling of selected glutathione transferase genes in Zea mays (L.) seedlings infested with cereal aphids. PloS One 9(11), e111863.
Yang, C.M., Yang, M.M., Hsu, J.M. & Jane, W.N. (2003) Herbivorous insect causes deficiency of pigment-protein complexes in an oval-pointed cecidomyiid gall of Machilus thunbergii leaf. Botanical Bulletin of Academia Sinica 44, 315321.
Yang, X., Wang, X., Wei, M., Hikosaka, S. & Goto, E. (2009) Changes in growth and photosynthetic capacity of cucumber seedlings in response to nitrate stress. Brazilian Journal of Plant Physiology 21(4), 309317.
Vassilev, A. & Manolov, P. (1999) Chlorophyll fluorescence of barley (H. vulgare l.) seedlings grown in excess of Cd. Bulgarian Journal of Plant Physiology 25(3–4), 6776.



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