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

Published online by Cambridge University Press:  13 June 2019

I. Kot ,
C. Sempruch ,
K. Rubinowska  and
W. Michałek
I. Kot*
Affiliation:
Department of Plant Protection, University of Life Sciences in Lublin, Leszczyńskiego 7, 20-069 Lublin, Poland
C. Sempruch
Affiliation:
Department of Biochemistry and Molecular Biology, Siedlce University of Natural Sciences and Humanities, Prusa 12, 08-110 Siedlce, Poland
K. Rubinowska
Affiliation:
Department of Botany and Plant Physiology, University of Life Sciences in Lublin, Akademicka 15, 20-950 Lublin, Poland
W. Michałek
Affiliation:
Department of Botany and Plant Physiology, University of Life Sciences in Lublin, Akademicka 15, 20-950 Lublin, Poland
*
*Author for correspondence Phone: +48 81 524 81 02 Fax: 81 524 81 03 E-mail: izabela.kot@up.lublin.pl
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Abstract

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.

Keywords

gall waspcytoplasmic membrane conditionH2O2 contentantioxidant enzymesamino acid decarboxylasechlorophyll fluorescence
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 110 , Issue 1 , February 2020 , pp. 34 - 43
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Copyright
Copyright © Cambridge University Press 2019 

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References

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, 221–232.Google Scholar
Ashraf, M. & Harris, P.J.C. (2013) Photosynthesis under stressful environments: an overview. Photosynthetica 51(2), 163–190Google Scholar
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.Google Scholar
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, 192–201.Google Scholar
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, 1511–1527.Google Scholar
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), 97–117.Google Scholar
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, 97–104.Google Scholar
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), 1011–1019.Google Scholar
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.Google Scholar
Dorchin, N., Cramer, M.D. & Hoffman, J.H. (2006) Photosynthesis and sink activity of wasp-induced galls in Acacia pycnantha. Ecology 87, 1781–1791.Google Scholar
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, https://doi.org/10.1371/journal.pone.0198093Google Scholar
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, 55–65. https://doi.org/10.1007/s11829-014-9339-7.Google Scholar
Gill, S. S. & Tuteja, N. (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiology and Biochemistry 48, 909–930.Google Scholar
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.Google Scholar
Guidi, L. & Degl'Innocenti, E. (2012) Chlorophyll a fluorescence in abiotic stress pp. 359–399 in Venkateswarlu, B., Shanker, A., Shanker, C., Maheswari, M. (Ed.) Crop Stress and its Management: Perspectives and Strategies. Dordrecht, the Netherlands, Springer.Google Scholar
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, 233–240.Google Scholar
Haiden, S.A., Hoffmann, J.H. & Cramer, M.D. (2012) Benefits of photosynthesis for insects in galls. Oecologia 170, 987–997.Google Scholar
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.Google Scholar
Heath, R.L. & Packer, L. (1968) Effect of light on lipid peroxidation in chloroplasts. Biochemical and Biophysical Research Communications 19, 716–720.Google Scholar
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), 973–979.Google Scholar
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, 151–154.Google Scholar
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), 475–485.Google Scholar
Isaias, R.M.S. & Oliveira, D. C. (2012) Gall phenotypes – product of plant cells defensive responses to the inducers attack 12, pp. 273–290 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.Google Scholar
Jena, S. & Choudhuri, M.A. (1981) Glycolate metabolism of three submerged aquatic angiosperms during aging. Aquatic Botany 12, 345–354.Google Scholar
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, 160–175. https://doi.org/10.1111/pce.13050.Google Scholar
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), 75–83.Google Scholar
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, 1–6.Google Scholar
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, 79–84.Google Scholar
Khattab, H. (2007) The defense mechanism of cabbage plant against phloem-sucking aphid (Brevicoryne brassicae L.). Australian Journal of Basic and Applied Sciences 1, 56–62.Google Scholar
Kierych, E. (1979) Galasówkowate (Cynipoidea) p. 103 in Catalogus faunae Poloniae. Warsaw, PWN.Google Scholar
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), 2489–2494. https://doi.org/10.1093/jee/tow236.Google Scholar
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), 840–847. doi: 10.1093/ee/nvy055Google Scholar
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.Google Scholar
Kot, I. & Rubinowska, K. (2018) Physiological response of pedunculated oak trees to gall-inducing Cynipidae. Environmental Entomology 47(3), 669–675Google Scholar
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), 494–500Google Scholar
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), 147–157.Google Scholar
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), 247–253.Google Scholar
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, 591–592.Google Scholar
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, 256–277.Google Scholar
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, 1937–1941.Google Scholar
Maffei, M.E., Mithöfer, A. & Boland, W. (2007) Insects feeding on plants: rapid signals and responses preceding the induction of phytochemical release. Phytochemistry 68, 2946–2959.Google Scholar
Małolepsza, A., Urbanek, H. & Polit, J. (1994) Some biochemical of strawberry plants to infection with Botrytis cinerea and salicylic acid treatment. Acta Agrobotanica 47, 73–81.Google Scholar
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, 3389–3406.Google Scholar
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.Google Scholar
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), 655–663.Google Scholar
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, 905–913.Google Scholar
Nakano, Y. & Asada, K. (1981) Hydrogen peroxide is scavenged by ascorbate specific peroxidase in spinach chloroplasts. Plant and Cell Physiology 22, 867–880.Google Scholar
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, 290–293.Google Scholar
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, 489–495.Google Scholar
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.Google Scholar
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.Google Scholar
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), 29–36.Google Scholar
Phan, A.P.H., Ngo, T.T. & Lenhoff, H.M. (1982) Spectrophotometric assay for lysine decarboxylase. Analytical Biochemistry 120, 193–197.Google Scholar
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, 127–133.Google Scholar
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, 2–18.Google Scholar
Rabino, I. & Mancinelli, A. (1986). Light, temperature and anthocyanin production. Plant Physiology 81, 922–924. http://dx.doi.org/10.1104/pp.81.3.922.Google Scholar
Ramakrishna, A. & Ravishankar, G.A. (2011) Influence of abiotic stress signals on secondary metabolites in plants. Plant Signaling & Behavior 6(11), 1720–1731.Google Scholar
Retuerto, R., Fernandez-Lema, B., Rodriguez, R. & Obeso, J.R. (2004) Increased photosynthetic performance in holly trees infested by scale insects. Functional Ecology 18, 664–669.Google Scholar
StatSoft Inc. (2016) Statistica (data analysis software system), version v. 13.1, www.statsoft.comGoogle Scholar
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, 15–26.Google Scholar
Schreiber, U. (2004) Pulse amplitude modulation (PAM) fluorometry and saturation pulse method: an overview pp. 279–319 in Papageorgiou, G.C. (Ed.) Chlorophyll A Fluorescence: A Signature of Photosynthesis. Dordrecht, Kluwer Academic.Google Scholar
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, 162–168.Google Scholar
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, 83–91.Google Scholar
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), 45–50.Google Scholar
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), 825–831. http://dx.doi.org/10.1080/17429145.2014.954014.Google Scholar
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, 368–377.Google Scholar
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, 633–668.Google Scholar
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.Google Scholar
Sytykiewicz, H. (2014) Differential expression of superoxide dismutase genes in aphid-stressed maize (Zea mays L.) seedlings. PloS ONE 9(4), e94847.Google Scholar
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.Google Scholar
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, 236–251.Google Scholar
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.Google Scholar
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, 315–321.Google Scholar
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), 309–317.Google Scholar
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), 67–76.Google Scholar