Hostname: page-component-cd9895bd7-gxg78 Total loading time: 0 Render date: 2024-12-26T07:22:10.012Z Has data issue: false hasContentIssue false

Biochemical responses induced in galls of three Cynipidae species in oak trees

Published online by Cambridge University Press:  24 October 2017

I. Kot*
Affiliation:
Department of Entomology, University of Life Sciences in Lublin, Leszczyńskiego 7, 20-069 Lublin, Poland
A. Jakubczyk
Affiliation:
Department of Biochemistry and Food Chemistry, University of Life Sciences in Lublin, Skromna 8, 20-704 Lublin, Poland
M. Karaś
Affiliation:
Department of Biochemistry and Food Chemistry, University of Life Sciences in Lublin, Skromna 8, 20-704 Lublin, Poland
U. Złotek
Affiliation:
Department of Biochemistry and Food Chemistry, University of Life Sciences in Lublin, Skromna 8, 20-704 Lublin, Poland
*
*Author for correspondence Phone: +48 815248102 E-mail: izabela.kot@up.lublin.pl

Abstract

Gall-making Cynipidae manipulate the leaves of host plant to form galls where offspring find shelter and food. The relationship between oak gallwasp and biochemical mechanisms of galls still requires a better understanding. So, in this research, protein and phenolic compound contents, as well as the activity of antioxidative enzymes and pathogenesis-related (PR) proteins were determined. Galls caused by asexual generation of Cynips quercusfolii L., Neuroterus numismalis (Fourc.) and N. quercusbaccarum L., as a model were used. All cynipid species modified the protein levels of gall tissues, but they cannot be treated as protein sinks. Significantly higher levels of phenols were observed in the galled leaves and galls of all cynipid species when compared with the control tissues. Peroxidase and polyphenol oxidase activity was usually low or showed no activity in galled tissues of all species. PR proteins, such as chitinase and β-1,3-glucanase, had a similar activity profile. Their activity significantly increased in the leaves with galls of all cynipid species, especially those infested with C. quercusfolii. Data generated in this study clearly indicate that galling Cynipidae manipulate the biochemical machinery of the galls for their own needs. However, the pattern of the biochemical features of leaves with galls and galled tissues depends on gall-making species.

Type
Research Papers
Copyright
Copyright © Cambridge University Press 2017 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Albert, S., Padhiar, A., Gandhi, D. & Nityanand, P. (2011) Morphological, anatomical and biochemical studies on the foliar galls of Alstonia scholaris (Apocynaceae). Revista Brasileira de Botanica 34(3), 343358.Google Scholar
Allison, S.D. & Schultz, J.C. (2005) Biochemical responses of chestnut oak to a galling cynipid. Journal of Chemical Ecology 31(1), 151166.CrossRefGoogle ScholarPubMed
Almagro, L., Gómez Ros, L.V., Belchi-Navarro, S., Bru, R., Ros Barceló, A. & Pedreňo, M.A. (2009) Class III peroxidases in plant defence reactions. Journal of Experimental Botany 60(2), 377390.CrossRefGoogle ScholarPubMed
Antony, B. & Palaniswami, M.S. (2006) Bemisia tabaci feeding induces pathogenesis-related proteins in cassava (Manihot esculenta Crantz). Indian Journal of Biochemistry and Biophysics 43, 182185.Google Scholar
Ashry, N.A. & Mohamed, H.I. (2012) Impact of secondary metabolites and related enzymes in flax resistance and/or susceptibility to powdery mildew. African Journal of Biotechnology 11(5), 10731077.Google Scholar
Barbehenn, R., Cheek, S., Gasperut, A., Lister, E. & Maben, R. (2005) Phenolic compounds in red oak and sugar maple leaves have prooxidant activities in the midgut fluids of Malacosoma disstria and Orgyia leucostigma caterpillars. Journal of Chemical Ecology 31(5), 969988.Google Scholar
Biswas, S.M., Chakraborty, N. & Baidyanath, P. (2014) Foliar gall and antioxidant enzyme responses in Alstonia scholaris, R. Br. After psylloid herbivory – an experimental and statistical analysis. Global Journal of Botanical Science 2, 1220.CrossRefGoogle Scholar
Boller, T., Gehri, A., Mauch, F. & Vögeli, U. (1983) Chitinase in bean leaves: induction by ethylene, purification, properties, and possible function. Planta 157, 2231.CrossRefGoogle ScholarPubMed
Bradford, M.M. (1976) A rapid and sensitive for the quantitation of microgram quantitites of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72, 248254.CrossRefGoogle Scholar
Castro, M.S. & Fontes, W. (2005) Plant defense and antimicrobial peptides. Protein and Peptide Letters 12(1), 1318.Google Scholar
Chance, B. & Maehly, A.C. (1955) Assay of catalases and peroxidases. Methods in Enzymology 2, 764775.CrossRefGoogle Scholar
Chen, H., Gonzales-Vigil, E., Wilkerson, C.G. & Howe, G.A. (2007) Stability of plant defense proteins in the gut of insect herbivores. Plant Physiology 143, 19541967.CrossRefGoogle ScholarPubMed
El-Khallal, S.M. (2007) Induction and modulation of resistance in tomato plants against Fusarium wilt disease by bioagent fungi (arbuscular mycorrhiza) and/or hormonal elicitors (jasmonic acid & salicylic acid): 2-Changes in the antioxidant enzymes, phenolic compounds and pathogen related-proteins. Australian Journal of Basic and Applied Sciences 1(4), 717732.Google Scholar
Fürstenberg-Hägg, J., Zagrobelny, M. & Bak, S. (2013) Plant defense against insect herbivores. International Journal of Molecular Sciences 14, 1024210297. doi: 10.3390/ijms140510242.Google Scholar
Gailite, A., Andersone, U. & Ievinsh, G. (2005) Arthropod-induced neoplastic formations on trees change photosynthetic pigment levels and oxidative enzyme activities. Journal of Plant Interactions 1(1), 6167.CrossRefGoogle Scholar
Golan, K., Rubinowska, K. & Górska-Drabik, E. (2013) Physiological and biochemical responses of fern Nephrolepsis biserrata (Sw.) Schott. to Coccus hesperidum L. infestation. Acta Biologica Cracoviensia Series Botanica 55/1, 9398. doi: 10.2478/abcsb-2013-0007.Google Scholar
Gulsen, O., Eickhoff, T., Heng-Moss, T., Shearman, R., Baxendale, F., Sarath, G. & Lee, D. (2010) Characterization of peroxidase changes in resistant and susceptible warm-season turfgrasses challenged by Blissus occiduus. Arthropod-Plant Interactions 4, 455.Google Scholar
Harper, L.J., Schönrogge, K., Lim, K.Y., Francis, P. & Lichtenstein, C.P. (2004) Cynipid galls: insect-induced modifications of plant development create novel plant organs. Plant, Cell and Environment 27, 327335.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, 492501.Google Scholar
He, J., Chen, F., Chen, S., Lv, G., Deng, Y., Fang, W., Liu, Z., Guan, Z. & He, C. (2011) Chrysanthemum leaf epidermal surface morphology and antioxidant and defense enzyme activity in response to aphid infestation. Journal of Plant Physiology 16, 687693.CrossRefGoogle 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) Leaf-derived cecidomyiid galls are sinks in Machilus thunbergii (Lauraceae) leaves. Physiologia Plantarum 152, 475485.Google Scholar
Huang, M.Y., Huang, W.D., Chou, H.M., Chen, C.C., Chen, P.J., Chang, Y.T. & Yang, C.M. (2015) Structural, biochemical and physiological characterization of photosynthesis in leaf-derived cup-shaped galls on Litsea acuminata. BMC Plant Biology 15, 61. doi: 10.1186/s12870-015-0446-0.CrossRefGoogle ScholarPubMed
Inbar, M., Mayer, R. & Doostdar, H. (2003) Induced activity of pathogenesis related (PR) proteins in aphid galls. Symbiosis 34, 110.Google Scholar
Isaias, R.M.S., Oliveira, D.C., Carneiro, R.G.S. & Kraus, J.E. (2014) Developmental anatomy of galls in the neotropics: arthropods stimuli versus host plant constraints. pp. 1534 in Fernandes, G.W. & Santos, J.C. (Eds) Neotropical Insect Galls. Science+Business Media Dordrecht, Springer. DOI 10.1007/978-94-017-8783-3_2.CrossRefGoogle Scholar
Jayamohan, N.S. & Kumudini, B.S. (2011) Host patogen interaction at the plant cell wall. International Research Journal of Pharmacy and Pharmacology 1(10), 242249.Google Scholar
Khattab, H. (2007) The defence mechanism of cabbage plant against phloem-sucking aphid (Brevicoryne brassicae L.). Australian Journal of Basic and Applied Sciences 1, 5662.Google Scholar
Kot, I., Kmieć, K., Górska-Drabik, E., Golan, K., Rubinowska, K. & Łagowska, B. (2015) The effect of mealybug Pseudococcus longispinus (Targioni Tozzetti) infestation of different density on physiological responses of Phalaenopsis × hybridum ‘Innocence’. Bulletin of Entomological Research 105, 373380. doi: 10.1017/S000748531500022X.Google Scholar
Larson, K.C. & Whitham, T.G. (1991) Manipulation of food resources by a gall-forming aphid: the physiology of sinksource interactions. Oecologia 88, 1521.CrossRefGoogle ScholarPubMed
Larson, K.C. & Whitham, T.G. (1997) Competition between gall aphids and natural plant sinks: plant architecture affects resistance to galling. Oecologia 109, 575582.CrossRefGoogle ScholarPubMed
Lattanzio, V., Lattanzio, V.M.T. & Cardinali, A. (2006) Role of phenolics in the resistance mechanisms of plants against fungal pathogens and insects. pp. 2367 in Imperato, F. (Ed.) Phytochemistry: Advances in Research. Trivandrum Kerala, Research Signpost.Google Scholar
Mayer, R.T., Inbar, M., McKenzie, C.L., Shstters, R., Borowicz, V., Albrecht, U., Powell, C.A. & Doostdar, H. (2002) Multitrophic interactions of the Silverleaf whitefly, host plants, competing herbivores, and phytopathogens. Archives of Insect Biochemistry and Physiology 51, 151169.Google Scholar
McCollum, T.G., Doostdar, H., McDonald, R.E., Shapiro, J.P., Mayer, R.T., Timmer, L.W. & Sonoda, R.M. (1995) Exploitation of plant pathogenesis-related proteins for enhanced pest resistance in citrus. Proceedings of the Florida State Horticultural Society 108, 8892.Google Scholar
Miller, G.L. (1959) Use of dinitrosalicylic acid for determination of reducing sugar. Analytical Chemistry 31, 426428.CrossRefGoogle Scholar
Mukherjee, S., Lokesh, G., Aruna, A.S., Sharma, S.P. & Sahay, A. (2016) Studies on the foliar biochemical changes in the gall (Trioza fletcheri minor) infested tasar food plants Terminalia arjuna and Terminalia tomentosa. Journal of Entomology and Zoology Studies 4(1), 154158.Google Scholar
Musser, R.O., Cipollini, D.F., Hum-Musser, S.M., Williams, S.A., Brown, J.K. & Felton, G.W. (2005) Evidence that the caterpillar salivary enzyme glucose oxidase provides herbivore offense in Solanaceous plants. Archives of Insect Biochemistry and Physiology 58, 128137.Google Scholar
Ni, X., Quisenberry, S.S., Heng_Moss, T., Markwell, J., Sarath, G., Klucas, R. & Baxendale, F. (2001) Oxidative responses of resistant and susceptible cerealaphid (Hemiptera: Aphididae) feeding. Journal of Economic Entomology 94, 743751.Google Scholar
Rifat, H., Minhaj, A.K., Mahboob, A., Malik, M.A., Malik, Z.A., Javed, M. & Saleem, J. (2013) Chitinases: an update. Journal of Pharmacy And Bioallied Sciences 5(1), 2129. doi: 10.4103/0975-7406.106559.Google Scholar
Rocha, S., Branco, M., Vilas Boas, L., Almeida, M.H., Protasov, A. & Mendel, Z. (2013) Gall induction may benefit host plant: a case of a gall wasp and eucalyptus tree. Tree Physiology 33, 388397. doi: 10.1093/treephys/tpt009.Google Scholar
Rokas, A., Melika, G., Abe, Y., Nieves-Aldrey, J.L., Cook, J.M. & Stone, G.N. (2003) Lifecycle closure, lineage sorting, and hybridization revealed in a phylogenetic analysis of European oak gallwasps (Hymenoptera: Cynipidae: Cynipini) using mitochondrial sequence data. Molecular Phylogenetics and Evolution 26, 3645.CrossRefGoogle Scholar
Sampson, M.N. & Gooday, G.W. (1998) Involvement of chitinases of Bacillus thuringiensis during pathogenesis in insects. Microbiology 144(8), 21892194.Google Scholar
Schönrogge, K., Harper, L.J. & Lichtenstein, C.P. (2000). The protein content of tissues in cynipid galls (Hymenoptera: Cynipidae): similarities between cynipid galls and seeds. Plant Cell and Environment 23, 215222.Google Scholar
Shivashankar, S., Sumathi, M. & Ranganath, H.R. (2012) Roles of reactive oxygen species and anti-oxidant systems in the resistance response of chayote fruit (Sechium edule) to melon fly [Bactrocera cucurbitae (Coquillett)]. Journal of Horticultural Science and Biotechnology 87(4), 391397.Google Scholar
Singh, H., Dixit, S., Verma, P.C. & Kumar, P. (2013) Differential peroxidase activities in three different crops upon insect feeding. Plant Signaling & Behavior 8, e25615. Available online at http://dx.doi.org/10.4161/psb.25615.Google Scholar
Singleton, V.L., Orthofer, R. & Lamuela-Raventos, R.M. (1974) Analysis of total phenols and other oxidation substrates and antioxidants by means of Folin-Ciocalteu reagent. Methods in Enzymology 299, 152178.Google Scholar
Soffan, A., Alghamdi, S.S. & Aldawood, A.S. (2014) Peroxidase and polyphenol oxidase activity in moderate resistant and susceptible Vicia faba induced by aphis craccivora (Hemiptera: Aphididae) infestation. Journal of Insect Science 14, 285–291. doi: 10.1093/jisesa/ieu147.CrossRefGoogle ScholarPubMed
Sprawka, I., Ciepiela, A., Sempruch, C., Chrzanowski, G., Sytykiewicz, H. & Czerniewicz, P. (2003) Nutritive value of soluble protein of spring triticale ears infested by the grain aphid (sitobion avenae /F./). Eelectronic Journal of Polish Agricultural Universities 6(2), #03. http://www.ejpau.media.pl/Google Scholar
Stone, G.N. & Schönrogge, K. (2003) The adaptive significance of insect gall morphology. Trends in Ecology & Evolution 18, 512522.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, 633668.CrossRefGoogle ScholarPubMed
Taggar, G.K., Gill, R.S., Gupta, A.K. & Sandhu, J.S. (2012) Fluctuations in peroxidase and catalase activities of resistant and susceptible black gram (Vigna mungo (L.) Hepper) genotypes elicited by Bemisia tabaci (Gennadius) feeding. Plant Signaling & Behavior 7(10), 13211329. doi: 10.4161/psb.21435.CrossRefGoogle ScholarPubMed
Vázquez-Garcidueňas, S., Leal-Morales, C.A. & Herrera-Estrella, A. (1998) Analysis of the β-1,3-glucanolytic system of the biocontrol agent Trichoderma harzianum. Applied and Environmental Microbiology 64, 14421446.CrossRefGoogle ScholarPubMed
War, A.R., Paulraj, M.G., Ahmad, T., Buhroo, A.A., Hussain, B., Ignacimuthu, S. & Sharma, H.C. (2012) Mechanisms of plant defense against insect herbivores. Plant Signaling & Behavior 7(10), 13061320.Google Scholar
Wei, H., Zhikuan, J. & Qingfang, H. (2007) Effects of herbivore stress by Aphis medicaginis Koch. on the malondialdehyde contents and the activities of protective enzymes in different alfalfa varieties. Acta Ecologica Sinica 27, 21772183.CrossRefGoogle Scholar
Wisserman, K.W. & Lee, C.Y. (1980) Purification of grape polyphenoloxidase with hydrophobic chromatography. Journal of Chromatography 192, 232235.CrossRefGoogle Scholar
Zhao, H., Zhang, X., Xuel, M. & Zhang, X. (2015) Feeding of whitefly on tobacco decreases aphid performance via increased salicylate signaling. PLoS ONE 10, e0138584. doi: 10.1371/journal.pone.0138584.Google Scholar