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The effect of Tetraneura ulmi L. galling process on the activity of amino acid decarboxylases and the content of biogenic amines in Siberian elm tissues

Published online by Cambridge University Press:  18 May 2017

K. Kmieć ,
C. Sempruch ,
G. Chrzanowski  and
P. Czerniewicz
K. Kmieć*
Affiliation:
Department of Entomology, 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
G. Chrzanowski
Affiliation:
Department of Biochemistry and Molecular Biology, Siedlce University of Natural Sciences and Humanities, Prusa 12, 08-110 Siedlce, Poland
P. Czerniewicz
Affiliation:
Department of Biochemistry and Molecular Biology, Siedlce University of Natural Sciences and Humanities, Prusa 12, 08-110 Siedlce, Poland
*
*Author for correspondence E-mail: [email protected]
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Abstract

Tetraneura ulmi (L.), a member of Eriosomatinae subfamily, is one of the gall-forming aphids occurring on elms. Sap-sucking behaviour of founding mothers results in the formation of new plant organs. This study documents the changes in the content of plant biogenic amines (putrescine, cadaverine, spermidine, tryptamine, spermine and histamine) and key enzymes of their biosynthesis: lysine decarboxylase (LDC), tyrosine decarboxylase and ornithine decarboxylase (ODC) in galls and other parts of Siberian elm (Ulmus pumila L.) leaves during the galling process. The direction and intensity of these changes for particular amines and enzymes were dependent on the stage of gall development and part of the galling leaf. Generally, the amine content tended to increase in gall tissues during the 1st and 2nd period of the galling process and decreased in later phases. LDC and ODC activities were markedly enhanced, especially in gall tissues at the initial stage of the galling process.

Keywords

polyaminesUlmus pumilalysine decarboxylasetyrosine decarboxylaseornithine decarboxylase
Type
Research Papers
Information
Bulletin of Entomological Research , Volume 108 , Issue 1 , February 2018 , pp. 69 - 76
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Copyright
Copyright © Cambridge University Press 2017 

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References

Agarrwal, R., Padmakumari, A.P., Bentur, J.S. & Nair, S. (2016). Metabolic and transcriptomic changes induced in host during hypersensitive response mediated resistance in rice against the Asian rice gall midge. Rice 9, 5 (doi: 10.1186/s12284-016-0077-6).Google Scholar
Alvarez, R., Gonzalez-Sierra, S., Candelas, A. & Martinez, J-J.I. (2013) Histological study of galls induced by aphids on leaves of Ulmus minor: Tetraneura ulmi induces globose galls and Eriosoma ulmi induces pseudogalls. Arthropod-Plant Interactions 7, 643–650.CrossRefGoogle Scholar
Bailey, S., Percy, D.M., Hefer, C.A. & Cronk, Q.C.B. (2015) The transcriptional landscape of insect galls: psyllid (Hemiptera) gall formation in Hawaiian Metrosideros polymorpha (Myrtaceae). BMC Genomics 16, 943 (doi: 10.1186/s12864-015-2109-9).Google Scholar
Bedetti, C.S., Modolo, L.V. & dos Santos Isaisas, R.M. (2014) The role of phenolics in the control of auxin in galls of Piptadenia gonoacantha (Mart.) MacBr (Fabaceae: Mimosoideae). Biochemical Systematics and Ecology 55, 53–59.Google Scholar
Blackman, R.L. & Eastop, V.F. (1994) Aphids on the World's Trees. An Identification and Information Guide, 986 pp. London, CAB International.CrossRefGoogle Scholar
Carter, M., Sacdev-Gupta, K. & Feeny, P. (1998) Tyramine from the leaves of wild parsnip: a stimulant and synergist for oviposition by the black swallowtail butterfly. Physiological Entomology 23, 303–312.Google Scholar
El-Akkad, S.S. (2004) Biochemical changes induced in Populus nigra leaves by galling aphid Pemphigous populi . International Journal of Agriculture and Biology 6, 659–664.Google Scholar
Fariduddin, Q., Varshney, P., Yusuf, M. & Ahmad, A. (2013) Polyamines: potent modulators of plant responses to stress. Journal of Plant Interactions 8, 1–16.Google Scholar
Fixon-Owoo, S., Lavasseur, F., Williams, K., Sabado, T.N., Lowe, M., Klose, M., Mercier, A.J., Fields, P. & Atkinson, J. (2003) Preparation and biological assessment of hydroxycinnamic acid amides of polyamines. Phytochemistry 63, 315–334.Google Scholar
Flores, H.E. & Galston, A.W. (1982) Analysis of polyamines in higher plants by high performance liquid chromatography. Plant Physiology 69, 701–706.CrossRefGoogle ScholarPubMed
Giron, D., Huguet, E., Stone, G.N. & Body, M. (2016) Insect-induced effects on plants and possible effectors used by galling and leaf-mining insect to manipulate their host-plant. Journal of Insect Physiology 84, 70–89.CrossRefGoogle ScholarPubMed
Horbowicz, M., Kosson, R., Wiczkowski, W., Koczkodaj, D. & Mitrus, J. (2011) The effect of methyl jasmonate on accumulation of 2-phenylethylamine and putrescine in seedlings of common buckwheat (Fagopyrum esculentum). Acta Physiologia Plantarum 33, 897–903.Google Scholar
Kmieć, K. & Kot, I. (2007) Tetraneura ulmi (L.) (Hemiptera, Eriosomatinae) on elm as its primary host. Aphids and Other Hemipterous Insects 13, 145–149.Google Scholar
Kmieć, K. & Kot, I. (2010) Występowanie mszyc z podrodziny Eriosomatinae na wiązach w parkach Lublina (Occurrence of aphids from Eriosomatinae subfamily on elms in the green area in Lublin). Annales Universitatis Mariae Curie-Skłodowska sec. EEE 20, 7–13 (doi: 10.2478/v10084-010-0002-6) (in Polish).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.CrossRefGoogle ScholarPubMed
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 21, 1937–1941.Google Scholar
Mandal, C., Gosh, N. & Adak, M.K. (2014) Effect of putrescine on oxidative stress induced by hydrogen peroxide in Salvinia natans L. Journal of Plant Interactions 9, 550–558.CrossRefGoogle Scholar
Mittempergher, L. & Santini, A. (2004) The history of elm breeding. Investigación agraria. Sistemas y recursos forestales 13, 161–177.Google Scholar
Moloi, M.J. & van der Westhuizen, A. (2006) The reactive oxygen species are involved in resistance responses of wheat to the Russian wheat aphid. Journal of Plant Physiology 163, 1118–1125.CrossRefGoogle ScholarPubMed
Nabity, P.D., Haus, M.J., Berenbaum, M.R. & DeLucia, E.H. (2013) Leaf-galling phylloxera on grapes reprograms host metabolism and morphology. PNAS Plant Biology 110, 16663–16668.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.CrossRefGoogle ScholarPubMed
Phan, A.P.H., Ngo, T.T. & Lenhoff, H.M. (1982) Spectrophotometric assay for lysine decarboxylase. Analytical Biochemistry 120, 193–197.CrossRefGoogle ScholarPubMed
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
Prade, P., Diaz, R., Vitorino, M.D., Cuda, J.P., Kumar, P., Gruber, B. & Overholt, W.A. (2016) Galls induced by Calophyta latiforceps (Hemiptera: Calophyidae) reduce leaf performance and growth of Brazilian peppertree. Biocontrol Science and Technology 26, 23–34.Google Scholar
Sempruch, C., Leszczyński, B., Kozik, A. & Chrzanowski, G. (2010) The influence of selected plant polyamines on feeding and survival of grain aphid (Sitobion avenae F.). Pesticides 1–4, 15–20.Google Scholar
Sempruch, C., Horbowicz, M., Kosson, R. & Leszczyński, B. (2012) Biochemical interactions between triticale (Triticosecale; Poaceae) amines and bird cherry-oat aphid (Rhopalosiphum padi; Aphididae). Biochemical Systematics and Ecology 40, 162–168.CrossRefGoogle Scholar
Sempruch, C., Marczuk, W., Leszczyński, B. & Czerniewicz, P. (2013) Participation of amino acid decarboxylases in biochemical interactions between triticale (Triticosecale; Poaceae) and bird cherry-oat aphid (Rhopalosiphum padi; Aphididae). Biochemical Systematics and Ecology 51, 349–356.Google Scholar
Sempruch, C., Leszczyński, B., Wilczewska, M., Chrzanowski, G., Sytykiewicz, H., Goławska, S., Kozak, A., Chwedczuk, M. & Klewek, A. (2015) Changes in amino acid decarboxylation in maize (Zea mays; Poaceae) tissues in response to bird cherry-oat aphid (Rhopalosiphum padi; Aphididae) infestation. Biochemical Systematics and Ecology 60, 158–164.Google Scholar
Sempruch, C., Goławska, S., Osiński, P., Leszczyński, B., Czerniewicz, P., Sytykiewicz, H. & Matok, H. (2016 a) 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
Sempruch, C., Leszczyński, B., Wilczewska, M., Sytykiewicz, H., Goławska, S. & Chrzanowski, G. (2016 b) Changes in enzyme activities involved in the biosynthesis of biogenic amines in wheat tissues of under bird cherry-oat aphid infestation. Biochemical Systematics and Ecology 65, 33–39.Google Scholar
Seneta, W. & Dolatowski, J. (2006) Dendrologia (Dendrology). Poland, PWN Warszawa (in Polish).Google Scholar
Statistica StatSoft Inc. (2010) Data Analysis Software System. Version 9.1 [Internet]. Available online at www.ststsoft.com.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
Suzuki, D.K., Fukushi, Y. & Akimoto, S. (2009) Do aphid galls provide good nutrients for the aphids?: comparisons of amino acid concentrations in galls among Tetraneura species (Aphididae: Eriosomatinae). Arthropod-Plant Interactions 3, 241–247.Google Scholar
Sytykiewicz, H. (2014) Differential expression of superoxide dismutase genes within aphid-stressed maize (Zea mays L.) seedlings. PLoS ONE 9, e94847.Google Scholar
Tomar, P.C., Lakrs, N. & Mishra, S.N. (2013) Cadaverine. A lysine catabolit involved in plant growth and development. Plant Signalling and Behavior 8(10), e25850.CrossRefGoogle Scholar
Urban, J. (2003) Bionomics and harmfulness of Tetraneura ulmi (L.) (Aphidinea, Pemphigidae) in elms. Journal of Forest Science 49, 159–181.CrossRefGoogle Scholar
Walters, D.R. (2003) Polyamines and plant diseases. Phytochemistry 64, 97–107.Google Scholar
Wool, D. (2004) Galling aphids: specialization, biological complexity, and variation. Annual Review of Entomology 49, 175–192.Google Scholar
Wu, S.B., Wang, M.Q. & Zhang, G. (2010) Effect of putrescine on diapause induction and intensity, and post-diapause development of Helicoverpa armigera . Entomologia Experimentalis et Applicata 136, 199–205.Google Scholar
Yoda, H., Fuijmura, K., Takahashi, H., Munemura, I., Uchimija, H. & Sano, H. (2009) Polyamines as a common source of hydrogen peroxide in host and nonhost hypersensitive response during pathogen infection. Plant Molecular Biology 70, 103–112.CrossRefGoogle ScholarPubMed
Zhang, Z.C., Wang, M.Q. & Zhang, G. (2008) Effects of polyamines and polyamine synthesis inhibitor on antennal electrophysiological responses of diamondback moths, Plutella xylostella . Entomologia Experimentalis et Applicata 129, 18–25.Google Scholar
Zhu, L., Liu, X., Liu, X., Jeannotte, R., Reese, J.C., Harris, M., Stuart, J.J. & Chen, M.S. (2008) Hessian fly (Mayetiola destructor) attack causes dramatic shift in carbon and nitrogen metabolism in wheat. Molecular Plant-Microbe Interactions 21, 70–78.Google Scholar