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Influence of selected plant amines on probing behaviour of bird cherry-oat aphid (Rhopalosiphum padi L.)

Published online by Cambridge University Press:  22 February 2016

C. Sempruch ,
S. Goławska ,
P. Osiński ,
B. Leszczyński ,
P. Czerniewicz ,
H. Sytykiewicz  and
H. Matok
C. Sempruch*
Affiliation:
Department of Biochemistry and Molecular Biology, University of Podlasie, ul. Prusa 12, 08-110 Siedlce, Poland
S. Goławska
Affiliation:
Department of Biochemistry and Molecular Biology, University of Podlasie, ul. Prusa 12, 08-110 Siedlce, Poland
P. Osiński
Affiliation:
Department of Biochemistry and Molecular Biology, University of Podlasie, ul. Prusa 12, 08-110 Siedlce, Poland
B. Leszczyński
Affiliation:
Department of Biochemistry and Molecular Biology, University of Podlasie, ul. Prusa 12, 08-110 Siedlce, Poland
P. Czerniewicz
Affiliation:
Department of Biochemistry and Molecular Biology, University of Podlasie, ul. Prusa 12, 08-110 Siedlce, Poland
H. Sytykiewicz
Affiliation:
Department of Biochemistry and Molecular Biology, University of Podlasie, ul. Prusa 12, 08-110 Siedlce, Poland
H. Matok
Affiliation:
Department of Biochemistry and Molecular Biology, University of Podlasie, ul. Prusa 12, 08-110 Siedlce, Poland
*
*Author for correspondence Phone: +48 25 6431224 Fax: +48 25 6445959 E-mail: cezar@ap.siedlce.pl
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Abstract

The study aimed to quantify the influence of common plant polyamines and tyramine on probing behaviour in the bird cherry-oat aphid (Rhopalosiphum padi L.). Electrical penetration graphs (DC) were used to monitor the probing and feeding behaviour of R. padi exposed to the amines agmatine, cadaverine, putrescine, spermidine, spermine and tyramine. The study results showed that the analyzed amines tended to shorten the stylet activity of aphids in the gels (as indicated by the g-C pattern), prolong the duration of non-probing behaviour (g-np pattern) and decrease salivation into the gels (g-E1pattern) and ingestion from the gels (g-G pattern). The 10 mM concentration of the studied amines, especially cadaverine, reduced or completely inhibited aphid ingestion. The obtained results demonstrate that plant amines participate in plant defence responses to R. padi through disturbance of its probing behaviour and the intensity of such effects is concentration dependent.

Keywords

polyaminestyraminebird cherry-oat aphidaphid probing behaviourinsect–plant interactions
Type
Research Papers
Information
Bulletin of Entomological Research , Volume 106 , Issue 3 , June 2016 , pp. 368 - 377
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Copyright
Copyright © Cambridge University Press 2016 

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References

Bassard, J.E., Ullmann, P., Bernier, F. & Werck-Reichhart, D. (2010) Phenoloamines: bridging polyamines to the phenolic metabolism. Phytochemistry 71, 1808–1824.CrossRefGoogle Scholar
Biondi, S., Scaramagli, S., Capitani, F., Altamura, M.M. & Torrigiani, P. (2001) Methyl jasmonate upregulates biosynthetic gene expression, oxidation and conjugation of polyamines, and inhibits shoot formation in tobacco thin layers. Journal of Experimental Botany 52, 231–242.Google Scholar
Biondi, S., Scoccianti, V., Scaramagli, S., Ziosi, V. & Torrigiani, P. (2003) Auxin and cytokinin modify methyl jasmonate effects on polyamine metabolism and ethylene biosynthesis in tobacco leaf discs. Plant Sciences 165, 95–101.Google Scholar
Chen, H., Jones, D.A. & Howe, G.A. (2006) Constitutive activation of the jasmonate signaling pathway enhances the production of secondary metabolites in tomato. FEBS Letters 580, 2540–2546.Google Scholar
Cherqui, A. & Tjallingii, W.F. (2000) Salivary proteins of aphids, a pilot study on identification, separation and immunolocalization. Journal of Insect Physiology 46, 1177–1186.Google Scholar
Douglas, A.E. (2006) Phloem-sap feeding by animals: problems and solutions. Journal of Experimental Botany 57, 747–754.Google Scholar
Facchini, P.J. (1998) Temporal correlation of tyramine metabolism with alkaloid and amide biosynthesis in elicited opium poppy cell cultures. Phytochemistry 49, 481–490.Google Scholar
Facchini, P.J., Hübner-Allanach, K.L. & Tari, L.W. (2000) Plant aromatic l-amino acid decarboxylases: evolution, biochemistry, regulation and metabolic engineering applications. Phytochemistry 54, 121–138.CrossRefGoogle ScholarPubMed
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
Felton, G.W. & Tumlinson, J.H. (2008) Plant-insect dialogs: complex interaction at the plant-insect interface. Current Opinion in Plant Biology 11, 457–463.Google Scholar
Ferry, N., Edwards, M.G., Gatehouse, J.A. & Gatehouse, A.M.R. (2004) Plant-insect interactions: molecular approach to insect resistance. Current Opinion in Biotechnology 15, 155–161.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
Giordanengo, P., Brunissen, L., Rusterucci, C., Vincent, C., van Bel, A., Dinant, S., Girousse, C., Faucher, M. & Bonnemain, J.L. (2010) Compatible plant-aphid interactions: how aphids manipulate plant responses. Comptes Rendus Biologies 333, 516–523.Google Scholar
Goggin, F.L. (2007) Plant-aphids interactions: molecular and ecological perspectives. Current Opinion in Plant Biology 10, 399–408.Google Scholar
Goławska, S. & Łukasik, I. (2012) Antifeedant activity of luteolin and genistein against the pea aphid, Acyrthosiphon pisum. Journal of Pest Science 85, 443–450.Google Scholar
Goławska, S., Leszczyński, B. & Oleszek, W. (2006) Effect of low and high-saponin lines of alfalfa on pea aphid. Journal of Insect Physiology 52, 737–743.Google Scholar
Goławska, S., Łukasik, I. & Leszczyński, B. (2008) Effect of alfalfa saponins and flavonoids on pea aphid. Entomologia Experimentalis et Applicata 128, 147–153.CrossRefGoogle Scholar
Goławska, S., Sprawka, I., Goławski, A. & Matok, H. (2014) Are agarose-sucrose gels useful for studying the probing and feeding behaviour of aphids? Australian Journal of Crop Science 8(2), 263–270.Google Scholar
Groppa, M.D. & Benavides, M.P. (2008) Polyamines and abiotic stress: recent advances. Amino Acids 34, 35–45.Google Scholar
Guillet, G. & De Luca, V. (2005) Wound-inducible biosynthesis of phytoalexin hydroxycinnamic acid amides of tyramine in tryptophan and tyrosine decarboxylase transgenic tobacco lines. Plant Physiology 137, 692–699.CrossRefGoogle ScholarPubMed
Hagel, J.M. & Facchini, P.J. (2005) Elevated tyrosine decarboxylase and tyramine hudroxycinnamoltransferase levels increase wound-induced tyramine-derived hydroxycinnamic acid amide accumulation in transgenic tobacco leaves. Planta 221, 904–914.Google Scholar
Horbowicz, M., Kosson, R., Sempruch, C., Dębski, H. & Koczkodaj, D. (2014) Effect of methyl jasmonate vapors on level of anthocyanins, biogenic amines and decarboxylases activity in seedlings of chosen vegetable species. Acta Scientarum Polonorum Hortorum Cultus 13, 3–15.Google Scholar
Horowitz, A.R. & Ishaaya, I. (2004) Insect Pest Management: Field and Protected Crops. Springer-Verlag.CrossRefGoogle Scholar
Igarashi, K. & Kashiwagi, K. (2010) Modulation of cellular function by polyamines. International Journal of Biochemical Cell Biology 42, 39–51.Google Scholar
Jiménez-Bremont, J.F., Marina, M., de la Luz Guerrero-González, M., Rosi, F.R., Sánchez-Rangel, D., Rodrigez-Kessler, M., Ruiz, O.A. & Gárriz, A. (2014) Physiological and molecular implications of plant polyamine metabolism during biotic interactions. Frontiers in Plant Sciences 5, Article 95.Google Scholar
Klose, M.K., Atkinson, J.K. & Mercier, A.J. (2002) Effect of hydroxy-cinnamoyl conjugate of spermidine on arthropod neuromuscular junctions. Journal of Comparative Physiology 187, 945–952.Google Scholar
Kordan, B., Gabryś, B., Dancewicz, K., Lahuta, L.B., Piotriwicz-Cieslak, A. & Rowińska, E. (2008) European yellow lupine, Lupinus luteus, and narrow-leaf lupine, Lupinus angustifolius, as hosts for the pea aphid, Acyrthosiphon pisum. Entomologia Experimentalis et Applicata 128, 139–146.Google Scholar
Kubo, I. (2006) New concept to search for alternate insect control agents from plants. pp. 61–80in Rai, M. & Carpinella, M. (Eds) Naturally Occurring Bioactive Compounds 3. Amsterdam, Elsevier.Google Scholar
Kulma, A. & Szopa, J. (2007) Catecholoamines are active compounds in plants. Plant Sciences 172, 433–440.Google Scholar
Kusano, T., Berberich, T., Takeda, C. & Takahashi, Y. (2008) Polyamines: essential factors for growth and survival. Planta 228, 367–381.Google Scholar
Kusano, T., Yamaguchi, K., Barberich, T. & Takahashi, Y. (2007) Advances in polyamine research in 2007. Journal of Plant Research 120, 345–350.Google Scholar
Mader, J.C. (1999) Effects of jasmonic acid, silver nitrate and L-AOPP on the distribution of free and conjugated polyamines in roots and shoots of Solanum tuberosum in vitro. Journal of Plant Physiology 154, 79–88.Google Scholar
Mattoo, A.K., Minocha, S.C., Minocha, R. & Handa, A.K. (2010) Polyamines and cellular metabolism in plants: transgenic approach reveal different responses to diamine putrescine versus higher polyamines spermidine and spermine. Amino Acids 38, 405–413.CrossRefGoogle ScholarPubMed
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.Google Scholar
Morant, A.V., Jørgensen, K., Jørgensen, C., Paquette, S.M., Sánchez-Pérez, R., Møller, B.L. & Bak, S. (2008) β-Glucosidases as detonators of plant chemical defense. Phytochemistry 69, 1795–1813.Google Scholar
Moret, S., Selma, D., Populin, T. & Conte, L.S. (2005) A survey of free biogenic amine content of fresh and preserved vegetables. Food Chemistry 89, 355–361.Google Scholar
Mortari, M.R., Cunha, A.O.S., Ferreira, L.B. & Ferreira dos Santos, W. (2007) Neurotoxins from invertebrates as anticonvulsants: from basic research to therapeutic application. Pharmacological Therapy 114, 171–183.Google Scholar
Ollerstam, O., Rohfritsch, O., Höglund, S. & Larsson, S. (2002) A rapid hypersensitive response associated with resistance in the willow Salix viminalis against gall midge Dasineura marginemptorques. Entomologia Experimentalis et Applicata 102, 153–162.Google Scholar
Pompon, J., Quiring, D., Giordanengo, P. & Pelletier, Y. (2010) Role of xylem consumption on osmoregulation in Macrosiphum euphorbie (Thomas). Journal of Insect Physiology 56, 610–615.Google Scholar
Ponder, K.L., Pritchard, J., Harrington, R. & Bale, J.S. (2000) Difficulties in location and acceptance of phloem sap combined with reduced concentration of phloem amino acids explain lowered performance of aphid Rhopalosiphum padi on nitrogen deficient barley (Hordeum vulgare) seedlings. Entomologia Experimentalis et Applicata 97, 203–210.Google Scholar
Rharrabe, K., Bakrim, A., Ghailani, N. & Sayah, F. (2007) Bioinsecticidal effect of harmaline on Plodia interpunctella development (Lepidoptera: Pyralidae). Pesticide Biochemistry and Physiology 89, 137–145.Google Scholar
Saheed, S.A., Liu, L., Jonsson, L. & Botha, C.E.J. (2007) Xylem – as well as phloem – sustain severe damage due to feeding by the Russian wheat aphid. South African Journal of Botany 73, 593–599.Google Scholar
Sempruch, C. & Ciepiela, A.P. (2005) The participation of polyamines in mechanism of winter triticale resistance to grain aphid (Sitobion avenae F.). IOBC Bulletin 28, 107–112.Google Scholar
Sempruch, C., Wójcicka, A., Makosz, M. & Leszczyński, B. (2008) Changes in activity of ornithine decarboxylase in winter triticale caused by grain aphid feeding. Zeszyty Problemowe Postępów Nauk Rolniczych 524, 401–408.Google Scholar
Sempruch, C., Leszczyński, B., Wójcicka, A., Makosz, M., Chrzanowski, G. & Matok, H. (2009) Changes in activity of triticale tyrosine decarboxylase caused by grain aphid feeding. Polish Journal of Environmental Studies 18, 901–906.Google Scholar
Sempruch, C., Leszczyński, B., Kozik, A. & Chrzanowski, G. (2010 a) 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., Leszczyński, B., Wójcicka, A., Makosz, M., Matok, H. & Chrzanowski, G. (2010 b) Changes in activity of lysine decarboxylase within winter triticale in response to grain aphid feeding. Acta Biologica Hungarica 61, 512–515.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.Google 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.CrossRefGoogle Scholar
Serafini-Fracassini, D., Della Mea, M.D., Tasco, G., Casadio, R. & Del Duca, S. (2009) Plant and animal transglutaminases: do similar functions imply similar structures. Amino Acids 36, 643–657.Google Scholar
Shalaby, A.R. (1996) Significance of biogenic amines to food safety and human health. Food Research International 29, 675–690.Google Scholar
Sprawka, I. & Goławska, S. (2010) Effect of the lectin PHA on the feeding behaviour of the grain aphid. Journal of Pest Science 83, 149–155.Google Scholar
Sprawka, I., Goławska, S., Czerniewicz, P. & Sytykiewicz, H. (2011) Insecticidal action of phytohemagglutinin (PHA) against the grain aphid, Sitobion avenae. Pesticide Biochemistry and Physiology 100, 64–69.Google Scholar
Spiller, N.J., Koenders, L. & Tjallingii, W.F. (1990) Xylem ingestion by aphids – a strategy for maintaining water balance. Entomologia Experimentalis et Applicata 55, 101–104.Google Scholar
StatSoft Inc, Statistica (2010) Data Analysis Software System version 9.0. www.statsoft.com.Google Scholar
Stotz, H.U., Kroymann, J. & Mitchell-Olds, T. (1999) Plant-insect interactions. Current Opinion in Plant Biology 2, 268–272.Google Scholar
Strømgaard, K., Jensen, L.S. & Vogensen, S.B. (2005) Polyamine toxins: development of selective ligands for ionotropic receptors. Toxicon 45, 249–254.Google Scholar
Sytykiewicz, H., Goławska, S. & Chrzanowski, G. (2011) Effect of the bird cherry-oat aphid Rhopalosiphum padi L. feeding on phytochemical responses within the bird cherry Prunus padus L. Polish Journal of Ecology 59, 329–338.Google Scholar
Tebayashi, S., Horibata, Y., Mikagi, E., Kashiwagi, T., Mekuria, D.B., Dekebo, A., Ishihara, A. & Kim, C.S. (2007) Induction of resistance against the leafminer, Liriomyza trifolii, by jasmonic acid in sweet pepper. Bioscience Biotechnology and Biochemistry 71, 1521–1526.Google Scholar
Tjallingii, W.F. (1985) Membrane potentials as an indication for plant cell penetration by aphid stylets. Entomologia Experimentalis et Applicata 38, 187–193.CrossRefGoogle Scholar
Tjallingii, W.F. (1988) Electrical recording of stylet penetration activities by aphids. pp. 89–99in Campbell, R.K. & Eikenbary, R.D. (Eds) Aphids, their Biology, Natural Enemies and Control, Vol. B. Amsterdam, Elsiver.Google Scholar
Tjallingii, W.F. (1990) Continuous recording of stylet penetration activities by aphids. pp. 88–89in Campbell, R.K. & Eikenbary, R.D. (Eds) Aphid – Plant Genotype Interactions. Amsterdam, Elsevier.Google Scholar
Tjallingii, W.F. (1994) Sieve element acceptance by aphids. European Journal of Entomology 91, 47–52.Google Scholar
Todorova, D., Katerova, Z., Sergiev, I. & Alexieva, V. (2014) Polyamines – involvement in plant stress tolerance and adaptation. pp. 194–221in Ajum, N.A. & Gill, R. (Eds) Plant Adaptation to Environmental Change. CAB International.Google Scholar
Tomar, P.C., Lakra, N. & Mishra, S.N. (2013) Cadaverine. A lysine catabolite involved in plant growth and development. Plant Signaling and Behaviour 8, e25850.Google Scholar
Urbanska, A., Tjallingii, W.F., Dixon, A.F.G. & Leszczynski, B. (1998) Phenol oxidizing enzymes in the grain aphid's saliva. Entomologia Experimentalis et Applicata 86, 197–20.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.CrossRefGoogle Scholar
Xu, B., Sheehan, M.J. & Timko, M.P. (2004) Differential induction of ornithine decarboxylase (ODC) gene family members in transgenic tobacco (Nicotiana tabacum L. cv. Bright yellow 2) cell suspension by methyl-jasmonate treatment. Plant Growth Regulators 44, 101–116.Google Scholar
Zhao, L.Y., Chen, J.L., Cheng, D.F., Sun, J.R., Liu, Y. & Tian, Z. (2009) Biochemical and molecular characterization of Sitobion avenae-induced wheat defense responses. Crop Protection 28, 435–442.Google Scholar