Acta Biologica Hungarica

, Volume 62, Issue 3, pp 316–327 | Cite as

Induced Proteolysis within the Bird Cherry Leaves Evoked by Rhopalosiphum PadiL. (Hemiptera, Aphidoidea)

  • H. SytykiewiczEmail author
  • P. Czerniewicz
  • Iwona Sprawka
  • Sylwia Goławska
  • G. Chrzanowski
  • B. Leszczyński


The objectives of this study were to elucidate the impact of bird cherry-oat aphid (Rhopalosiphum padi L.) feeding on functioning of the proteolytic machinery in bird cherry leaves. Biochemical analyses proved that R. padi feeding in tissues of primary host stimulated activity of the two major fractions of proteinases (extracted at the optimal pH values: 5.0 and 7.0). Additionally, it has been demonstrated that aphids’ feeding on bird cherry led to a. decline in levels of albumins and globulins (main protein fractions in P. padus leaves). The opposite tendency, regarding the amounts of these protein fractions was ascertained at the phase of disappearance of R. padi population on tested shoots. Furthermore, it is reported that an increase in activity of the analysed enzymes and a. decline in the content of tested protein fractions, were proportional to density of aphid individuals developing on P. padus side shoots. It is hypothesized that long-term R. padi feeding may lead to intensifying the catabolic processing of proteins by the activated proteolytic machinery in bird cherry leaves. The multi-level biological functions of endogenous plant proteinases and their significance in triggering the defense reactions in aphid-infested plant tissues are discussed.


Proteolysis proteinases albumins globulins aphid-plant interactions 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. 1.
    Beers, E. P., Jones, A. M., Dickerman, A. W. (2004) The S8 serine, CIA cysteine and Al aspartic protease families in Arabidopsis. Phytochem. 65, 43–58.CrossRefGoogle Scholar
  2. 2.
    Beyene, G., Foyer, C. H., Kunert, K. J. (2006) Two new cysteine proteinases with specific expression patterns in mature and senescent tobacco (Nicotiana tabacum L.) leaves. J. Exp. Bot. 57, 1431–1443.CrossRefGoogle Scholar
  3. 3.
    Bolter, B., Nada, A., Fulgosi, H., Soil, J. (2006) A. chloroplastic inner envelope membrane protease is essential for plant development. FEES Lett. 580, 789–794.CrossRefGoogle Scholar
  4. 4.
    Bonnemain, J.-L. (2010) Aphids as biological models and agricultural pests. Comptes Rend Biol. 333, 461–463.CrossRefGoogle Scholar
  5. 5.
    Book, A. J., Smalle, J., Lee, K.-H., Yang, P., Walker, J. M., Casper, S., Holmes, J. H., Russo, L. A., Buzzinotti, Z. W., Jenik, P. D., Vierstra, R. D. (2009) The RPN5 subunit of the 26S proteasome is essential for gametogenesis, sporophyte development, and complex assembly in Arabidopsis. Plant Cell 21, 460–478.CrossRefGoogle Scholar
  6. 6.
    Carolan, J. C., Fitzroy, C. I. J., Ashton, P. D., Douglas, A. E., Wilkinson, T. L. (2009) The secreted salivary proteome of the pea aphid, Acyrthosiphon pisum characterised by mass spectrometry. Proteomics 9, 2457–2467.CrossRefGoogle Scholar
  7. 7.
    Chen, C. H., Bushuk, A. (1970) Nature of proteins in triticale and its parental species. I. Solubility characteristics and amino acid composition of endosperm proteins. Can. J. Plant Sci. 50, 9–14.CrossRefGoogle Scholar
  8. 8.
    Chichkova, N. V., Shaw, J., Galiullina, R. A., Drury, G. E., Tuzhikov, A. I., Kim, S. H., Kalkum, M., Hong, T. B., Gorshkova, E. N., Torrance, L., Vartapetian, A. B., Taliansky, M. (2010) Phytaspase, a. relocalisable cell death promoting plant protease with caspase specificity. EMBO J. 29, 1149–1161.CrossRefGoogle Scholar
  9. 9.
    Ciepiela, A. P. (1984) Effect of the grain aphid (Sitobion avenae /F./) feeding on accumulation and processing of proteins and amino acids in selected cereal cultivars. Ph.D. Thesis, SGGW-AR, Warsaw, Poland (In Polish).Google Scholar
  10. 10.
    Dinant, S., Bonnemain, J.-L., Girousse, C., Kehr, J. (2010) Phloem sap intricacy and interplay with aphid feeding. Comptes Rend. Biol. 333, 504–515.CrossRefGoogle Scholar
  11. 11.
    Giordanengo, P., Brunissen, L., Rusterucci, C., Vincent, C., van Bel, A., Dinant, S., Giroussee, C. Faucherf M., Bonnemain, J.-L. (2010) Compatible plant-aphid interactions: how aphids manipulate plant responses. Comptes Rend. Biol. 333, 516–523.CrossRefGoogle Scholar
  12. 12.
    Gruis, D., Schulze, J., Jung, R. (2004) Storage protein accumulation in the absence of the vacuolar processing enzyme family of cysteine proteases. Plant Cell 16, 270–290.CrossRefGoogle Scholar
  13. 13.
    Kim, J., Rudella, A., Rodriguez, V. R., Zybailov, B., Olinares, P. D. B., van Wijk, K. J. (2009) Subunits of the plastid ClpPR protease complex have differential contributions to embryogenesis, plastid biogenesis, and plant development in Arabidopsis. Plant Cell 21, 1669–1692.CrossRefGoogle Scholar
  14. 14.
    Lowry, O. H., Rosebrough, N. J., Farr, A. L., Randall, R. J. (1951) Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193, 265–275.Google Scholar
  15. 15.
    Malinowski, R., Higgins, R., Luo, Y., Piper, L., Nazir, A., Bajwa, V. S., Clouse, S. D., Thompson, P. R., Stratmann, J. W. (2009) The tomato brassinosteroid receptor BRI1 increases binding of sys-temin to tobacco plasma membranes, but is not involved in systemin signaling. Plant Mol. Biol. 70, 603–616.CrossRefGoogle Scholar
  16. 16.
    Martinez, D. E., Bartoli, C. G., Grbic, V., Guiamet, J. J. (2007) Vacuolar cysteine proteases of wheat (Triticum aestivum L.) are common to leaf senescence induced by different factors. J. Exp. Bot. 58, 1099–1107.CrossRefGoogle Scholar
  17. 17.
    Matarasso, N., Schuster, S., Avni, A. (2005) A. novel plant cysteine protease has a. dual function as a. regulator of 1-aminocyclopropane-l-carboxylic acid synthase gene expression. Plant Cell 17, 1205–1216.CrossRefGoogle Scholar
  18. 18.
    Medina-Ortega, K. J., Bosque-Perez, N. A., Ngumbi, E., Jimenez-Martinez, E. S., Eigenbrode, S. D. (2009) Rhopalosiphum padi (Hemiptera: Aphididae) responses to volatile cues from barley yellow dwarf virus-infected wheat. Environ. Entomol. 38, 836–845.CrossRefGoogle Scholar
  19. 19.
    Miintz, K., Blattner, F. R., Shutov, A. D. (2002) Legumains: A. family of asparagine-specific cysteine endopeptidases involved in propolypeptide processing and protein breakdown in plants. J. Plant Physiol. 159, 1281–1293.CrossRefGoogle Scholar
  20. 20.
    Pearce, G., Bhattacharya, R., Chen, Y. C., Barona, G., Yamaguchi, Y., Ryan, C. A. (2009) Isolation and characterization of hydroxyproline-rich glycopeptide signals in black nightshade leaves. Plant Physiol. 150, 1422–1433.CrossRefGoogle Scholar
  21. 21.
    Pechan, T., Ye, L., Chang, Y., Mitra, A., Lin, L., Davis, F. M., Williams, W. B., Luthe, D. S. (2000) A. unique 33-kDa cysteine proteinase accumulates in response to larval feeding in maize genotypes resistant to fall armyworm and other Lepidoptera. PlantCell 12, 1031–1040.Google Scholar
  22. 22.
    Pena, L. B., Tomaro, M. L., Gallego, S. M. (2006) Effect of different metals on protease activity in sunflower cotyledons. Electron. J. Biotechnol. 9, 18.Google Scholar
  23. 23.
    Rotari, V. I., He, R., Gallois, P. (2005) Death by proteases in plants: whodunit. Physiol. Plant. 123, 376–385.CrossRefGoogle Scholar
  24. 24.
    Sabelli, P. A., Larkins, B. A. (2009) The development of endosperm in grasses. Plant Physiol. 149, 14–26.CrossRefGoogle Scholar
  25. 25.
    Schmidt, S., Baldwin, I. T. (2009) Down-regulation of systemin after herbivory is associated with increased root allocation and competitive ability in Solarium nigrum. Oecologia 159, 473–482.CrossRefGoogle Scholar
  26. 26.
    Schubert, M. (2006) The chloroplast lumen proteome of Arabidopsis thaliana. Ph.D. Thesis. Karolinska Institute & School of Life Science, Stockholm, Sweden ( Scholar
  27. 27.
    Smith, C. M., Liu, X., Wang, L. J., Liu, X., Chen, M.-S, Starkey, S., Bai, J. (2010) Aphid feeding activates expression of a. transcriptome of oxylipin-based defense signals in wheat involved in resistance to herbivory. J. Chem. Ecol. 36, 260–276.CrossRefGoogle Scholar
  28. 28.
    Song, J., Win, J., Tian, M., Schornack, S., Kaschani, F., Ilyas, M., van der Hoorn, R. A. L., Kamoun, S. (2009) Apoplastic effectors secreted by two unrelated eukaryotic plant pathogens target the tomato defense protease RcrS. PNAS 106, 1654–1659.CrossRefGoogle Scholar
  29. 29.
    Sprawka, I., Ciepiela, A. P., Chrzanowski, G., Stecihska, A. (2005) The activity of selected proteases in winter triticale infested by grain aphid (Sitobion avenae IV.I). Aphids and other Hemipterous Insects 11, 169–174.Google Scholar
  30. 30.
    Sun, X., Ouyang, M., Guo, J., Ma, J., Lu, C., Adam, Z., Zhang, L. (2010) The thylakoid protease Degl is involved in photosystem II assembly in Arabidopsis thaliana. Plant J. 62, 240–249.CrossRefGoogle Scholar
  31. 31.
    Sytykiewicz, H. (2008) Influence of bird cherry-oat aphid feeding on the activity of P-glucosidase in tissues of its primary host. Aphids and other Hemipterous Insects 14, 155–164.Google Scholar
  32. 32.
    Sytykiewicz, H., Lukasik, I., Czerniewicz, P., Chrzanowski, G., Leszczyhski, B. (2009) The participation of glutathione S-transferase in limiting oxidative stress within tissues of primary host of Rhopalosiphum padi L. 4th Conference of Polish Society of Experimental Plant Biology, Krakow September 21–25. Acta Biol. Cracov. Ser Bot. 51(suppl.2), 4.63.Google Scholar
  33. 33.
    Tripathi, S. K., Singh, A. P., Sane, A. P., Nath, P. (2009) Transcriptional activation of a. 37 kDa ethylene responsive cysteine protease gene, RbCPl, is associated with protein degradation during petal abscission in rose. J. Exp. Bot. 60, 2035–2044.CrossRefGoogle Scholar
  34. 34.
    van der Hoorn, R. A. L., Jones, J. D. G. (2004) The plant proteolytic machinery and its role in defence. Curr Opin. Plant Biol. 7, 400–407.CrossRefGoogle Scholar
  35. 35.
    Watanabe, N., Lam, E. (2005) Two Arabidopsis metacaspases AtMCPlb and AtMCP2b are arginine/ lysine-specific cysteine proteases and activate apoptosis-like cell death in yeast. J. Biol. Chem. 280, 14691–14699.CrossRefGoogle Scholar
  36. 36.
    Whitaker, J. R. (1994) Principles of Enzymology for the Food Sciences. New York, USA.Google Scholar
  37. 37.
    Will, T., van Bel, A. J. E. (2006) Physical and chemical interactions between aphids and plants. J. Exp. Bot. 57, 729–737.CrossRefGoogle Scholar
  38. 38.
    Wu, FL, Ji, Y., Du, J., Kong, D., Liang, H., Ling, H.-Q. (2010) ClpCl, an ATP-dependant Clp protease in plastids, is involved in iron homeostasis in Arabidopsis leaves. Ann. Bot. 105, 823–833.CrossRefGoogle Scholar
  39. 39.
    Zhang, FL, Dong, S., Wang, M., Wang, W., Song, W., Dou, X., Zheng, X., Zhang, Z. (2010) The role of vacuolar processing enzyme (VPE) from Nicotiana benthamiana in the elicitor-triggered hypersensitive response and stomatal closure. J. Exp. Bot. (doi:10.1093/jxb/erql89).Google Scholar
  40. 40.
    Zybailov, B., Friso, G., Kim, J., Rudella, A., Rodriguez, V. R., Asakura, Y., Sun, Q., van Wijk, K. J. (2009) Large scale comparative proteomics of a. chloroplast Clp protease mutant reveals folding stress, altered protein homeostasis, and feedback regulation of metabolism. Mol. Cell. Proteomics 8, 1789–1810.CrossRefGoogle Scholar

Copyright information

© Akadémiai Kiadó, Budapest 2011

This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (, which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.

Authors and Affiliations

  • H. Sytykiewicz
    • 1
    Email author
  • P. Czerniewicz
    • 1
  • Iwona Sprawka
    • 1
  • Sylwia Goławska
    • 1
  • G. Chrzanowski
    • 1
  • B. Leszczyński
    • 1
  1. 1.Department of Biochemistry and Molecular BiologySiedlce University of Natural Sciences and HumanitiesSiedlcePoland

Personalised recommendations