Export file:


  • RIS(for EndNote,Reference Manager,ProCite)
  • BibTex
  • Text


  • Citation Only
  • Citation and Abstract

Evaluation of eliciting activity of peptidil prolyl cys/trans isomerase from Pseudonomas fluorescens encapsulated in sodium alginate regarding plant resistance to viral and fungal pahogens

1 Department of Molecular Biology, All-Russian Research Institute of Phytopathology, Bolshie Vyazemy, Moscow region, 143050, Russia
2 Department of Potato and Vegetable Diseases, All-Russian Research Institute of Phytopathology, Bolshie Vyazemy, Moscow region, 143050, Russia
3 Federal Research Centre “Fundamentals of Biotechnology” of the Russian Academy of Sciences, Moscow, 119071, Russia

Topical Section: Microbial Enzyme

Use of chemical pesticides poses a threat for environment and human health, so green technologies of crop protection are of high demand. Some microbial proteins able to activate plant defense mechanisms and prevent the development of resistance in plant pathogens, may be good alternative to chemicals, but practical use of such elicitors is limited due to need to protect them against adverse environment prior their delivery to target receptors of plant cells. In this study we examined a possibility to encapsulate heat resistant FKBP-type peptidyl prolyl cis-trans isomerase (PPIase) from Pseudomonas fluorescens, which possesses a significant eliciting activity in relation to a range of plant pathogens, in sodium alginate microparticles and evaluated the stability of resulted complex under long-term UV irradiation and in the presence of proteinase K, as well as its eliciting activity in three different “plant-pathogen” models comparing to that of free PPIase. The obtained PPIase-containing microparticles consisted of 70% of sodium alginate, 20% of bovine serum albumin, and 10% of PPIase. In contrast to free PPIase, which lost its eliciting properties after 8-h UV treatment, encapsulated PPIase kept its eliciting ability unchanged; after being exposed to proteinase K, its eliciting ability twice exceeded that of free PPIase. Using “tobacco-TMV”, “tobacco-Alternaria longipes”, and “wheat-Stagonospora nodorum” model systems, we showed that encapsulation process did not influence on the eliciting activity of PPIase. In the case of the “wheat-S. nodorum” model system, we also observed a significant eliciting activity of alginate-albumin complex and almost doubled activity of encapsulated PPIase as compared to the free PPIase. As far as we know, this is the first observation of a synergistic interaction between alginate and other compound possessing any bioactive properties. The results of the study show some prospects for a PPIase use in agriculture.
  Article Metrics

Keywords FKBP-type peptidyl prolyl cis-trans isomerase; PPIase; sodium alginate; encapsulation; protein elicitors; induced resistance of plants; plant pathogens; tobacco mosaic virus; Alternaria longipes; Stagonospora nodorum

Citation: Sophya B. Popletaeva, Natalia V. Statsyuk, Tatiana M. Voinova, Lenara R. Arslanova, Anton L. Zernov, Anton P. Bonartsev, Garina A. Bonartseva, Vitaly G. Dzhavakhiya. Evaluation of eliciting activity of peptidil prolyl cys/trans isomerase from Pseudonomas fluorescens encapsulated in sodium alginate regarding plant resistance to viral and fungal pahogens. AIMS Microbiology, 2018, 4(1): 192-208. doi: 10.3934/microbiol.2018.1.192


  • 1. Mejía-Teniente L, Torres-Pacheco I, González-Chavira MM, et al. (2010) Use of elicitors as an approach for sustainable agriculture. Afr J Biotechnol 9: 9155–9162.
  • 2. Dodds PN, Rathjen JP (2010) Plant immunity: towards an integrated view of plant-pathogen interactions. Nat Rev Genet 11: 539–548.
  • 3. Wei ZM, Qiu D, Kropp MJ, et al. (1998) Harpin, an HR elicitor, activates both defense and growth systems in many commercially important crops. Phytopathology 88: 96.
  • 4. Djavakhia VG, Nikolaev ON, Voinova TM, et al. (2000) DNA sequence of gene and amino acid sequence of protein from Bacillus thuringiensis, which induces non-specific resistance of plants to viral and fungal diseases. J Russ Phytopathol Soc 1: 1563–3683.
  • 5. Gómez-Gómez L, Boller T (2002) Flagellin perception: a paradigm for innate immunity. Trends Plant Sci 7: 251–256.    
  • 6. Felix G, Boller T (2003) The highly conserved RNA-binding motif RNP-1 of bacterial cold shock proteins is recognized as an elicitor signal in tobacco. J Biol Chem 278: 6201–6208.    
  • 7. Kunze G, Zipfel C, Robatzek S, et al. (2004) The N terminus of bacterial elongation factor Tu elicits innate immunity in Arabidopsis plants. Plant Cell 16: 3496–3507.    
  • 8. Shcherbakova LA, Odintsova TI, Stakheev AA, et al. (2016) Identification of a novel small cysteine-rich protein in the fraction from the biocontrol Fusarium oxysporum strain CS-20 that mitigates fusarium wilt symptoms and triggers defense responses in tomato. Front Plant Sci 6: 1–15.
  • 9. Shumilina D, Krämer R, Klocke E, et al. (2006) MF3 (peptidyl-prolyl cis-trans isomerase of FKBP type from Pseudomonas fluorescens)-an elicitor of non-specific plant resistance against pathogens. Phytopathol Pol 41: 39–49.
  • 10. Shumilina DV, Dzhavakhiya VG (2007) Study of the ability of MF3 protein (FKBP-type peptidyl prolyl cis-trans isomerase) from Pseudomonas fluorescens to improve resistance of tobacco plants to viral and fungal pathogens. Agro XXI 1: 7–9.
  • 11. Shiraishi T, Toyoda K, Yamada T, et al. (2001) Suppressors of defense-supprescins and plant receptor molecules, In: Delivery and perception of pathogen signals in plants, St. Paul, Minnesota: APS Press, 112–117.
  • 12. Tyuterev SL (2015) Economically significant inductors of plant resistance to diseases and physiological stresses. Vestnik Zashchity Rastenii 1: 3–13.
  • 13. Kromina KA, Dzhavakhiya VG (2006) Expression of the bacterial gene CspD in tobacco plants increases their resistance to fungal and viral pathogens. Mol Gen Microbiol Virol 1: 31–34.
  • 14. Thakur M, Sohal BS (2013) Role of elicitors in inducing resistance in plants against pathogen infection: a review. ISRN Biochem 2013: 762412.
  • 15. Park HY, Park HC, Yoon MY (2009) Screening for peptides binding on Phytophthora capsici extracts by phage display. J Microbiol Meth 78: 54–58.    
  • 16. Abriouel H, Franz CMAP, Omar NB, et al. (2011) Diversity and applications of Bacillus bacteriocins. FEMS Microbiol Rev 35: 201–232.    
  • 17. Karpachev V, Voropaeva N, Tkachev A, et al. (2015) Innovative application technology for challenging inducers of disease resistance in spring rape in (nano)chips. Int Lett Chem Phys Astron 42: 36–44.
  • 18. Neves-Petersen MT, Gajula GP, Petersen SB (2012) UV light effects on proteins: from photochemistry to nanomedicine, In: Satyen Saha, Editor, Molecular Photochemistry-Various Aspects, Rijeka: InTechOpen, 125–161.
  • 19. Keefe AJ, Jiang S (2011) Poly(zwitterionic)protein conjugates offer increased stability without sacrificing binding affinity or bioactivity. Nat Chem 4: 59–63.
  • 20. Roberts MJ, Bentley MD, Harris JM (2012) Chemistry for peptide and protein PEGylation. Adv Drug Deliver Rev 64: 116–127.    
  • 21. Liechty WB, Kryscio DR, Slaughter BV, et al. (2010) Polymers for drug delivery systems. Annu Rev Chem Biomol 1: 149–173.    
  • 22. Ulery BD, Nair LS, Laurencin CT (2011) Biomedical applications of biodegradable polymers. J Polym Sci Pol Phys 49: 832–864.
  • 23. Naeem M, Aftab T, Ansari AA, et al. (2015) Radiolytically degraded sodium alginate enhances plant growth, physiological activities and alkaloids production in Catharanthus roseus L. J Radiat Res Appl Sci 8: 606–616.    
  • 24. Xu A, Zhan JC, Huang WD (2015) Oligochitosan and sodium alginate enhance stilbene production and induce defense responses in Vitis vinifera cell suspension cultures. Acta Physiol Plant 37: 144.    
  • 25. Pestovskiy YS (2013) Generatrion of nanomeric protein aggregates by tyramide enhancement. Vserossiiskii Zhurnal Nauchnyh Publikatsii-Khimicheskie Nauki 18: 1–6.
  • 26. Bashan LE, Moreno M, Hernandez J, et al. (2002) Removal of ammonium and phosphorus ions from synthetic wastewater by the microalgae Chlorella vulgaris coimmobilized in alginate beads with the microalgae growth-promoting bacterium Azospirillum brasilense. Water Res 36: 2941–2948.    
  • 27. Paredes-Juarez GL, de Haan B, Faas MM, et al. (2014) A technology platform to test the efficacy of purification of alginate. Materials 7: 2087–2103.    
  • 28. Gopi S, Amalraj A, Thomas S (2016) Effective drug delivery system of biopolymers based on nanomaterials and hydrogels-a review. Drug Des 5: 129.
  • 29. Schoebitz M, López M, Roldán A (2013) Bioencapsulation of microbial inoculants for better soil-plant fertilization. A review. Agron Sustain Dev 33: 751–765.    
  • 30. Vinceković M, Jalšenjak N, Topolovec-Pintarić S, et al. (2016) Encapsulation of biological and chemical agents for plant nutrition and protection: chitosan/alginate microcapsules loaded with copper cations and Trichoderma viride. J Agr Food Chem 64: 8073–8083.    
  • 31. Dzhavakhia V, Filipov A, Skryabin K, et al. (2005) Proteins inducing multiple resistance of plants to phytopathogens and pests. International Patent Application WO2005/061533.
  • 32. Dzhavakhiya VG, Voinova TM, Shumilina DV (2016) Search for the active center pf peptidyl-prolyl cys/trans isomerase from Pseudomonas fuorescens responsible for the induction of tobacco (Nicotiana tabacum L.) plant resistance to tobacco mosaic virus. Sel'skokhozyaistvennaya Biologiya 51: 392–400.
  • 33. Jay SM, Shepherd BR, Bertram JP, et al. (2008) Engineering of multifunctional gels integrating highly efficient growth factor delivery with endothelial cell transplantation. FASEB J 22: 2949–2956.    
  • 34. Sijmons PC, Dekker BM, Schrammeijer B, et al. (1990) Production of correctly processed human serum albumin in transgenic plants. Nat Biotechnol 8: 217–221.    
  • 35. Pyzhikova GV, Sanina AA, Suprun LM, et al. (1989) Methods for evaluation of resistance of breeding material to Septoria-caused diseases. Moscow: VNIIF.
  • 36. Richer DL (1987) Synergism: a patent view. Pest Manag Sci 19: 309–315.    
  • 37. Goh CH, Heng PWS, Chan LW (2012) Alginates as a useful natural polymer for microencapsulation and therapeutic applications. Carbohyd Polym 88: 1–12.    
  • 38. Gombotz WR, Wee SF (2012) Protein release from alginate matrices. Adv Drug Deliver Rev 64: 194–205.    
  • 39. González A, Castro J, Vera J, et al. (2013) Seaweed oligosaccharides stimulate plant growth by enhancing carbon and nitrogen assimilation, basal metabolism, and cell division. J Plant Growth Reg 32: 443.    
  • 40. Laporte D, Vera J, Chandia NP, et al. (2007) Structurally unrelated algal oligosaccharides differentially stimulate growth and defense against tobacco mosaic virus in tobacco plants. J Appl Phycol 19: 79–88.    
  • 41. Zhang L, Zhang X, Zhang I, et al. (2016) A new formulation of Bacillus thuringiensis: UV protection and sustained release mosquito larvae studies. Sci Rep 6: 39425.    
  • 42. Khorramvatan S, Marzban R, Ardjmand M, et al. (2017) Optimising microencapsulated formulation stability of Bacillus thuringiensis subsp. kurstaki (Bt-KD2) against ultraviolet condition using response surface methodology. Arch Phytopathol Plant Protect 50: 275–285.
  • 43. Coppi G, Iannuccelli V, Leo E, et al. (2002) Protein immobilization in crosslinked alginate microparticles. J Microencapsul 19: 37–44.    
  • 44. Gagné-Bourque F, Xu M, Dumont MJ, et al. (2015) Pea protein alginate encapsulated Bacillus subtilis B26, a plant biostimulant, provides controlled release and increased storage survival. J Fertil Pestic 6: 157–165.


Reader Comments

your name: *   your email: *  

© 2018 the Author(s), licensee AIMS Press. This is an open access article distributed under the terms of the Creative Commons Attribution Licese (http://creativecommons.org/licenses/by/4.0)

Download full text in PDF

Export Citation

Copyright © AIMS Press All Rights Reserved