Skip to main content

Study on Antiviral Activity of Two Recombinant Antimicrobial Peptides Against Tobacco Mosaic Virus

Probiotics and Antimicrobial Proteins volume 11, pages 1370–1378 (2019)Cite this article

Abstract

Antimicrobial peptides (AMPs) are generally small peptides with less than 50 amino acid residues, which have been considered as the first line of defense system in plants and animals. These small cationic peptides belong to a family of antimicrobials that are multifunctional effectors of innate immunity. The direct antimicrobial activity of AMPs against different bacteria, viruses, fungi, and parasites has been confirmed in different studies. In this study, the antiviral activity of two recombinant AMPs named thanatin and lactoferricin+lactoferrampin was evaluated against Tobacco mosaic virus (TMV) using half-leaf and leaf disk methods under in vivo and in vitro condition, respectively. The obtained result indicated that both recombinant AMPs have shown an antiviral activity against TMV. Compared to the chimeric lactoferricin+lactoferrampin, recombinant thanatin showed a higher rate of antiviral activity against TMV. Three types of effects, including protective, curative, and inactivation, were evaluated during an antiviral activity test. In the present study, the antiviral activity of two recombinant AMPs is represented for the first time: thanatin and chimeric lactoferricin+lactoferrampin against TMV as a viral plant pathogen.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

43,34 €

Price includes VAT (Finland)
Tax calculation will be finalised during checkout.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  1. Agrios GN (2005) Plant pathology, 5th edn. Academic Press, San Diego

    Google Scholar 

  2. Hadidi A, Khetarpal RK, Koganezawa H (1998) Plant virus disease control. APS Press, Minnesota

    Google Scholar 

  3. Fan H, Song B, Bhadury PS, Jin L, Hu D, Yang S (2011) Antiviral activity and mechanism of action of novel thiourea containing chiral phosphonate on tobacco mosaic virus. Int J Mol Sci 12:4522–4535. https://doi.org/10.3390/ijms12074522

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  4. Ritzenthaler C (2005) Resistance to plant viruses: old issue, news answers? Curr Opin Biotechnol 16:118–122. https://doi.org/10.1016/j.copbio.2005.02.009

    CAS  Article  PubMed  Google Scholar 

  5. Scholthof KBG (2004) Tobacco mosaic virus: a model system for plant biology. Annu Rev Phytopathol 42:13–34. https://doi.org/10.1146/annurev.phyto.42.040803.140322

    CAS  Article  PubMed  Google Scholar 

  6. Montesinos E (2007) Antimicrobial peptides and plant disease control. FEMS Microbiol Lett 270:1–11. https://doi.org/10.1111/j.1574-6968.2007.00683.x

    CAS  Article  PubMed  Google Scholar 

  7. Jung YJ, Kang KK (2014) Application of antimicrobial peptides for disease control in plants. Plant Breed Biotech 2:1–13. https://doi.org/10.9787/PBB.2014.2.1.001

    Article  Google Scholar 

  8. Sinha S, Zheng L, Mu Y, Ng WJ, Bhattacharjya S (2017) Structure and interactions of a host defense antimicrobial peptide thanatin in lipopolysaccharide micelles reveal mechanism of bacterial cell agglutination. Sci Rep 7:17795. https://doi.org/10.1038/s41598-017-18102-6

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  9. Mamarabadi M, Tanhaeian A, Ramezany Y (2018) Antifungal activity of recombinant thanatin in comparison with two plant extracts and a chemical mixture to control fungal plant pathogens. AMB Express 8(1):180. https://doi.org/10.1186/s13568-018-0710-4

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  10. Pagès JM, Dimarcq JL, Quenin S, Hetru C (2003) Thanatin activity on multidrug resistant clinical isolates of Enterobacter aerogenes and Klebsiella pneumoniae. Int J Antimicrob Agents 22:265–269. https://doi.org/10.1016/S0924-8579(03)00201-2

    CAS  Article  PubMed  Google Scholar 

  11. Schubert M, Houdelet M, Kogel KH, Fischer R, Schillberg S, Nölke G (2015) Thanatin confers partial resistance against aflatoxigenic fungi in maize (Zea mays). Transgenic Res 24:885–895. https://doi.org/10.1007/s11248-015-9888-2

    CAS  Article  PubMed  Google Scholar 

  12. Fehlbaum P, Bulet P, Chernysh S, Briand JP, Roussel JP, Letellier L, Hetru C, Hoffmann JA (1996) Structure-activity analysis of thanatin, a 21-residue inducible insect defense peptide with sequence homology to frog skin antimicrobial peptides. Proc Natl Acad Sci 93:1221–1225. https://doi.org/10.1073/pnas.93.3.1221

    CAS  Article  PubMed  Google Scholar 

  13. Koch A, Khalifa W, Langen G, Vilcinskas A, Kogel K, Imani J (2012) The antimicrobial peptide thanatin reduces fungal infections in Arabidopsis. J Phytopathol 160:606–610. https://doi.org/10.1111/j.1439-0434.2012.01946.x

    CAS  Article  Google Scholar 

  14. Khan JA, Kumar P, Paramasivam M, Yadav RS, Sahani MS, Sharma S, Srinivasan A, Singh TP (2001) Camel lactoferrin, a transferrin-cum-lactoferrin: crystal structure of camel apolactoferrin at 2.6 Å resolution and structural basis of its dual role. J Mol Biol 309:751–761. https://doi.org/10.1006/jmbi.2001.4692

    CAS  Article  PubMed  Google Scholar 

  15. Baker EN, Baker HM, Kidd RD (2002) Lactoferrin and transferrin: functional variations on a common structural framework. Biochem Cell Biol 80:27–34. https://doi.org/10.1139/o01-153

    CAS  Article  PubMed  Google Scholar 

  16. Duran A, Ibrahim Kahve H (2017) The use of lactoferrin in food industry. Acad J Sci 07:89–94

    Google Scholar 

  17. Tanhaieian A, Sekhavati MH, Ahmadi FS, Mamarabadi M (2018) Heterologous expression of a broad-spectrum chimeric antimicrobial peptide in Lactococcus lactis: its safety and molecular modeling evaluation. Microb Pathog 1-8:51–59. https://doi.org/10.1016/j.micpath.2018.09.016

    CAS  Article  Google Scholar 

  18. Abdelbacki AM, Taha SH, Sitohy MZ, Dawood AIA, Abd-El Hamid MM, Rezk AA (2010) Inhibition of tomato yellow leaf curl virus (TYLCV) using whey proteins. Virol J 7:26–31. https://doi.org/10.1186/1743-422X-7-26

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  19. Wang J, Zhu YK, Wang HY, Zhang H, Wang KY (2012) Inhibitory effects of esterified whey protein fractions by inducing chemical defense against tobacco mosaic virus (TMV) in tobacco seedlings. Ind Crop Prod 37:207–212. https://doi.org/10.1016/j.indcrop.2011.11.023

    CAS  Article  Google Scholar 

  20. Wang J, Wang HY, Xia XM, Li PP, Wang KY (2013) Inhibitory effect of esterified lactoferin and lactoferin against tobacco mosaic virus (TMV) in tobacco seedlings. Pestic Biochem Physiol 105:62–68. https://doi.org/10.1016/j.pestbp.2012.11.009

    CAS  Article  PubMed  Google Scholar 

  21. Taha SH, Mokbel SA, Abdel-Hamid M, Hamed AH (2015) Antiviral activity of lactoferrin against potato virus X in vitro and in vivo. Science 10:86–94. https://doi.org/10.3923/ijds.2015.86.94

    CAS  Article  Google Scholar 

  22. Sinha M, Kaushik S, Kaur P, Sharma S, Singh TP (2013) Antimicrobial lactoferrin peptides: the hidden players in the protective function of a multifunctional protein. Int J Pept 2013:1–12. https://doi.org/10.1155/2013/390230

    CAS  Article  Google Scholar 

  23. Bolscher JG, Adao R, Nazmi K, van den Keybus PA, van’t Hof W, Amerongen AVN, Bastos M Veerman EC (2009) Bactericidal activity of LF chimera is stronger and less sensitive to ionic strength than its constituent lactoferricin and lactoferrampin peptides. Biochimie 91:123–132. https://doi.org/10.1016/j.biochi.2008.05.019

    CAS  Article  PubMed  Google Scholar 

  24. Tang XS, Tang ZR, Wang SP, Feng ZM, Zhou D, Li TJ, Yin YL (2012) Expression, purification, and antibacterial activity of bovine lactoferrampin–lactoferricin in Pichia pastoris. Appl Biochem Biotechnol 166:640–651. https://doi.org/10.1007/s12010-011-9455-0

    CAS  Article  PubMed  Google Scholar 

  25. Tanhaeian A, Ahmadi FS, Sekhavati MH, Mamarabadi M (2018) Expression and purification of the main component contained in camel milk and its antimicrobial activities against bacterial plant pathogens. Probiotics Antimicro 10:1–7. https://doi.org/10.1007/s12602-018-9416-9

    CAS  Article  Google Scholar 

  26. Schägger H, Aquila H, Von Jagow G (1988) Coomassie blue-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for direct visualization of polypeptides during electrophoresis. Anal Biochem 173:201–205. https://doi.org/10.1016/0003-2697(88)90179-0

    Article  PubMed  Google Scholar 

  27. Kim YS, Hwang EI, O JH, Kim KS, Ryu MH, Yeo WH (2004) Inhibitory effects of Acinetobacter sp. KTB3 on infection of tobacco mosaic. Plant Pathol J 20:293–296. https://doi.org/10.5423/PPJ.2004.20.4.293

    Article  Google Scholar 

  28. Zhao L, Hao X, Wu Y (2015) Inhibitory effect of polysaccharide peptide (PSP) against tobacco mosaic virus (TMV). Int J Biol Macromol 75:474–478. https://doi.org/10.1016/j.ijbiomac.2015.01.058

    CAS  Article  PubMed  Google Scholar 

  29. Ball EM (1990) Agar double diffusion, plates (Ouchterlony): viruses. In: Hampton R, Ball E, DeBoer S (eds) Serological methods for detection and identification of viral and bacterial plant pathogens, a laboratory manual. APS Press, Minnesota, pp 111–120

    Google Scholar 

  30. SAS S (2002) 9.1 for Windows. SAS Institute Inc, Cary, North Carolina

    Google Scholar 

  31. Shah DM (1997) Genetic engineering for fungal and bacterial diseases. Curr Opin Biotechnol 8:208–214. https://doi.org/10.1016/S0958-1669(97)80104-8

    CAS  Article  PubMed  Google Scholar 

  32. Mourgues F, Brisset MN, Chevreau E (1998) Strategies to improve plant resistance to bacterial diseases through genetic engineering. Trends Biotechnol 16:203–210. https://doi.org/10.1016/S0167-7799(98)01189-5

    CAS  Article  PubMed  Google Scholar 

  33. Donini M, Lico C, Baschieri S, Conti S, Magliani W, Polonelli L, Benvenuto E (2005) Production of an engineered killer peptide in Nicotiana benthamiana by using a potato virus X expression system. Appl Environ Microbiol 71:6360–6367. https://doi.org/10.1128/AEM.71.10.6360-6367.2005

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  34. Palumbo JC, Horowitz AR, Prabhaker N (2001) Insecticidal control and resistance management for Bemisia tabaci. Crop Prot 20:739–765. https://doi.org/10.1016/S0261-2194(01)00117-X

    CAS  Article  Google Scholar 

  35. Navot N, Pichersky E, Zeidan M, Zamir D, Czosnek H (1991) Tomato yellow leaf curl virus: a whitefly-transmitted geminivirus with a single genomic component. Virology 185:151–161. https://doi.org/10.1016/0042-6822(91)90763-2

    CAS  Article  PubMed  Google Scholar 

  36. Cahill M, Gorman K, Day S, Denholm I, Elbert A, Nauen R (1996) Baseline determination and detection of resistance to imidacloprid in Bemisia tabaci (Homoptera: Aleyrodidae). Bull Entomol Res 86:343–349. https://doi.org/10.1017/S000748530003491X

    CAS  Article  Google Scholar 

  37. Elbert A, Nauen R (2000) Resistance of Bemisia tabaci (Homoptera: Aleyrodidae) to insecticides in southern Spain with special reference to neonicotinoids. Pest Manag Sci 56:60–64. https://doi.org/10.1002/(SICI)1526-4998(200001)56:1<60::AID-PS88>3.0.CO;2-K

    CAS  Article  Google Scholar 

  38. Li H, Ding X, Wang C, Ke H, Wu Z, Wang Y, Liu H, Guo J (2016) Control of tomato yellow leaf curl virus disease by Enterobacter asburiae BQ9 as a result of priming plant resistance in tomatoes. Turk J Biol 40:150–159. https://doi.org/10.3906/biy-1502-12

    CAS  Article  Google Scholar 

  39. Brogden KA (2005) Antimicrobial peptides: pore formers or metabolic inhibitors in bacteria? Nat Rev Microbiol 3:238–250. https://doi.org/10.1038/nrmicro1098

    CAS  Article  PubMed  Google Scholar 

  40. Park SC, Park Y, Hahm KS (2011) The role of antimicrobial peptides in preventing multidrug-resistant bacterial infections and biofilm formation. Int J Mol Sci 12:5971–5992. https://doi.org/10.3390/ijms12095971

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  41. Wakabayashi H, Hiratani T, Uchida K, Yamaguchi H (1996) Antifungal spectrum and fungicidal mechanism of an N-terminal peptide of bovine lactoferrin. J Infect Chemother 1:185–189. https://doi.org/10.1007/BF02350646

    CAS  Article  PubMed  Google Scholar 

  42. Yamauchi K, Tomita M, Giehl TJ, Ellison RT (1993) Antibacterial activity of lactoferrin and a pepsin-derived lactoferrin peptide fragment. Infect Immun 61:719–728

    CAS  Article  Google Scholar 

  43. Mygind PH, Fischer RL, Schnorr KM, Hansen MT, Sönksen CP, Ludvigsen S, Raventós D, Buskov S, Christensen B, De Maria L, Taboureau O (2005) Plectasin is a peptide antibiotic with therapeutic potential from a saprophytic fungus. Nature 437:975–980. https://doi.org/10.1038/nature04051

    CAS  Article  PubMed  Google Scholar 

  44. Marcos JF, Beachy RN, Houghten RA, Blondelle SE, Perez-Paya E (1995) Inhibition of a plant virus infection by analogs of melittin. Proc Natl Acad Sci U S A 92:12466–12469. https://doi.org/10.1073/pnas.92.26.12466

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  45. Baghian A, Jaynes J, Enright F, Kousoulas KG (1997) An amphipathic α-helical synthetic peptide analogue of melittin inhibits herpes simplex virus-1 (HSV-1)-induced cell fusion and virus spread. Peptides 18:177–183. https://doi.org/10.1016/S0196-9781(96)00290-2

    CAS  Article  PubMed  Google Scholar 

  46. Wachinger M, Kleinschmidt A, Winder D, von Pechmann N, Ludvigsen A, Neumann M, Holle R, Salmons B, Erfle V, Brack-Werner R (1998) Antimicrobial peptides melittin and cecropin inhibit replication of human immunodeficiency virus 1 by suppressing viral gene expression. J Gen Virol 79:731–740. https://doi.org/10.1099/0022-1317-79-4-731

    CAS  Article  PubMed  Google Scholar 

  47. Park JY, Yang SY, Kim YC, Kim JC, Le Dang Q, Kim JJ, Kim IS (2012) Antiviral peptide from Pseudomonas chlororaphis O6 against tobacco mosaic virus (TMV). J Korean Soc Appl Biol Chem 55:89–94. https://doi.org/10.1007/s13765-012-0015-2

    CAS  Article  Google Scholar 

  48. Whitham S, Dinesh-Kumar SP, Choi D, Hehl R, Corr C, Baker B (1994) The product of the tobacco mosaic virus resistance gene N: similarity to toll and the interleukin-1 receptor. Cell 78:1101–1115. https://doi.org/10.1016/0092-8674(94)90283-6

    CAS  Article  PubMed  Google Scholar 

  49. Mestre P, Baulcombe DC (2006) Elicitor-mediated oligomerization of the tobacco N disease resistance protein. Plant Cell 18:491–501. https://doi.org/10.1105/tpc.105.037234

    CAS  Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

We thank Dr. Mojtaba Hosseini for his helpful discussion during statistical analysis.

Funding

This study was funded by the Deputy of Research and Technology, Ferdowsi University of Mashhad, Mashhad, Iran (Grant No. 43239).

Author information

Affiliations

  1. Department of Plant Protection, Faculty of Agriculture, Ferdowsi University of Mashhad, Mashhad, Iran

    Mohammad Ali Sabokkhiz

  2. Department of Biotechnology and Plant Breeding, Faculty of Agriculture, Ferdowsi University of Mashhad, Mashhad, Iran

    Abbas Tanhaeian

  3. Department of Plant Protection, Faculty of Agriculture, Ferdowsi University of Mashhad, Mashhad, Iran

    Mojtaba Mamarabadi

Authors
  1. Mohammad Ali Sabokkhiz
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Abbas Tanhaeian
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mojtaba Mamarabadi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Mojtaba Mamarabadi.

Ethics declarations

Conflict of Interest

Mohammad Ali Sabokkhiz declares that he has no conflict of interest. Abbas Tanhaeian declares that he has no conflict of interest. Mojtaba Mamarabadi declares that he has no conflict of interest.

Ethical Approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Informed Consent

For this type of study, formal consent is not required.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

ESM 1

(DOCX 192 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Sabokkhiz, M.A., Tanhaeian, A. & Mamarabadi, M. Study on Antiviral Activity of Two Recombinant Antimicrobial Peptides Against Tobacco Mosaic Virus. Probiotics & Antimicro. Prot. 11, 1370–1378 (2019). https://doi.org/10.1007/s12602-019-09539-4

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12602-019-09539-4

Keywords

  • Thanatin
  • Lactoferricin
  • Lactoferrampin
  • TMV
  • Plant viruses
  • Disease control