Journal of Microbiology and Biotechnology

The Korean Society for Microbiology and Biotechnology (한국미생물·생명공학회)
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In Vitro and In Vivo Anti-Tobacco Mosaic Virus Activities of Essential Oils and Individual Compounds

  • Lu, Min (Aromatic Plant R & D Center, School of Agriculture and Biology, Shanghai Jiao Tong University) ;
  • Han, Zhiqiang (Flavor & Fragrance Research Center, Yunnan Academy of Tobacco Science) ;
  • Xu, Yun (Institute of Agricultural Environment and Resources, Yunnan Academy of Agricultural Sciences) ;
  • Yao, Lei (Aromatic Plant R & D Center, School of Agriculture and Biology, Shanghai Jiao Tong University)
  • Received : 2012.10.29
  • Accepted : 2013.02.06
  • Published : 2013.06.28
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Abstract

Essential oils are increasingly of interest for use as novel drugs acting as antimicrobial and antiviral agents. In the present study, we report the in vitro antiviral activities of 29 essential oils, extracted from Chinese indigenous aromatic plants, against the tobacco mosaic virus (TMV). Of these essential oils, those oils from ginger, lemon, tea tree, tangerine peel, artemisia, and lemongrass effected a more than 50% inhibition of TMV at 100 ${\mu}g/ml$. In addition, the mode of antiviral action of the active essential oils was also determined. Essential oils isolated from artemisia and lemongrass possessed potent inactivation and curative effects in vivo and had a directly passivating effect on TMV infection in a dose-dependent manner. However, all other active essential oils exhibited a moderate protective effect in vivo. The chemical constitutions of the essential oils from ginger, lemon, tea tree, tangerine peel, artemisia, and lemongrass were identified by gas chromatography and gas chromatography-mass spectrometry. The major components of these essential oils were ${\alpha}$-zingiberene (35.21%), limonene (76.25%), terpinen-4-ol (41.20%), limonene (80.95%), 1,8-cineole (27.45%), and terpinolene (10.67%). The curative effects of 10 individual compounds from the active essential oils on TMV infection were also examined in vivo. The compounds from citronellal, limonene, 1,8-cineole, and ${\alpha}$-zingiberene effected a more than 40% inhibition rate for TMV infection, and the other compounds demonstrated moderate activities at 320 ${\mu}g/ml$ in vivo. There results indicate that the essential oils isolated from artemisia and lemongrass, and the individual compound citronellal, have the potential to be used as an effective alternative for the treatment of tobacco plants infected with TMV under greenhouse conditions.

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References

  1. Adams, R. P. 2001. Identificantion of Essential Oil Components by Gas Chromatography/Quadruple Mass Spectroscopy, pp. 9-51. 3th Ed. Allured Publishing Co., Illinois.
  2. Aleksandra, P., S. R. Marina, B. Tijana, and A. Marko. 2009. Antimutagenic effect of sage tea in the wing spot test of Drosophila melanogaster. Food Chem. Toxicol. 47: 180-183. https://doi.org/10.1016/j.fct.2008.10.024
  3. Armaka, M., E. Papanikolaou, A. Sivropoulou, and M. Arsenakis. 1999. Antiviral properties of isoborneol, a potent inhibitor of herpes simplex virus type 1. Antiviral Res. 43: 79-92. https://doi.org/10.1016/S0166-3542(99)00036-4
  4. Astani, A., J. Reichling, and P. Schnitzler. 2009. Screening for antiviral activities of isolated compounds from essential oils. Evid Based Complement. Alternat. Med. 187: 1-8.
  5. Benner, J. P. 1993. Pesticidal compounds from higher plants. Pestic. Sci. 39: 95-102. https://doi.org/10.1002/ps.2780390202
  6. Bishop, C. D. 1995. Antiviral activity of the essential oil of Melaluca alternifolia (Maiden & Betche) cheel (tea tree) against tobacco mosaic virus. J. Essent. Oil Res. 7: 641-644. https://doi.org/10.1080/10412905.1995.9700519
  7. Burt, S. 2004. Essential oils: Their antibacterial properties and potential applications in foods - a review. Int. J. Food Microbiol. 94: 223-253. https://doi.org/10.1016/j.ijfoodmicro.2004.03.022
  8. Chen, J., X. H. Yan, J. H. Dong, P. Sang, X. Fang, Y. T. Di, et al. 2009. Tobacco mosaic virus (TMV) inhibitors from Picrasma quassioides Benn. J. Agric. Food Chem. 57: 6590-6595. https://doi.org/10.1021/jf901632j
  9. Chen, M. H., Z. Chen, B. A. Song, P. S. Bhadury, S. Yang, X. J. Cai, et al. 2009. Synthesis and antiviral activities of chiral thiourea derivatives containing an α-aminophosphonate moiety. J. Agric. Food Chem. 57: 1383-1388. https://doi.org/10.1021/jf803215t
  10. De Logu, A., G. Loy, M. L. Pellerano, L. Bonsignore, and M. L. Schivo. 2000. Inactivation of HSV-1 and HSV-2 and prevention of cell-to-cell virus spread by Santolina insularis essential oil. Antivir. Res. 48: 177-185. https://doi.org/10.1016/S0166-3542(00)00127-3
  11. Garozzo, A., R. Timpanaro, B. Bisignano, P. M. Furneri, G. Bisignano, and A. Castro. 2009. In vitro antiviral activity of Melaleuca alternifolia essential oil. Lett. Appl. Microbiol. 49: 806-808. https://doi.org/10.1111/j.1472-765X.2009.02740.x
  12. Gooding, G. V. J. and T. T. Hebert. 1967. A simple technique for purification of tobacco mosaic virus in large quantities. Phytopathology 57: 1285-1287.
  13. Hayashi, K., N. Imanishi, Y. Kashiwayama, A. Kawano, K. Terasawa, Y. Shimada, and H. Ochiai. 2007. Inhibitory effect of cinnamaldehyde, derived from Cinnamomi cortex, on the growth of influenza A/PR/8 virus in vitro and in vivo. Antivir. Res. 74: 1-8. https://doi.org/10.1016/j.antiviral.2007.01.003
  14. Hedin, P. A., R. M. Hollingworth, E. P. Masler, J. Miyamoto, and D. G. Thompson. 1997. Phytochemicals for Pest Control. American Chemical Society, Washington.
  15. Loizzo, M. R., A. M. Saabb, R. Tundisa, G. A. Stattia, F. Menichinia, I. Lamprontic, et al. 2008. Phytochemical analysis and in vitro antiviral activities of the essential oils of seven Lebanon species. Chem. Biodivers. 5: 461-470. https://doi.org/10.1002/cbdv.200890045
  16. Lukas, B., C. Schimiderer, C. Franz, and J. Noak. 2009. Composition of essential oil compounds from different Syrian populations of Origanum syriacum L. (Lamiaceae). J. Agric. Food Chem. 57: 1362-1365. https://doi.org/10.1021/jf802963h
  17. Murray, B. I. 2000. Plant essential oils for pest and disease management. Crop Prot. 19: 603-608. https://doi.org/10.1016/S0261-2194(00)00079-X
  18. Muthaiyan, A., E. M. Martin, S. Natesan, P. G. Crandall, B. J. Wilkinson, and S. C. Ricke. 2012. Antimicrobial effect and mode of action of terpeneless cold-pressed valencia orange essential oil on methicillin-resistant Staphylococcus aureus. J. Appl. Microbiol. 112: 1020-1033. https://doi.org/10.1111/j.1365-2672.2012.05270.x
  19. Othman, B. A. and S. A. Shoman. 2004. Antiphytoviral activity of the Plectranthus tenuiflorus on some important viruses. Int. J. Agric. Biol. 6: 843-849.
  20. Pajohi, M. R., H. Tajik, A. A. Farshid, and M. Hadian. 2011. Synergistic antibacterial activity of the essential oil of Cuminum cyminum L. seed and nisin in a food model. J. Appl. Microbiol. 110: 943-951. https://doi.org/10.1111/j.1365-2672.2011.04946.x
  21. Pandey, M. P., J. Prasad, and L. P. Awasthi. 1988. Antiviral effect of the essential oils from lemon grass (Cymbopogon flexuosus), mentha (Mentha arvensis) and vetiver (Vetiveria zizanoides), In Purshotam Kaushik (ed.). Indigenous Medicinal Plants Including Microbes and Fungi, 2nd Ed. Today & Tomorrow's printers and Publishers, New Dehli, pp. 55-58.
  22. Pfleger, F. L. and R. J. Zeyen. 2008. Tomato-Tobacco Mosaic Virus Disease. University of Minnesota Extension, Saint Paul.
  23. Pusztai, R., J. Hohmann, D. Rédei, H. Engi, and J. Molnár. 2008. Inhibition of human cytomegalovirus IE gene expression by dihydro-$\beta$-agarofuran sesquiterpenes isolated from Euonymus species. In Vivo 22: 787-792.
  24. Ritzenthaler, C. 2005. Resistance to plant viruses: Old issue, new answer. Curr. Opin. Biotechnol. 16: 118-122. https://doi.org/10.1016/j.copbio.2005.02.009
  25. Sarikurkcua, C., M. S. Ozer, M. Eskici, B. Tepe, S. Can, and E. Mete. 2010. Essential oil composition and antioxidant activity of Thymus longicaulis C. Presl subsp. longicaulis var. longicaulis. Food Chem. Toxicol. 48: 1801-1805. https://doi.org/10.1016/j.fct.2010.04.009
  26. Schnitzler, P., A. Schuhmacher, A. Astani, and J. Reichling. 2008. Melissa officinalis oil affects infectivity of enveloped herpesviruses. Phytomedicine 15: 734-740. https://doi.org/10.1016/j.phymed.2008.04.018
  27. Siddiqui, Y. M., M. Ettayebi, A. M. Haddad, and M. N. AlAhdal. 1996. Effect of essential oils on the enveloped viruses: Antiviral activity of oregano and clove oils on herpes simplex virus type 1 and Newcastle disease virus. Med. Sci. Res. 24: 185-186.
  28. Song, B. A., H. P. Zhang, H. Wang, S. Yang, L. H. Jin, D. Y. Hu, et al. 2005. Synthesis and antiviral activity of novel chiral cyanoacrylate derivatives. J. Agric. Food Chem. 53: 7886-7891. https://doi.org/10.1021/jf051050w
  29. Tian, J., X. Q. Ban, H. Zeng, J. S. He, B. Huang, and Y. W. Wang. 2011. Chemical composition and antifungal activity of essential oil from Cicuta virosa L. var. latisecta Celak. Int. J. Food Microbiol. 145: 464-470. https://doi.org/10.1016/j.ijfoodmicro.2011.01.023
  30. Tolouee, M., S. Alinezhad, R. Saberi, A. Eslamifar, S. J. Zad, K. Jaimand, et al. 2010. Effect of Matricaria chamomilla L. flower essential oil on the growth and ultrastructure of Aspergillus niger van Tieghem. Int. J. Food Microbiol. 139: 127-133. https://doi.org/10.1016/j.ijfoodmicro.2010.03.032
  31. Valerija, D., B. Nada, V. Elma, and C. Dubravka. 2010. Antiphytoviral activity of Satureja montana L. ssp. variegata (Host) P. W. Ball essential oil and phenol compounds on CMV and TMV. Molecules 15: 6713-6721. https://doi.org/10.3390/molecules15106713
  32. Wang, K. L., B. Su, Z. W. Wang, M. Wu, Z. Li, Y. N. Hu, et al. 2010. Synthesis and antiviral activities of phenanthroindolizidine alkaloids and their derivatives. J. Agric. Food Chem. 58: 2703- 2709. https://doi.org/10.1021/jf902543r
  33. Yan, X. H., J. Chen, Y. T. Di, X. Fang, J. H. Dong, S. Pang, et al. 2010. Anti-tobacco mosaic virus (TMV) quassinoids from Brucea javanica (L.) Merr. J. Agric. Food Chem. 58: 1572-1577. https://doi.org/10.1021/jf903434h

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