The Plant Pathology Journal

The Korean Society of Plant Pathology (한국식물병리학회)
권호 표지
DOI QR코드

DOI QR Code

Antifungal Effect of Chitosan as Ca2+ Channel Blocker

  • Lee, Choon Geun (Department of Life Science, College of BioNano, Gachon University) ;
  • Koo, Ja Choon (Division of Science Education and Institute of Fusion Science, Chonbuk National University) ;
  • Park, Jae Kweon (Department of Life Science, College of BioNano, Gachon University)
  • Received : 2015.08.17
  • Accepted : 2016.02.15
  • Published : 2016.06.01
Download PDF
⟨ Previous Next ⟩

Abstract

The aim of this study was to investigate antifungal activity of a range of different molecular weight (MW) chitosan against Penicillium italicum. Our results demonstrate that the antifungal activity was dependent both the MW and concentration of the chitosan. Among a series of chitosan derived from the hydrolysis of high MW chitosan, the fractions containing various sizes of chitosan ranging from 3 to 15 glucosamine units named as chitooligomers-F2 (CO-F2) was found to show the highest antifungal activity against P. italicum. Furthermore, the effect of CO-F2 toward this fungus was significantly reduced in the presence of $Ca^{2+}$, whereas its effect was recovered by ethylenediaminetetraacetic acid, suggesting that the CO-F2 acts via disruption of $Ca^{2+}$ gradient required for survival of the fungus. Our results suggest that CO-F2 may serve as potential compounds to develop alternatives to synthetic fungicides for the control of the postharvest diseases.

Keywords

References

  1. Al-Samarrai, G., Singh, H. and Syarhabil, M. 2012. Evaluating eco-friendly botanicals (natural plant extracts) as alternatives to synthetic fungicides. Ann. Agric. Environ. Med. 19:673-676.
  2. Badawy, M. E., Rabea, E. I., Steurbaut, W., Rogge, T. M., Stevens, C. V., Smagghe, G. and Hofte, M. 2004. Insecticidal and fungicidal activity of new N,O-acyl Chitosan derivatives. Commun. Agric. Appl. Biol. Sci. 69:793-797.
  3. Badawy, M. E., Rabea, E. I., Steurbaut, W., Rogge, T. M., Stevens, C. V., Smagghe, G. and Hofte, M. 2005. Fungicidal activity of some O-acyl chitosan derivatives against grey mould Botrytis cinerea and rice leaf blast Pyricularia grisea. Commun. Agric. Appl. Biol. Sci. 70:215-218.
  4. Bencina, M., Legisa, M. and Read, N. D. 2005. Cross-talk between cAMP and calcium signalling in Aspergillus niger. Mol. Microbiol. 56:268-281. https://doi.org/10.1111/j.1365-2958.2005.04541.x
  5. Bhaskara Reddy, M. V., Arul, J., Angers, P. and Couture, L. 1999. Chitosan treatment of wheat seeds induces resistance to Fusarium graminearum and improves seed quality. J. Agric. Food Chem. 47:1208-1216. https://doi.org/10.1021/jf981225k
  6. Brand, A., Lee, K., Veses, V. and Gow, N. A. 2009. Calcium homeostasis is required for contact-dependent helical and sinusoidal tip growth in Candida albicans hyphae. Mol. Microbiol. 71:1155-1164. https://doi.org/10.1111/j.1365-2958.2008.06592.x
  7. Brand, A., Shanks, S., Duncan, V. M., Yang, M., Mackenzie, K. and Gow, N. A. 2007. Hyphal orientation of Candida albicans is regulated by a calcium-dependent mechanism. Curr. Biol. 17:347-352.
  8. Chafer, M., Sanchez-Gonzalez, L., Gonzalez-Martinez, C. and Chiralt, A. 2012. Fungal decay and shelf life of oranges coated with chitosan and bergamot, thyme, and tea tree essential oils. J. Food Sci. 77:E182-E187. https://doi.org/10.1111/j.1750-3841.2012.02827.x
  9. Cohen, E. 1993. Chitin synthesis and degradation as targets for pesticide action. Arch. Insect. Biochem. Physiol. 22:245-261. https://doi.org/10.1002/arch.940220118
  10. Fisichella, M., Dabboue, H., Bhattacharyya, S., Saboungi, M. L., Salvetat, J. P., Hevor, T. and Guerin, M. 2009. Mesoporous silica nanoparticles enhance MTT formazan exocytosis in HeLa cells and astrocytes. Toxicol. In Vitro 23:697-703. https://doi.org/10.1016/j.tiv.2009.02.007
  11. Hadwiger, L. A. 2013. Multiple effects of chitosan on plant systems:solid science or hype. Plant Sci. 208:42-49. https://doi.org/10.1016/j.plantsci.2013.03.007
  12. Jackson, S. L. and Heath, I. B. 1993. Roles of calcium ions in hyphal tip growth. Microbiol. Rev. 57:367-382.
  13. Kaya, M., Akata, I., Baran, T. and Mentes, A. 2015a. Physicochemical properties of chitin and chitosan produced from medicinal fungus (Fomitopsis pinicola). Food Biophys. 10:162-168. https://doi.org/10.1007/s11483-014-9378-8
  14. Kaya, M., Mujtaba, M., Bulut, E., Akyuz, B., Zelencova, L. and Sofi, K. 2015b. Fluctuation in physicochemical properties of chitins extracted from different body parts of honeybee. Carbohydr. Polym. 132:9-16. https://doi.org/10.1016/j.carbpol.2015.06.008
  15. Kendra, D. F. and Hadwiger, L. A. 1984. Characterization of the smallest chitosan oligomer that is maximally antifungal to Fusarium solani and elicits pisatin formation in Pisum sativum. Exp. Mycol. 8:276-281. https://doi.org/10.1016/0147-5975(84)90013-6
  16. Koo, J. C., Lee, S. Y., Chun, H. J., Cheong, Y. H., Choi, J. S., Kawabata, S., Miyagi, M., Tsunasawa, S., Ha, K. S., Bae, D. W., Han, C. D., Lee, B. L. and Cho, M. J. 1998. Two hevein homologs isolated from the seed of Pharbitis nil L. exhibit potent antifungal activity. Biochim. Biophys. Acta 1382:80-90. https://doi.org/10.1016/S0167-4838(97)00148-9
  17. LaFayette, S. L., Collins, C., Zaas, A. K., Schell, W. A., Betancourt-Quiroz, M., Gunatilaka, A. A., Perfect, J. R. and Cowen, L. E. 2010. PKC signaling regulates drug resistance of the fungal pathogen Candida albicans via circuitry comprised of Mkc1, calcineurin, and Hsp90. PLoS Pathog. 6:e1001069. https://doi.org/10.1371/journal.ppat.1001069
  18. Lahlali, R., Serrhini, M. N. and Jijakli, M. H. 2005. Development of a biological control method against postharvest diseases of citrus fruits. Commun. Agric. Appl. Biol. Sci. 70:47-58.
  19. Levin, D. E., Fields, F. O., Kunisawa, R., Bishop, J. M. and Thorner, J. 1990. A candidate protein kinase C gene, PKC1, is required for the S. cerevisiae cell cycle. Cell 62:213-224. https://doi.org/10.1016/0092-8674(90)90360-Q
  20. Levina, N. N., Lew, R. R., Hyde, G. J. and Heath, I. B. 1995. The roles of $Ca^{2+}$ and plasma membrane ion channels in hyphal tip growth of Neurospora crassa. J. Cell Sci. 108:3405-3417.
  21. Lu, L., Liu, Y., Yang, J., Azat, R., Yu, T. and Zheng, X. 2014. Quaternary chitosan oligomers enhance resistance and biocontrol efficacy of Rhodosporidium paludigenum to green mold in satsuma orange. Carbohydr. Polym. 113:174-181. https://doi.org/10.1016/j.carbpol.2014.06.077
  22. Mazur, S. and Waksmundzka, A. 2001. Effect of some compounds on the decay of strawberry fruits caused by Botrytis cinerea Pers. Meded. Rijksuniv. Gent. Fak. Landbouwkd. Toegep. Biol. Wet. 66:227-231.
  23. Miller, A. J., Vogg, G. and Sanders, D. 1990. Cytosolic calcium homeostasis in fungi: roles of plasma membrane transport and intracellular sequestration of calcium. Proc. Natl. Acad. Sci. U. S. A. 87:9348-9352. https://doi.org/10.1073/pnas.87.23.9348
  24. Munoz, Z. and Moret, A. 2010. Sensitivity of Botrytis cinerea to chitosan and acibenzolar-S-methyl. Pest. Manag. Sci. 66:974-979. https://doi.org/10.1002/ps.1969
  25. Ngamwongsatit, P., Banada, P. P., Panbangred, W. and Bhunia, A. K. 2008. WST-1-based cell cytotoxicity assay as a substitute for MTT-based assay for rapid detection of toxigenic Bacillus species using CHO cell line. J. Microbiol. Methods 73:211-215. https://doi.org/10.1016/j.mimet.2008.03.002
  26. Olicon-Hernandez, D. R., Hernandez-Lauzardo, A. N., Pardo, J. P., Pena, A., Velazquez-del Valle, M. G. and Guerra-Sanchez, G. 2015. Influence of chitosan and its derivatives on cell development and physiology of Ustilago maydis. Int. J. Biol. Macromol. 79:654-660. https://doi.org/10.1016/j.ijbiomac.2015.05.057
  27. Ortelli, D., Edder, P. and Corvi, C. 2005. Pesticide residues survey in citrus fruits. Food Addit. Contam. 22:423-428. https://doi.org/10.1080/02652030500089903
  28. Palma-Guerrero, J., Lopez-Jimenez, J. A., Perez-Berna, A. J., Huang, I. C., Jansson, H. B., Salinas, J., Villalain, J., Read, N. D. and Lopez-Llorca, L. V. 2010. Membrane fluidity determines sensitivity of filamentous fungi to chitosan. Mol. Microbiol. 75:1021-1032. https://doi.org/10.1111/j.1365-2958.2009.07039.x
  29. Rabea, E. I., El Badawy, M., Rogge, T. M., Stevens, C. V., Steurbaut, W., Hofte, M. and Smagghe, G. 2006. Enhancement of fungicidal and insecticidal activity by reductive alkylation of chitosan. Pest. Manag. Sci. 62:890-897. https://doi.org/10.1002/ps.1263
  30. Robles-Martinez, L., Guerra-Sanchez, M. G., Hernandez-Lauzardo, A. N., Pardo, J. P. and Velazquez-del Valle, M. G. 2014. Effects of chitosan and oligochitosan on development and mitochondrial function of Rhizopus stolonifer. J. Basic. Microbiol. 54 Suppl 1:S42-S49. https://doi.org/10.1002/jobm.201300790
  31. Silverman-Gavrila, L. B. and Lew, R. R. 2001. Regulation of the tip-high [$Ca^{2+}$] gradient in growing hyphae of the fungus Neurospora crassa. Eur. J. Cell Biol. 80:379-390. https://doi.org/10.1078/0171-9335-00175
  32. Sun, X., Wang, J., Feng, D., Ma, Z. and Li, H. 2011. PdCYP51B, a new putative sterol $14{\alpha}$-demethylase gene of Penicillium digitatum involved in resistance to imazalil and other fungicides inhibiting ergosterol synthesis. Appl. Microbiol. Biotechnol. 91:1107-1119. https://doi.org/10.1007/s00253-011-3355-7
  33. Tayel, A. A., Moussa, S., el-Tras, W. F., Knittel, D., Opwis, K. and Schollmeyer, E. 2010. Anticandidal action of fungal chitosan against Candida albicans. Int. J. Biol. Macromol. 47:454-457. https://doi.org/10.1016/j.ijbiomac.2010.06.011
  34. Tayel, A. A., Moussa, S. H., Salem, M. F., Mazrou, K. E. and El-Tras, W. F. 2016. Control of citrus molds using bioactive coatings incorporated with fungal chitosan/plant extracts composite. J. Sci. Food Agric. 96:1306-1312. https://doi.org/10.1002/jsfa.7223
  35. Tsyhankova, V. A., Andrusevych, I. V., Biliavs'ka, L. O., Kozyryts'ka, V. I., Iutyns'ka, H. O., Halkin, A. P., Halahan, T. O. and Boltovs'ka, O. V. 2012. Growth stimulating, fungicidal and nematicidal properties of new microbial substances and their impact on si/miRNA synthesis in plant cells. Mikrobiol. Z. 74:36-45.
  36. Vitalini, S., Ruggiero, A., Rapparini, F., Neri, L., Tonni, M. and Iriti, M. 2014. The application of chitosan and benzothiadiazole in vineyard (Vitis vinifera L. cv Groppello Gentile) changes the aromatic profile and sensory attributes of wine. Food Chem. 162:192-205. https://doi.org/10.1016/j.foodchem.2014.04.040
  37. Wojdyla, A. T. 2004. Chitosan (biochikol 020 PC) in the control of some ornamental foliage diseases. Commun. Agric. Appl. Biol. Sci. 69:705-715.
  38. Yoshioka, N., Akiyama, Y. and Teranishi, K. 2004. Rapid simultaneous determination of o-phenylphenol, diphenyl, thiabendazole, imazalil and its major metabolite in citrus fruits by liquid chromatography-mass spectrometry using atmospheric pressure photoionization. J. Chromatogr. A 1022:145-150. https://doi.org/10.1016/j.chroma.2003.09.021
  39. Younes, I., Sellimi, S., Rinaudo, M., Jellouli, K. and Nasri, M. 2014. Influence of acetylation degree and molecular weight of homogeneous chitosans on antibacterial and antifungal activities. Int. J. Food Microbiol. 185:57-63. https://doi.org/10.1016/j.ijfoodmicro.2014.04.029
  40. Zahid, N., Ali, A., Manickam, S., Siddiqui, Y. and Maqbool, M. 2012. Potential of chitosan-loaded nanoemulsions to control different Colletotrichum spp. and maintain quality of tropical fruits during cold storage. J. Appl. Microbiol. 113:925-939. https://doi.org/10.1111/j.1365-2672.2012.05398.x
  41. Zhang, H., Li, R. and Liu, W. 2011. Effects of chitin and its derivative chitosan on postharvest decay of fruits: a review. Int. J. Mol. Sci. 12:917-934. https://doi.org/10.3390/ijms12020917

Cited by

  1. Synergistic antimicrobial properties of active molecular chitosan with EDTA-divalent metal ion compounds vol.165, pp.10, 2017, https://doi.org/10.1111/jph.12603