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p-Anisaldehyde Exerts Its Antifungal Activity Against Penicillium digitatum and Penicillium italicum by Disrupting the Cell Wall Integrity and Membrane Permeability

  • Che, Jinxin (School of Chemical Engineering, Xiangtan University) ;
  • Chen, Xiumei (School of Chemical Engineering, Xiangtan University) ;
  • Ouyang, Qiuli (School of Chemical Engineering, Xiangtan University) ;
  • Tao, Nengguo (School of Chemical Engineering, Xiangtan University)
  • Received : 2019.11.15
  • Accepted : 2020.03.06
  • Published : 2020.06.28

Abstract

Penicillium digitatum and P. italicum are the two important postharvest pathogens in citrus, causing about 90% of the total loss of citrus fruit during storage and transportation. Natural fungicides such as essential oils have been widely used instead of chemical fungicides for preventing and controlling postharvest diseases. In this research, p-anisaldehyde exhibited a strong inhibitory effect on P. digitatum and P. italicum, with the minimum inhibitory concentration and minimum fungicidal concentration values of both being 2.00 μl/ml. Additionally, p-anisaldehyde visibly inhibited both the green mold and blue mold development of citrus fruits inoculated with P. digitatum and P. italicum. The mycelia morphologies of these pathogens were greatly altered, and the membrane permeability and cell wall integrity of mycelia were severely disrupted under p-anisaldehyde treatment. These results suggest that the antifungal activity of p-anisaldehyde against P. digitatum and P. italicum can be attributed to the disruption of the cell wall integrity.

References

  1. Papoutsis K, Mathioudakis MM, Hasperue JH, Ziogas V. 2019. Non-chemical treatments for preventing the postharvest fungal rotting of citrus caused by Penicillium digitatum (green mold) and Penicillium italicum (blue mold). Trends Food Sci. Technol. 86: 479-491. https://doi.org/10.1016/j.tifs.2019.02.053
  2. Droby S, Eick A, Macarisin D, Cohen L, Rafael G, Stange R, et al. 2008. Role of citrus volatiles in host recognition, germination and growth of Penicillium digitatum and Penicillium italicum. Postharvest Biol. Technol. 49: 386-396. https://doi.org/10.1016/j.postharvbio.2008.01.016
  3. Zhu C, Lei M, Andargie M, Zeng J, Li J. 2019. Antifungal activity and mechanism of action of tannic acid against Penicillium digitatum. Physiol. Mol. Plant Pathol. 107: 46-50. https://doi.org/10.1016/j.pmpp.2019.04.009
  4. Li L, Tang X, Ouyang Q, Tao N. 2019. Combination of sodium dehydroacetate and sodium silicate reduces sour rot of citrus fruit. Postharvest Biol. Technol. 151: 19-25. https://doi.org/10.1016/j.postharvbio.2019.01.006
  5. Macarisin D, Cohen L, Eick A, Rafael G, Belausov E, Wisniewski M, et al. 2007. Penicillium digitatum suppresses production of hydrogen peroxide in host tissue during infection of citrus fruit. Phytopathology 97: 1491-1500. https://doi.org/10.1094/PHYTO-97-11-1491
  6. Berk Z. 2016. Chapter 6 - Postharvest changes. Citrus Fruit Processing.
  7. Hao W, Hui L, Hu M, Liu Y, Rizwan-Ul-Haq M. 2011. Integrated control of citrus green and blue mold and sour rot by Bacillus amyloliquefaciens in combination with tea saponin. Postharvest Biol. Technol. 59: 316-323. https://doi.org/10.1016/j.postharvbio.2010.10.002
  8. Sancheztorres, Paloma, Tuset, Juan J. 2011. Molecular insights into fungicide resistance in sensitive and resistant Penicillium digitatum strains infecting citrus. Postharvest Biol.Technol. 59: 159-165. https://doi.org/10.1016/j.postharvbio.2010.08.017
  9. Simas DLR, de Amorim SHBM, Goulart FRV, Alviano CS, Alviano DS, da Silva AJR. 2017. Citrus species essential oils and their components can inhibit or stimulate fungal growth in fruit. Ind. Crops Prod. 98: 108-115. https://doi.org/10.1016/j.indcrop.2017.01.026
  10. Chen CY, Cai N, Chen JY, Wan CP. 2019. Clove essential oil as an alternative approach to control postharvest blue mold caused by Penicillium italicum in Citrus Fruit. Biomolecules 9: 197. https://doi.org/10.3390/biom9050197
  11. Zhang J, Wu H, Jiang D, Yang Y, Tang W, Xu K. 2019. The antifungal activity of essential oil from Melaleuca leucadendra (L.) L. grown in China and its synergistic effects with conventional antibiotics against Candida. Nat. Prod. Res. 33: 2545-2548. https://doi.org/10.1080/14786419.2018.1448979
  12. Shreaz S, Bhatia R, Khan N, Muralidhar S, Basir SF, Manzoor N, et al. 2011. Exposure of Candida to p-anisaldehyde inhibits its growth and ergosterol biosynthesis. J. Gen. Appl. Microbiol. 57: 129-136. https://doi.org/10.2323/jgam.57.129
  13. Showler AT, Harlien JL. 2019. Lethal and repellent effects of the botanical p-anisaldehyde on Musca domestica (Diptera: Muscidae). J. Econ. Entomol. 112: 485-493. https://doi.org/10.1093/jee/toy351
  14. Chen X, Zhang X, Meng R, Zhao Z, Liu Z, Zhao X, et al. 2016. Efficacy of a combination of nisin and p-anisaldehyde against Listeria monocytogenes. Food Control 66: 100-106. https://doi.org/10.1016/j.foodcont.2016.01.025
  15. Shi C, Zhao X, Meng R, Liu Z, Zhang G, Guo N. 2017. Synergistic antimicrobial effects of nisin and p-anisaldehyde on Staphylococcus aureus in pasteurized milk. Lwt-Food Sci. Technol. 84: 222-230. https://doi.org/10.1016/j.lwt.2017.05.056
  16. Yu L, Guo N, Yang Y, Wu X, Meng R, Fan J, et al. 2010. Microarray analysis of p-anisaldehyde-induced transcriptome of Saccharomyces cerevisiae. J. Ind. Microbiol. Biotechnol. 37: 313-322. https://doi.org/10.1007/s10295-009-0676-y
  17. Tao N, Fan F, Jia L, Zhang M. 2014. Octanal incorporated in postharvest wax of Satsuma mandarin fruit as a botanical fungicide against Penicillium digitatum. Food Control 45: 56-61. https://doi.org/10.1016/j.foodcont.2014.04.025
  18. Dou S, Ouyang Q, You K, Qian J, Tao N. 2018. An inclusion complex of thymol into beta-cyclodextrin and its antifungal activity against Geotrichum citri-aurantii. Postharvest Biol. Technol. 138: 31-36. https://doi.org/10.1016/j.postharvbio.2017.12.011
  19. Liu J, Zong YY, Qin GZ, Li BQ, Tian SP. 2010. Plasma membrane damage contributes to antifungal activity of silicon against Penicillium digitatum. Curr. Microbiol. 61: 274-279. https://doi.org/10.1007/s00284-010-9607-4
  20. Talibi I, Askarne L, Boubaker H, Boudyach EH, Msanda F, Saadi B, et al. 2012. Antifungal activity of Moroccan medicinal plants against citrus sour rot agent Geotrichum candidum. Lett. Appl. Microbiol. 55: 155-161. https://doi.org/10.1111/j.1472-765X.2012.03273.x
  21. Shao X, Cheng S, Wang H, Yu D, Mungai C. 2013. The possible mechanism of antifungal action of tea tree oil on Botrytis cinerea. J. Appl. Microbiol. 114: 1642-1649. https://doi.org/10.1111/jam.12193
  22. Regnier T, Combrinck S, Veldman W, Du Plooy W. 2014. Application of essential oils as multi-target fungicides for the control of Geotrichum citri-aurantii and other postharvest pathogens of citrus. Ind. Crops Prod. 61: 151-159. https://doi.org/10.1016/j.indcrop.2014.05.052
  23. Neri F, Mari M, Brigati S, Bertolini P. 2009. Control of Neofabraea alba by plant volatile compounds and hot water. Postharvest Biol. Technol. 51: 425-430. https://doi.org/10.1016/j.postharvbio.2008.08.006
  24. Sharopov F, Valiev A, Satyal P, Gulmurodov I, Yusufi S, Setzer WN, et al. 2017. Cytotoxicity of the essential oil of fennel (Foeniculum vulgare) from Tajikistan. Foods 6: 73. https://doi.org/10.3390/foods6090073
  25. Shao X, Cao B, Xu F, Xie S, Yu D, Wang H. 2015. Effect of postharvest application of chitosan combined with clove oil against citrus green mold. Postharvest Biol. Technol. 99: 37-43. https://doi.org/10.1016/j.postharvbio.2014.07.014
  26. Liu K, Zhou X, Fu M. 2017. Inhibiting effects of epsilon-poly-lysine ($\varepsilon$-PL) on Pencillium digitatum and its involved mechanism. Postharvest Biol. Technol. 123: 94-101. https://doi.org/10.1016/j.postharvbio.2016.08.015
  27. Kang J, Liu L, Wu X, Sun Y, Liu Z. 2018. Effect of thyme essential oil against Bacillus cereus planktonic growth and biofilm formation. Appl.Microbiol. Biotechnol. 102: 10209-10218. https://doi.org/10.1007/s00253-018-9401-y
  28. da Rocha Neto AC, Navarro BB, Canton L, Maraschin M, Di Piero RM. 2019. Antifungal activity of palmarosa (Cymbopogon martinii), tea tree (Melaleuca alternifolia) and star anise (Illicium verum) essential oils against Penicillium expansum and their mechanisms of action. Lwt-Food Sci. Technol. 105: 385-392. https://doi.org/10.1016/j.lwt.2019.02.060
  29. Yang S, Liu L, Li D, Xia H, Su X, Peng L, et al. 2016. Use of active extracts of poplar buds against Penicillium italicum and possible modes of action. Food Chem. 196: 610-618. https://doi.org/10.1016/j.foodchem.2015.09.101
  30. Lengeler KB, Wasserstrom L, Walther A, Wendland J. 2013. Analysis of the cell wall integrity pathway of Ashbya gossypii. Microbiol. Res. 168: 607-614. https://doi.org/10.1016/j.micres.2013.06.008
  31. Arokiyaraj S, Bharanidharan R, Agastian P, Shin H. 2018. Chemical composition, antioxidant activity and antibacterial mechanism of action from Marsilea minuta leaf hexane: methanol extract. Chem. Cent. J. 12: 105. https://doi.org/10.1186/s13065-018-0476-4
  32. Sun X, Zhou T, Wei C, Lan W, Zhao Y, Pan Y, et al. 2018. Antibacterial effect and mechanism of anthocyanin rich Chinese wild blueberry extract on various foodborne pathogens. Food Control 94: 155-161. https://doi.org/10.1016/j.foodcont.2018.07.012
  33. OuYang QL, Duan XF, Li L, Tao NG. 2019. Cinnamaldehyde exerts its antifungal activity by disrupting the cell wall integrity of Geotrichum citri-aurantii. Front.Microbiol. 10: 9. https://doi.org/10.3389/fmicb.2019.00009