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Cestrum tomentosum L.f. Extracts against Colletotrichum scovillei by Altering Cell Membrane Permeability and Inducing ROS Accumulation

  • Guogeng Jia (Department of Applied Biology, Chungnam National University) ;
  • Sun Ha Kim (Department of Applied Biology, Chungnam National University) ;
  • Jiyoung Min (Department of Applied Biology, Chungnam National University) ;
  • Nelson Villalobos Zamora (Instituto Nacional de Biodiversidad (INBio)) ;
  • Silvia Soto Montero (Instituto Nacional de Biodiversidad (INBio)) ;
  • Soo-Yong Kim (International Biological Material Research Center, Korea Research Institute of Bioscience & Biotechnology (KRIBB)) ;
  • Sang-Keun Oh (Department of Applied Biology, Chungnam National University)
  • Received : 2024.07.25
  • Accepted : 2024.08.20
  • Published : 2024.10.01

Abstract

Chili pepper anthracnose, caused by Colletotrichum spp., is a significant biotic stress affecting chili fruits globally. While fungicide application is commonly used for disease management due to its efficiency and cost-effectiveness, excessive use poses risks to human health and the environment. Botanical fungicides offer advantages such as rapid degradation and low toxicity to mammals, making them increasingly popular for sustainable plant disease control. This study investigated the antifungal properties of Cestrum tomentosum L.f. crude extracts (CTCE) against Colletotrichum scovillei. The results demonstrated that CTCE effectively inhibited conidia germination and germ tube elongation at 40 ㎍/ml concentrations. Moreover, CTCE exhibited strong antifungal activity against C. scovillei mycelial growth, with an EC50 value of 18.81 ㎍/ml. In vivo experiments confirmed the protective and curative effects of CTCE on chili pepper fruits infected with C. scovillei. XTT analysis showed that the CTCE could significantly inhibit the cell viability of C. scovillei. Mechanistic studies revealed that CTCE disrupted the plasma membrane integrity of C. scovillei and induced the accumulation of reactive oxygen species in hyphal cells. These findings highlight CTCE as a promising eco-friendly botanical fungicide for managing C. scovillei infections in chili peppers.

Keywords

Acknowledgement

This work was supported by Project No. RS-2020-IP120086 of the Institute of Planning and Evaluation for Technology in Food, Agriculture and Forestry (IPET), Republic of Korea. The authors thank to the Comision Nacional para la Gestion de la Biodiversidad (CONAGEBIO) and the conservation area for the permission of the plant collection from the Amistad Pacifico Conservation Area under resolution RCM-INBio-168-2013-OT and RCM-INBio-170-2013-OT.

References

  1. Alengebawy, A., Abdelkhalek, S. T., Qureshi, S. R. and Wang, M.-Q. 2021. Heavy metals and pesticides toxicity in agricultural soil and plants: ecological risks and human health implications. Toxics 9:42.
  2. Ali, A., Bordoh, P. K., Singh, A., Siddiqui, Y. and Droby, S. 2016. Post-harvest development of anthracnose in pepper (Capsicum spp): etiology and management strategies. Crop Prot. 90:132-141.
  3. Bhutia, D. D., Zhimo, Y., Kole, R. and Saha, J. 2016. Antifungal activity of plant extracts against Colletotrichum musae, the post harvest anthracnose pathogen of banana cv. Martaman. Nutr. Food Sci. 46:2-15.
  4. Cannon, P. F., Damm, U., Johnston, P. R. and Weir, B. S. 2012. Colletotrichum: current status and future directions. Stud. Mycol. 73:181-213.
  5. Chang, A. L. and Doering, T. L. 2018. Maintenance of mitochondrial morphology in Cryptococcus neoformans is critical for stress resistance and virulence. mBio 9:e01375-18.
  6. Chechi, A., Stahlecker, J., Dowling, M. E. and Schnabel, G. 2019. Diversity in species composition and fungicide resistance profiles in Colletotrichum isolates from apples. Pestic. Biochem. Physiol. 158:18-24.
  7. Chen, S., Guo, X., Zhang, B., Nie, D., Rao, W., Zhang, D., Lu, J., Guan, X., Chen, Z. and Pan, X. 2023. Mesoporous silica nanoparticles induce intracellular peroxidation damage of Phytophthora infestans: a new type of green fungicide for late blight control. Environ. Sci. Technol. 57:3980-3989.
  8. Chowdhury, M. F. N., Yusop, M. R., Ismail, S. I., Ramlee, S. I., Oladosu, Y., Hosen, M. and Miah, G. 2020. Development of anthracnose disease resistance and heat tolerance chili through conventional breeding and molecular approaches: a review. Biocell 44:269-278.
  9. Damm, U., Cannon, P. F., Woudenberg, J. H. C. and Crous, P. W. 2012. The Colletotrichum acutatum species complex. Stud. Mycol. 73:37-113.
  10. Dean, R., Van Kan, J. A. L., Pretorius, Z. A., Hammond-Kosack, K. E., Di Pietro, A., Spanu, P. D., Rudd, J. J., Dickman, M., Kahmann, R., Ellis, J. and Foster, G. D. 2012. The Top 10 fungal pathogens in molecular plant pathology. Mol. Plant Pathol. 13:414-430.
  11. de Silva, D. D., Groenewald, J. Z., Crous, P. W., Ades, P. K., Nasruddin, A., Mongkolporn, O. and Taylor, P. W. J. 2019. Identification, prevalence and pathogenicity of Colletotrichum species causing anthracnose of Capsicum annuum in Asia. IMA Fungus 10:8.
  12. Fu, T., Shin, J.-H., Lee, N.-H., Lee, K. H. and Kim, K. S. 2022. Mitogen-activated protein kinase CsPMK1 is essential for pepper fruit anthracnose by Colletotrichum scovillei. Front. Microbiol. 13:770119.
  13. Gao, Y., He, L., Li, X., Lin, J., Mu, W. and Liu, F. 2018. Toxicity and biochemical action of the antibiotic fungicide tetramycin on Colletotrichum scovillei. Pestic. Biochem. Physiol. 147:51-58.
  14. Gessler, N. N., Aver'yanov, A. A. and Belozerskaya, T. A. 2007. Reactive oxygen species in regulation of fungal development. Biochemistry (Mosc) 72:1091-1109.
  15. Gurjar, M. S., Ali, S., Akhtar, M. and Singh, K. S. 2012. Efficacy of plant extracts in plant disease management. Agric. Sci. 3:425-433.
  16. Jayawardena, R. S., Hyde, K. D., Damm, U., Cai, L., Liu, M., Li, X. H., Zhang, W., Zhao, W. S. and Yan, J. Y. 2016. Notes on currently accepted species of Colletotrichum. Mycosphere 7:1192-1260.
  17. Khalimi, K., Darmadi, A. A. K. and Suprapta, D. N. 2019. First report on the prevalence of Colletotrichum scovillei associated with anthracnose on chili pepper in Bali, Indonesia. Int. J. Agric. Biol. 22:363-368.
  18. Li, W., Yuan, S., Sun, J., Li, Q., Jiang, W. and Cao, J. 2018. Ethyl p-coumarate exerts antifungal activity in vitro and in vivo against fruit Alternaria alternata via membrane-targeted mechanism. Int. J. Food Microbiol. 278:26-35.
  19. Li, Y., Chang, W., Zhang, M., Li, X., Jiao, Y. and Lou, H. 2015. Diorcinol D exerts fungicidal action against Candida albicans through cytoplasm membrane destruction and ROS accumulation. PLoS ONE 10:e0128693.
  20. Li, Y., Shao, X., Xu, J., Wei, Y., Xu, F. and Wang, H. 2017. Tea tree oil exhibits antifungal activity against Botrytis cinerea by affecting mitochondria. Food Chem. 234:62-67.
  21. Liao, C.-Y., Chen, M.-Y., Chen, Y.-K., Wang, T.-C., Sheu, Z.-M., Kuo, K.-C., Chang, P.-F. L., Chung, K.-R. and Lee, M.-H. 2012. Characterization of three Colletotrichum acutatum isolates from Capsicum spp. Eur. J. Plant Pathol. 133:599-608.
  22. Mongkolporn, O. and Taylor, P. W. J. 2018. Chili anthracnose: Colletotrichum taxonomy and pathogenicity. Plant Pathol. 67:1255-1263.
  23. Olatunji, T. L. and Afolayan, A. J. 2018. The suitability of chili pepper (Capsicum annuum L.) for alleviating human micronutrient dietary deficiencies: a review. Food Sci. Nutr. 6:2239-2251.
  24. Onaran, A. and Yanar, Y. 2016. In vivo and in vitro antifungal activities of five plant extracts against various plant pathogens. Egypt. J. Biol. Pest Control 26:405-411.
  25. Oo, M. M., Lim, G., Jang, H. A. and Oh, S.-K. 2017. Characterization and pathogenicity of new record of anthracnose on various chili varieties caused by Colletotrichum scovillei in Korea. Mycobiology 45:184-191.
  26. Pan, J., Hao, X., Yao, H., Ge, K., Ma, L. and Ma, W. 2019. Ma-trine inhibits mycelia growth of Botryosphaeria dothidea by affecting membrane permeability. J. For. Res. 30:1105-1113.
  27. Reddy, G. K. K. and Nancharaiah, Y. V. 2020. Alkylimidazolium ionic liquids as antifungal alternatives: antibiofilm activity against Candida albicans and underlying mechanism of action. Front. Microbiol. 11:730.
  28. Ridzuan, R., Rafii, M. Y., Ismail, S. I., Mohammad Yusoff, M., Miah, G. and Usman, M. 2018. Breeding for anthracnose disease resistance in chili: progress and prospects. Int. J. Mol. Sci. 19:3122.
  29. Sales, M. D. C., Costa, H. B., Fernandes, P. M. B., Ventura, J. A. and Meira, D. D. 2016. Antifungal activity of plant extracts with potential to control plant pathogens in pineapple. Asian Pac. J. Trop. Biomed. 6:26-31.
  30. Seyedjavadi, S. S., Khani, S., Eslamifar, A., Ajdary, S., Goudarzi, M., Halabian, R., Akbari, R., Zare-Zardini, H., Imani Fooladi, A. A., Amani, J. and Razzaghi-Abyaneh, M. 2019. The antifungal peptide MCh-AMP1 derived from Matricaria chamomilla inhibits Candida albicans growth via inducing ROS generation and altering fungal cell membrane permeability. Front. Microbiol. 10:3150.
  31. Shao, X., Cheng, S., Wang, H., Yu, D. and Mungai, C. 2013. The possible mechanism of antifungal action of tea tree oil on Botrytis cinerea. J. Appl. Microbiol. 114:1642-1649.
  32. Souza, D. P., Pimentel, R. B. Q., Santos, A. S., Albuquerque, P. M., Fernandes, A. V., Junior, S. D., Oliveira, J. T. A., Ramos, M. V., Rathinasabapathi, B. and Goncalves, J. F. C. 2020. Fungicidal properties and insights on the mechanisms of the action of volatile oils from Amazonian Aniba trees. Ind. Crops Prod. 143:111914.
  33. Tian, J., Ban, X., Zeng, H., He, J., Chen, Y. and Wang, Y. 2012. The mechanism of antifungal action of essential oil from dill (Anethum graveolens L.) on Aspergillus flavus. PLoS ONE 7:e30147.
  34. Wang, B., Liu, F., Li, Q., Xu, S., Zhao, X., Xue, P. and Feng, X. 2019. Antifungal activity of zedoary turmeric oil against Phytophthora capsici through damaging cell membrane. Pestic. Biochem. Physiol. 159:59-67.
  35. Xu, Y., Wei, J., Wei, Y., Han, P., Dai, K., Zou, X., Jiang, S., Xu, F., Wang, H., Sun, J. and Shao, X. 2021. Tea tree oil controls brown rot in peaches by damaging the cell membrane of Monilinia fructicola. Postharvest Biol. Technol. 175:11474.
  36. Yan, Y.-F., Yang, C.-J., Shang, X.-F., Zhao, Z.-M., Liu, Y.-Q., Zhou, R., Liu, H., Wu, T.-L., Zhao, W.-B., Wang, Y.-L., Hu, G.-F., Qin, F., He, Y.-H., Li, H.-X. and Du, S.-S. 2020. Bioassay-guided isolation of two antifungal compounds from Magnolia officinalis, and the mechanism of action of honokiol. Pestic. Biochem. Physiol. 170:104705.
  37. Yang, Q., Wang, J., Zhang, P., Xie, S., Yuan, X., Hou, X., Yan, N., Fang, Y. and Du, Y. 2020. In vitro and in vivo antifungal activity and preliminary mechanism of cembratrien-diols against Botrytis cinerea. Ind. Crops Prod. 154:112745.