The Plant Pathology Journal

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

DOI QR Code

Antifungal Activity of Green and Chemically Synthesized ZnO Nanoparticles against Alternaria citri, the Causal Agent Citrus Black Rot

  • Hazem S. Elshafie (School of Agricultural, Forestry, Food and Environmental Sciences, University of Basilicata) ;
  • Ali Osman (Biochemistry Department, Faculty of Agriculture, Zagazig University) ;
  • Mahmoud M El-Saber (Biochemistry Unit, Genetic Resources Department, Desert Research Center) ;
  • Ippolito Camele (School of Agricultural, Forestry, Food and Environmental Sciences, University of Basilicata) ;
  • Entsar Abbas (Plant Pathology Department, Faculty of Agriculture, Zagazig University)
  • 투고 : 2023.03.02
  • 심사 : 2023.05.02
  • 발행 : 2023.06.01
PDF 다운로드
⟨ 이전 논문 다음 논문 ⟩

초록

Citrus black rot is a serious disease of citrus plants caused by Alternaria citri. The current study aimed to synthesize zinc oxide nanoparticles (ZnO-NPs) by chemically or green method and investigate their antifungal activity against A. citri. The sizes of synthesized as measured by transmission electron microscope of ZnO-NPs were 88 and 65 nm for chemical and green methods, respectively. The studied prepared ZnO-NPs were applied, in vitro and in situ, at different concentrations (500, 1,000, and 2,000 ㎍/ml) in post-harvest treatment on navel orange fruits to verify the possible control effect against A. citri. Results of in vitro assay demonstrated that, at concentration 2,000 ㎍/ml, the green ZnO-NPs was able to inhibit about 61% of the fungal growth followed by 52% of chemical ZnO-NPs. In addition, scanning electron microscopy of A. citri treated in vitro with green ZnO-NPs showed swelling and deformation of conidia. Results showed also that, using a chemically and green ZnO-NPs at 2,000 ㎍/ml in situ in post-harvest treatment of orange, artificially-infected with A. citri, has reduced the disease severity to 6.92% and 9.23%, respectively, compared to 23.84% of positive control (non-treated fruits) after 20 days of storage. The out findings of this study may contribute to the development of a natural, effective, and eco-friendly strategy for eradicating harmful phytopathogenic fungi.

키워드

과제정보

This research was funded by the project entitled "Fighting plant fungi post-harvest using environmentally friendly bio products', financially supported by the Science and Technology Development Fund (STDF), Egypt. Grant type/name: Research Support. Project ID: 43673.

참고문헌

  1. Abbas, E., Osman, A. and Sitohy, M. 2020. Biochemical control of Alternaria tenuissima infecting post-harvest fig fruit by chickpea vicilin. J. Sci. Food Agric. 100:2889-2897. https://doi.org/10.1002/jsfa.10314
  2. Abd-Ellatif, S., Ibrahim, A. A., Safhi, F. A., Abdel Razik, E. S., Kabeil, S. S. A., Aloufi, S., Alyamani, A. A., Basuoni, M. M., ALshamrani, S. M. and Elshafie, H. S. 2022. Green synthesized of Thymus vulgaris chitosan nanoparticles induce relative WRKY-genes expression in Solanum lycopersicum against Fusarium solani, the causal agent of root rot disease. Plants 11:3129.
  3. Abdull Razis, A. F., Ibrahim, M. D. and Kntayya, S. B. 2014. Health benefits of Moringa oleifera. Asian Pac. J. Cancer Prev. 15:8571-8576. https://doi.org/10.7314/APJCP.2014.15.20.8571
  4. Altschul, S. F., Madden, T. L., Schaffer, A. A., Zhang, J., Zhang, Z., Miller, W. and Lipman, D. J. 1997. Gapped BLAST and PSIBLAST: a new generation of protein database search programs. Nucleic Acids Res. 25:3389-3402. https://doi.org/10.1093/nar/25.17.3389
  5. Arora, A. K., Devi, S., Jaswal, V. S., Singh, J., Kinger, M. and Gupta, V. D. 2014. Synthesis and characterization of ZnO nanoparticles. Orient. J. Chem. 30:1671-1679. https://doi.org/10.13005/ojc/300427
  6. Bobo, D., Robinson, K. J., Islam, J., Thurecht, K. J. and Corrie, S. R. 2016. Nanoparticle-based medicines: a review of FDA-approved materials and clinical trials to date. Pharm. Res. 33:2373-2387. https://doi.org/10.1007/s11095-016-1958-5
  7. Camele, I., Marcone, C. and Cristinzio, G. 2005. Detection and identification of Phytophthora species in southern Italy by RFLP and sequence analysis of PCR-amplified nuclear ribosomal DNA. Eur. J. Plant Pathol. 113:1-14. https://doi.org/10.1007/s10658-005-8915-1
  8. Canaparo, R., Foglietta, F., Limongi, T. and Serpe, L. 2020. Biomedical applications of reactive oxygen species generation by metal nanoparticles. Materials 14:53.
  9. Cheng, Y., Lin, Y., Cao, H. and Li, Z. 2020. Citrus postharvest green mold: recent advances in fungal pathogenicity and fruit resistance. Microorganisms 8:449.
  10. Das, K., Tiwari, R. K. S. and Shrivastava, D. K. 2010. Techniques for evaluation of medicinal plant products as antimicrobial agent: current methods and future trends. J. Med. Plants Res. 4:104-111.
  11. El-Saber, M. M. 2021. Effect of biosynthesized Zn and Se nanoparticles on the productivity and active constituents of garlic subjected to saline stress. Egypt. J. Desert Res. 71:99-128. https://doi.org/10.21608/ejdr.2021.81793.1085
  12. Elshafie, H. S., Camele, I., Sofo, A., Mazzone, G., Caivano, M., Masi, S. and Caniani, D. 2020a. Mycoremediation effect of Trichoderma harzianum strain T22 combined with ozonation in diesel-contaminated sand. Chemosphere 252:126597.
  13. Elshafie, H. S., Caputo, L., De Martino, L., Grulova, D., Zheljazkov, V. Z., De Feo, V. and Camele, I. 2020b. Biological investigations of essential oils extracted from three Juniperus species and evaluation of their antimicrobial, antioxidant and cytotoxic activities. J. Appl. Microbiol. 129:1261-1271. https://doi.org/10.1111/jam.14723
  14. Elshafie, H. S., Caputo, L., De Martino, L., Sakr, S. H., De Feo, V. and Camele, I. 2021. Study of bio-pharmaceutical and antimicrobial properties of pomegranate (Punica granatum L.) leathery exocarp extract. Plants 10:153.
  15. Elshafie, H. S., Sakr, S., Bufo, S. A. and Camele, I. 2017a. An attempt of biocontrol the tomato-wilt disease caused by Verticillium dahliae using Burkholderia gladioli pv. agaricicola and its bioactive secondary metabolites. Int. J. Plant Biol. 8:7263.
  16. Elshafie, H. S., Viggiani, L., Mostafa, M. S., El-Hashash, M. A., Camele, I. and Bufo, S. A. 2017b. Biological activity and chemical identification of ornithine lipid produced by Burkholderia gladioli pv. agaricicola ICMP 11096 using LC-MS and NMR analyses. J. Biol. Res. 90:6534.
  17. Espitia, P. J. P., Soares, N. F. F., Coimbra, J. S. R., de Andrade, N. J., Cruz, R. S. and Medeiros, E. A. A. 2012. Zinc oxide nanoparticles: synthesis, antimicrobial activity and food packaging applications. Food Bioprocess Technol. 5:1447-1464. https://doi.org/10.1007/s11947-012-0797-6
  18. FAOSTAT. 2018. Statistical databases, fisheries data, 2001. Food and Agriculture Organization of the United Nations, Rome, Italy. URL https://www.fao.org/ [2 March 2023].
  19. Garganese, F., Sanzani, S. M., Di Rella, D., Schena, L. and Ippolito, A. 2019. Pre- and postharvest application of alternative means to control Alternaria Brown spot of citrus. Crop Prot. 121:73-79. https://doi.org/10.1016/j.cropro.2019.03.014
  20. Gold, K., Slay, B., Knackstedt, M. and Gaharwar, A. K. 2018. Antimicrobial activity of metal and metal-oxide based nanoparticles. Adv. Ther. 1:1700033.
  21. Isshiki, A., Akimitsu, K., Yamamoto, M. and Yamamoto, H. 2001. Endopolygalacturonase is essential for citrus black rot caused by Alternaria citri but not brown spot caused by Alternaria alternata. Mol. Plant-Microbe Interact. 14:749-757. https://doi.org/10.1094/MPMI.2001.14.6.749
  22. Katoh, H., Isshiki, A., Masunaka, A., Yamamoto, H. and Akimitsu, K. 2006. A virulence-reducing mutation in the postharvest citrus pathogen Alternaria citri. Phytopathology 96:934-940. https://doi.org/10.1094/PHYTO-96-0934
  23. Khan, I., Saeed, K. and Khan, I. 2019. Nanoparticles: properties, applications and toxicities. Arab. J. Chem. 12:908-931. https://doi.org/10.1016/j.arabjc.2017.05.011
  24. Khorram, F. and Ramezanian, A. 2021. Cinnamon essential oil incorporated in shellac, a novel bio-product to maintain quality of 'Thomson navel' orange fruit. J. Food Sci. Technol. 58:2963-2972. https://doi.org/10.1007/s13197-020-04798-4
  25. Marcous, A., Rasouli, S. and Ardestani, F. 2017. Low-density polyethylene films loaded by titanium dioxide and zinc oxide nanoparticles as a new active packaging system against Escherichia coli O157:H7 in fresh calf minced meat. Packag. Technol. Sci. 30:693-701. https://doi.org/10.1002/pts.2312
  26. Meruvu, S., Hugendubler, L. and Mueller, E. 2011. Regulation of adipocyte differentiation by the zinc finger protein ZNF638. J. Biol. Chem. 286:26516-26523. https://doi.org/10.1074/jbc.M110.212506
  27. Nicolopoulou-Stamati, P., Maipas, S., Kotampasi, C., Stamatis, P. and Hens, L. 2016. Chemical pesticides and human health: the urgent need for a new concept in agriculture. Front. Public Health 4:148.
  28. Nisar, P., Ali, N., Rahman, L., Ali, M. and Shinwari, Z. K. 2019. Antimicrobial activities of biologically synthesized metal nanoparticles: an insight into the mechanism of action. J. Biol. Inorg. Chem. 24:929-941. https://doi.org/10.1007/s00775-019-01717-7
  29. O'Rourke, T. A., Scanlon, T. T., Ryan, M. H., Wade, L. J., McKay, A. C., Riley, I. T., Li, H., Sivasithamparam, K. and Barbetti, M. J. 2009. Severity of root rot in mature subterranean clover and associated fungal pathogens in the wheatbelt of Western Australia. Crop Pasture Sci. 60:43-50. https://doi.org/10.1071/CP08187
  30. Pal, S., Mondal, S., Maity, J. and Mukherjee, R. 2018. Synthesis and characterization of ZnO nanoparticles using Moringa oleifera leaf extract: investigation of photocatalytic and antibacterial activity. Int. J. Nanosci. Nanotechnol. 14:111-119.
  31. Peever, T. L., Su, G., Carpenter-Boggs, L. and Timmer, L. W. 2004. Molecular systematics of citrus-associated Alternaria species. Mycologia 96:119-134. https://doi.org/10.1080/15572536.2005.11833002
  32. Piccirillo, G., Carrieri, R., Polizzi, G., Azzaro, A., Lahoz, E., Fernandez-Ortuno, D. and Vitale, A. 2018. In vitro and in vivo activity of QoI fungicides against Colletotrichum gloeosporioides causing fruit anthracnose in Citrus sinensis. Sci. Hortic. 236:90-95. https://doi.org/10.1016/j.scienta.2018.03.044
  33. Pillai, A. M., Sivasankarapillai, V. S., Rahdar, A., Joseph, J., Sadeghfar, F., Anuf, A. R., Rajesh, K. and Kyzas, G. Z. 2020. Green synthesis and characterization of zinc oxide nanoparticles with antibacterial and antifungal activity. J. Mol. Struct. 1211:128107.
  34. Ruffo Roberto, S., Youssef, K., Hashim, A. F. and Ippolito, A. 2019. Nanomaterials as alternative control means against postharvest diseases in fruit crops. Nanomaterials 9:1752.
  35. Sadowsky, A., Kimchi, M., Oren, Y. and Solel, Z. 2002. Occurrence and management of Alternaria brown spot in Israel. Phytoparasitica 30:19.
  36. Sanchez-Torres, P. and Tuset, J. 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
  37. Sardar, M., Ahmed, W., Al Ayoubi, S., Nisa, S., Bibi, Y., Sabir, M., Khan, M. M., Ahmed, W. and Qayyum, A. 2022. Fungicidal synergistic effect of biogenically synthesized zinc oxide and copper oxide nanoparticles against Alternaria citri causing citrus black rot disease. Saudi J. Biol. Sci. 29:88-95. https://doi.org/10.1016/j.sjbs.2021.08.067
  38. Sharma, D., Rajput, J., Kaith, B. S., Kaur, M. and Sharma, S. 2010. Synthesis of ZnO nanoparticles and study of their antibacterial and antifungal properties. Thin Solid Films 519:1224-1229. https://doi.org/10.1016/j.tsf.2010.08.073
  39. Shyla, K. K., Natarajan, N. and Nakkeeran, S. 2014. Antifungal activity of zinc oxide, silver and titanium dioxide nanoparticles against Macrophomina phaseolina. J. Mycol. Plant Pathol. 44:268-273.
  40. Sitohy, M., Mahgoub, S., Osman, A., El-Masry, R. and Al-Gaby, A. 2013. Extent and mode of action of cationic legume proteins against Listeria monocytogenes and Salmonella enteritidis. Probiotics Antimicrob. Proteins 5:195-205. https://doi.org/10.1007/s12602-013-9134-2
  41. Stanic, V. and Tanaskovic, S. B. 2020. Antibacterial activity of metal oxide nanoparticles. In: Nanotoxicity: prevention and antibacterial applications of nanomaterials, eds. by S. Rajendran, A. Mukherjee, T. A. Nguyen, C. Godugu, R. K. Shukla, pp. 241-274. Elsevier, Amsterdam, The Netherlands.
  42. Strano, M. C., Altieri, G., Allegra, M., Di Renzo, G. C., Paterna, G., Matera, A. and Genovese, F. 2022. Postharvest technologies of fresh citrus fruit: advances and recent developments for the loss reduction during handling and storage. Horticulturae 8:612.
  43. Talibi, I., Boubaker, H., Boudyach, E. H. and Ait Ben Aoumar, A. 2014. Alternative methods for the control of postharvest citrus diseases. J. Appl. Microbiol. 117:1-17. https://doi.org/10.1111/jam.12495
  44. Umer, M., Mubeen, M., Ateeq, M., Shad, M. A., Atiq, M. N., Kaleem, M. M., Iqbal, S., Shaikh, A. A., Ullah, I., Khan, M., Kalhoro, A. A. and Abbas A. 2021. Etiology, epidemiology and management of citrus black rot caused by Alternaria citri: an outlook. Plant Prot. 5:105-115. https://doi.org/10.33804/pp.005.02.3701
  45. Vitale, A., Aiello, D., Azzaro, A., Guarnaccia, V. and Polizzi, G. 2021. An eleven-year survey on field disease susceptibility of citrus accessions to Colletotrichum and Alternaria species. Agriculture 11:536.
  46. White, T. J., Bruns, T., Lee, S. and Taylor, J. 1990. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: PCR protocols: a guide to methods and applications, eds. by M. A. Innis, D. H. Gelfand, J. J. Sninsky, T. J. White, pp. 315-322. Academic Press, New York, NY, USA.
  47. Yang, L.-N., He, M.-H., Ouyang, H.-B., Zhu, W., Pan, Z.-C., Sui, Q.-J., Shang, L.-P. and Zhan, J. 2019. Cross-resistance of the pathogenic fungus Alternaria alternata to fungicides with different modes of action. BMC Microbiol. 19:205.
  48. Zambri, N. D. S., Taib, N. I., Abdul Latif, F. and Mohamed, Z. 2019. Utilization of neem leaf extract on biosynthesis of iron oxide nanoparticles. Molecules 24:3803.
  49. Zelmat, L., Mansi, J. M., Aouzal, S., Gaboun, F., Khayi, S., Ibriz, M., El Guilli, M. and Mentag, R. 2021. Genetic diversity and population structure of moroccan isolates belong to Alternaria spp. causing black rot and brown spot in citrus. Int. J. Genomics 2021:9976969.