In Vitro Evaluation of the Antifungal Effect of AgNPs on Fusarium oxysporum f. sp. lycopersici
Abstract
:1. Introduction
2. Materials and Methods
2.1. Biologic Material and Chemical Reagents
2.2. Extract Preparation
2.3. Synthesis of Nanoparticles
2.4. Nanoparticles’ Characterization
2.5. Antifungal Effect on Mycelial Growth In Vitro
2.6. Determination of the Minimum Inhibitory Concentration
2.7. Antifugal Effect on Tomatoes
3. Results
3.1. AgNPs’ Synthesis and Characterization
3.2. Evaluation of the Antifungal Effect of the AgNPs
4. Discussion
5. Conclusions
Author Contributions
Funding
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Doley, K.; Borde, M.; Kulkarni, M. AM fungi and Trichoderma interaction for biological control of soilborne plant pathogen Fusarium oxysporum. In Plant Microbe Interface; Springer: Berlin/Heidelberg, Germany, 2019. [Google Scholar] [CrossRef]
- Li, P.; Bhattacharjee, P.; Wang, S.; Zhang, L.; Ahmed, I.; Guo, L. Mycoviruses in Fusarium species: An update. Front. Cell. Infect. Microbiol. 2019, 9, 257. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Villa, A.; Pérez, R.; Morales, H.A.; Basurto, M.; Soto, J.M.; Martínez, E. Situación actual en el control de Fusarium Spp. y evaluación de la actividad antifúngica de extractos vegetales. Acta Agron. 2015, 64, 194–205. [Google Scholar] [CrossRef]
- 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.; et al. The top 10 fungal pathogens in molecular plant pathology. Mol. Plant Pathol. 2012, 13, 414–430. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- González, I.; Yailén, A.; Peteira, B. Aspectos generales de la interacción Fusarium oxysporum f. Sp. Ilycopersici-Tomate. Rev. Protección Veg. 2012, 27, 1–7. [Google Scholar]
- Trujillo, F.J.; Ramírez, F.; Gay, J.; Vélez, A.; Leyva, J.L.; Calderón, F.J. Primer reporte de Fusarium oxysporum f. Sp. Cubense raza 4 tropial (Foc R4T) en Turquía-monitor sanitario. INFO Senasica 2019, 7, 2–3. [Google Scholar]
- Essarioui, A.; Mokrini, F.; Afechtal, M. Molecular interactions between tomato and its wilt pathogen Fusarium oxysporum f. Sp. Lycopersici. Rev. Mar. Sci. Agron. Vét. 2016, 4, 66–74. [Google Scholar]
- Vásquez, L.; Castaño, J. Manejo integrado de La marchitez vascular del tomate Fusarium Oxysporu f. Sp. lycopersici (Sacc.) W.C. Snyder & H.N. Hansen: Una Revisión. Rev. U.D.C.A Actual. Divulg. Científica 2017, 20, 363–374. [Google Scholar]
- Landeros de la Isla, A.; Macías Sánchez, K.L. Fusarium oxysporum f. Sp. Lycopersici: How can we control this fungus? Adv. Biotechnol. Microbiol. 2017, 4, 55–56. [Google Scholar] [CrossRef]
- Ballari, M.S.; Herrera Cano, N.; Lopez, A.G.; Wunderlin, D.A.; Feresín, G.E.; Santiago, A.N. Green synthesis of potential antifungal agents: 2-Benzyl substituted thiobenzoazoles. J. Agric. Food Chem. 2017, 65, 10325–10331. [Google Scholar] [CrossRef]
- Michelm, A.; Otero, M.; Martínez, R. Control biológico in vitro de enfermedades fungosas en tomate Lycopersicum esculentum Mill. Investig. Agropecu. 2008, 12, 55–68. [Google Scholar]
- Singh, M.; Srivastava, M.; Kumar, A.; Pandey, K. Biosynthesis of Nanoparticles and Applications in Agriculture; Elsevier Inc.: Amsterdam, The Netherlands, 2019. [Google Scholar] [CrossRef]
- Lira-Saldivar, R.H.; Argüello Méndez, B.; Villarreal, G.D.; Los, S.; Vera Reyes, I. Nanotechnology potential in sustainable agriculture. Acta Univ. 2018, 28, 9–24. [Google Scholar] [CrossRef]
- Dos Santos, C.A.; Seckler, M.M.; Ingle, A.P.; Gupta, I.; Galdiero, S.; Galdiero, M.; Gade, A.; Rai, M. Silver nanoparticles: Therapeutical uses, toxicity, and safety issues. J. Pharm. Sci. 2014, 103, 1931–1944. [Google Scholar] [CrossRef]
- Duhan, J.S.; Kumar, R.; Kumar, N.; Kaur, P.; Nehra, K.; Duhan, S. Nanotechnology: The new perspective in precision agriculture. Biotechnol. Rep. 2017, 15, 11–23. [Google Scholar] [CrossRef]
- Khan, M.; Khan, A.U.; Alam, M.J.; Park, S.; Alam, M. Biosynthesis of silver nanoparticles and its application against phytopathogenic bacterium and fungus. Int. J. Environ. Anal. Chem. 2019, 99, 1390–1401. [Google Scholar] [CrossRef]
- Capaldi Arruda, S.C.; Diniz Silva, A.L.; Moretto Galazzi, R.; Antunes Azevedo, R.; Zezzi Arruda, M.A. Nanoparticles applied to plant science: A review. Talanta 2015, 131, 693–705. [Google Scholar] [CrossRef]
- Xiang, S.; Ma, X.; Shi, H.; Ma, T.; Tian, C.; Chen, Y.; Chen, H.; Chen, X.; Luo, K.; Cai, L.; et al. Green synthesis of an alginate-coated silver nanoparticle shows high antifungal activity by enhancing its cell membrane penetrating ability. ACS Appl. Bio. Mater. 2019, 2, 4087–4096. [Google Scholar] [CrossRef]
- Gudkov, S.V.; Serov, D.A.; Astashev, M.E.; Semenova, A.A.; Lisitsyn, A.B. Ag2O Nanoparticles as a candidate for antimicrobial compounds of the new generation. Pharmaceuticals 2022, 15, 968. [Google Scholar] [CrossRef]
- Atef, A.H.; Mogda, K.M.; Mahmoud, H.H. Biosynthesis of silver nanoparticles (Ag-Nps) (a model of metals) by Candida albicans and its antifungal activity on some fungal pathogens (Trichophyton mentagrophytes and Candida albicans). N. Y. Sci. J. 2013, 6, 27–34. [Google Scholar]
- Lekamge, S.; Ball, A.S.; Shukla, R.; Nugegoda, D. The toxicity of nanoparticles to organisms in freshwater. In Reviews of Environmental Contamination and Toxicology; Springer New York LLC.: New York, NY, USA, 2020; Volume 248, pp. 1–80. [Google Scholar] [CrossRef]
- Beyene, H.D.; Werkneh, A.A.; Bezabh, H.K.; Ambaye, T.G. Synthesis paradigm and applications of silver nanoparticles (AgNPs), a review. Sustain. Mater. Technol. 2017, 13, 18–23. [Google Scholar] [CrossRef]
- Ashajyothi, C.; Prabhurajeshwar, C.; Handral, H.K.; Kelmani, C.R. Investigation of antifungal and anti-mycelium activities using biogenic nanoparticles: An eco-friendly approach. Environ. Nanotechnol. Monit. Manag. 2016, 5, 81–87. [Google Scholar] [CrossRef]
- Mabey, T.; Andrea Cristaldi, D.; Oyston, P.; Lymer, K.P.; Stulz, E.; Wilks, S.; William Keevil, C.; Zhang, X. Bacteria and nanosilver: The quest for optimal production. Crit. Rev. Biotechnol. 2019, 39, 272–287. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Srikar, S.K.; Giri, D.D.; Pal, D.B.; Mishra, P.K.; Upadhyay, S.N. Green Synthesis of silver nanoparticles: A review. Green and sustainable chemistry. Green Sustain. Chem. 2016, 6, 34–56. [Google Scholar] [CrossRef] [Green Version]
- Syafiuddin, A.; Salmiati; Salim, M.R.; Beng Hong Kueh, A.; Hadibarata, T.; Nur, H. A Review of silver nanoparticles: Research trends, global consumption, synthesis, properties, and future challenges. J. Chin. Chem. Soc. 2017, 64, 732–756. [Google Scholar] [CrossRef]
- Boukhris, M.; Simmonds, M.S.J.J.; Sayadi, S.; Bouaziz, M. Chemical composition and biological activities of polar extracts and essential oil of rose-scented Geranium, Pelargonium graveolens. Phyther. Res. 2013, 27, 1206–1213. [Google Scholar] [CrossRef] [PubMed]
- Mohammadlou, M.; Jafarizadeh-Malmiri, H.; Maghsoudi, H. Hydrothermal green synthesis of silver nanoparticles using Pelargonium/Geranium leaf extract and evaluation of their antifungal activity. Green Process. Synth. 2017, 6, 31–42. [Google Scholar] [CrossRef]
- Kim, S.W.; Jung, J.H.; Lamsal, K.; Kim, Y.S.; Min, J.S.; Lee, Y.S. Antifungal effects of silver nanoparticles (AgNPs) against various plant pathogenic fungi. Mycobiology 2012, 40, 53–58. [Google Scholar] [CrossRef] [Green Version]
- Syed, H.; Bilal Haider, A.; Lubna, R.; Mehreen, Z.; Adnan, Z.; Hashmi, S.S.; Abbasi, B.H.; Rahman, L.; Zaka, M.; Zahir, A. Phytosynthesis of organo-metallic silver nanoparticles and their anti-phytopathogenic potency against soil borne Fusarium Spp. Mater. Res. Express 2019, 6, 1150a9. [Google Scholar] [CrossRef]
- Wrobel, K.; Wrobel, K.; Garcia Lara, B.; Guerrero Esperanza, M.; Gonzalez Roncero, M.I.; Corrales Escobosa, A.R. Comparative evaluation of Two Fusarium f. Sp. Lycopersici strains grown on two different carbon sources: LC-MS-based secretome study in vivo 15N metabolic labeling. Int. J. Mass Spectrom. 2020, 229, 116288. [Google Scholar] [CrossRef]
- Martínez Espinosa, J.C.; Carrera Cerritos, R.; Ramírez Morales, M.A.; Guerrero Sánchez, K.P.; Silva Contreras, R.A.; Macías, J.H. Characterization of silver nanoparticles obtained by a green route and their evaluation in the bacterium of Pseudomonas aeruginosa. Crystals 2020, 10, 395. [Google Scholar] [CrossRef]
- Macías Sánchez, K.L.; García Soto, J.; Roncero, M.I.G.; Hernández Monjaraz, W.; Caudillo Pérez, C.; Martínez Cadena, M.G. Isolation and expression of enolase gene in Fusarium oxysporum f. Sp. lycopersici. Appl. Biochem. Biotechnol. 2015, 175, 902–908. [Google Scholar] [CrossRef]
- Barhate, B.G.; Musmade, N.A.; Nikhate, T.A. Management of Fusarium wilt of tomato by bioagents, fungicides and varietal resistance. Int. J. Plant Prot. 2015, 8, 49–52. [Google Scholar] [CrossRef]
- Al-Hatmi, A.M.S.; Curfs-Breuker, I.; de Hoog, G.S.; Meis, J.F.; Verweij, P.E. Antifungal susceptibility testing of Fusarium: A practical approach. J. Fungi 2017, 3, 19. [Google Scholar] [CrossRef] [Green Version]
- Lass-Flörl, C.; Perkhofer, S.; Mayr, A. In Vitro susceptibility testing in fungi: A global perspective on a variety of methods. Mycoses 2010, 53, 1–11. [Google Scholar] [CrossRef]
- Morón, R.E.; León Paredes, P.H.; Bustamante Rufino, A.B. Evaluación de la Susceptibilidad Anifúngica In Vitro de Tres Especies de Hongos Causantes de Queratitis Fúngica: Candida albicans, Aspergillus fumigatus y Fusarium solani del Gel Oftálmico de Voriconazol; Universidad peruana Cayetano Heredia: Lima, Peru, 2017. [Google Scholar]
- Pilaquinga, M.; Pazmiño, V.K.; Robalino, T.A.; Jara, N.E.; López, F.F.; Meneses, O.L.; Vizuete, A.K.; Debut, M.A.; Pilaquinga, M.; Pazmiño, V.K.; et al. Síntesis verde de nanopartículas de plata usando el extracto acuoso de las hojas de ajo (Allium sativum). Infoanalítica 2019, 7, 41–55. [Google Scholar] [CrossRef]
- Okafor, F.; Janen, A.; Kukhtareva, T.; Edwards, V.; Curley, M. Green synthesis of silver nanoparticles, their characterization, application and antibacterial activity. Int. J. Environ. Res. Public Health 2013, 10, 5221–5238. [Google Scholar] [CrossRef] [Green Version]
- Zhang, T.; Wang, L.; Chen, Q.; Chen, C. Cytotoxic potential of silver nanoparticles. Yonsei Med. J. 2014, 55, 283–291. [Google Scholar] [CrossRef] [Green Version]
- Qing, Y.Y.; Cheng, L.; Li, R.; Liu, G.; Zhang, Y.; Tang, X.; Wang, J.; Liu, H.; Qin, Y. Potential antibacterial mechanism of silver nanoparticles and the optimization of orthopedic implants by advanced modification technologies. Int. J. Nanomed. 2018, 13, 3311–3327. [Google Scholar] [CrossRef] [Green Version]
- Ávalos, A.; Haza, A.; Mateo, D.; Morales, P. Nanopartículas de plata: Aplicaciones y riesgos tóxicos para la salud humana y el medio ambiente. Rev. Complut. Ciencias Vet. 2013, 7, 1–23. [Google Scholar] [CrossRef] [Green Version]
- Sikder, M.; Lead, J.R.; Chandler, G.T.; Baalousha, M. A rapid approach for measuring silver nanoparticle concentration and dissolution in seawater by UV–Vis. Sci. Total Environ. 2018, 618, 597–607. [Google Scholar] [CrossRef]
- Navarro Gallón, S.M.; Alpaslan, E.; Wang, M.; Larese-Casanova, P.; Londoño, M.E.; Atehortúa, L.; Pavón, J.J.; Webster, T.J. Characterization and study of the antibacterial mechanisms of silver nanoparticles prepared with microalgal exopolysaccharides. Mater. Sci. Eng. C 2019, 99, 685–695. [Google Scholar] [CrossRef]
- Ashraf, H.; Anjum, T.; Riaz, S.; Naseem, S. Microwave-assisted green synthesis and characterization of silver nanoparticles using Melia Azedarach for the Management of Fusarium Wilt in tomato. Front. Microbiol. 2020, 11, 1–22. [Google Scholar] [CrossRef]
- Borrego, A. Las Enmiendas Orgánicas del Suelo en el Control de las Fusariosis del Espárrago y del Tomate; Universidad de Córdoba: Córdoba, Spain, 2014. [Google Scholar]
- Rodríguez, H.A.; Guevara, R.G.; Romero Gómez, S.; Feregrino Pérez, A.A. Antifungal activity of mexican endemic plants on agricultural phytopathogens: A review. In Proceedings of the 2018 XIV International Engineering Congress (CONIIN), Queretaro, Mexico, 14–19 May 2018; Volume 18, pp. 1–11. [Google Scholar] [CrossRef]
- Nisa, T.U.; Wani, A.H.; Bhat, M.Y.; Pala, S.A.; Mir, R.A. In vitro inhibitory effect of fungicides and botanicals on mycelial growth and spore germination of Fusarium oxysporum. J. Biopestic. 2011, 4, 53. [Google Scholar]
- Gordon, E.B. Captan and Folpet, 3rd ed.; Elsevier Inc.: Washington, WA, USA, 2010; Volume 2. [Google Scholar] [CrossRef]
- Xue, B.; He, D.; Gao, S.; Wang, D.; Yokoyama, K.; Wang, L. Biosynthesis of silver nanoparticles by the fungus Arthroderma Fulvum and its antifungal activity against genera of Candida, Aspergillus and Fusarium. Int. J. Nanomed. 2016, 11, 1899–1906. [Google Scholar] [CrossRef] [Green Version]
- Shen, T.; Wang, Q.; Li, C.; Zhou, B.; Li, Y.; Liu, Y. Transcriptome sequencing analysis reveals silver nanoparticles antifungal molecular mechanism of the soil fungi Fusarium Solani Species Complex. J. Hazard. Mater. 2020, 388, 122063. [Google Scholar] [CrossRef] [PubMed]
- Shang, Y.; Kamrul Hasan, M.; Ahammed, G.J.; Li, M.; Yin, H.; Zhou, J. Applications of nanotechnology in plant growth and crop protection: A review. Molecules 2019, 24, 2558. [Google Scholar] [CrossRef] [Green Version]
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Macías Sánchez, K.L.; González Martínez, H.D.R.; Carrera Cerritos, R.; Martínez Espinosa, J.C. In Vitro Evaluation of the Antifungal Effect of AgNPs on Fusarium oxysporum f. sp. lycopersici. Nanomaterials 2023, 13, 1274. https://doi.org/10.3390/nano13071274
Macías Sánchez KL, González Martínez HDR, Carrera Cerritos R, Martínez Espinosa JC. In Vitro Evaluation of the Antifungal Effect of AgNPs on Fusarium oxysporum f. sp. lycopersici. Nanomaterials. 2023; 13(7):1274. https://doi.org/10.3390/nano13071274
Chicago/Turabian StyleMacías Sánchez, Karla Lizbeth, Hiram Deusdedut Rashid González Martínez, Raúl Carrera Cerritos, and Juan Carlos Martínez Espinosa. 2023. "In Vitro Evaluation of the Antifungal Effect of AgNPs on Fusarium oxysporum f. sp. lycopersici" Nanomaterials 13, no. 7: 1274. https://doi.org/10.3390/nano13071274