Growth inhibition of Fusarium oxysporum f. sp. nicotianae by two in vitro poisoning methods with fungicides of different toxicological groups
Keywords:
Chemical combat, fusarium, tobacco, sensitivity, fungitoxicity, wilt
Abstract
Wilt caused by Fusarium oxysporum f. sp. nicotianae is one of the most important fungal diseases in tobacco cultivation, being also one of the most difficult to control. The in vitro effectiveness of two poisoning methods was evaluated; sensi-disc (SD) and medium dilution (DMC) to determine the inhibitory effect of four fungicides of different toxicological groups on F. oxysporum isolated from tobacco in different regions of the province of Granma, Cuba. A differential response was observed in the susceptibility levels of all strains tested, regardless of the method of poisoning. The DMC method was more efficient than the SD, observing increases from 4.37 % (S) to 45.57 % (Ip+Pr) with respect to the SD. The highest inhibition values were observed in DMC with mancozeb (100 %), Tz+Az (79.74 %), and Ip+Pr (96.9 %). The greatest effectiveness in sporulation inhibition was with mancozeb by the SD method (0 %). The in vitro inhibitory effect of the fungicides evaluated (alone or in combination) is indicative of the fungicidal effect on the fungus under study and establishes the importance of inhibition methods for the study of fungicides used in management programs of diseases caused by Fusarium spp., in the tobacco growing areas of Cuba and other parts of the world.
Downloads
Download data is not yet available.
References
Avenot, H. F. and Michailides, T. J. (2010). Progress in understanding molecular mechanisms and evolution of resistance to succinate dehydrogenase inhibiting (SDHI) fungicides in phytopathogenic fungi. Crop Protection, 29(7), 643-651. DOI: https://doi.org/10.1016/j.cropro.2010.02.019
Blancard, D. (1998). Maladies du tabac (observer, identifier, lutter). INRA. Pp. 310-312.
Castellanos-González, B. L., Muriño-García, M. Lorenzo-Nicao, E., Rodríguez-Fernández, A. & Gómez-Albernal, M. (2011). Efecto in vitro de siete fungicidas químicos sobre Beauveria bassiana (Bals.) Vuil. Fitosanidad, 15(1), 31-38. http://scielo.sld.cu/scielo.php?script=sci_arttext&pid=S1562-30092011000100005
Ceiro, W. G., Arévalo, J. & Hidalgo-Díaz, L. (2015). Efectos de plaguicidas y bioestimulantes vegetales sobre la germinación de clamidosporas y el desarrollo in vitro del hongo nematófago Pochonia chlamydosporia. Revista Iberoamericana de Micología, 32(4), 277-280. DOI: https://doi.org/10.1016/j.riam.2014.07.008
Ceiro, W. G., Vega-González, Y., Taco-Sánchez, M. E., Gaibor-Fernández, R. & Sosa-Sánchez, O. (2021). Antagonismo de Trichoderma harzianum y Trichoderma viride sobre aislados de Fusarium spp. procedentes de Nicotiana tabacum. Revista de la Facultad de Agronomía de la Universidad de Zulia (LUZ), 38(4), 867-886. DOI: https://doi.org/10.47280/RevFacAgron(LUZ).v38.n4.07
Clinical Laboratory and Standards Institute (CLSI) (2008). Performance standards for antimicrobial susceptibility testing; 18th informational supplements. CLSI document standard M100-S18. Wayne (PA). Crago, B., Ferrato, C., Drews, S. J., Svenson, L. W., Tyrrell, G., y Louie, M.
Cosner, C. (2015). The golden leaf: how tobacco shaped Cuba and the Atlantic World. Vanderbilt University Press.
Edel-Hermann, V. and Lecomte, C. (2019). Current status of Fusarium oxysporum formae speciales and races. Phytopathology, 109, 512-530. DOI: https://doi.org/10.1094/PHYTO-08-18-0320-RVW
Förster, H., Kanetis, L. & Adaskaveg, J. E. (2004). Spiral gradient dilution, a rapid method for determining growth responses and 50 % effective concentration values in fungus-fungicide interactions. Phytopathology, 94(2), 163-170. DOI: https://doi.org/10.1094/PHYTO.2004.94.2.163
García, V., Santana, N. & Mena, E. (2015). Burley Pinar 2010: primer cultivar cubano de tabaco burley resistente al marchitamiento por fusarium (Fusarium oxysporum) ya otras enfermedades de importancia en el cultivo. Cultivos Tropicales, 36(2), 91. https://shorturl.at/hipQ9
González‐Merino, A. M, Hernández‐Juárez, A., Betancourt‐Galindo, R., Ochoa‐Fuentes, Y. M., Valdez‐Aguilar, L. A. & Limón‐Corona, M. L. (2021). Antifungal activity of zinc oxide nanoparticles in Fusarium oxysporum‐Solanum lycopersicum pathosystem under controlled conditions. Journal of Phytopathology, 169(9), 533-544. DOI: https://doi.org/10.1111/jph.13023
Gullino M. L., Tinivella, F., Garibaldi, A., Kemmitt, G. M., Bacci, L. & Sheppard, B. (2010). Mancozeb: pest, present and future. Plant Disease, 94(9), 1076-1087. DOI: https://doi.org/10.1094/PDIS-94-9-1076
Holguín-Peña, R. J. (2007). Fusarium wilt of tomato caused by Fusarium oxysporum f. sp. lycopersici race 3 in Baja California Sur, Mexico. Plant Disease, 89(12). 1360. DOI: https://doi.org/10.1094/PD-89-1360C
InfoStat (2008). InfoStat versión 2008. Di Rienzo, J. A., Casanoves, F., Balzarini, M. G., González, l., Tablada, M., & Robledo, C. W. Grupo InfoStat, FCA, Universidad Nacional de Córdoba, Argentina.
Lombard, L., Sandoval-Denis, M., Lamprecht, S. C. & Crous, P. W. (2019). Epitypification of Fusarium oxysporum – clearing the taxonomic chaos. Persoonia - Molecular Phylogeny and Evolution of Fungi, 43, 1-47. DOI: https://doi.org/10.3767/persoonia.2019.43.01
López, D. (2004). Especies de Fusarium de Cuba sobre nuevos sustratos. Revista de Protección Vegetal, 19(1), 14-18. https://agris.fao.org/agris-search/search.do?recordID=CU2006101981
Lucas, J. A., Hawkins, N. J. & Fraaije, B. A. (2015). The evolution of fungicide resistance. Advances in Applied Microbiology, 90, 29-92. DOI: https://doi.org/10.1016/bs.aambs.2014.09.001
Mariña de la Huerta, C., Nieto-Martínez, M., Rosalba-Quintana, A., Castillo-Fonseca, P. I. & Pérez-Machado, B. (2005). Efecto del Biobrás 16 sobre algunos indicadores del crecimiento en la variedad de tabaco negro ‘Habana-92’ cultivada en suelos fluvisoles. Cuba Tabaco, 6(1), 1-8. https://1library.co/document/q75p6xoz-efecto-biobras-indicadores-crecimiento-variedad-tabaco-cultivada-fluvisoles.html
Martín, M. C., Leyva, L., Suárez, M. A., Pichardo, T., Caraballoso, I. B. & Capó, Y. A. (2021). Antifungal activity of Bacillus amyloliquefaciens against Fusarium oxysporum f. sp. cubense race 1. Agronomy Mesoamerican, 32(2), 466-478. https://www.scielo.sa.cr/pdf/am/v32n2/2215-3608-am-32-02-00466.pdf
Miguel, T., Bordini, J., Saito, G., Andrade, C., Ono, M., Hirooka, E. & Ono, E. (2015). Effect of fungicide on Fusarium verticillioides mycelial morphology and fumonisin B1 production. Brazilian Journal of Microbiology, 46(1), 293-299. DOI: 10.1590/s1517-838246120120383
Nelson, P. E. (1990). Taxonomy of fungi in the genus Fusarium with emphasis on Fusarium oxysporum. p. 27-35. In: Re. Ploetz (ed.). Fusarium wilt of banana. American Phytopathological Society. Press. St. Paul.
Nisa, T. U., Wani, A. H., Bhat, M. Y., Pala, S. E. & Mir, R. A. (2011). In vitro inhibitory effect of fungicides and botanicals on mycelial growth and spore germination of Fusarium oxysporum. Journal of Biopesticides, 4(1), 53-56. https://cutt.ly/RXQzoN5
Olivares, B. O., Rey, J. C., Lobo, D., Navas-Cortés, J. A., Gómez, J. A. & Landa, B. B. (2021). Fusarium wilt of bananas: a review of agro-environmental factors in the Venezuelan production system affecting its development. Agronomy, 11(5), 986. DOI: https://doi.org/10.3390/agronomy11050986
Rentería-Martínez, M. E., Guerra, M. A., Ochoa, A., Moreno, S. F. Meza, A. & Guzmán, J. M. (2019). Descripción y comparación entre morfotipos de Fusarium brachygibbosum, F. falciforme y F. oxysporum patogénicos en sandía cultivada en Sonora, México. Revista Mexicana de Fitopatología, 37(1), 16-34. DOI: https://doi.org/10.18781/r.mex.fit.1808-1
Runkle, J., Flocks., J., Economos, J. & Dunlop, A. L. (2017). A systematic review of Mancozeb as a reproductive and developmental hazard. Environment International, 99, 29-42. DOI: https://doi.org/10.1016/j.envint.2016.11.006
Savin-Molina, J., Hernández-Montiel, L. G., Cerio-Catasu, W., Ávila-Quezada, G. D., Palacios-Espinoza, A., Ruiz-Espinoza, F. H. & Romero-Bastidas, M. (2021). Caracterización morfológica y potencial de biocontrol de especies de Trichoderma aisladas de suelos del semiárido. Revista Mexicana de Fitopatología, 39 (3), 435-451. DOI: https://doi.org/10.18781/r.mex.fit.2106-7
Silva-Marrufo, O. and Marín-Tinoco, R. I. (2021). Sustituto de fungicidas químicos sintéticos con aceite esencial de orégano para el control del Fusarium oxysporum. Gestión y Ambiente, 24(Supl.3), 73-80. https://revistas.unal.edu.co/index.php/gestion/article/view/95526
Sultana, N. and Ghaffar, A. (2013). Effect of fungicides, microbial antagonists and oil cakes in the control of Fusarium oxysporum, the cause of seed rot and root infection of bottle gourd and cucumber. Pakistan Journal of Botany, 45(6), 2149-2156. http://pakbs.org/pjbot/PDFs/45(6)/45.pdf
Summerell, B. A., Salleh, B. & Leslie, J. F. (2007). A utilitarian approach to Fusarium identification. Plant Disease, 87(2), 117-128. DOI: https://doi.org/10.1094/PDIS.2003.87.2.117
Villa, A., Pérez, R., Morales, H., Basurto, H., Soto, J. & Martínez, E. (2015). Situación actual en el control de Fusarium spp. y evaluación de la actividad anti fúngica de extractos vegetales. Acta Agronómica, 64(2), 194-205. http://www.scielo.org.co/scielo.php?script=sci_arttext&pid=S0120-28122015000200011
Wang, H., Wang, J., Chen, Q., Wang, M., Hsiang, T., Shang, S. & Yu, Z. (2016). Metabolic effects of azoxystrobin and kresoxim-methyl against Fusarium kyushuense examined using the Biolog FF MicroPlate. Pesticide Biochemistry and Physiology, 130, 52-58. DOI: https://doi.org/10.1016/j.pestbp.2015.11.013
Watanabe, M. (2013). Molecular phylogeny and identification of Fusarium species based on nucleotide sequences. Mycotoxins, 63(2), 133-142. https://www.jstage.jst.go.jp/article/myco/63/2/63_133/_pdf
Webster, D., Tschereau, P., Belland, R., Sand, C. & Rennie, R. P. (2008). Antifungal activity of medicinal plant extracts; preliminary screening studies. Journal of Ethnopharmacology, 115(1), 140-146. DOI: https://doi.org/10.1016/j.jep.2007.09.014
Wikle, T. A. (2015). Tobacco farming, cigar production and Cuba’s Viñales Valley. Focus Geography, 58(1), 153-162. DOI: 10.1111/foge.12058
Zgoda, J. R. and Porter, J. R. (2001). A convenient micro dilution method for screening natural products against bacteria and fungi. Pharmacology Biology, 39(3), 221-225. DOI: https://doi.org/10.1076/phbi.39.3.221.5934
Blancard, D. (1998). Maladies du tabac (observer, identifier, lutter). INRA. Pp. 310-312.
Castellanos-González, B. L., Muriño-García, M. Lorenzo-Nicao, E., Rodríguez-Fernández, A. & Gómez-Albernal, M. (2011). Efecto in vitro de siete fungicidas químicos sobre Beauveria bassiana (Bals.) Vuil. Fitosanidad, 15(1), 31-38. http://scielo.sld.cu/scielo.php?script=sci_arttext&pid=S1562-30092011000100005
Ceiro, W. G., Arévalo, J. & Hidalgo-Díaz, L. (2015). Efectos de plaguicidas y bioestimulantes vegetales sobre la germinación de clamidosporas y el desarrollo in vitro del hongo nematófago Pochonia chlamydosporia. Revista Iberoamericana de Micología, 32(4), 277-280. DOI: https://doi.org/10.1016/j.riam.2014.07.008
Ceiro, W. G., Vega-González, Y., Taco-Sánchez, M. E., Gaibor-Fernández, R. & Sosa-Sánchez, O. (2021). Antagonismo de Trichoderma harzianum y Trichoderma viride sobre aislados de Fusarium spp. procedentes de Nicotiana tabacum. Revista de la Facultad de Agronomía de la Universidad de Zulia (LUZ), 38(4), 867-886. DOI: https://doi.org/10.47280/RevFacAgron(LUZ).v38.n4.07
Clinical Laboratory and Standards Institute (CLSI) (2008). Performance standards for antimicrobial susceptibility testing; 18th informational supplements. CLSI document standard M100-S18. Wayne (PA). Crago, B., Ferrato, C., Drews, S. J., Svenson, L. W., Tyrrell, G., y Louie, M.
Cosner, C. (2015). The golden leaf: how tobacco shaped Cuba and the Atlantic World. Vanderbilt University Press.
Edel-Hermann, V. and Lecomte, C. (2019). Current status of Fusarium oxysporum formae speciales and races. Phytopathology, 109, 512-530. DOI: https://doi.org/10.1094/PHYTO-08-18-0320-RVW
Förster, H., Kanetis, L. & Adaskaveg, J. E. (2004). Spiral gradient dilution, a rapid method for determining growth responses and 50 % effective concentration values in fungus-fungicide interactions. Phytopathology, 94(2), 163-170. DOI: https://doi.org/10.1094/PHYTO.2004.94.2.163
García, V., Santana, N. & Mena, E. (2015). Burley Pinar 2010: primer cultivar cubano de tabaco burley resistente al marchitamiento por fusarium (Fusarium oxysporum) ya otras enfermedades de importancia en el cultivo. Cultivos Tropicales, 36(2), 91. https://shorturl.at/hipQ9
González‐Merino, A. M, Hernández‐Juárez, A., Betancourt‐Galindo, R., Ochoa‐Fuentes, Y. M., Valdez‐Aguilar, L. A. & Limón‐Corona, M. L. (2021). Antifungal activity of zinc oxide nanoparticles in Fusarium oxysporum‐Solanum lycopersicum pathosystem under controlled conditions. Journal of Phytopathology, 169(9), 533-544. DOI: https://doi.org/10.1111/jph.13023
Gullino M. L., Tinivella, F., Garibaldi, A., Kemmitt, G. M., Bacci, L. & Sheppard, B. (2010). Mancozeb: pest, present and future. Plant Disease, 94(9), 1076-1087. DOI: https://doi.org/10.1094/PDIS-94-9-1076
Holguín-Peña, R. J. (2007). Fusarium wilt of tomato caused by Fusarium oxysporum f. sp. lycopersici race 3 in Baja California Sur, Mexico. Plant Disease, 89(12). 1360. DOI: https://doi.org/10.1094/PD-89-1360C
InfoStat (2008). InfoStat versión 2008. Di Rienzo, J. A., Casanoves, F., Balzarini, M. G., González, l., Tablada, M., & Robledo, C. W. Grupo InfoStat, FCA, Universidad Nacional de Córdoba, Argentina.
Lombard, L., Sandoval-Denis, M., Lamprecht, S. C. & Crous, P. W. (2019). Epitypification of Fusarium oxysporum – clearing the taxonomic chaos. Persoonia - Molecular Phylogeny and Evolution of Fungi, 43, 1-47. DOI: https://doi.org/10.3767/persoonia.2019.43.01
López, D. (2004). Especies de Fusarium de Cuba sobre nuevos sustratos. Revista de Protección Vegetal, 19(1), 14-18. https://agris.fao.org/agris-search/search.do?recordID=CU2006101981
Lucas, J. A., Hawkins, N. J. & Fraaije, B. A. (2015). The evolution of fungicide resistance. Advances in Applied Microbiology, 90, 29-92. DOI: https://doi.org/10.1016/bs.aambs.2014.09.001
Mariña de la Huerta, C., Nieto-Martínez, M., Rosalba-Quintana, A., Castillo-Fonseca, P. I. & Pérez-Machado, B. (2005). Efecto del Biobrás 16 sobre algunos indicadores del crecimiento en la variedad de tabaco negro ‘Habana-92’ cultivada en suelos fluvisoles. Cuba Tabaco, 6(1), 1-8. https://1library.co/document/q75p6xoz-efecto-biobras-indicadores-crecimiento-variedad-tabaco-cultivada-fluvisoles.html
Martín, M. C., Leyva, L., Suárez, M. A., Pichardo, T., Caraballoso, I. B. & Capó, Y. A. (2021). Antifungal activity of Bacillus amyloliquefaciens against Fusarium oxysporum f. sp. cubense race 1. Agronomy Mesoamerican, 32(2), 466-478. https://www.scielo.sa.cr/pdf/am/v32n2/2215-3608-am-32-02-00466.pdf
Miguel, T., Bordini, J., Saito, G., Andrade, C., Ono, M., Hirooka, E. & Ono, E. (2015). Effect of fungicide on Fusarium verticillioides mycelial morphology and fumonisin B1 production. Brazilian Journal of Microbiology, 46(1), 293-299. DOI: 10.1590/s1517-838246120120383
Nelson, P. E. (1990). Taxonomy of fungi in the genus Fusarium with emphasis on Fusarium oxysporum. p. 27-35. In: Re. Ploetz (ed.). Fusarium wilt of banana. American Phytopathological Society. Press. St. Paul.
Nisa, T. U., Wani, A. H., Bhat, M. Y., Pala, S. E. & Mir, R. A. (2011). In vitro inhibitory effect of fungicides and botanicals on mycelial growth and spore germination of Fusarium oxysporum. Journal of Biopesticides, 4(1), 53-56. https://cutt.ly/RXQzoN5
Olivares, B. O., Rey, J. C., Lobo, D., Navas-Cortés, J. A., Gómez, J. A. & Landa, B. B. (2021). Fusarium wilt of bananas: a review of agro-environmental factors in the Venezuelan production system affecting its development. Agronomy, 11(5), 986. DOI: https://doi.org/10.3390/agronomy11050986
Rentería-Martínez, M. E., Guerra, M. A., Ochoa, A., Moreno, S. F. Meza, A. & Guzmán, J. M. (2019). Descripción y comparación entre morfotipos de Fusarium brachygibbosum, F. falciforme y F. oxysporum patogénicos en sandía cultivada en Sonora, México. Revista Mexicana de Fitopatología, 37(1), 16-34. DOI: https://doi.org/10.18781/r.mex.fit.1808-1
Runkle, J., Flocks., J., Economos, J. & Dunlop, A. L. (2017). A systematic review of Mancozeb as a reproductive and developmental hazard. Environment International, 99, 29-42. DOI: https://doi.org/10.1016/j.envint.2016.11.006
Savin-Molina, J., Hernández-Montiel, L. G., Cerio-Catasu, W., Ávila-Quezada, G. D., Palacios-Espinoza, A., Ruiz-Espinoza, F. H. & Romero-Bastidas, M. (2021). Caracterización morfológica y potencial de biocontrol de especies de Trichoderma aisladas de suelos del semiárido. Revista Mexicana de Fitopatología, 39 (3), 435-451. DOI: https://doi.org/10.18781/r.mex.fit.2106-7
Silva-Marrufo, O. and Marín-Tinoco, R. I. (2021). Sustituto de fungicidas químicos sintéticos con aceite esencial de orégano para el control del Fusarium oxysporum. Gestión y Ambiente, 24(Supl.3), 73-80. https://revistas.unal.edu.co/index.php/gestion/article/view/95526
Sultana, N. and Ghaffar, A. (2013). Effect of fungicides, microbial antagonists and oil cakes in the control of Fusarium oxysporum, the cause of seed rot and root infection of bottle gourd and cucumber. Pakistan Journal of Botany, 45(6), 2149-2156. http://pakbs.org/pjbot/PDFs/45(6)/45.pdf
Summerell, B. A., Salleh, B. & Leslie, J. F. (2007). A utilitarian approach to Fusarium identification. Plant Disease, 87(2), 117-128. DOI: https://doi.org/10.1094/PDIS.2003.87.2.117
Villa, A., Pérez, R., Morales, H., Basurto, H., Soto, J. & Martínez, E. (2015). Situación actual en el control de Fusarium spp. y evaluación de la actividad anti fúngica de extractos vegetales. Acta Agronómica, 64(2), 194-205. http://www.scielo.org.co/scielo.php?script=sci_arttext&pid=S0120-28122015000200011
Wang, H., Wang, J., Chen, Q., Wang, M., Hsiang, T., Shang, S. & Yu, Z. (2016). Metabolic effects of azoxystrobin and kresoxim-methyl against Fusarium kyushuense examined using the Biolog FF MicroPlate. Pesticide Biochemistry and Physiology, 130, 52-58. DOI: https://doi.org/10.1016/j.pestbp.2015.11.013
Watanabe, M. (2013). Molecular phylogeny and identification of Fusarium species based on nucleotide sequences. Mycotoxins, 63(2), 133-142. https://www.jstage.jst.go.jp/article/myco/63/2/63_133/_pdf
Webster, D., Tschereau, P., Belland, R., Sand, C. & Rennie, R. P. (2008). Antifungal activity of medicinal plant extracts; preliminary screening studies. Journal of Ethnopharmacology, 115(1), 140-146. DOI: https://doi.org/10.1016/j.jep.2007.09.014
Wikle, T. A. (2015). Tobacco farming, cigar production and Cuba’s Viñales Valley. Focus Geography, 58(1), 153-162. DOI: 10.1111/foge.12058
Zgoda, J. R. and Porter, J. R. (2001). A convenient micro dilution method for screening natural products against bacteria and fungi. Pharmacology Biology, 39(3), 221-225. DOI: https://doi.org/10.1076/phbi.39.3.221.5934
Published
2022-08-25
How to Cite
Ceiro-Catasú, W. G., Rueda-Puente, E. O., Rondón-Fonseca, R., Sosa-Sánchez, O., & Holguín-Peña, R. J. (2022). Growth inhibition of Fusarium oxysporum f. sp. nicotianae by two in vitro poisoning methods with fungicides of different toxicological groups. Revista De La Facultad De Agronomía De La Universidad Del Zulia, 39(3), e223944. Retrieved from https://mail.produccioncientificaluz.org/index.php/agronomia/article/view/38626
Issue
Section
Crop Production
Copyright (c) 2022 Wilson Geobel Ceiro-Catasú, Edgar Omar Rueda-Puente, Richard Rondón-Fonseca, Oandis Sosa-Sánchez and Ramón Jaime Holguín-Peña
This work is licensed under a Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International License.
