olletotrichum species associated with anthracnose in orange (Citrus sinensis (L.) Osb.) and its in vitro control with fungicides
DOI:
https://doi.org/10.15517/am.v34i2.52190Keywords:
fugal diseases, citrus, pesticidesAbstract
Introduction. Orange (Citrus sinensis (L.) Osb.) cultivation is one of the most important worldwide. Among the main limitations in its production is the fall of flowers caused by Colletotrichum. Objective. To determine the species of Colletotrichum associated with anthracnose in orange and to estimate the in vitro effectiveness of four fungicides on its control. Materials and methods. This study was carried out between June 2021 and February 2022. Six fungal isolates, obtained from orange floral tissues, were identified via polymerase chain reaction (PCR). The efficacy of the fungicides tebuconazole, pyraclostrobin, difenoconazole, and ferbam on two Colletotrichum isolates was evaluated. Two tests were carried out to determine the degree of inhibition of mycelial growth and the percentage of effectiveness of each fungicide. Results. Colletotrichum abscissum was identified on petals with symptoms and Colletotrichum gloeosporioides on calyxes. The effectiveness of the doses used of the fungicides tebuconazole and difenoconazole was verified by presenting inhibition of mycelial growth from a tenth of the commercial dose evaluated. Pyraclostrobin showed little control over both isolates. Ferbam did not present an efficient control in any of the doses evaluated in both strains. Conclusion. The fungi associated with anthracnose in orange, on the farm studied, were C. abscissum, present on petals with initial and advanced symptoms, and C. gloeosporioides present on persistent calyxes. The effectiveness of the fungicides evaluated was higher for triazoles, tebuconazole, and difenoconazole, in that order. Pyraclostrobin showed a poor control on both isolates. Ferbam was not effective in in vitro tests.
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References
Arce-Araya, C., Varela-Benavides, I., & Torres-Portuguez, S. (2019). Inhibición del crecimiento micelial de hongos asociados a antracnosis en ñame (Dioscorea alata). Agronomía Mesoamericana, 30(2), 381–393. https://doi.org/10.15517/am.v30i2.32653
Artavia Mejía, J. D. (2019). Efecto de la poda de fructificación por ventanas sobre la brotación, floración y fructificación del limón Mesina (Citrus latifolia Tan.) en Finca Artaca S.A., Heredia, Sarapiquí, Costa Rica [Tesis de licenciatura, Instituto Tecnológico de Costa Rica]. Repositorio TEC del Instituto Tecnológico de Costa Rica. https://hdl.handle.net/2238/11146
Barquero Quiros, M., Peres, N. A., & Arauz, L. F. (2013). Presencia de Colletotrichum acutatum y Colletotrichum gloeosporioides en helecho hoja de cuero, limón criollo, papaya, carambola y mango en Costa Rica y Florida (Estados Unidos). Agronomía Costarricense, 37(1), 23–38. https://doi.org/10.15517/rac.v37i1.10710
Cañedo, V., & Ames, T. (2004). Manual de laboratorio para el manejo de hongos entomopatógenos. Centro Internacional de la Papa. http://cipotato.org/wp-content/uploads/2014/09/AN65216.pdf
Crous, P. W., Wingfield, M. J., Guarro, J., Hernández-Restrepo, M., Sutton, D. A., Acharya, K., Barber, P. A., Boekhout, T., Dimitrov, R. A., Dueñas, M., Dutta, A. K., Gené, J., Gouliamova, D. E., Groenewald, M., Lombard, L., Morozova, O. V., Sarkar, J., Smith, M. T. H., Stchigel, A. M., … Groenewald, J. Z. (2015). Fungal planet description sheets: 320–370, Colletotrichum abscissum. Persoonia - Molecular Phylogeny and Evolution of Fungi, 34, 167–226. https://doi.org/10.3767/003158515X688433
da Silva Junior, G. J. (2011). Podridão floral dos citros: dinâmicas temporal e espacial, sensibilidade de Colletotrichum acutatum a fungicidas e controle da doença [Tesis de doctorado, Universidade de São Paulo]. Biblioteca Digital de Teses e Dissertações da Universidade de São Paulo. https://doi.org/10.11606/T.11.2011.tde-13092011-095157
Damm, U., Cannon, P. F., Woudenberg, J. H. C., & Crous, P. W. (2012). The Colletotrichum acutatum species complex. Studies in Mycology, 73(1), 37–113. https://doi.org/10.3114/sim0010
Dowling, M., Peres, N., Villani, S., & Schnabel, G. (2020). Managing Colletotrichum on fruit crops. A “complex” challenge. Plant Disease, 104(9), 2301–2316. https://doi.org/10.1094/PDIS-11-19-2378-FE
Ezrari, S., Lahlali, R., Radouane, N., Tahiri, A., Asfers, A., Boughalleb-M’Hamdi, N., Amiri, S., & Lazraq, A. (2021). Characterization of Fusarium species causing dry root rot disease of citrus trees in Morocco. Journal of Plant Diseases and Protection, 128, 431–447. https://doi.org/10.1007/s41348-020-00392-0
Fagan, H. J. (1979). Postbloom fruit drop, a new disease of citrus associated with a form of Colletotrichum gloeosporioides. Annals of Applied Biology, 91(1), 13–20. https://doi.org/10.1111/j.1744-7348.1979.tb07408.x
Fungicide Resistance Action Committee. (2020, June). FRAC Recommendations for Resistance Management for Qol Fungicides. https://bit.ly/3K3YOr3
Gama, A. B., Baggio, J. S., Rebello, C. S., de Afonseca Lourenço, S., de G. Gasparoto, M. C., da Silva Junior, G. J., Peres, N. A., & Amorim, L. (2020). Sensitivity of Colletotrichum acutatum isolates from citrus to carbendazim, difenoconazole, tebuconazole, and trifloxystrobin. Plant Disease, 104(6), 1621–1628. https://doi.org/10.1094/PDIS-10-19-2195-RE
Gao, Y. -Y., He, L. -F., Li, B. -X., Mu, W., Lin, J., & Liu, F. (2017). Sensitivity of Colletotrichum acutatum to six fungicides and reduction in incidence and severity of chili anthracnose using pyraclostrobin. Australasian Plant Pathology, 46, 521–528. https://doi.org/10.1007/s13313-017-0518-8
Gaviria-Hernández, V., Patiño-Hoyos, L. F., & Saldarriaga-Cardona, A. (2013). Evaluación in vitro de fungicidas comerciales para el control de Colletotrichum spp., en mora de castilla. Ciencia y Tecnología Agropecuaria, 14(1), 67–75. https://doi.org/10.21930/rcta.vol14_num1_art:344
Guarnaccia, V., Gilardi, G., Martino, I., Garibaldi, A., & Gullino, M. L. (2019). Species diversity in Colletotrichum causing anthracnose of aromatic and ornamental Lamiaceae in Italy. Agronomy, 9(10), Article 613. https://doi.org/10.3390/agronomy9100613
Guerber, J. C., Liu, B., Correll, J. C., & Johnston, P. R. (2003). Characterization of diversity in Colletotrichum acutatum sensu lato by sequence analysis of two gene introns, mtDNA and Intron RFLPs, and mating compatibility. Mycologia, 95(5), 872–895. https://doi.org/10.1080/15572536.2004.11833047
Guerreiro Lima, W., Bellato Spósito, M. Amorim, L., Packer Gonçalves, F., & Albuquerque Melo de Filho, P. (2011). Colletotrichum gloeosporioides, a new causal agent of citrus post-bloom fruit drop. European Journal of Plant Pathology, 131, 157–165. https://doi.org/10.1007/s10658-011-9795-1
Guillén Sánchez, D., Cadenas Vásquez, C. I., Alia Tejaca, I., López Martínez, V., Andrade Rodríguez, M., & Juárez-Lopez, P. (2017). Inhibición colonial in vitro de un aislado de Colletotrichum acutatum Simmonds a tratamientos con fungicidas. Revista Centro Agrícola, 44(4), 11–16. https://bit.ly/3x13AzU
Hall, T. A. (1999). BioEdit: A user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series, 41, 95–98.
Han, Y. -C., Zeng, X. -G., Xiang, F. -Y., Zhang, Q. -H., Guo, C., Chen, F. -Y., & Gu, Y. -C. (2018). Carbendazim sensitivity in populations of Colletotrichum gloeosporioides complex infecting strawberry and yams in Hubei Province of China. Journal of Integrative Agriculture, 17(6), 1391–1400. https://doi.org/10.1016/S2095-3119(17)61854-9
Hernández Medina, C. A. (2016). Especies de Fusarium y Penicillium asociadas a frutales en los departamentos del Cauca y Valle de Cauca, Colombia [Tesis de maestría, Universidad Nacional de Colombia]. Repositorio Institucional de la Universidad Nacional de Colombia. https://repositorio.unal.edu.co/handle/unal/56918
Infostat. (2020). Infostat versión 2020. Universidad Nacional de Córdoba. http://www.infostat.com.ar
International Trade Center. (n.d.). Trade Map. Trade statistics for international business development. Retrieved June, 2022 from https://www.trademap.org/Index.aspx
Marques, J., Amorim, L., Spósito, M., & Appezzato-da-Glória, B. (2013). Histopathology of postbloom fruit drop caused by Colletotrichum acutatum in citrus flowers. European Journal of Plant Pathology, 135(4), 783–790. https://doi.org/10.1007/s10658-012-0120-4
O’Donnell, K., & Cigelnik, E. (1997). Two divergent intragenomic rDNA ITS2 types within a monophyletic lineage of the fungus Fusarium are nonorthologous. Molecular Phylogenetics and Evolution, 7(1), 103–116. https://doi.org/10.1006/mpev.1996.0376
Peres, N. A., & Dewdney, M. M. (2021). 2021–2022 Florida citrus production guide: Postbloom fruit drop: CG007/PP-45, rev. 4/2021. EDIS 2021(CPG). University of Florida. https://doi.org/10.32473/edis-cg007-2021
Peres, N. A., MacKenzie, S. J., Peever, T. L., & Timmer, L. W. (2008). Postbloom fruit drop of citrus and key lime anthracnose are caused by distinct phylogenetic lineages of Colletotrichum acutatum. Phytopathology, 98(3), 345–352. https://doi.org/10.1094/PHYTO-98-3-0345
Peres, N. A. R., Souza, N. L., Furtado, E. L., & Timmer, L. W. (2004). Evaluation of systems for timing of fungicide sprays for control of postbloom fruit drop of citrus in Brazil. Plant Disease, 88(7), 731–735. https://doi.org/10.1094/PDIS.2004.88.7.731
Piccirillo, G., Carrieri, R., Polizzi, G., Azzaro, A., Lahoz, E., Fernández-Ortuño, D., & Vitale, A. (2018). In vitro and in vivo activity of QoI fungicides against Colletotrichum gloeosporioides causing fruit anthracnose in Citrus sinensis. Scientia Horticulturae, 236, 90–95. https://doi.org/10.1016/j.scienta.2018.03.044
Rodrigues Marques, J. P., Bellato Spósito, M., Amorim, L., Sgarbiero Montanha, G., Silva Junior, G. J., Pereira de Carvalho, H. W., & Appezzato-da-Glória, B. (2020). Persistent calyxes in postbloom fruit drop: A microscopy and microanalysis perspective. Pathogens, 9(4), Article 251. https://doi.org/10.3390/pathogens9040251
Rogers, S. O., & Bendich, A. J. (1989). Extraction of DNA from plant tissues. In S. B. Gelvin, R. S. Schilperoort, & D. P. S. Verma (Eds.), Plant molecular biology manual (pp. 73–83). Springer. https://doi.org/10.1007/978-94-009-0951-9_6
Ruiz-Campos, C., Umaña-Rojas, G., & Gómez-Alpízar, L. (2021). Identificación multilocus de especies de Colletotrichum asociadas a la antracnosis de papaya. Agronomía Mesoamericana, 33(1), Artículo 45495. https://doi.org/10.15517/am.v33i1.45495
Sáenz Pérez, C. A., Osorio Hernández, E., Estrada Drouaillet, B., Poot Poot, W. A., Delgado Martínez, R., & Rodríguez Herrera, R. (2019). Principales enfermedades en cítricos. Revista Mexicana de Ciencias Agrícolas, 10(7), 1653–1665. https://doi.org/10.29312/remexca.v10i7.1827
Salazar, E., Hernández, R., Tapia, A., & Gómez-Alpízar, L. (2012). Identificación molecular del hongo Colletotrichum spp., aislado de banano (Musa spp) de altura en la zona de Turrialba y determinación de su sensibilidad a fungicidas poscosecha. Agronomía Costarricense, 36(1), 53–68. https://doi.org/10.15517/RAC.V36I1.9964
Santamaría Basulto, F., Días Plaza, R., Gutiérrez Alonso, O., Santamaría Fernandez, J., & Larqué Saavedra, A. (2011). Control de dos especies de Colletotrichum causantes de antracnosis en frutos de papaya maradol. Revista Mexicana de Ciencias Agrícolas, 2(5), 631–643. https://doi.org/10.29312/remexca.v2i5.1614
Savi, D. C., Jnoski Rossi, B., Rodrigues Rossi, G., Santos Ferreira-Maba, L., Bini, I. H., da Silva Trindade, E., Goulin, E. H., Machado, M. A., & Glienke, C. (2019). Microscopic analysis of colonization of Colletotrichum abscissum in citrus tissues. Microbiological Research, 226, 27–33. https://doi.org/10.1016/j.micres.2019.05.005
Schiller, M., Lübeck, M., Sundelin, T., Campos Melendez, L. F., Danielsen, S., Funk Jensen, D., & Madriz Ordenana, K. (2006). Two subpopulations of Colletotrichum acutatum are responsible for anthracnose in strawberry and leatherleaf fern in Costa Rica. European Journal of Plant Pathology, 116, 107–118. https://doi.org/10.1007/s10658-006-9045-0
Sharma, G., Maymon, M., & Freeman, S. (2017). Epidemiology, pathology, and identification of Colletotrichum including a novel species associated with avocado (Persea americana) anthracnose in Israel. Scientific Reports, 7, Article 15839. https://doi.org/10.1038/s41598-017-15946-w
Silva, A. O., Savi, D. C., Gomes, F. B., Gos, F. M. W. R., Silva Jr, G. J., & Glienke, C. (2017). Identification of Colletotrichum species associated with postbloom fruit drop in Brazil through GAPDH sequencing analysis and multiplex PCR. European Journal of Plant Pathology, 147, 731–748. https://doi.org/10.1007/s10658-016-1038-z
Šišić, A., Baćanović-Šišić, J., Al-Hatmi, A. M. S., Karlovsky, P., Ahmed, S. A., Maier, W., Sybren de Hoog, G., & Finckh, M. R. (2018). The ‘forma specialis’ issue in Fusarium: a case study in Fusarium solani f. sp. pisi. Scientific Reports, 8, Article 1252. https://doi.org/10.1038/s41598-018-19779-z
Timmer, L. W., & Peres, N. A. (2015). Where have all the flowers gone? Postbloom fruit drop of citrus in the Americas. Journal of Citrus Pathology, 2(1), Article 28302. https://doi.org/10.5070/C421028302
Torres-Calzada, C., Tapia-Tussell, R., Higuera-Ciapara, I., Martin-Mex, R., Nexticapan-Garcez, A., & Perez-Brito, D. (2015). Sensitivity of Colletotrichum truncatum to four fungidices and characterization of thiabendazole-resistan isolates. Plant Disease, 99(11), 1590–1595. https://doi.org/10.1094/PDIS-11-14-1183-RE
United States Department of Agriculture. (2020, December 15th). Citrus Annual. https://bit.ly/3I27GOE
Wharton, P. S., & Diéguez-Uribeondo, J. (2004). The biology of Colletotrichum acutatum. Anales del Jardín Botánico de Madrid, 61(1), 3–22. https://doi.org/10.3989/ajbm.2004.v61.i1.61
White, T. J., Bruns, T., Lee, S., & Taylor, J. (1990). Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In M. A. Innis, S. H. Gelfand, J. J. Sninsky, & T. J. White (Eds.), PCR protocols: A guide to methods and applications (pp. 315–322). Academic Press, New York. http://doi.org/10.1016/B978-0-12-372180-8.50042-1
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