Abstract
Anthracnose is the most limiting disease in mango crops in the department of Magdalena (Colombia), causing crop losses between 40 and 50%; worldwide, losses in the field of up to 51% of the crop have been reported and between 20 and 30% in postharvest. The causal agent, Colletotrichum spp., has a hemibiotrophic lifestyle, initially does not induce symptoms in its host, but later it changes to a necrotrophic stage. Endophytism is a lifestyle of Colletotrichum, but its role in pathogenicity is still uncertain, which led us to characterize endophytic isolates of Colletotrichum spp. from leaves and branches of mango, cultivar Azúcar, from a crop located in Ciénaga (Magdalena). The prevalence of the isolates in leaves and branches was determined considering three strata of the tree using three extraction protocols: (1) Chlorine chamber; (2) 4% sodium hypochlorite, and (3) 2% sodium hypochlorite. Morphometric descriptions included the colony, the conidia, and the appressoria. We tested pathogenicity in fruits and carried out the molecular identification of the most pathogenic isolates. We obtained nine endophytic isolates, eight in leaves and one in branches. The best extraction (18.2%) protocol was the one using 2% sodium hypochlorite. The highest prevalence was found in the upper strata of the tree (10% of the samples) and in the leaves (8.9% of the samples). The endophytic strains induced lesions diameter between 0,65-19,7 mm in diameter in fruits. The most virulent strain (HP3A-4) was identified as C. tropicale by molecular techniques. This is the first report in Colombia of this fungus acting as pathogenic endophyte on mango. The present study indicated that it is possible to find Colletotrichum as an endophyte in mango leaves and branches, which can cause infection when inoculated in fruits and evidences its high hidden inoculum potential for the development of anthracnosis. © 2019. Acad. Colomb. Cienc. Ex. Fis. Nat.
References
Afanador-Kafuri, L., Minz, D., Maymon, M., Freeman, S. (2003). Characterisation of Colletotrichum isolates from tamarillo, passiflora, and mango in Colombia and identification of a unique species from the genus. Phytopathology. 93: 579-587.
Afanador-Kafuri, L., González, A., Gañan, L., Mejía, J. F., Cardona, N., Álvarez, E. (2014). Characterization of the Colletotrichum species causing anthracnose in Andean blackberry in Colombia. Plant Disease. 98 (11): 1503-1513.
Arauz, L. (2000). Mango anthracnose: Economic impact and current options for integrated management. Plant Disease. 84:600‐608.
Akem, C.N. (2006). Mango anthracnose disease: Present status and future research priorities. Plant Pathology Journal. 5(3): 266‐273.
Arnold, E., Henk, D., Eells, R., Vilgalys, R. (2007). Diversity and phylogenetic affinities of foliar fungal endophytes in loblolly pine inferred by culturing and environmental PCR. Mycologia, 99(2). 33: 185-206.
Cannon, P. & Simmons, C. (2002). Diversity and host preference of leaf endophytic fungi in the Iwokrama Forest Reserve, Guyana. Mycologia, 94(2). 33: 210-220.
Cannon, P. F., Damm, U., Johnston, P. R., Weir, B. S. (2012). Colletotrichum–current status and future directions. Studies in mycology. 73: 181-213.
Cai, L., Hide, K. D., Taylor, P. W. J., Weir, B. S., Waller, J., Abang, M. M., Zhang, J. Z., Yang, Y. L., Phoulivong, S., Liu, Z. Y., Prihastuti, H., Shivas, R. G., Mckenzie, E. H. C., Jhonston, P. R. (2009). A polyphasic approach for studying Colletotrichum. Fungal Diversity. 39: 183-204.
Cartagena, J. & Vega, D. (2001) Fruticultura colombiana. El Mango. Manual de asistencia técnica Nº 43. ICA, Sección Nacional de Frutícolas. p.124.
Carrol, G. (1988). Fungal endophytes in stems and leaves: From latent pathogen to mutualistic symbiont. Ecology. 69: 2-9.
Chiangsin, R., Wanichkul, K., Guest, D. I., Sangchote, S. (2016). Reduction of anthracnose on ripened mango fruits by chemicals, fruit bagging, and postharvest treatments. Australasian Plant Pathology. 45 (6): 629-635.
Chonhenchob, V., Kamhangwong, D., Kruenate, J., Khongrat, K., Tangchantra, N., Wichai, U., Singh, S.P. (2011). Preharvest bagging with wavelength-selective materials enhances development and quality of mango (Mangifera indica L.) cv. Nam Dok Mai #4. J Sci Food Agric. 91: 664-671.
Damm, U., Cannon, P., Woudenberg, J., Crous, P. (2012). The Colletotrichum acutatum species complex. Studies in mycology. 73: 37-113.
Damm, U., Baroncelli, R., Cai, L., Kubo, Y., O’Connell, R., Weir, B., ... Cannon, P. F. (2010). Colletotrichum: Species, ecology and interactions. IMA fungus. 1 (2): 161-165.
De Silva, D., Crous, P., Ades, P., Hyde, K., Taylor, P. (2017). Life styles of Colletotrichum and implications for plants biosecurity. British Mycological Society. 31: 155-168.
Delaye, L., García-Guzmán, G., Heil, M. (2013). Endophytes versus biotrophic and necrotrophic pathogens—are fungal lifestyles evolutionarily stable traits. Fungal Diversity. 60(1): 125-135.
Dinh, S. Q. (2002). Post-harvest loss of mango due to anthracnose and its infection biology and resistance of mango to the disease. Kasetsart University. p. 2-70.
Dodd, J., Estrada, A., Matcham, J., Jeffries, P. (1991). The effect of climatic factors on Colletotricum gloeosporioides, causal agent of mango anthracnose, in the Philippines. Plant Pathology. 12: 568-575.
Doyle, V.P., Oudemans, P.V., Rehner, S.A., Litt, A. (2013) Habitat and host indicate lineage identity in Colletotrichum gloeosporioides s. l. from wild and agricultural landscapes in North America. PLoS One 8:e62394.
Freeman, S., Katan, T., Shabi, E. (1998). Characterization of Colletotrichum species responsible for anthracnose diseases of various fruits. Plant Disease. 82: 596-605.
Freeman, S., Horowitz, S., Sharon, A. (2001). Pathogenic and Nonpathogenic Lifestyles in Colletotrichum acutatum from Strawberry and Other Plants. Phytopathology. 91:986-991.
Gañán, L., Álvarez, E., Zapata, J. C. (2015). Identificación genética de aislamientos de Colletotrichum spp. causantes de antracnosis en frutos de aguacate, banano, mango y tomate de árbol. Revista de la Academia Colombiana de Ciencias Exactas, Físicas y Naturales. 39 (152): 339-347.
Gañán, L. (2014). Identificación taxonómica de aislamientos de Colletotrichum spp., asociados con la antracnosis de frutas tropicales en Colombia mediante análisis filogenético multilocus. Tesis, Magister en Fitopatología, Facultad de Ciencias Agropecuarias, Universidad de Caldas. Manizales. Colombia. p. 26-27.
Gamboa, M. & Bayman, P. (2001). Communities of Endophytic Fungi in Leaves of a Tropical Timber Tree (Guarea Guidonia: Meliaceae). Biotropica. 33 (2): 352-360.
Gamboa, M. (2006). Hongos endófitos tropicales: conocimiento actual y perspectivas. Acta Biológica Colombiana. 11: 3-20.
Hernández, P., Arangurenb, M., Reigc, C., Fernández, D., Mesejoc, C., Martínez, A., Galán, V., Agustí, M. (2011).
Phenological growth stages of mango (Mangifera indica L.) according to the BBCH scale. Scientia Horticulturae. 130:536-540.
Higgins, K., Arnold, A., Coley, P., Kusar, T. (2014). Communities of fungal endophytes in tropical forest grasses: highly diverse host – and hábitat generalists characterized by strong spatial structure. Fungal Ecology. 8: 1-1.
Hyde, K. & Soytong, K. (2008). The fungal endophyte dilemma. Fungal Diversity. 33: 163-173.
Hofman, P. J., Smith, L. G., Joyce, D. C., Johnson, G. I., Meiburg, G. F. (1997). Bagging of mango (Mangifera indica cv.Keitt’) fruit influences fruit quality and mineral composition. Postharvest Biology and Technology. 12 (1): 83-91.
Hyde, K. D., Cai, L., McKenzie, E. H. C., Yang, Y. L., Zhang, J. Z., Prihastuti, H. (2009). Colletotrichum: A catalogue of confusion. Fungal Diversity. 39 (1): 1-17.
Ismail, A. M., Cirvilleri, G., Yaseen, T., Epifani, F., Perrone, G., Polizzi, G. (2015). Characterisation of Colletotrichum species causing anthracnose disease of mango in Italy. Journal of Plant Pathology. 97 (1): 167-171.
Jaber, R. & Salem, M. (2014). Endophyte colonization of squash by the fungal entomopathogen Beauveria bassiana (Ascomycota: Hypocreales) for managing zucchini yellow mosaic virus in cucurbits. Biocontrol science and technology. 24: 1096-1109.
Kamle, M., Kumar, P. (2016). Colletotrichum gloeosporioides: Pathogen of Anthracnose Disease in Mango (Mangifera indica L.). In Current Trends in Plant Disease Diagnostics and Management Practices. Springer, Cham. p. 207-219.
Larran, S., Mónaco, C., Alippi, H. (2001). Endophytic fungi in leaves of lycopersicon esculentum Mill. World Journal of Microbiology & Biotechnology. 17: 181-184.
Lima, N., Batista, M., De Morais Jr, M., Barbosa, M., Michereff, S., Hyde, K., Camara, M. (2013). Five Colletotrichum species are responsible for mango anthracnose in northeastern Brazil. Fungal Diversity. 61: 81-86.
Lu, G., Cannon, P., Reid, A., Simmons, C. (2004). Diversity and molecular relationships of endophytic Colletotrichum isolates from the Iwokrama Forest Reserve, Guyana. Mycological Research. 108 (1): 53-63.
Mariano, R., Fernández De Lira, R., Barbosa Da Silveira, E., Menezes, M. (1997). Levantamento de fungos endofíticos e epifíticos em folhas de coqueiro no nordeste do Brasil. I. Freqüência da populaçao fúngica e efeito da hospedeira. Agrotrópica. 9: 127-134.
Marshall, D., Tunali, B., Nelson, R. (1999). Occurrence of fungal endophytes in species of wild triticum. Crop Science Society of American. 39: 1507-1512.
Morales, V. & Rodríguez, M. (2009). Microbiota endofítica asociada al cultivo del mango “Haden” (Mangifera indica L.) en el oriente de Venezuela. En Revista UDO Agrícola. 9(2): 396-398.
Morales, V. & Rodríguez, M. (2006). Hongos endófitos en plantaciones de mango “Haden” de la planicie de Maracaibo, Venezuela. Instituto Nacional de Investigaciones Agrícolas (INIA), Maracaibo, Venezuela. Rev. Fac. Agron. (LUZ).23: 273-282.
Murphy, R., Doohan, M., Hodkinson, R. (2015). Persistentfungal root endophytes isolate from a wild barley species suppress seed-borne infections in a barley cultivar. Bio-Control. 60: 281-292.
Osorio, J., Martínez, E., Hio, J., Aguirre, J. (2009). Estudios de epidemiología y control no convencional de la antracnosis del mango. Informe Técnico Corpoica. Colombia. p 17.
Otero, T., Ackerman, D., Bayman, P. (2002). Diversity and host specificity of endophytic Rhizoctonia – Like fungi from Tropical Orchids. Am J Bot. 89: 1852-1858.
Páez, A. (2018). Diversidad de endófitos en mango cultivar Azúcar. Tesis de doctorado. En proceso.
Páez, A. (2003). Tecnologías sostenibles para el manejo de la antracnosis en papaya y mango. Boletín Técnico Nº 8. CORPOICA. p. 1-18.
Páez, A. (1997). Respuesta de cultivares de mango (Magnifera indica L.) a la antracnosis en la Costa Atlántica colombiana. Corpoica Ciencia y Tecnología Agropecuaria. 2: 45-53.
Pardo‐De la Hoz, C. J., Calderón, C., Rincón, A. M., Cárdenas, M., Danies, G., López‐Kleine, L., ..., Jiménez, P. (2016).
Species from the Colletotrichum acutatum, Colletotrichum boninense and Colletotrichum gloeosporioides species complexes associated with tree tomato and mango crops in Colombia. Plant Pathology. 65 (2): 227-237. Doi: 10.1111/ppa.12410.
Pavitra Kumari, R. & Singh, R. (2017). Anthracnose of mango incited by Colletotrichum gloeosporioides: A comprehensive review. Int. J. Pure App. Biosci. 5 (1): 48-56.
Petrini, O. (1991). Fungal Endophytes of Tree Leaves. Microbial Ecology of Leaves. Microbial Ecology of Leaves (J. Andrews & S. Hirano, eds). p. 179-197.
Ploetz, R. (2003). Diseases of Mango. pp. 327‐363. In: R.C. Ploetz (ed.) Diseases of Tropical Fruit Crops. CABI Publishing. Wallingford, UK. p. 544.
Photita, W., Lumyong, S., Lumyong, P., Mckenzie, E.H.C., Hyde, K.D. (2004). Are some endophytes of Musa acuminata latent pathogens? Fungal Diversity. 16: 131-140.
Phoulivong, S., Cai, L., Chen, H., McKenzie, E. H., Abdelsalam, K., Chukeatirote, E., Hyde, K. D. (2010). Colletotrichum gloeosporioides is not a common pathogen on tropical fruits. Fungal Diversity. 44 (1): 33-43.
Prusky, D. & Lichter, A. (2007). Activation of quiescent infections by postharvest pathogens during transition from the biotrophic to the necrotrophic stage. FEMS Microbiology Letters. 268 (1):1-8. Doi: http://dx.doi.org/10.1111/j.1574-6968.2006.00603.x
Prihastuti, H., Cai, L., Chen, H., McKenzie, E.H.C., Hyde, K.D. (2009). Characterization of Colletotrichum species associated with coffee berries in northern Thailand. Fungal Diversity. 39: 89-109.
Prusky, D., Alkan, N., Mengiste, T., Fluhr, R. (2013). Quiescent and necrotrophic lifestyle choice during postharvest disease development. Annual Review of Phytopathology. 51:155-176. Doi: 10.1146/annurev-phyto-082712-102349
Rojas, E., Rehner, S., Samuels, G., Van Bael, S., Herre, E., Cannon, P., Chen, R., Pang, J., Wang, R., Zhang, Y., Peng, Y., Sha, T. (2010). Colletotrichum gloeosporoides s.l. associated with Theobroma cacao and othbbbbber plants in Panamá: Multilocus phylogenenies distinguish host-associated pathogens from asymptomatic endophytes.Mycology. 102 (6):1328-1338.
Rubini, M., Silva-Ribeiro, R., Pomella, A., Maki, C., Welington L. Araújo, W., Deise R. dos Santos, D., Azevedo, J. (2005). Diversity of endophytic fungal community of cacao (Theobroma cacao L.) and biological control of Crinipellis perniciosa, causal agent of Witches’ Broom Disease. International Journal of Biological Sciences. 1: 24-33.
Ruiz, C. M., Gutiérrez, L. G., Umaña, G. (2003). Caracterización morfológica y bioquímica de aislamientos de Colletotrichum spp. y su patogenicidad en mango (Mangifera indica L.). Tecnología en Marcha. 16 (1): 55-65.
Sangeetha, C. & Rawal, R. (2008). Nutritional studies of Colletotrichum gloeosporioides (Penz.) Penz. & Sacc. The Incitant of Mango Anthracnose. World Journal of Agricultural Sciences. 4 (6): 717-720.
Schena, L., Nigro, F., Pentimone, I., Ligorio, A., Ippolot, A. (2003). Control of postharvest rots of sweet cherries and table grapes with endophytic isolates of Aureobasidium pullulans. Postharvest biology technology. 30: 209-220.
Scot, N. (2008). Mango anthracnose (Colletotrichum gloeosporoides). University of Hawai. Departament of Plan and Environmental Protection Sciences. p. 1-7.
Stone, J., Bacon, C., White, J. (2000). An overview of endophytic microbes: Endophytism defined. En: Bacon, C & White, J. Microbial endophytes. New York: Marcel Dekker. p. 3-29.
Taylor, J. W., Jacobson, D. J., Kroken, S., Kasuga, T., Geiser, D. M., Hibbett, D. S., Fisher, M. C. (2000). Phylogeneticspecies recognition and species concepts in fungi. Fungal genetics and biology. 31 (1): 21-32.
Vieira, W., Michereff, S., De Morais Jr, M., Hyde, K., Câmara, M. (2014). Endophytic species of Colletotrichum associated with mango in northeastern Brasil. En. Fungal Divers.67: 181-202.
Watanabe, T. (2010). Pictorials atlas of soil and seed fungi: Morphologies of cultured fungi and key to species. 3rd edition. CRC press. p. 3-385.
Wanderley, I., Costa, L., Cavalcanti, M. (2012). Diversity of leaf endophytic fungi in mangrove plants of northeast Brazil. Brazilian Journal of Microbiology. 43 (3): 1165-1173.
Weir, B.S., Johnston, P.R., Damm U. (2012). The Colletotrichum gloeosporioides species complex. Stud Mycol. 73: 115-180.
Xiang, S. & Liang, D. (2012). Endophytic fungal diversity: Review of traditional and molecular techniques. Mycology.3 (1): 65-76.
Declaration of originality and transfer author's rights
The authors declare:
- The published data and reference materials have been duly identified with their respective credits and have been included in the bibliographic notes and citations that have been so identified and that should it be required, I have all releases and permissions from any copyrighted material.
- All material presented is free from any copyright and that I accept full legal responsibility for any legal claims relating to copyrighted intellectual property, fully exonerating from responsibility the Revista de la Academia Colombiana de Ciencias Exactas, Físicas y Naturales.
- This work is unpublished and will not be sent to any other journal while waiting for the editorial decision of this journal. I declare that there is no conflict of interest in this manuscript.
- In case of publication of this article, all author´s rights are transferred to the Revista de la Academia Colombiana de Ciencias Exactas, Físicas y Naturales, and so cannot be reproduced in any form without the express permission of it.
- By means of this document, if the article is accepted for publication by the Revista de la Academia Colombiana de Ciencias Exactas, Físicas y Naturales, the Revista assumes the right to edit and publish the articles in national and international indices or data bases for academic and scientific use in paper, electronic, CD-ROM, internet form either of the complete text or any other known form known or to be known and non-commercial, respecting the rights of the authors.
Transfer of author rights
In case the article is approved for publication, the main author in representation of himself and his co-authors or the main author and his co-authors must cede the author rights of the corresponding article to the Revista de la Academia Colombiana de Ciencias Exactas, Físicas y Naturales, except in the following cases:
The authors and co-authors will retain the right to revise, adapt, prepare derived works, oral presentations, and distribution to some colleagues of reprints of their own published work, if the corresponding credit is given to the Revista de la Academia Colombiana de Ciencias Exactas, Físicas y Naturales. It is also permissible to publish the title of the work, summary, tables, and figures of the work in the corresponding web sites of the authors or their employers, also giving credit to the Revista.
If the work has been realized under contract, the author’s employer has the right to revise, adapt, prepare derivative works, reproduce, or distribute in hard copy the published work, in a secure manner and for the exclusive use of his employees.
If the Revista de la Academia Colombiana de Ciencias Exactas, Físicas y Naturales were approached for permission by a third party for using, printing, or publishing specifically articles already published, the Revista must obtain the express permission of the author and co-authors of the work or of the employer except for use in classrooms, libraries, or reprinted in a collective work. The Revista de la Academia Colombiana de Ciencias Exactas, Físicas y Naturales reserves the possible use in its front cover of figures submitted with the manuscripts.
No other right, other than the author’s right, can be claimed by the Revista de la Academia Colombiana de Ciencias Exactas, Físicas y Naturales.