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Colletotrichum species causing anthracnose disease on avocado fruit in Taiwan

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Abstract

Anthracnose disease caused by Colletotrichum spp. is a limiting factor in avocado production worldwide. In Taiwan, Colletotrichum spp. cause post-harvest disease on avocado and greatly reduce the shelf life of the fruit. The aim of this study was to identify the species causing avocado anthracnose in Taiwan and characterize their pathogenicity. In this study, mature avocado fruits with brown lesions were collected from 13 orchards in avocado production areas in Taiwan from 2008 to 2010 and from 2019 to 2020. Eighty-seven Colletotrichum isolates were isolated from the lesions of avocado fruits. Eighty-six isolates were assigned to the Colletotrichum gloeosporioides species complex according to the Apn2-Mat1-2 intergenic spacer and partial mating type (Mat1-2) gene (ApMat) sequence. A preliminary phylogenetic analysis based on ApMat sequences indicated that the 86 isolates formed four clades, C1 to C4. A multi-gene phylogeny based on partial actin, calmodulin, chitin synthase (CHS), GAPDH, ribosomal internal transcribed spacer, and beta-tubulin (TUB) sequences further confirmed the species in the four clades, namely Colletotrichum fructicola (C1), Colletotrichum siamense (C2 and C4), and Colletotrichum tropicale (C3). One isolate, Col-735, was identified to be Colletotrichum eriobotryae according to a phylogenetic tree constructed with the CHS, GAPDH, and TUB sequences. Pathogenicity tests on wounded ‘Choquette’ and ‘Zhongpu green peel’ avocado fruits showed the above four Colletotrichum species were pathogenic on these fruits. This is the first report studying Colletotrichum species and their pathogenicity on avocado in Taiwan, and C. eriobotryae is reported as an avocado fruit pathogen for the first time.

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References

  • Cabral, A., Azinheira, H. G., Talhinhas, P., Batista, D., Ramos, A. P., Silva, M. d. C., Oliveira, H., & Várzea, V. (2020). Pathological, morphological, cytogenomic, biochemical and molecular data support the distinction between Colletotrichum cigarro comb. et stat. nov. and Colletotrichum kahawae. Plants, 9, 502.

  • Cao, X. R., Xu, X. M., Che, H. Y., West, J. S., & Luo, D. Q. (2019). Characteristics and distribution of Colletotrichum species in coffee plantations in Hainan, China. Plant Pathology, 68, 1146–1156.

    Article  CAS  Google Scholar 

  • Carbone, I., & Kohn, L. M. (1999). A method for designing primer sets for speciation studies in filamentous ascomycetes. Mycologia, 91, 553–556.

    Article  CAS  Google Scholar 

  • Cheng, B. P., Huang, Y. H., Song, X. B., Peng, A. T., Ling, J. F., & Chen, X. (2013). First Report of Colletotrichum siamense causing leaf drop and fruit spot of Citrus reticulata Blanco cv. Shiyue Ju in China. Plant Disease, 97, 1508.

  • Chung, P. C., Wu, H. Y., Wang, Y. W., Ariyawansa, H. A., Hu, H. P., Hung, T. H., Tzean, S. S., & Chung, C. L. (2020). Diversity and pathogenicity of Colletotrichum species causing strawberry anthracnose in Taiwan and description of a new species, Colletotrichum miaoliense sp. nov. Scientific Report, 10(1), 14664.

  • Damm, U., Cannon, P. F., Woudenberg, J. H. C., & Crous, P. W. (2012). The Colletotrichum acutatum species complex. Studies in Mycology, 73, 37–113. https://doi.org/10.3114/sim0010

  • Damm, U., Sun, Y. C., & Huang, C. J. (2020). Colletotrichum eriobotryae sp. nov. and C. nymphaeae, the anthracnose pathogens of loquat fruit in central Taiwan, and their sensitivity to azoxystrobin. Mycological Progress, 19, 367–380.

    Article  Google Scholar 

  • De Silva, D. D., Groenewald, J. Z., Crous, P. W., Ades, P. K., Nasruddin, A., Mongkolporn, O., & Taylor, P. W. J. (2019). Identification, prevalence and pathogenicity of Colletotrichum species causing anthracnose of Capsicum annuum in Asia. IMA Fungus, 10, 8.

    Article  PubMed  PubMed Central  Google Scholar 

  • Dreistadt, S. H. (2008). Integrated pest management for avocados. University of California.

    Google Scholar 

  • Echeverrigaray, S., Scariot, F. J., Fontanella, G., Favaron, F., Sella, L., Santos, M. C., Schwambach, J., Pedrotti, C., & Delamare, A. P. L. (2020). Colletotrichum species causing grape ripe rot disease in Vitis labrusca and V. vinifera varieties in the highlands of southern Brazil. Plant Pathology, 69(8), 1504–1512.

  • FAO. (2020). Major tropical fruits - preliminary market results 2019. Rome: Food and Agriculture Organization of the United Nation. https://www.fao.org/3/ca7566en/ca7566en.pdf

  • Freeman, S., Katan, T., & Shabi, E. (1996). Characterization of Colletotrichum gloeosporioides isolates from avacado and almond fruits with molecular and pathogenicity tests. Applied Environmental Microbiology, 62, 1014–1020.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fu, D. D., Wang, W., Qin, R. F., Zhang, R., Sun, G. Y., & Gleason, M. L. (2013). Colletotrichum fructicola, first record of bitter rot of apple in China. Mycotaxon, 126, 23–30.

    Article  Google Scholar 

  • Fuentes-Aragón, D., Silva-Rojas, H. V., Guarnaccia, V., Mora-Aguilera, J. A., Aranda-Ocampo, S., Bautista-Martínez, N., & Téliz-Ortíz, D. (2020). Colletotrichum species causing anthracnose on avocado fruit in Mexico: Current status. Plant Pathology, 69, 1513–1528.

    Article  Google Scholar 

  • Gardes, M., & Bruns, T. D. (1993). ITS primers with enhanced specificity for basidiomycetes–application to the identification of mycorrhizae and rusts. Molecular Ecology, 2, 113–118.

    Article  CAS  PubMed  Google Scholar 

  • Giblin, F. R., Tan, Y. P., Mitchell, R., Coates, L. M., Irwin, J. A. G., & Shivas, R. G. (2018). Colletotrichum species associated with pre- and post-harvest diseases of avocado and mango in eastern Australia. Australasian Plant Pathology., 47(3), 269–276.

    Article  CAS  Google Scholar 

  • Glass, N. L., & Donaldson, G. C. (1995). Development of primer sets designed for use with the PCR to amplify conserved genes from filamentous ascomycetes. Applied and Environmental Microbiology, 61, 1323–1330.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guarnaccia, V., Vitale, A., Cirvilleri, G., Aiello, D., Susca, A., Epifani, F., Perrone, G., & Polizzi, G. (2016). Characterisation and pathogenicity of fungal species associated with branch cankers and stem-end rot of avocado in Italy. European Journal Plant Pathology, 146, 963–976.

    Article  CAS  Google Scholar 

  • Han, Y. C., Zeng, X. G., Xiang, F. Y., Ren, L., Chen, F. Y., & Gu, Y. C. (2016). Distribution and characteristics of Colletotrichum spp. associated with anthracnose of strawberry in Hubei, China. Plant Disease, 100(5), 996–1006.

  • Hofer, K. M., Braithwaite, M., Braithwaite, L. J., Sorensen, S., Siebert, B., Pather, V., Goudie, L., Williamson, L., Alexander, B. J. R, & Toome-Heller, M. (2021). First report of Colletotrichum fructicola, C. perseae, and C. siamense causing anthracnose disease of avocado (Persea americana) in New Zealand. Plant Disease, 105, 1564.

  • Kalyaanamoorthy, S., Minh, B. Q., Wong, T. K. F., von Haeseler, A., & Jermiin, L. S. (2017). ModelFinder: Fast model selection for accurate phylogenetic estimates. Nature Methods, 14, 587–589.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kwon, J. H., Choi, O., Lee, Y., Kim, S., Kang, B., & Kim, J. (2020). Anthracnose on postharvest avocado caused by Colletotrichum kahawae subsp. ciggaro in South Korea. Canadian Journal of Plant Pathology, 42, 508–513.

    Article  Google Scholar 

  • Larkin, M. A., Blackshields, G., Brown, N. P., Chenna, R., & McGettigan, P. A. (2007). Clustal W and Clustal X v. 2.0. Bioinformatics, 23, 2947–2948.

    Article  CAS  PubMed  Google Scholar 

  • Lee, D. M., Hassan, O., Kim, C. H., & Chang, T. (2020). First report of anthracnose of peach (Prunus persica) caused by Colletotrichum fructicola in Korea. Plant Disease, 104, 1556.

    Article  Google Scholar 

  • Li, M., Feng, W., Yang, J., Gao, Z., Zhang, Z., Zhang, W., Wang, S., Wang, W., Gong, D., & Hu, M. (2022). First report of anthracnose caused by Colletotrichum siamense on avocado fruits in China. Crop Protection, 155, 105922.

    Article  CAS  Google Scholar 

  • Lin, S. R., Yu, S. Y., Chang, T. D., Lin, Y. J., Wen, C. J., & Lin, Y. H. (2021). First report of anthracnose caused by Colletotrichum fructicola on tea in Taiwan. Plant Disease, 105, 710–710.

    Article  Google Scholar 

  • Liu, F., Weir, B. S., Damm, U., Crous, P. W., Wang, Y., Liu, B., Wang, M., Zhang, M., & Cai, L. (2015). Unravelling Colletotrichum species associated with Camellia: Employing ApMat and GS loci to resolve species in the C. gloeosporioides complex. Persoonia, 35, 63–86.

    Article  PubMed  PubMed Central  Google Scholar 

  • Menge, J. A., & Pleotz, R. C. (2003). Disease of avocado. In R. C. Ploetz (Ed.), Disease of tropical fruit crops (pp. 35–72). CABI Publishing.

    Chapter  Google Scholar 

  • Mo, J., Zhao, G., Li, Q., Solangi, G. S., Tang, L., Guo, T., Huang, S., & Hsiang, T. (2018). Identification and characterization of Colletotrichum species associated with mango anthracnose in Guangxi, China. Plant Disease, 102, 1283–1289.

    Article  CAS  PubMed  Google Scholar 

  • Munir, M., Amsden, B., Dixon, E., Vaillancourt, L., & Ward Gauthier, N. A. (2016). Characterization of Colletotrichum species causing bitter rot of apple in Kentucky orchards. Plant Disease, 100, 2194–2203.

    Article  CAS  PubMed  Google Scholar 

  • Nguyen, L. T., Schmidt, H. A., von Haeseler, A., & Minh, B. Q. (2015). IQ-TREE: A fast and effective stochastic algorithm for estimating maximum likelihood phylogenies. Molecular Biology and Evolution, 32, 268–274.

    Article  CAS  PubMed  Google Scholar 

  • Ni, H. F., Huang, C. W., Wu, C. J., Yang, H. R., Lin, C. Y., Chang, J. Y., & Chang, J. W. (2017). First report of pepper spot disease of lychee caused by Colletotrichum siamense in Taiwan. Journal of Plant Pathology, 99, 799.

    Google Scholar 

  • Nirenberg, H. I. (1981). A simplified method for identifying Fusarium spp. occurring on wheat. Canadian Journal of Botany, 59, 1599–1609.

    Article  Google Scholar 

  • 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, 103–116.

    Article  PubMed  Google Scholar 

  • Oo, M. M., Yoon, H. Y., Jang, H. A., & Oh, S. K. (2018). Identification and characterization of Colletotrichum species associated with bitter rot disease of apple in South Korea. The Plant Pathology Journal, 34, 480–489.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Phoulivong, S., Cai, L., Chen, H., McKenzie, E. H. C., Abdelsalam, K., Chukeatirote, E., & Hyde, K. D. (2010). Colletotrichum gloeosporioides is not a common pathogen on tropical fruits. Fungal Diversity, 44, 33–43.

    Article  Google Scholar 

  • Posada, D. (2008). jModelTest: Phylogenetic model averaging. Molecular Biology and Evolution, 25, 1253–1256.

    Article  CAS  PubMed  Google Scholar 

  • Rodriguez-Palafox, E. E., Vasquez-Lopez, A., Marquez-Licona, G., Lima, N. B., Lagunes-Fortiz, E., & Tovar-Pedraza, J. M. (2021). First report of Colletotrichum siamense causing anthracnose of guava (Psidium guajava) in Mexico. Plant Disease, 105, 3290.

    Article  Google Scholar 

  • Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D., & Darling, A. (2012). MrBayes v. 3.2: Efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology, 61, 539–542.

    Article  PubMed  PubMed Central  Google Scholar 

  • Serrato-Diaz, L. M., Marino, Y. A., Guadalupe, I., Bayman, P., and Goenaga, R. (2020). First report of Lasiodiplodia pseudotheobromae and Colletotrichum siamense causing cacao pod rot, and first report of C. tropicale causing cacao pod rot in Puerto Rico. Plant Disease, 104, 592.

  • 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 Report, 7, 15839.

    Article  Google Scholar 

  • Silva, D., Talhinhas, P., Várzea, V., Cai, L., Paulo, O., & Batista, D. (2011). Application of the Apn2/MAT locus to improve the systematics of the Colletotrichum gloeosporioides complex: An example from coffee (Coffea spp.) hosts. Mycologia, 104, 396–409.

    Article  PubMed  Google Scholar 

  • Templeton, M. D., Rikkerink, E. H. A., Solon, S. L., & Crowhurst, R. N. (1992). Cloning and molecular characterization of the glyceraldehyde-3-phosphate dehydrogenase encoding gene and cDNA from the plant pathogenic fungus Glomerella cingulata. Gene, 122, 225–230.

    Article  CAS  PubMed  Google Scholar 

  • Tzeng, S. S., Tzeng, K. C., Chang, C. A., Tsai, T. T., & Yen, H. F. (2019). List of plant diseases in Taiwan (5th ed.). Taiwan Phytopathology Society.

    Google Scholar 

  • Uysal, A., & Kurt, S. (2020a). First report of Colletotrichum siamense causing anthracnose on banana fruits in Turkey. Journal Plant Pathology, 102, 967.

    Article  Google Scholar 

  • Uysal, A., & Kurt, S. (2020b). First report of fruit and leaf anthracnose caused by Colletotrichum karstii on avocado in Turkey. Crop Protection, 133, 105145.

    Article  CAS  Google Scholar 

  • Vaidya, G., Lohman, D. J., & Meier, R. (2011). SequenceMatrix: Concatenation software for the fast assembly of multi-gene datasets with character set and codon information. Cladistics, 27, 171–180.

    Article  PubMed  Google Scholar 

  • Weir, B. S., Johnston, P. R., & Damm, U. (2012). The Colletotrichum gloeosporioides species complex. Studies in Mycology, 73, 115–180.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • White, T. J., Bruns, T., Lee, S., & Taylor, J. W. (1990). Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In M. A. Innis, D. H. Gelfand, J. J. Sninsky, & T. J. White (Eds.), PCR Protocols: A Guide to Methods and Applications (pp. 315–322). Academic Press.

    Google Scholar 

  • Wu, C. J., Chen, H. K., & Ni, H. F. (2020). Identification and characterization of Colletotrichum species associated with mango anthracnose in Taiwan. European Journal of Plant Pathology, 157, 1–15.

    Article  CAS  Google Scholar 

  • Zhang, Y., Sun, W., Ning, P., Guo, T., Huang, S., Tang, L., Li, Q., & Mo, J. (2021). First report of anthracnose of papaya (Carica papaya) caused by Colletotrichum siamense in China. Plant Disease, 105, 2252.

    Article  Google Scholar 

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This research was funded by Taiwan Agricultural Research Institute.

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  1. Department of Plant Protection, Chiayi Agricultural Experiment Branch, Taiwan Agricultural Research Institute, Chiayi, Taiwan

    Chao-Jung Wu, Miao-Chun Lin & Hui-Fang Ni

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Wu, CJ., Lin, MC. & Ni, HF. Colletotrichum species causing anthracnose disease on avocado fruit in Taiwan. Eur J Plant Pathol 165, 629–647 (2023). https://doi.org/10.1007/s10658-022-02635-2

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