DOI QR코드

DOI QR Code

Re-identification of Korean Isolates in the Colletotrichum dematium, C. magnum, C. orchidearum, and C. orbiculare Species Complexes

  • Le Dinh Thao (Korean Agricultural Culture Collection, Agricultural Microbiology Division, National Institute of Agricultural Sciences, Rural Development Administration) ;
  • Hyorim Choi (Korean Agricultural Culture Collection, Agricultural Microbiology Division, National Institute of Agricultural Sciences, Rural Development Administration) ;
  • Donghun Kang (Korean Agricultural Culture Collection, Agricultural Microbiology Division, National Institute of Agricultural Sciences, Rural Development Administration) ;
  • Anbazhagan Mageswari (Korean Agricultural Culture Collection, Agricultural Microbiology Division, National Institute of Agricultural Sciences, Rural Development Administration) ;
  • Daseul Lee (Korean Agricultural Culture Collection, Agricultural Microbiology Division, National Institute of Agricultural Sciences, Rural Development Administration) ;
  • Dong-Hyun Kim (Korean Agricultural Culture Collection, Agricultural Microbiology Division, National Institute of Agricultural Sciences, Rural Development Administration) ;
  • In-Young Choi (Department of Agricultural Biology, Jeonbuk National University) ;
  • Hyeon-Dong Shin (Division of Environmental Science and Ecological Engineering, Korea University) ;
  • Seung-Beom Hong (Korean Agricultural Culture Collection, Agricultural Microbiology Division, National Institute of Agricultural Sciences, Rural Development Administration)
  • Received : 2024.05.24
  • Accepted : 2024.08.01
  • Published : 2024.10.01

Abstract

A large number of species in the genus Colletotrichum have been reported as causal agents of anthracnose on crops and wild plants in Korea. Many Colletotrichum isolates from the country preserved in the Korean Agricultural Culture Collection (KACC) were previously identified based on host plants and morphological characteristics, and it may lead to species misidentification. Thus, accurate fungal species identification using multilocus sequence analyses is essential for understanding disease epidemiology and disease management strategies. In this study, combined DNA sequence analyses of internal transcribed spacer, gapdh, chs-1, his3, act, tub2, and gs were applied to re-identify 27 Colletotrichum isolates in KACC. The phylogenetic analyses showed that the isolates resulted in 11 known species, they belong to the C. dematium species complex (C. hemerocallidis, C. jinshuiense, and C. spinaciae), the C. magnum complex (C. kaifengense and C. cf. ovatense), the C. orchidearum complex (C. cattleyicola, C. plurivorum, C. reniforme, and C. sojae) and the C. orbiculare complex (C. malvarum and C. orbiculare). Of them, C. cattleyicola, C. hemerocallidis, C. kaifengense, and C. reniforme were unrecorded species in Korea. In the view of host-fungus combinations, 10 combinations are newly reported in the world and 12 are new reports in Korea, although their pathogenicity on the host was not confirmed.

Keywords

Acknowledgement

This study was supported by the grant (PJ017286) from the Rural Development Administration and the grant (M3H9A1081254) from the Ministry of Science and ICT in Korea. We are sincerely thankful to Nan-Hee Lee, Seon-Hee Kim, and Eun-Ha Yuk for their laboratory assistance.

References

  1. Boufleur, T. R., Castro, R. R. L., Rogerio, F., Ciampi-Guillardi, M., Baroncelli, R. and Massola Junior, N. S. 2020. First report of Colletotrichum musicola causing soybean anthracnose in Brazil. Plant Dis. 104:1858. 
  2. Boufleur, T. R., Ciampi-Guillardi, M., Tikami, I., Rogerio, F., Thon, M. R., Sukno, S. A., Massola Junior, N. S. and Baroncelli, R. 2021. Soybean anthracnose caused by Colletotrichum species: current status and future prospects. Mol. Plant Pathol. 22:393-409. 
  3. Cannon, P. F., Damm, U., Johnston, P. R. and Weir, B. S. 2012. Colletotrichum: current status and future directions. Stud. Mycol. 73:181-213. 
  4. Carbone, I. and Kohn, L. M. 1999. A method for designing primer sets for speciation studies in filamentous ascomycetes. Mycologia 91:553-556. 
  5. Chikuo, Y., Sugimoto, T. and Endo, T. 1984. Sugar beet anthracnose caused by Colletotrichum dematium f. spinaciae (Ellis et Halst.) v. Arx. Ann. Phytopathol. Soc. Jpn. 50:46-52. 
  6. Correll, J. C., Morelock, T. E., Black, M. C., Koike, S. T., Brandenberger, L. P. and Dainello, F. J. 1994. Economically important diseases of spinach. Plant Dis. 78:653-660. 
  7. Crous, P. W., Groenewald, J. Z., Risede, J.-M., Simoneau, P. and Hywel-Jones, N. L. 2004. Calonectria species and their Cylindrocladium anamorphs: species with sphaeropedunculate vesicles. Stud. Mycol. 50:415-430. 
  8. Dada, A. O., Dania, V. O., Oyatomi, O. A., Abberton, M. and Ortega-Beltran, A. 2023. First report of Colletotrichum cliviicola causing anthracnose disease of cowpea (Vigna unguiculata) in Nigeria. Plant Dis. 107:2254. 
  9. Damm, U., Cannon, P. F., Liu, F., Barreto, R. W., Guatimosim, E. and Crous, P. W. 2013. The Colletotrichum orbiculare species complex: important pathogens of field crops and weeds. Fungal Divers. 61:29-59. 
  10. Damm, U., Sato, T., Alizadeh, A., Groenewald, J. Z. and Crous, P. W. 2019. The Colletotrichum dracaenophilum, C. magnum and C. orchidearum species complexes. Stud. Mycol. 92:1-46. 
  11. Damm, U., Woudenberg, J. H. C., Cannon, P. F. and Crous, P. W. 2009. Colletotrichum species with curved conidia from herbaceous hosts. Fungal Divers. 39:45-87. 
  12. de Silva, D. D., Groenewald, J. Z., Crous, P. W., Ades, P. K., Nasruddin, A., Mongkolporn, O. and Taylor, P. W. J. 2019. Identification, prevalence and pathogenicity of Colletotrichum species causing anthracnose of Capsicum annuum in Asia. IMA Fungus 10:8. 
  13. Diao, Y.-Z., Zhang, C., Liu, F., Wang, W.-Z., Liu, L., Cai, L. and Liu, X.-L. 2017. Colletotrichum species causing anthracnose disease of chili in China. Persoonia 38:20-37. 
  14. Farr, D. F., Rossman, A. Y. and Castlebury, L. A. 2021. United States National Fungus Collections Fungus-Host Dataset. Ag Data Commons. URL https://doi.org/10.15482/USDA.ADC/1524414 [28 December 2023]. 
  15. Fu, M., Crous, P. W., Bai, Q., Zhang, P. F., Xiang, J., Guo, Y. S., Zhao, F. F., Yang, M. M., Hong, N., Xu, W. X. and Wang, G. P. 2019. Colletotrichum species associated with anthracnose of Pyrus spp. in China. Persoonia 42:1-35. 
  16. Glass, N. L. and Donaldson, G. C. 1995. Development of primer sets designed for use with the PCR to amplify conserved genes from filamentous ascomycetes. Appl. Environ. Microbiol. 61:1323-1330. 
  17. Guan, Y. M., Zhang, L. L., Ma, Y. Y., Zhang, Y. and Zhang S. N. 2021. First report of anthracnose of American ginseng caused by Colletotrichum sojae in Northeast China. Plant Dis. 105:3755. 
  18. Guerber, J. C., Liu, B., Correll, J. C. and 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 95:872-895. 
  19. Guo, Z., Luo, C.-X., Wu, H.-J., Peng, B., Kang, B.-S., Liu, L.-M., Zhang, M. and Gu, Q.-S. 2022. Colletotrichum species associated with anthracnose disease of watermelon (Citrullus lanatus) in China. J. Fungi 8:790. 
  20. Han, K. D., Alam, S., Lee, T. S. and Lee, M. W. 2004. Ginseng anthracnose caused by Colletotrichum dematium. Plant Pathol. J. 20:196-199. 
  21. Hassan, O., Kim, J. S., Romain, B. B. N. D. and Chang, T. 2022. An account of Colletotrichum species associated with anthracnose of Atractylodes ovata in South Korea based on morphology and molecular data. PLoS ONE 17:e0263084. 
  22. Hassan, O., Lee, Y. S. and Chang, T. 2019. Colletotrichum species associated with Japanese plum (Prunus salicina) anthracnose in South Korea. Sci. Rep. 9:12089. 
  23. Jayawardena, R. S., Bhunjun, C. S., Hyde, K. D., Gentekaki, E. and Itthayakorn, P. 2021. Colletotrichum: lifestyles, biology, morpho-species, species complexes and accepted species. Mycosphere 12:519-669. 
  24. Jin, M., Yang, C., Yang, L., Cui, L. and Wei, L. 2021. Isolation and identification of a new Colletotrichum species causing anthracnose of Astragalus membranaceus. Crop Prot. 143:105470. 
  25. Kim, C. H., Hassan, O. and Chang, T. 2020. Diversity, pathogenicity, and fungicide sensitivity of Colletotrichum species associated with apple anthracnose in South Korea. Plant Dis. 104:2866-2874. 
  26. Kim, G. H., Choi, D. H., Park, S. Y. and Koh, Y. J. 2018a. First report of anthracnose caused by Colletotrichum nymphaeae on kiwiberry in Korea. Plant Dis. 102:1455. 
  27. Kim, S. J., Ko, E. J., Hong, J. K. and Jeun, Y. C. 2018b. Ultra-structures of Colletotrichum orbiculare in cucumber leaves expressing systemic acquired resistance mediated by Chlorella fusca. Plant Pathol. J. 34:113-120. 
  28. Kim, W. G., Hong, S. K. and Kim, J. H. 2008. Occurrence of anthracnose on Chinese mallow caused by Colletotrichum malvarum. Mycobiology 36:139-141. 
  29. Lee, D. H. 1983. Present status and problems of chemical seed treatment of seedborne disease. Korean J. Plant Prot. 22:130-137. 
  30. Lee, D. M., Hassan, O. and Chang, T. 2020. Identification, characterization, and pathogenicity of Colletotrichum species causing anthracnose of peach in Korea. Mycobiology 48:210-218. 
  31. Lee, S.-Y. and Jung, H.-Y. 2018. Colletotrichum kakivorum sp. nov., a new leaf spot pathogen of persimmon in Korea. Mycol. Prog. 17:1113-1121. 
  32. Lee, S.-Y., Ten, L. N., Ryu, J.-J., Kang, I.-K. and Jung, H.-Y. 2021. Colletotrichum aenigma associated with apple bitter rot on newly bred cv. RubyS Apple. Res. Plant Dis. 27:70-75. 
  33. Liu, F., Ma, Z. Y., Hou, L. W., Diao, Y. Z., Wu, W. P., Damm, U., Song, S. and Cai, L. 2022. Updating species diversity of Colletotrichum, with a phylogenomic overview. Stud. Mycol. 101:1-56. 
  34. Liu, J.-W., Manawasinghe, I. S., Liao, X.-N, Mao, J., Dong, Z.-Y., Jayawardena, R. S., Wanasinghe, D. N., Shu, Y.-X. and Luo, M. 2023. Endophytic Colletotrichum (Sordariomycetes, Glomerellaceae) species associated with Citrus grandis cv. "Tomentosa" in China. MycoKeys 95:163-188. 
  35. Machado, S. C. S., Silva Veloso, J., Camara, M. P. S., Campos, F. S., Damascena, J. F., de Souza Ferreira, T. P., dos Santos, M. M. and dos Santos, G. R. 2022. Occurrence of Colletotrichum musicola causing anthracnose on Manihot esculenta. Plant Dis. 106:2758. 
  36. Nam, M. H., Park, M. S., Yoo, J. H., Lee, B. J. and Lee, J. N. 2022. First report of anthracnose crown rot caused by Colletotrichum siamense on strawberry in Korea. Korean J. Mycol. 50:235-241. 
  37. O'Donnell, K. and Cigelnik, E. 1997. Two divergent intragenomic rDNA ITS2 types within a monophyletic lineage of the fungus Fusarium are nonorthologous. Mol. Phylogenet. Evol. 7:103-116. 
  38. Oo, M. M. and Oh, S.-K. 2017. Identification and characterization of new record of grape ripe rot disease caused by Colletotrichum viniferum in Korea. Mycobiology 45:421-425. 
  39. Oo, M. M., Lim, G., Jang, H. A. and Oh, S.-K. 2017. Characterization and pathogenicity of new record of anthracnose on various chili varieties caused by Colletotrichum scovillei in Korea. Mycobiology 45:184-191. 
  40. Park, K. S. and Kim, C. H. 1992. Identification, distribution and etiological characteristics of anthracnose fungi of red pepper in Korea. Korean J. Plant Pathol. 8:61-69. 
  41. Sato, T., Moriwaki, J., Uzuhashi, S., Degawa, Y., Ono, T. and Nishimura, K. 2012. Molecular phylogenetic analyses and morphological re-examination of strains belonging to three rare Colletotrichum species in Japan. Microbiol. Cult. Coll. 28:121-134. 
  42. Sherriff, C., Whelan, M. J., Arnold, G. M., Lafay, J.-F., Brygoo, Y. and Bailey, J. A. 1994. Ribosomal DNA sequence analysis reveals new species groupings in the genus Colletotrichum. Exp. Mycol. 18:121-138. 
  43. Shim, S.-A., Jang, K. S., Choi, Y. H., Kim, J.-C., Kim, H. T. and Choi, G. J. 2013. Resistance degree of cucurbits cultivars to Colletotrichum orbiculare. Korean J. Hortic. Sci. Technol. 31:371-379. 
  44. Sutton, B. C. 1980. The Coelomycetes. Fungi imperfecti with pycnidia, acervuli and stromata. Commonwealth Mycological Institute, Kew, UK, pp. 523-527. 
  45. Talhinhas, P. and Baroncelli, R. 2023. Hosts of Colletotrichum. Mycosphere 14:158-261. 
  46. Tamura, K., Stecher, G. and Kumar, S. 2021. MEGA11: molecular evolutionary genetics analysis version 11. Mol. Biol. Evol. 38:3022-3027. 
  47. Tao, G., Liu, Z.-Y., Liu, F., Gao, Y.-H. and Cai, L. 2013. Endophytic Colletotrichum species from Bletilla ochracea (Orchidaceae), with descriptions of seven new speices. Fungal Divers. 61:139-164. 
  48. Thao, L. D., Choi, H., Choi, Y., Mageswari, A., Lee, D. and Hong, S.-B. 2023. Re-identification of Colletotrichum acutatum species complex in Korea and their host plants. Plant Pathol. J. 39:384-396. 
  49. Thao, L. D., Choi, H., Choi, Y., Mageswari, A., Lee, D., Kim, D.-H., Shin, H.-D., Choi, H., Ju, H.-J. and Hong, S.-B. 2024. Re-identification of Colletotrichum gloeosporioides species complex isolates in Korea and their host plants. Plant Pathol. J. 40:16-29. 
  50. The Korean Society of Plant Pathology. 2022. List of plant diseases in Korea. 6th ed. Korean Society of Plant Pathology, Seoul, Korea. 620 pp. 
  51. Uysal, A. and Kurt, S. 2017. Influence of inoculum density, temperature, wetness duration, and leaf age on infection and development of spinach anthracnose caused by the fungal pathogen Colletotrichum spinaciae. Eur. J. Plant Pathol. 149:1041-1052. 
  52. Vasquez-Lopez, A., Palacios-Torres, R. E., Camacho-Tapia, M., Granados-Echegoyen, C., Lima, N. B., Vera-Reyes, I., Tovar-Pedraza, J. M. and Leyva-Mir, S. G. 2019. Colletotrichum brevisporum and C. musicola causing leaf anthracnose of taro (Colocasia esculenta) in Mexico. Plant Dis. 103:2963. 
  53. von Arx, J. A. 1957. Die Arten der Gattung Colletotrichum Cda. Phytopathol. Zeits. 29:413-468 (in German).
  54. Wang, Q., Duan, T. Y. and Nan, Z. B. 2019. First report of anthracnose caused by Colletotrichum spinaciae on Vicia sativa in China. Plant Dis. 103:2138. 
  55. Wang, Y. R., Hu, Z., Zhong, J., Chen, Y. and Zhu, J. Z. 2022. First report of Colletotrichum cliviicola causing leaf spot on tobacco (Nicotiana tabacum) in Hunan province of China. Plant Dis. 106:316. 
  56. Wei, L., Li, W., Hu, R., Shen, S. and Wang, J. 2023. First report of Colletotrichum spinaciae causing leaf anthracnose on quinoa in China. Plant Dis. 107:4028. 
  57. Weir, B. S., Johnston, P. R. and Damm, U. 2012. The Colletotrichum gloeosporioides species complex. Stud. Mycol. 73:115-180. 
  58. White, T. J, Bruns, T., Lee, S. and Taylor, J. 1990. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: PCR protocols: a guide to methods and applications, eds. by Innis, M. A., Gelfand, D. H., Sninsky, J. J. and White, T. J., pp. 315-322. Academic Press, New York, USA. 
  59. Yang, Y., Liu, Z., Cai, L. and Hyde, K. D. 2012. New species and notes of Colletotrichum on daylilies (Hemerocallis spp.). Trop. Plant Pathol. 37:165-174. 
  60. Zaw, M., Aye, S. S. and Matsumoto, M. 2020. Colletotrichum and Diaporthe species associated with soybean stem disease in Myanmar. J. Gen. Plant Pathol. 86:114-123.