The Plant Pathology Journal

The Korean Society of Plant Pathology (한국식물병리학회)
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Re-identification of Colletotrichum gloeosporioides Species Complex Isolates in Korea and Their Host Plants

  • 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) ;
  • Yunhee, Choi (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) ;
  • Hyeon-Dong Shin (Division of Environmental Science and Ecological Engineering, Korea University) ;
  • Hyowon Choi (Crop Protection Division, National Institute of Agricultural Sciences, Rural Development Administration) ;
  • Ho-Jong Ju (Department of Agricultural Biology, Jeonbuk National University) ;
  • Seung-Beom Hong (Korean Agricultural Culture Collection, Agricultural Microbiology Division, National Institute of Agricultural Sciences, Rural Development Administration)
  • Received : 2023.09.27
  • Accepted : 2023.12.03
  • Published : 2024.02.01
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Abstract

The Colletotrichum gloeosporioides species complex includes many phytopathogenic species, causing anthracnose disease on a wide range of host plants and appearing to be globally distributed. Seventy-one Colletotrichum isolates in the complex from different plants and geographic regions in Korea were preserved in the Korean Agricultural Culture Collection (KACC). Most of them had been identified based on hosts and morphological features, this could lead to inaccurate species names. Therefore, the KACC isolates were re-identified using DNA sequence analyses of six loci, comprising internal transcribed spacer, gapdh, chs-1, his3, act, and tub2 in this study. Based on the combined phylogenetic analysis, KACC strains were assigned to 12 known species and three new species candidates. The detected species are C. siamense (n = 20), C. fructicola (n = 19), C. gloeosporioides (n = 9), C. aenigma (n = 5), C. camelliae (n = 3), C. temperatum (n = 3), C. musae (n = 2), C. theobromicola (n = 2), C. viniferum (n = 2), C. alatae (n = 1), C. jiangxiense (n = 1), and C. yulongense (n = 1). Of these, C. jiangxiense, C. temperatum, C. theobromicola and C. yulongense are unrecorded species in Korea. Host plant comparisons showed that 27 fungus-host associations are newly reported in the country. However, plant-fungus interactions need to be investigated by pathogenicity tests.

Keywords

Acknowledgement

This study was supported by a grant (PJ017286) from the National Institute of Agricultural Sciences and was a part of the "2023 KoRAA Long-term Training Program", Rural Development Administration, Republic of Korea.

References

  1. Cannon, P. F., Damm, U., Johnston, P. R. and Weir, B. S. 2012. Colletotrichum: current status and future directions. Stud. Mycol. 73:181-213. https://doi.org/10.3114/sim0014
  2. Carbone, I. and Kohn, L. M. 1999. A method for designing primer sets for speciation studies in filamentous ascomycetes. Mycologia 91:553-556. https://doi.org/10.1080/00275514.1999.12061051
  3. Cheon, W., Lee, S. G. and Jeon, Y. 2016. First report on fruit spot caused by Colletotrichum gloeosporioides in apple (Malus pumila Mill.) in Korea. Plant Dis. 100:210.
  4. Cho, S.-E., Oh, J. Y., Lee, D.-H. and Kim, C.-W. 2023. First report of anthracnose on Juglans regia caused by Colletotrichum siamense in Korea. Plant Dis. 107:218.
  5. Choi, H.-W., Lee, Y. K. and Hong, S. K. 2017. First report of Colletotrichum aenigma causing anthracnose on Sedum kamtschaticum in Korea. Plant Dis. 101:2150.
  6. 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.
  7. 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. https://doi.org/10.1016/j.simyco.2018.04.001
  8. Doyle, V. P., Oudemans, P. V., Rehner, S. A. and 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.
  9. Farr, D. F. and Rossman, A. Y. 2021. Fungal databases, systematic mycology and microbiology laboratory, ARS, USDA. URL http://nt.ars-grin.gov/fungaldatabases/ [27 September 2023].
  10. 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. https://doi.org/10.3767/persoonia.2019.42.01
  11. 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. https://doi.org/10.1128/aem.61.4.1323-1330.1995
  12. 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. https://doi.org/10.1080/15572536.2004.11833047
  13. 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.
  14. Hassan, O., Kim, S.-H., Kim, K.-M. and Chang, T. 2023. First report of leaf anthracnose caused by Colletotrichum camelliae on tea plants (Camellia sinensis) in South Korea. Plant Dis. Online publication. https://doi.org/10.1094/PDIS-11-22-2622-PDN.
  15. Hong, S. K., Kim, W. G., Yun, H. K. and Choi, K. J. 2008. Morphological variations, genetic diversity and pathogenicity of Colletotrichum species causing grape ripe rot in Korea. Plant Pathol. J. 24:269-278.
  16. Huang, L., Li, Q.-C., Zhang, Y., Li, D.-W. and Ye, J.-R. 2016. Colletotrichum gloeosporioides sensu stricto is a pathogen of leaf anthracnose on evergreen spindle tree (Euonymus japonicus). Plant Dis. 100:672-678. https://doi.org/10.1094/PDIS-07-15-0740-RE
  17. Hyde, K. D., Cai, L., Cannon, P. F., Crouch, J. A., Crous, P. W., Damm, U., Goodwin, P. H., Chen, H., Johnston, P. R., Jones, E. B. G., Liu, Z. Y., McKenzie, E. H. C., Moriwaki, J., Noireung, P., Pennycook, S. R., Pfenning, L. H., Prihastuti, H., Sato, T., Shivas, R. G., Tan, Y. P., Taylor, P. W. J., Weir, B. S., Yang, Y. L. and Zhang, J. Z. 2009. Colletotrichum: names in current use. Fungal Divers. 39:147-182.
  18. 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. https://doi.org/10.5943/mycosphere/12/1/7
  19. Jayawardena, R. S., Hyde, K. D., Damm, U., Cai, L., Liu, M., Li, X. H., Zhang, W., Zhao, W. S. and Yan, J. Y. 2016. Notes on currently accepted species of Colletotrichum. Mycosphere 7:1192-1260. https://doi.org/10.5943/mycosphere/si/2c/9
  20. Jiang, N., Fan, X. and Tian, C. 2021. Identification and characterization of leaf-inhabiting fungi from Castanea plantations in China. J. Fungi 7:64.
  21. Joa, J. H., Lim, C. K., Choi, I. Y., Park, M. J. and Shin, H. D. 2016. First report of Colletotrichum fructicola causing anthracnose on mango in Korea. Plant Dis. 100:1793.
  22. Johnston, P. R. 2000. The importance of phylogeny in understanding host relationships within Colletotrichum. In: Colletotrichum: host specificity, pathogenicity, and host-pathogen interactions, eds. by D. Prusky, S. Freeman and M. B. Dickman, pp. 21-28. APS Press, St. Paul, MN, USA.
  23. Johnston, P. R., Pennycook, S. R. and Manning, M. A. 2005. Taxonomy of fruit-rotting fungal pathogens: what's really out there? N. Z. Plant Prot. 58:42-46.
  24. Kim, C., Hassan, O., Lee, D. and Chang, T. 2018a. First report of anthracnose of apple caused by Colletotrichum fructicola in Korea. Plant Dis. 102:2653.
  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. https://doi.org/10.1094/PDIS-01-20-0050-RE
  26. Kim, D.-H., Jeon, Y.-A., Go, S.-J., Lee, J.-K. and Hong, S.-B. 2006. Reidentification of Colletotrichum gloeosporioides and C. acutatum isolates stored in Korean Agricultural Culture Collection (KACC). Res. Plant Dis. 12:168-177 (in Korean). https://doi.org/10.5423/RPD.2006.12.3.168
  27. Kim, G. H., Choi, D. H., Park, S. Y. and Koh, Y. J. 2018b. First report of anthracnose caused by Colletotrichum nymphaeae on kiwiberry in Korea. Plant Dis. 102:1455.
  28. Kim, G. H., Kim, D. R., Park, S.-Y., Lee, Y. S., Jung, J. S. and Koh, Y. J. 2017. Incidence rates of major diseases of kiwiberry in 2015 and 2016. Plant Pathol. J. 33:434-439. https://doi.org/10.5423/PPJ.NT.01.2017.0010
  29. Kim, J. S., Hassan, O., Go, M. J. and Chang, T. 2021. First report of Colletotrichum aenigma causing anthracnose of grape (Vitis vinifera) in Korea. Plant Dis. 105:2729.
  30. Kim, Y. H., Jun, O. K., Sung, M. J., Shin, J.-S., Kim, J. H. and Jeoung, M.-I. 2000. Occurrence of Colletotrichum stem rot caused by Glomerella cingulata on graft-cactus in Korea. Plant Pathol. J. 16:242-245.
  31. Kobayashi, T. 2007. Index of fungi inhabiting woody plants in Japan. Host, distribution and literature. Kyokai Publishing Co., Ltd., Zenkoku-Noson-Kyoiku, Japan. 1227 pp. (in Japanese).
  32. Korean Society of Plant Pathology. 2022. List of plant diseases in Korea. 6th ed. Korean Society of Plant Pathology, Seoul, Korea. 630 pp.
  33. Latocha, P. 2017. The nutritional and health benefits of kiwiberry (Actinidia arguta): a review. Plant Foods Hum. Nutr. 72:325-334. https://doi.org/10.1007/s11130-017-0637-y
  34. Lee, D. H., Kim, D.-H., Jeon, Y.-A., Uhm, J. Y. and Hong, S.-B. 2007. Molecular and cultural characterization of Colletotrichum spp. causing bitter rot of apples in Korea. Plant Pathol. J. 23:37-44. https://doi.org/10.5423/PPJ.2007.23.2.037
  35. Lee, D. M., Hassan, O. and Chang, T. 2020a. Identification, characterization, and pathogenicity of Colletotrichum species causing anthracnose of peach in Korea. Mycobiology 48:210-218. https://doi.org/10.1080/12298093.2020.1763116
  36. Lee, D. M., Hassan, O., Kim, C. H. and Chang, T. 2020b. First report of anthracnose of peach (Prunus persica) caused by Colletotrichum fructicola in Korea. Plant Dis. 104:1556.
  37. 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. https://doi.org/10.5423/RPD.2021.27.2.70
  38. Li, Q., Bu, J., Shu, J., Yu, Z., Tang, L., Huang, S., Guo, T., Mo, J., Luo, S., Solangi, G. S. and Hsiang, T. 2019. Colletotrichum species associated with mango in southern China. Sci. Rep. 9:18891.
  39. Lim, J., Lim, T. H. and Cha, B. 2002. Isolation and identification of Colletotrichum musae from imported bananas. Plant Pathol. J. 18:161-164.
  40. 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. https://doi.org/10.3114/sim.2022.101.01
  41. Liu, F., Tang, G., Zheng, X., Li, Y., Sun, X., Qi, X., Zhou, Y., Xu, J., Chen, H., Chang, X., Zhang, S., and Gong, G. 2016. Molecular and phenotypic characterization of Colletotrichum species associated with anthracnose disease in peppers from Sichuan Province, China. Sci. Rep. 6:32761.
  42. Lu, G., Cannon, P. F., Reid, A. and Simmons, C. M. 2004. Diversity and molecular relationships of endophytic Colletotrichum isolates from the Iwokrama Forest Reserve, Guyana. Mycol. Res. 108:53-63. https://doi.org/10.1017/S0953756203008906
  43. Meetum, P., Leksomboon, C. and Kanjanamaneesathian, M. 2015. First report of Colletotrichum aenigma and C. siamense, the causal agent of anthracnose disease of dragon fruit in Thailand. J. Plant Pathol. 97:402.
  44. Nam, M. H., Park, M. S., Lee, H. D. and Yu, S. H. 2013. Taxonomic re-evaluation of Colletotrichum gloeosporioides isolated from strawberry in Korea. Plant Pathol. J. 29:317-322. https://doi.org/10.5423/PPJ.NT.12.2012.0188
  45. 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.
  46. 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. https://doi.org/10.1006/mpev.1996.0376
  47. Oh, J. Y., Heo, J.-I. and Lee D.-H. 2021. First report of anthracnose on pecan (Carya illinoiensis) caused by Colletotrichum siamense in Korea. Plant Dis. 105:3296.
  48. 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. https://doi.org/10.5941/MYCO.2017.45.3.184
  49. Oo, M. M. and Oh, S.-K. 2016. Chilli anthracnose (Colletotrichum spp.) disease and its management approach. Korean J. Agric. Sci. 43:153-162.
  50. 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. https://doi.org/10.5941/MYCO.2017.45.4.421
  51. Oo, M. M. and Oh, S.-K. 2020. First report of anthracnose of chili pepper fruit caused by Colletotrichum truncatum in Korea. Plant Dis. 104:564.
  52. Oo, M. M., Yoon, H.-Y., Jang, H. A. and Oh, S.-K. 2018. Identification and characterization of Colletotrichum species associated with bitter rot disease of apple in South Korea. Plant Pathol. J. 34:480-489.
  53. Park, J. C., Kim, B. W. and Young, H. S. 1990. Further study on the flavonoids from the leaves of Machilus thunbergii in Korea. Korean J. Pharmacogn. 21:197-200.
  54. 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.
  55. Park, M. S., Kim, B.-R., Park, I.-H. and Hahm, S.-S. 2018. First report of two Colletotrichum species associated with bitter rot on apple fruit in Korea: C. fructicola and C. siamense. Mycobiology 46:154-158. https://doi.org/10.1080/12298093.2018.1478220
  56. Paul, N. C., Lee, H. B., Lee, J. H., Shin, K. S., Ryu, T. H., Kwon, H. R., Kim, Y. K., Youn, Y. N. and Yu, S. H. 2014. Endophytic fungi from Lycium chinense Mill and characterization of two new Korean records of Colletotrichum. Int. J. Mol. Sci. 15:15272-15286. https://doi.org/10.3390/ijms150915272
  57. Penzig, A. G. O. 1882. Fungi agrumicoli. Contribuzione allo studio dei funghi parassiti degli agrumi. Michelia 2:385-508 (in Italian).
  58. Poti, T., Kisaki, G., Arita, K. and Akimitsu, K. 2023. Identification and characterization of Colletotrichum species causing kiwifruit anthracnose in Kagawa Prefecture, Japan. J. Gen. Plant Pathol. 89:84-90. https://doi.org/10.1007/s10327-023-01115-7
  59. Sharma, G., Maymon, M. and Freeman, S. 2017. Epidemiology, pathology and identification of Colletotrichum including a novel species associated with avocado (Persea americana) anthracnose in Israel. Sci. Rep. 7:15839.
  60. Sharma, G., Pinnaka, A. K. and Shenoy, B. D. 2013. ITS-based diversity of Colletotrichum from India. Curr. Res. Environ. Appl. Mycol. 3:194-220. https://doi.org/10.5943/cream/3/2/3
  61. Simmonds, J. H. 1966. Host index of plant diseases in Queensland. Queensland Department of Primary Industries, Brisbane, Australia. 111 pp.
  62. Tamura, K., Stecher, G. and Kumar, S. 2021. MEGA11: molecular evolutionary genetics analysis version 11. Mol. Biol. Evol. 38:3022-3027. https://doi.org/10.1093/molbev/msab120
  63. 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.
  64. Truong, H. H., Sato, T., Ishikawa, S., Minoshima, A., Nishimura, T. and Hirooka, Y. 2018. Three Colletotrichum species responsible for anthracnose on Synsepalum dulcificum (miracle fruit). Int. J. Phytopathol. 7:89-101. https://doi.org/10.33687/phytopath.007.03.2658
  65. Wang, Q., Liu, X., Ma, H., Shen, X. and Hou, C. 2019a. Colletotrichum yulongense sp. nov. and C. rhombiforme isolated as endophytes from Vaccinium dunalianum var. urophyllum in China. Phytotaxa 394:285-298. https://doi.org/10.11646/phytotaxa.394.4.6
  66. Wang, X., Liu, X., Wang, R., Fa, L., Chen, L., Xin, X., Zhang, Y., Tian, H., Xia, M. and Hou, X. 2021. First report of Colletotrichum aenigma causing walnut anthracnose in China. Plant Dis. 105:225.
  67. Wang, Y., Qin, H. Y., Liu, Y. X., Fan, S. T., Sun, D., Yang, Y. M., Li, C. Y. and Ai, J. 2019b. First report of anthracnose caused by Colletotrichum aenigma on Actinidia arguta in China. Plant Dis. 103:372.
  68. Weir, B. S., Johnston, P. R. and Damm, U. 2012. The Colletotrichum gloeosporioides species complex. Stud. Mycol. 73:115-180. https://doi.org/10.3114/sim0011
  69. 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 M. A. Innis, D. H. Gelfand, J. J. Sninsky and T. J. White, pp. 315-322. Academic Press, New York, USA.
  70. Yan, J.-Y., Jayawardena, M. M. R. S., Goonasekara, I. D., Wang, Y., Zhang, W., Liu, M., Huang, J.-B., Wang, Z.-Y., Shang, J.- J., Peng, Y.-L., Bahkali, A., Hyde, K. D. and Li, X.-H. 2015. Diverse species of Colletotrichum associated with grapevine anthracnose in China. Fungal Divers. 71:233-246. https://doi.org/10.1007/s13225-014-0310-9
  71. Zhang, Q., Nizamani, M. M., Feng, Y., Yang, Y. Q., Jayawardena, R. S., Hyde, K. D., Wang, Y. and Li, C. 2023. Genome-scale and multi-gene phylogenetic analyses of Colletotrichum spp. host preference and associated with medicinal plants. Mycosphere 14:1-106.
  72. Zheng, H., Yu, Z., Jiang, X., Fang, L. and Qiao, M. 2022. Endophytic Colletotrichum species from aquatic plants in Southwest China. J. Fungi 8:87.