Research in Plant Disease (식물병연구)

The Korean Society of Plant Pathology (한국식물병리학회)
권호 표지
DOI QR코드

DOI QR Code

Colletotrichum Diversity within Different Species Complexes Associated with Fruit Anthracnose in South Korea and Their Fungicides In-Vitro Sensitivity

국내 과실 탄저병을 일으키는 종 복합체와 종 다양성 및 살균제 감수성

  • Taehyun Chang (Department of Crop Science, College of Ecology and Environmental Sciences, Kyungpook National University) ;
  • Oliul Hassan (Crop Protection Division, National Institute of Agricultural Science) ;
  • Jong Yeob Jeon (Central Research Institute, Kyung Nong Co.) ;
  • Chi Hyun Kim (Gimcheon Nong Hyup) ;
  • Dae Min Lee (SUNGBO Research Center) ;
  • Ju Sung Kim (J-agro Co. Ltd. Research Center) ;
  • Eun Chan Kang (J-agro Co. Ltd. Research Center) ;
  • Jaewon Kim (Department of Crop Science, College of Ecology and Environmental Sciences, Kyungpook National University)
  • Received : 2023.10.05
  • Accepted : 2023.12.04
  • Published : 2023.12.31
Download PDF
⟨ Previous Next ⟩

Abstract

Anthracnose, caused by the Colletotrichum genus, comprises a significant number of plant pathogens and poses a major threat to fruit production worldwide, including South Korea. Colletotrichum species were identified associated with anthracnose in fruits such as apple, persimmon, plum, peach, jujube, walnut, and grape. A polyphasic approach, including morphology, multigene phylogenetics, and pathogenicity testing, was used. Additionally, the in-vitro sensitivity of identified Colletotrichum species to common fungicides was also evaluated. A total of nine Colletotrichum species within two complexes, namely gloeosporioides and acutatum, have been identified as the causal agents of anthracnose in common fruits in South Korea. In the gloeosporioides complex, we found Colletotrichumaenigma, C. fructicola, C. gloeosporioides, C. horii, C. siamense, and C. viniferum. Meanwhile, in the acutatum complex, C. fioriniae, C. nymphaeae, and C. orientalis were identified. Notably, C. fructicola, C. siamense, C. fioriniae, and C. nymphaeae were reported for the first time from apple, C. siamense, C. fioriniae and C. nymphaeae from plum, C. siamense, C. fructicola, and C. fioriniae frompeach, C. siamense and C. horii from persimmon, C. fioriniae from Omija (Schisandra), C. orientalis from walnut, C. nymphaeae from jujube, and C. aenigma, C. fructicola, and C. siamense fromgrape. Fungicide sensitivity tests revealed significant variation in the EC50 values among specific Colletotrichum species when exposed to different fungicides. Moreover, the same Colletotrichum species isolated from different host plants displayed varying sensitivity to the same fungicide.

탄저병원균(Colletotrichum) 속의 많은 식물병원균은 한국을 비롯하여 전 세계 과수 생산에 큰 위협이 된다. 사과, 감, 자두, 복숭아, 대추, 포도 및 호두와 같은 과실에서 탄저병과 관련된 탄저병원균의 종이 동정되었다. 형태적, 다중 유전자의 계통발생적 및 병원성 시험이 다양한 접근으로 실시되었다. 동정된 탄저병원균의 종에 대한 감수성은 살균제에 대하여 평가하였다. 2종의 종복합체인 gloeosporioides와 acutatum에 속한 9종의 탄저병원균이 국내 과실에 탄저병의 주요 원인균으로 동정되었다. Colletotrichum gloeosporioides 종 복합체 안에는 6종인 C. aenigma, C. fructicola, C. gloeosporioides, C. horii, C. siamense 및 C. viniferum이 있는 반면, Colletotrichum acutatum 종 복합체 안에 종은 C. fioriniae, C. nymphaeae 및 C. orientalis이 동정되었다. 사과 탄저병원균은 C. fructicola, C. siamense, C. fioriniae 및 C. nymphaeae, 자두 탄저병원균은 C. siamense, C. fioriniae 및 C. nymphaeae, 복숭아 탄저병원균은 C. siamense, C. fructicola 및 C. fioriniae, 감 탄저병원균은 C. siamense, C. horii 및 C. nymphaeae, 오미자 탄저병원균은 C. fioriniae, 호두탄저병원균은 C. orientalis, 대추탄저병원균은 C. nymphaeae, 포도 탄저병원균인 C. aenigma, C. fructicola 및 C. siamense를 국내 과수류의 과실에 병을 일으키는 병원균의 종류로 처음 국제학술지에 보고되었다. 이들 병원균의 종에 대한 살균제의 감수성 시험에서 여러 살균제에 대한 탄저병원균의 종 간에 EC50값이 매우 다양하여 감수성의 차이가 크게 나타났다.

Keywords

Acknowledgement

We would like to thank all the members of the Plant Pathology Lab, School of Ecology Environmental System, Kyungpook National University, Sangju, Gyeongbuk 37224, Korea (Republic of) for their help conducting the experiments.

References

  1. Alaniz, S., Cuozzo, V., Martinez, V., Stadnik, M. J. and Mondino, P. 2019. Ascospore infection and Colletotrichum species causing glomerella leaf spot of apple in Uruguay. Plant Pathol. J. 35: 100-111.  https://doi.org/10.5423/PPJ.OA.07.2018.0145
  2. An, H. J., Na, H. B., Lim, T. H., Chang, T., Song, J. and Lee, D. W. 2018. Sensitivity variation to demethylation inhibiting fungicides of Colletotrichum horii, isolated anthracnose pathogens from persimmon tree in Sangju and Yeongdong. Korean J. Pestic. Sci. 22: 177-183.  https://doi.org/10.7585/kjps.2018.22.3.177
  3. Bailey, J. A and Jegger, M. J. 1992. Colletotrichum: Biology, Pathology and Control. BSPP/CAB International, Wallingford, UK. 388 pp. 
  4. Baroncelli, R., Talhinhas, P., Pensec, F., Sukno, S. A., Le Floch, G. and Thon, M. R. 2017. The Colletotrichum acutatum species complex as a model system to study evolution and host specialization in plant pathogens. Front. Microbiol. 8: 2001. 
  5. Batista, D., Silva, D. N., Vieira, A., Cabral, A., Pires, A. S., Loureiro, A. et al. 2017. Legitimacy and implications of reducing Collectotrichum kahawae to subspecies in plant pathology. Front. Plant Sci. 7: 2051. 
  6. Bhunjun, C. S., Phukhamsakda, C., Jayawardena, R. S., Jeewon, R., Promputtha, I. and Hyde, K. D. 2021. Investigating species boundaries in Colletotrichum. Fungal Divers. 107: 107-127.  https://doi.org/10.1007/s13225-021-00471-z
  7. Cannon, P. F., Bridge, P. D. and Monte, E. 2000. Linking the past, present, and future of Colletotrichum systematics. In: Colletotrichum: Host Specificity, Pathology, and Host-Pathogen Interaction, eds. by D. Prusky, S. Freeman and M. B. Dickman, pp. 1-20. APS Press, St. Paul, MN, USA. 
  8. Cannon, P. F., Buddie, A. G. and Bridge, P. D. 2008. The typifcation of Colletotrichum gloriousness. Mycotaxon 104: 189-204. 
  9. 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
  10. 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
  11. Chang, T., Hassan, O., Jeon, J. Y., Shin, J. S., Oh, N. K. and Lim, T. H. 2018a. First report of anthracnose of persimmon (Diospyros kaki L. f.) caused by Colletotrichum siamense in Korea. Plant Dis. 102: 443. 
  12. Chang, T. H., Hassan, O. and Lee, Y. S. 2018b. First report of anthracnose of Japanese plum (Prunus salicina) caused by Colletotrichum nymphaeae in Korea. Plant Dis. 102: 1461. 
  13. 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. 
  14. Chen, Y., Fu, D., Wang, W., Gleason, M. L., Zhang, R., Liang, X. et al. 2022. Diversity of Colletotrichum species causing apple bitter rot and Glomerella leaf spot in China. J. Fungi 8: 740. 
  15. Crouch, J., O'Connell, R., Gan, P., Buiate, E., Torres, M. F., Beirn, L. et al. 2014. The genomics of Colletotrichum. In: Genomics of Plant-Associated Fungi: Monocot Pathogens, eds. by R. A. Dean, A. Lichens-Park and C. Kole, pp. 69-102. Springer, Berlin, Germany. 
  16. Crous, P. W., Gams, W., Stalpers, J. A., Robert, V. and Stegehuis, G. 2004. MycoBank: an online initiative to launch mycology into the 21st century. Stud. Mycol. 50: 19-22. 
  17. Damm, U., Cannon, P. F., Woudenberg, J. H. C. and Crous, P. W. 2012a. The Colletotrichum acutatum species complex. Stud. Mycol. 73: 37-113.  https://doi.org/10.3114/sim0010
  18. Damm, U., Cannon, P. F., Woudenberg, J. H. C., Johnston, P. R., Weir, B. S., Tan, Y. P. et al. 2012b. The Colletotrichum boninense species complex. Stud. Mycol. 73: 1-36.  https://doi.org/10.3114/sim0002
  19. 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
  20. Dean, R., Van Kan, J. A. L., Pretorius, Z. A., Hammond-Kosack, K. E., Di Pietro, A., Spanu, P. D. et al. 2012. The Top 10 fungal pathogens in molecular plant pathology: corrigendum. Mol. Plant Pathol. 13: 804. 
  21. De Silva, D. D., Ades, P. K., Crous, P. W. and Taylor, P. W. J. 2017. Colletotrichum species associated with chili anthracnose in Australia. Plant Pathol. 66: 254-267.  https://doi.org/10.1111/ppa.12572
  22. Dowling, M., Peres, N., Villani, S. and Schnabel, G. 2020. Managing Colletotrichum on fruit crops: a "complex" challenge. Plant Dis. 104: 2301-2316.  https://doi.org/10.1094/PDIS-11-19-2378-FE
  23. Fantinel, V. S., Muniz, M. F. B., Blume, E., Araujo, M. M., Poletto, T., da Silva, T. T. et al. 2017. First report of Colletotrichum siamense causing anthracnose on Acca sellowiana fruits in Brazil. Plant Dis. 101: 1035. 
  24. Fu, M., Crous, P. W., Bai, Q., Zhang, P. F., Xiang, J., Guo, Y. S. et al. 2019. Colletotrichum species associated with anthracnose of Pyrus spp. in China. Persoonia 42: 1-35.  https://doi.org/10.3767/persoonia.2019.42.01
  25. Gardes, M. and Bruns, T. D. 1993. ITS primers with enhanced specificity for basidiomycetes: application to the identification of mycorrhizae and rusts. Mol. Ecol. 2: 113-118.  https://doi.org/10.1111/j.1365-294X.1993.tb00005.x
  26. 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
  27. Grammen, A., Wenneker, M., Van Campenhout, J., Pham, K. T. K., Van Hemelrijck, W., Bylemans, D. et al. 2019. Identification and pathogenicity assessment of Colletotrichum isolates causing bitter rot of apple fruit in Belgium. Eur. J. Plant Pathol. 153: 47-63.  https://doi.org/10.1007/s10658-018-1539-z
  28. 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
  29. Han, F.-Y., Qi, Y.-K., Zhang, Y.-T., Qi, J.-H., Wang, J.-W., Liu, W.-Z. et al. 2023. First report of jujube anthracnose caused by Colletotrichum siamense in China. Plant Dis. 107: 2538. 
  30. Hassan, O, Jeon, J. Y., Chang, T., Shin, J. S., Oh. N. K. and Lee, Y. S. 2018. Molecular and morphological characterization of Colletotrichum species in the Colletotrichum gloeosporioides complex associated with persimmon anthracnose in South Korea. Plant Dis.102: 1015-1024.  https://doi.org/10.1094/PDIS-10-17-1564-RE
  31. Hassan, O., Lee, D. W. and Chang, T. 2019a. First report of anthracnose of persimmon caused by Colletotrichum nymphaeae in Korea. Plant Dis. 103: 1772. 
  32. Hassan, O., Lee, Y. S. and Chang, T. 2019b. Colletotrichum species associated with Japanese plum (Prunus salicina) anthracnose in South Korea. Sci. Rep. 9: 12089. 
  33. Hofstetter, V., Buyck, B., Eyssartier, G., Schnee, S. and Gindro, K. 2019. The unbearable lightness of sequenced-based identification. Fungal Divers. 96: 243-284.  https://doi.org/10.1007/s13225-019-00428-3
  34. 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.  https://doi.org/10.5423/PPJ.2008.24.3.269
  35. Hu, M.-J., Grabke, A. and Schnabel, G. 2015. Investigation of the Colletotrichum gloeosporioides species complex causing peach anthracnose in South Carolina. Plant Dis. 99: 797-805.  https://doi.org/10.1094/PDIS-10-14-1076-RE
  36. Hyde, K. D., Cai, L., Cannon, P. F., Crouch, J. A., Crous, P. W., Damm, U. et al. 2009. Colletotrichum: names in current use. Fungal Divers. 39: 147-182. 
  37. Jang, H. S., Hassan, O. and Chang, T. 2023. First report of walnut anthracnose caused by Colletotrichum orientalis in South Korea. Plant Dis. 107: 3633. 
  38. Jayawardena, R. S., Bhunjun, C. S., Hyde, K. D., Gentekaki, E. and Itthayakorn, P. 2021. Colletotrichum: lifestyles, biology, morphospecies, species complexes and accepted species. Mycosphere 12: 519-669.  https://doi.org/10.5943/mycosphere/12/1/7
  39. Jayawardena, R. S., Hyde, K. D., Damm, U., Cai, L., Liu, M., Li, X. H. et al. 2016. Notes on currently accepted species of Colletotrichum. Mycosphere 7: 1192-1260.  https://doi.org/10.5943/mycosphere/si/2c/9
  40. Jeon, J. Y. 2017. Incidence, identification and invitro fungicides sensitivity analysis of Colletotrichum gloeosporioides the causal agents of anthracnose on persimmon tree in Korea. M.D. thesis. Kyungpook National University, Daegu, Korea. 48 pp. 
  41. Jeon, J. Y., Hassan, O., Chang, T., Lee, D. W., Shin, J. S. and Oh, N. K. 2017. Anthracnose of persimmon (Diospyros kaki) caused by Colletotrichum horii in Sangju, Korea. Plant Dis. 101: 1035. 
  42. Kang, E. C. 2021. Diversity, pathogenicity and fungicides sensitivity of Colletotrichum species associated with jujube anthracnose in South Korea. M.S. thesis. Kyungpook National University, Daegu, Korea. 78 pp. 
  43. Kang, E. C., Hassan, O., Kim, K.-M. and Chang, T. 2023. Molecular characterization and fungicide sensitivity of jujube pathogens Colletotrichum gloeosporioides sensu stricto and Colletotrichum nymphaeae in South Korea. Plant Dis. 107: 861-869.  https://doi.org/10.1094/PDIS-04-22-0942-RE
  44. Katoh, K. and Standley, D. M. 2013. MAFFT Multiple Sequence Alignment Software version 7: improvements in performance and usability. Mol Biol. Evol. 30: 772-780.  https://doi.org/10.1093/molbev/mst010
  45. Kim, C., Hassan, O., Lee, D. and Chang, T. 2018. First report of anthracnose of apple caused by Colletotrichum fructicola in Korea. Plant Dis. 102: 2653. 
  46. Kim, C. H. 2019. Diversity, pathogenicity and fungicides sensitivity of Colletotrichum species associated with apple anthracnose in South Korea. M.S. thesis. Kyungpook National University, Daegu, Korea. 88 pp. 
  47. 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
  48. 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. 
  49. Kim, J., Hassan, O., Kim, K.-M. and Chang, T. 2022. First report of Colletotrichum fioriniae causing anthracnose on the fruit of Omija (Schisandra) in South Korea. Plant Dis. 106: 2991. 
  50. Kim, S., Kim, J., Shin, Y., Hassan, O. and Chang, T. 2023. In vitro sensitivity of Colletotrichum species associate with grape anthracnose in Korea to tebuconazole and carbendazim. In: The 2023 KSPP Conference, p. 105. The Korean Society of Plant Pathology, Seoul, Korea.
  51. Kim, W. G. and Hong, S. K. 2008. Occurrence of anthracnose on peach tree caused by Colletotrichum species. Plant Pathol. J. 24: 80-83.  https://doi.org/10.5423/PPJ.2008.24.1.080
  52. Korean Society of Plant Pathology. 2009. List of Plant Disease in Korea. Korean Society of Plant Pathology, Seoul, Korea. 853 pp. 
  53. Kumar, S., Stecher, G. and Tamura, K. 2016. MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Mol. Biol. Evol. 33: 1870-1874.  https://doi.org/10.1093/molbev/msw054
  54. Kwon, J.-H., Kim, J., Choi, O., Gang, G.-H., Han, S. and Kwak, Y.-S. 2013. Anthracnose caused by Colletotrichum horii on sweet persimmon in Korea: dissemination of conidia and disease development. J. Phytopathol. 161: 497-502.  https://doi.org/10.1111/jph.12096
  55. Lardner, R., Johnston, P. R., Plummer, K. M. and Pearson, M. N. 1999. Morphological and molecular analysis of Colletotrichum acutatum sensu lato. Mycol. Res. 103: 275-285.  https://doi.org/10.1017/S0953756298007023
  56. Laura, L., Galli, M., Garaguso, I., Petrucci, M. and Vitale, S. 2022. First report of Colletotrichum fioriniae and C. nymphaeae as causal agents of anthracnose on walnut in Italy. Plant Dis. 106: 327. 
  57. Lee, D. 2019. Diversity, pathogenicity and fungicides sensitivity of Colletotrichum species associated with peach anthracnose in South Korea. M.S. thesis. Kyungpook National University, Daegu, Korea. 90 pp. 
  58. Lee, D., Hassan, O., Kim, C. and Chang, T. 2018. First report of peach (Prunus persica) anthracnose caused by Colletotrichum fioriniae in Korea. Plant Dis. 102: 2650. 
  59. 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
  60. 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. 
  61. 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.  https://doi.org/10.1007/s11557-018-1424-3
  62. Liang, X., Yao, L., Hao, X., Li, B., Kong, Y., Lin, Y. et al. 2021. Molecular dissection of perithecial mating line development in Colletotrichum fructicola, a species with a nontypical mating system featured by plus-to-minus switch and plus-minus-mediated sexual enhancement. Appl. Environ. Microbiol. 87: e0047421 
  63. Lim, Y.-S., Hassan, O. and Chang, T. 2020. First report of anthracnose of shine muscat caused by Colletotrichum fructicola in Korea. Mycobiology 48: 75-79.  https://doi.org/10.1080/12298093.2019.1697190
  64. Liu, F., Cai, L., Crous, P. W. and Damm, U. 2013. Circumscription of the anthracnose pathogens Colletotrichum lindemuthianum and C. nigrum. Mycologia 105: 844-860.  https://doi.org/10.3852/12-315
  65. Liu, F., Cai, L., Crous, P. W. and Damm, U. 2014. The Colletotrichum gigasporum species complex. Persoonia 33: 83-97.  https://doi.org/10.3767/003158514X684447
  66. Liu, T., Chen, D., Liu, Z. and Hou, J. M. 2018. First report of anthracnose caused by Colletotrichum tropicale on Sauropus androgynus in China. Plant Dis. 102: 2030. 
  67. Marin-Felix, Y., Groenewald, J. Z., Cai, L., Chen, Q., Marincowitz, S., Barnes, I. et al. 2017. Genera of phytopathogenic fungi: GOPHY 1. Stud. Mycol. 86: 99-216.  https://doi.org/10.1016/j.simyco.2017.04.002
  68. May De Mio, L. L., Da Silva, F. A., Blood, R. Y. and Figueiredo, J. A. G. 2015. Twig blight and defoliation caused by Colletotrichum horii in persimmon in Brazil. Rev. Bras. Frutic. 37: 256-260.  https://doi.org/10.1590/0100-2945-044/14
  69. Menat, J., Armstrong-Cho, C. and Banniza, S. 2016. Lack of evidence for sexual reproduction in field populations of Colletotrichum lentis. Fungal Ecol. 20: 66-74.  https://doi.org/10.1016/j.funeco.2015.11.001
  70. Munda, A. 2014. First report of Colletotrichum fioriniae and C. godetiae causing apple bitter rot in Slovenia. Plant Dis. 98: 1282. 
  71. Munir, M., Amsden, B., Dixon, E., Vaillancourt, L. and Gauthier, N. A. W. 2016. Characterization of Colletotrichum species causing bitter rot of apple in Kentucky orchards. Plant Dis. 100: 2194-2203.  https://doi.org/10.1094/PDIS-10-15-1144-RE
  72. Nam, M. H., Yoo, J. H., Yun, T., Kim, H. and Kim, K. H. 2023. Anthracnose of strawberry: etiological and ecological characteristics, and management. Res. Plant Dis. 29: 205-219.  https://doi.org/10.5423/RPD.2023.29.3.205
  73. 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
  74. 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
  75. 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.  https://doi.org/10.5423/PPJ.FT.10.2018.0201
  76. Pan, F. Y., Huang, Y., Lin, L., Zhou, Y. M., Wei, R. F., Guo, W. F. et al. 2016. First rport of Colletotrichum capsici causing grape ripe rot in Guangxi, China. Plant Dis. 100: 2531. 
  77. 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
  78. Penzig, A. 1882. Fungi agrumicoli: contribuzione allo studio dei funghi parassiti degli agrumi. Michelia 2: 385-508. 
  79. Price, M. N., Dehal, P. S. and Arkin, A. P. 2010. FastTree 2: approximately maximum-likelihood trees for large alignments. PLoS ONE 5: e9490. 
  80. Prihastuti, H., Cai, L., Chen, H., McKenzie, E. H. C. and Hyde, K. D. 2009. Characterization of Colletotrichum species associated with coffee berries in northern Thailand. Fungal Divers. 39: 89-109. 
  81. Rojas, E. I., Rehner, S. A., Samuels, G. J., Van Bael, S. A., Herre, E. A., Cannon, P. et al. 2010. Colletotrichum gloeosporioides s.l. associated with Theobroma cacao and other plants in Panama: multilocus phylogenies distinguish host-associated pathogens from asymptomatic endophytes. Mycologia 102: 1318-1338.  https://doi.org/10.3852/09-244
  82. Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D. L., Darling, A., Hohna, S. et al. 2012. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst. Biol. 61: 539-542.  https://doi.org/10.1093/sysbio/sys029
  83. Sharma, G., Pinnaka, A. K. and Shenoy, B. D. 2015. Resolving Colletotrichum siamense species complex using ApMat marker. Fungal Divers. 71: 247-264.  https://doi.org/10.1007/s13225-014-0312-7
  84. Shi, Y.-X., Zhang, X.-H., Zhao, Q. and Li, B.-J. 2019. First report of Colletotrichum gloeosporioides causing Anthracnose on Okra in China. Plant Dis. 103: 1023. 
  85. Shivas, R. G. and Tan, Y. P. 2009. A taxonomic re-assessment of Colletotrichum acutatum, introducing C. fioriniae comb. et stat. nov. and C. simmondsii sp. nov. Fungal Divers. 39: 111-122. 
  86. Silva D. N., Talhinas, P., Varzea, V., Cai, L., Paulo, O. S. and Batista, D. 2012. 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.  https://doi.org/10.3852/11-145
  87. Sreenivasaprasad, S. and Talhinhas, P. 2005. Genotypic and phenotypic diversity in Colletotrichum acutatum, a cosmopolitan pathogen causing anthracnose on a wide range of hosts. Mol. Plant Pathol. 6: 361-378.  https://doi.org/10.1111/j.1364-3703.2005.00291.x
  88. Sutton, B. C. 1980. The Coelomycetes. Fungi Imperfecti with Pycnidia, Acervuli and Stromata. Commonwealth Mycological Institute, Kew, Surrey, UK. 696 pp. 
  89. Sutton, B. C. 1992. The genus Glomerella and its anamorph Colletotrichum. In: Colletotrichum: Biology, Pathology and Control, eds. by J. A. Bailey and M. J. Jeger, pp. 1-26. CAB International, Wallingford, UK. 
  90. Talhinhas, P. and Baroncelli, R. 2021. Colletotrichum species and complexes: geographic distribution, host range and conservation status. Fungal Divers. 110: 109-198.  https://doi.org/10.1007/s13225-021-00491-9
  91. Templeton, M. D., Rikkerink, E. H., Solon, S. L. and 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.  https://doi.org/10.1016/0378-1119(92)90055-T
  92. Van Der AA, H. A. 1978. A leaf spot disease of Nymphaea alba in the Netherlands. Neth. J. Plant Pathol. 84: 109-115.  https://doi.org/10.1007/BF01981538
  93. Velho, A. C., Stadnik, M. J. and Wallhead, M. 2019. Unraveling Colletotrichum species associated with Glomerella leaf spot of apple. Trop. Plant Pathol. 44: 197-204.  https://doi.org/10.1007/s40858-018-0261-x
  94. Von Arx, J. A. 1957. Die Arten der Gattung Colletotrichum Cda. Phytopathol. Z. 29: 413-468. 
  95. Waller, J. M., Bridge, P. D., Black, R. and Hakiza, G. 1993. Characterization of the coffee berry disease pathogen, Colletotrichum kahawae sp. nov. Mycol. Res. 97: 989-994.  https://doi.org/10.1016/S0953-7562(09)80867-8
  96. Weir, B. S. and Johnston, P. R. 2010. Characterisation and neotypification of Gloeosporium kaki Hori as Colletotrichum horii nom. nov. Mycotaxon 111: 209-219.  https://doi.org/10.5248/111.209
  97. 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
  98. White T. J., Bruns T., Lee S. and Taylor J. W. 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 TJ, pp. 315-322. Academic Press, New York, NY, USA. 
  99. Yang, Y. L., Liu, Z. Y., Cai, L., Hyde, K. D., Yu, Z. N. and McKenzie, E. H. C. 2009. Colletotrichum anthracnose of Amaryllidaceae. Fungal Divers. 39: 123-146.