European Journal of Plant Pathology

, Volume 139, Issue 2, pp 325–338 | Cite as

Diversity and pathogenicity of Colletotrichum species isolated from soursop in Colombia

  • Elizabeth Álvarez
  • Lederson Gañán
  • Alberto Rojas-Triviño
  • Juan F. Mejía
  • Germán A. Llano
  • Alonso González
Article

Abstract

Anthracnose, caused by Colletotrichum species is a highly limiting disease for the production of the tropical fruit tree crop, soursop (Annona muricata L.). In this study, 83 single-spore isolates of Colletotrichum were obtained from diseased soursoup tissues and subjected to a species complex-specific PCR assay. The isolates were identified as C. gloeosporioides sensu lato (n = 60), C. boninense s. lat. (n = 22), or C. acutatum s. lat. (n = 1). A subset of 21 selected isolates was identified to species level by means of a multi-locus phylogenetic analysis using sequences from the ITS region and partial sequences of the actin, β-tubulin-2, glyceraldehyde-3-phosphate dehydrogenase, and chitin synthase-1 genes. The multi-locus phylogenetic analysis resolved C. theobromicola, C. tropicale, C. siamense, and C. gloeosporioides sensu stricto in the C. gloeosporioides complex; C. karstii and one undetermined species in the C. boninense complex; as well as one undetermined species in the C. acutatum complex. Significant differences in anthracnose severity were observed between Colletotrichum species when tested for pathogenicity on attached twigs of soursop cv. Elita. Colletotrichum theobromicola and C. tropicale were associated with high and intermediate virulence, respectively, whereas the remaining species were associated with low virulence.

Keywords

Annona muricata Anthracnose Characterization Phylogenetic analysis Virulence 

Notes

Acknowledgments

We are grateful to Corporación BIOTEC, Ministerio de Agricultura y Desarrollo Rural de Colombia, Agencia Colombiana de Cooperación Internacional (ACCI), and COLCIENCIAS for their financial support. We thank Dr Jairo Castaño-Zapata for his contributions to this research; Juan B. Cuasquer (Systems Engineer, CIAT); and Elizabeth L. McAdam and Matthew Blair for reviewing the manuscript.

References

  1. Afanador-Kafuri, L., Minz, D., Maymon, M., & Freeman, S. (2003). Characterization of Colletotrichum isolates from tamarillo, passiflora, and mango in Colombia and identification of a unique species from the genus. Phytopathology, 93(5), 579–587.PubMedCrossRefGoogle Scholar
  2. Alahakoon, P. W., Brown, A. E., & Sreenivasaprasad, S. (1994). Cross-infection potential of genetic groups of Colletotrichum gloeosporioides on tropical fruits. Physiological and Molecular Plant Pathology, 44(2), 93–103.CrossRefGoogle Scholar
  3. Álvarez, E., Ospina, C., Mejía, J. F., & Llano, G. A. (2004). Caracterización morfológica, patogénica y genética del agente causal de la antracnosis (Colletotrichum gloeosporioides) en guanábana (Annona muricata) en el Valle del Cauca. Fitopatología Colombiana, 28, 1–8.Google Scholar
  4. Cai, L., Hyde, K. D., Taylor, P. W. J., Weir, B. S., Waller, J., Abang, M. M., et al. (2009). A polyphasic approach for studying Colletotrichum. Fungal Diversity, 39, 183–204.Google Scholar
  5. Cannon, P. F., Bridge, P. D., & Monte, E. (2000). Linking the past, present, and future of Colletotrichum systematics. In D. Prusky, S. Freeman, & M. Dickman (Eds.), Colletotrichum: Host Specificity, Pathology, and Host-Pathogen Interaction (pp. 1–20). St. Paul: American Phytopathological Society.Google Scholar
  6. Cannon, P. F., Buddie, A. G., & Bridge, P. D. (2008). The typification of Colletotrichum gloeosporioides. Mycotaxon, 104, 189–204.Google Scholar
  7. Cannon, P. F., Damm, U., Johnston, P. R., & Weir, B. S. (2012). Colletotrichum - current status and future directions. Studies in Mycology, 73(1), 181–213.PubMedCentralPubMedGoogle Scholar
  8. Carbone, I., & Kohn, L. M. (1999). A method for designing primer sets for speciation studies in filamentous ascomycetes. Mycologia, 91(3), 553–556.CrossRefGoogle Scholar
  9. Crouch, J. A., Clarke, B. B., & Hillman, B. I. (2009). What is the value of ITS sequence data in Colletotrichum systematics and species diagnosis? A case study using the falcate-spored graminicolous Colletotrichum group. Mycologia, 101(5), 648–656.PubMedCrossRefGoogle Scholar
  10. Damm, U., Mostert, L., Crous, P. W., & Fourie, P. H. (2008). Novel Phaeoacremonium species associated with necrotic wood of Prunus trees. Persoonia, 20, 87–102.PubMedCentralPubMedCrossRefGoogle Scholar
  11. Damm, U., Cannon, P. F., Woudenberg, J. H. C., & Crous, P. W. (2012a). The Colletotrichum acutatum species complex. Studies in Mycology, 73(1), 37–113.PubMedCentralPubMedGoogle Scholar
  12. 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. Studies in Mycology, 73(1), 1–36.PubMedCentralPubMedGoogle Scholar
  13. Freeman, S., Katan, T., & Shabi, E. (1998). Characterization of Colletotrichum species responsible for anthracnose diseases of various fruits. Plant Disease, 82(6), 596–605.CrossRefGoogle Scholar
  14. Freeman, S., Shabi, E., & Katan, T. (2000). Characterization of Colletotrichum acutatum causing anthracnose of anemone (Anemone coronaria L.). Applied and Environmental Microbiology, 66(12), 5267–5272.PubMedCentralPubMedCrossRefGoogle Scholar
  15. 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(4), 1323–1330.PubMedCentralPubMedGoogle Scholar
  16. Huang, F., Chen, G. Q., Hou, X., Fu, Y. S., Cai, L., Hyde, K. D., et al. (2013). Colletotrichum species associated with cultivated citrus in China. Fungal Diversity, 61(1), 61–74.CrossRefGoogle Scholar
  17. International Centre for Underutilized Cultures (ICUC). (2002). Fruits for the future: Annona. Available from: http://www.cropsforthefuture.org/publication/Factsheets/Factsheet-annona.pdf [Nov, 2012]. Institute of Irrigation and Development Studies, University of Southampton, Southampthon, UK.
  18. Kück, P., & Meusemann, K. (2010). FASconCAT: convenient handling of data matrices. Molecular Phylogenetics and Evolution, 56(3), 1115–1118.PubMedCrossRefGoogle Scholar
  19. Lima, N. B., Batista, M., De Morais, M. A., Jr., Barbosa, M. A. G., Michereff, S. J., Hyde, K. D., et al. (2013). Five Colletotrichum species are responsible for mango anthracnose in northeastern Brazil. Fungal Diversity, 61(1), 75–88.CrossRefGoogle Scholar
  20. Liu, F., Cai, L., Crous, P. W., & Damm, U. (2013a). Circumscription of the anthracnose pathogens Colletotrichum lindemuthianum and C. nigrum. Mycologia, 105(4), 844–860.PubMedCrossRefGoogle Scholar
  21. Liu, F., Damm, U., Cai, L., & Crous, P. W. (2013b). Species of the Colletotrichum gloeosporioides complex associated with anthracnose diseases of Proteaceae. Fungal Diversity, 61(1), 89–105.CrossRefGoogle Scholar
  22. Love, K., & Paull, R. E. (2011). Soursop. Fruits and Nuts F_N-22. USA: College of Tropical Agriculture and Human Resources, University of Hawai’i, HI.Google Scholar
  23. Maddison, W. P. & Maddison, D. R. (2011). Mesquite: a modular system for evolutionary analysis. Version 2.75. Available from: http://mesquiteproject.org. [Mar, 2013].
  24. Mills, P. R., Sreenivasaprasad, S., & Brown, A. E. (1992). Detection and differentiation of Colletotrichum gloeosporioides isolates using PCR. FEMS Microbiology Letters, 98(1), 137–143.CrossRefGoogle Scholar
  25. O’Connell, R. J., Thon, M. R., Hacquard, S., Amyotte, S. G., Kleemann, J., et al. (2012). Life-style transitions in plant pathogenic Colletotrichum fungi deciphered by genome and transcriptome analyses. Nature Genetics, 44, 1060–1065.PubMedCrossRefGoogle Scholar
  26. Pareek, S., Yahia, E. M., Pareek, O. P., & Kaushik, R. A. (2011). Postharvest physiology and technology of Annona fruits. Food Research International, 44(7), 1741–1751.CrossRefGoogle Scholar
  27. Phoulivong, S. (2011). Colletotrichum, naming, control, resistance, biocontrol of weeds and current challenges. Current Research in Environmental & Applied Mycology, 1(1), 53–73.Google Scholar
  28. Phoulivong, S., Cai, L., Chen, H., McKenzie, E. H. C., Abdelsalam, K., Chukeatirote, E., et al. (2010). Colletotrichum gloeosporioides is not a common pathogen on tropical fruits. Fungal Diversity, 44(1), 33–43.CrossRefGoogle Scholar
  29. Phoulivong, S., McKenzie, E. H. C., & Hyde, K. D. (2012). Cross infection of Colletotrichum species; a case study with tropical fruits. Current Research in Environmental & Applied Mycology, 2(2), 99–111.Google Scholar
  30. Pileggi, S. A., Vieira de Oliveira, S. F., Andrade, C. W., Vicente, V. A., Dalzoto, P. d. R., da Cruz, G., et al. (2009). Molecular and morphological markers for rapid distinction between two Colletotrichum species. Canadian Journal of Microbiology, 55(9), 1076–1088.PubMedCrossRefGoogle Scholar
  31. Posada, D. (2008). jModelTest: phylogenetic model averaging. Molecular Biology and Evolution, 25(7), 1253–1256.PubMedCrossRefGoogle Scholar
  32. 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.Google Scholar
  33. 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 Panamá: multilocus phylogenies distinguish host-associated pathogens from asymptomatic endophytes. Mycologia, 102(6), 1318–1338.PubMedCrossRefGoogle Scholar
  34. Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D., Darling, A., Höhna, S., et al. (2012). MrBayes v. 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology, 61(3), 539–542.PubMedCentralPubMedCrossRefGoogle Scholar
  35. Schena, L., Mosca, S., Cacciola, S. O., Faedda, R., Sanzani, S. M., Agosteo, G. E., et al. (2013). Species of the Colletotrichum gloeosporioides and C. boninense complexes associated with olive anthracnose. Plant Pathology. doi: 10.1111/ppa.12110.Google Scholar
  36. Sreenivasaprasad, S., Sharada, K., Brown, A. E., & Mills, P. R. (1996). PCR-based detection of Colletotrichum acutatum on strawberry. Plant Pathology, 45(4), 650–655.CrossRefGoogle Scholar
  37. Stöver, B. C., & Müller, K. F. (2010). TreeGraph 2: combining and visualizing evidence from different phylogenetic analyses. BMC Bioinformatics, 11, 7. doi: 10.1186/1471-2105-11-7.PubMedCentralPubMedCrossRefGoogle Scholar
  38. Sutton, B. C. (1992). The genus Glomerella and its anamorph Colletotrichum. In J. A. Bailey & M. J. Jeger (Eds.), Colletotrichum: Biology, Pathology and Control (pp. 1–26). Wallingford: CAB International.Google Scholar
  39. Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., & Kumar, S. (2011). MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution, 28(10), 2731–2739.PubMedCentralPubMedCrossRefGoogle Scholar
  40. Templeton, M. D., Rikkerink, E. H., 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(1), 225–230.PubMedCrossRefGoogle Scholar
  41. Than, P. P., Jeewon, R., Hyde, K. D., Pongsupasamit, S., Mongkolporn, O., & Taylor, P. W. J. (2008). Characterization and pathogenicity of Colletotrichum species associated with anthracnose on chilli (Capsicum spp.) in Thailand. Plant Pathology, 57(3), 562–572.CrossRefGoogle Scholar
  42. Udayanga, D., Manamgoda, D. S., Liu, X., Chukeatirote, E., & Hyde, K. D. (2013). What are the common anthracnose pathogens of tropical fruits? Fungal Diversity, 61(1), 165–179.CrossRefGoogle Scholar
  43. Weir, B. S., Johnston, P. R., & Damm, U. (2012). The Colletotrichum gloeosporioides species complex. Studies in Mycology, 73(1), 115–180.PubMedCentralPubMedGoogle Scholar
  44. White, T. J., Bruns, T., Lee, S., & Taylor, J. (1990). Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In M. A. Innis, D. H. Gelfand, & J. J. Sninsky (Eds.), PCR Protocols: A Guide to Methods and Applications (pp. 315–322). San Diego: Academic Press.Google Scholar

Copyright information

© KNPV 2014

Authors and Affiliations

  • Elizabeth Álvarez
    • 1
  • Lederson Gañán
    • 1
    • 2
  • Alberto Rojas-Triviño
    • 1
  • Juan F. Mejía
    • 1
  • Germán A. Llano
    • 1
  • Alonso González
    • 1
  1. 1.Plant Pathology, Tropical Fruit ProjectInternational Center for Tropical Agriculture (CIAT)CaliColombia
  2. 2.Laboratorio de Fitopatología, Departamento de Producción AgropecuariaUniversidad de CaldasManizalesColombia

Personalised recommendations