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Colletotrichum fructicola, a Member of Colletotrichum gloeosporioides sensu lato, is the Causal Agent of Anthracnose and Soft Rot in Avocado Fruits cv. "Hass"

  • 투고 : 2017.11.10
  • 심사 : 2018.01.11
  • 발행 : 2018.06.01

초록

The filamentous Ascomycota Colletotrichum gloeosporioides sensu lato is a fungus that has been reported worldwide as a causal agent of anthracnose disease in avocado and other crops. In Mexico, this species affects fruits from an early stage of development in the orchard until the post-harvest stage. Although fungicides are continuously applied to control Colletotrichum species, pericarp cankers and soft rot mesocarp in fruits are still frequently observed. Considering the lack of a precise description of the causative agent, the aim of the current study was to determine the pathogens involved in this symptomatology. Twenty-four isolates were consistently obtained from the pericarp of avocado fruits cv. "Hass" collected in the central avocado-producing area of Mexico. Morphological features such as colony growth, conidia size, and mycelial appressorium were assessed. Bayesian multilocus phylogenetic analyses were performed using amplified sequences of the internal transcribed spacer region of the nuclear ribosomal DNA; actin, chitin synthase, glyceraldehyde-3-phosphate dehydrogenase partial genes; and APn2-Mat1-2 intergenic spacer and mating type Mat1-2 partial gene from the nine selected isolates. In addition, fruits were inoculated with a conidial suspension and reproducible symptoms confirmed the presence of Colletotrichum fructicola in this area. This pathogenic species can now be added to those previously reported in the country, such as C. acutatum, C. boninense, C. godetiae, C. gloeosporioides, and C. karstii. Disease management programs to reduce the incidence of anthracnose should include C. fructicola to determine its response to fungicides that are routinely applied, considering that the appearance of new species is affecting the commercial quality of the fruits and shifting the original population structure.

키워드

참고문헌

  1. Freeman S, Katan T, Shabi E. Characterization of Colletotrichum species responsible for anthracnose diseases of various fruits. Plant Dis. 1998;82:596-605. https://doi.org/10.1094/PDIS.1998.82.6.596
  2. Silva DN, Talhinhas P, Varzea V, et al. Application of the Apn2/MAT locus to improve the systematics of the Colletotrichum gloeosporioides complex: an example from coffee (Coffea spp.) hosts. Mycologia. 2012;104:396-409. https://doi.org/10.3852/11-145
  3. Lima NB, Batista MV de A, De Morais MA Jr, et al. Five Colletotrichum species are responsible for mango anthracnose in north-eastern Brazil. Fungal Divers. 2013;61:75-88. https://doi.org/10.1007/s13225-013-0237-6
  4. Cristobal-Martinez AL, Ya-nez-Morales MJ, Solano-Vidal R, et al. Diversity of Colletotrichum species in coffee (Coffea arabica) plantantions in Mexico. Eur J Plant Pathol. 2017;147:605-614. https://doi.org/10.1007/s10658-016-1029-0
  5. Li H, Zhou G-Y, Liu J-A, et al. Population genetic analyses of the fungal pathogen Colletotrichum fructicola on tea-oil trees in China. PLoS One. 2016;11:e0156841. https://doi.org/10.1371/journal.pone.0156841
  6. Farr DF, Rossman AY. Fungal database:fungus-host distributions, U.S. National Fungus Collections, ARS, USDA [Internet]. [cited 2017 May 15]. Available from: https://nt.ars-grin.gov/fungaldatabases/
  7. Weir BS, Johnston PR, Damm U. The Colletotrichum gloeosporioides species complex. Stud Mycol. 2012;73:115-180. https://doi.org/10.3114/sim0011
  8. Jayawardena RS, Hyde KD, Damm U, et al. Notes of currently accepted species of Colletotrichum. Mycosphere. 2016;7:1192-1260. https://doi.org/10.5943/mycosphere/si/2c/9
  9. Diao YZ, Zhang C, Liu F, et al. Colletotrichum species causing anthracnose disease of chili in China. Persoonia. 2017;38:20-37. https://doi.org/10.3767/003158517X692788
  10. Guarnaccia V, Groenewald JZ, Polizzi G, et al. High species diversity in Colletotrichum associated with citrus diseases in Europe. Persoonia. 2017;39:32-50. https://doi.org/10.3767/persoonia.2017.39.02
  11. Dann EK, Ploetz RC, Coates LM, et al. Foliar, fruit and soil borne diseases. In: Schaffer B, Wolstenholme BN, Whiley AW, editors. The avocado, botany, production and uses. London: CAB International; 2013. p. 380-422.
  12. Sanders GM, Korsten L. A comparative morphological study of South African avocado and mango isolates of Colletotrichum gloeosporioides. Can J Bot. 2003;81:877-885. https://doi.org/10.1139/b03-073
  13. Freeman S, Minz D, Jurkevitch E, et al. Molecular analyses of Colletotrichum species from almond and other fruits. Phytopathology. 2000;90:608-614. https://doi.org/10.1094/PHYTO.2000.90.6.608
  14. Damm U, Cannon PF, Woudenberg JHC, et al. The Colletotrichum acutatum species complex. Stud Mycol. 2012;73:37-113. https://doi.org/10.3114/sim0010
  15. Silva-Rojas HV, Avila-Quezada GD. Phylogenetic and morphological identification of Colletotrichum boninense: a novel causal agent of anthracnose in avocado. Plant Pathol. 2011;60:899-908. https://doi.org/10.1111/j.1365-3059.2011.02452.x
  16. Hernandez-Lauzardo AN, Campos-Martinez A, Velazquez-del-Valle MG, et al. First report of Colletotrichum godetiae causing anthracnose on avocado in Mexico. Plant Dis. 2015;99:555.
  17. Velazquez-del-Valle MG, Campos-Martinez A, Flores-Moctezuma HE, et al. First report of avocado anthracnose caused by Colletotrichum karstii in Mexico. Plant Dis. 2016;100:534.
  18. Schoch CL, Seifert KA, Huhndorf S, et al. Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for fungi. Proc Natl Acad Sci USA. 2012;109:6241-6246. https://doi.org/10.1073/pnas.1117018109
  19. Abang MM, Winter S, Green KR, et al. Molecular identification of Colletotrichum gloeosporioides causing yam anthracnose in Nigeria. Plant Pathol. 2002;51:63-71. https://doi.org/10.1046/j.0032-0862.2001.00655.x
  20. Chung WH, Ishii H, Nishimura K, et al. Fungicide sensitivity and phylogenetic relationship of anthracnose fungi isolated from various fruit crops in Japan. Plant Dis. 2006;90:506-512. https://doi.org/10.1094/PD-90-0506
  21. Shivas RG, Tan YP. A taxonomic re-assessment of Colletotrichum acutatum, introducing C. fioriniae comb. et stat. nov. and C. simmondsii sp. nov. Fungal Divers. 2009;39:111-122.
  22. Damm U, Cannon PF, Woudenberg JHC, et al. The Colletotrichum boninense species complex. Stud Mycol. 2012;73:1-36. https://doi.org/10.3114/sim0002
  23. Liu F, Wang M, Damm U, et al. Species boundaries in plant pathogenic fungi: a Colletotrichum case study. BMC Evol Biol. 2016;16:81. https://doi.org/10.1186/s12862-016-0649-5
  24. Braganca CA, Damm U, Baroncelli R, et al. Species of Colletotrichum acutatum complex associated with anthracnose diseases of fruit in Brazil. Fungal Biol. 2016;120:547-561. https://doi.org/10.1016/j.funbio.2016.01.011
  25. Suzaki K. Improving method to induce sporulation of Colletotrichum gloeosporioides, causal fungus of grape ripe rot. J Gen Plant Pathol. 2011;77:81-84. https://doi.org/10.1007/s10327-011-0296-z
  26. Cai L, Hyde KD, Taylor PWJ, et al. A polyphasic approach for studying Colletotrichum. Fungal Divers. 2009;39:183-204.
  27. Doyle JJ, Doyle JL. Isolation of plant DNA from fresh tissue. Focus. 1990;12:13-15.
  28. White TJ, Bruns T, Lee S, et al. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, et al., editors. PCR protocols: a guide to methods and applications. New York: Academic Press; 1990. p. 315-322.
  29. Carbone I, Kohn LM. A method for designing primer sets for speciation studies in filamentous ascomycetes. Mycologia. 1999;91:553-556. https://doi.org/10.2307/3761358
  30. Templeton MD, Rikkerink EH, Solon SL, et al. Cloning and molecular characterization of the glyceraldehyde-3-phosphate dehydrogenase-encoding gene and cDNA from the plant pathogenic fungus Glomerella cingulata. Gene. 1992;122:225-230. https://doi.org/10.1016/0378-1119(92)90055-T
  31. Rojas EI, Renher SA, Samuels GJ, et al. Colletotrichum gloeosporioides s.l. associated with Theobroma cacao and other plants in Panama:multilocus phylogenies distinguish host-associated pathogens from asymptomatic endophytes. Mycologia. 2010;102:1318-1338. https://doi.org/10.3852/09-244
  32. Hall TA. BioEdit: a user-friendly biological sequence alignment editor and analysis program for windows 95/98/NT. Nucleic Acids Symp Ser. 1999;41:95-98.
  33. Maddison WP, Maddison DR. Mesquite: a modular system for evolutionary analysis version 3.10 [Internet]. 2016. Available from: http://mesquiteproject.org
  34. Ronquist F, Teslenko M, van der Mark P, et al. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol. 2012;61:539-542. https://doi.org/10.1093/sysbio/sys029
  35. Silvestro D, Michalak I. raxmlGUI: a graphical front-end for RAxML. Org Divers Evol. 2012;12:335-337. https://doi.org/10.1007/s13127-011-0056-0
  36. Nylander JAA. MrModeltest v2. Program distributed by the author. Evolutionary Biology Centre, Uppsala University; 2004.
  37. Johnston PR, Jones D. Relationship among Colletotrichum isolates from fruit-rots assessed using rDNA sequences. Mycologia. 1997;89:420-430. https://doi.org/10.1080/00275514.1997.12026801
  38. Yang YL, Liu ZY, Cai L, et al. Colletotrichum anthracnose of Amaryllidaceae. Fungal Divers. 2009;39:123-146.
  39. Prihastuti H, Cai L, Chen H, et al. Characterization of Colletotrichum species associated with coffee berries in northern Thailand. Fungal Divers. 2009;39:89-109.
  40. FAO. FAOSTAT [Internet] [cited 2017 Jan 20]. Available from: http://faostat.fao.org
  41. Flores D. Greater volume of Mexican avocados to the U. S. market. USDA [Internet]. USA; [cited 2017 Jan 25]. Available from: https://gain.fas.usda.gov/Recent%20GAIN%20Publications/Avocado%20Annual_Mexico%20City_Mexico_11-30-2016.pdf
  42. Campos-Martinez A, Velazquez-del-Valle MG, Flores-Moctezuma HE, et al. Antagonistic yeasts with potential to control Colletotrichum gloeosporioides (Penz.) & Sacc. and Colletotrichum acutatum J. H. Simmonds on avocado fruits. Crop Prot. 2016;89:101-104. https://doi.org/10.1016/j.cropro.2016.07.001
  43. Zhang PF, Zhai LF, Zhang XK, et al. Characterization of Colletotrichum fructicola, a new causal agent of leaf black spot disease of sandy pear (Pyrus pyrifolia). Eur J Plant Pathol. 2015;143:651-662. https://doi.org/10.1007/s10658-015-0715-7
  44. Alaniz S, Hernandez L, Mondino P. Colletotrichum fructicola is the dominant and one of the most aggressive species causing bitter rot of apple in Uruguay. Trop Plant Pathol. 2015;40:265-274. https://doi.org/10.1007/s40858-015-0025-9
  45. Gan P, Nakata N, Suzuki T, et al. Markers to differentiate species of anthracnose fungi identify Colletotrichum fructicola as the predominant virulent species in strawberry plants in Chiba Prefecture of Japan. J Gen Plant Pathol. 2017;83:14-22. https://doi.org/10.1007/s10327-016-0689-0
  46. Huang F, Chen GQ, Hou X, et al. Colletotrichum species associated with cultivated citrus in China. Fungal Divers. 2013;61:61-64. https://doi.org/10.1007/s13225-013-0232-y
  47. Nam MH, Park MS, Lee HD, et al. Taxonomic reevaluation of Colletotrichum gloeosporioides isolated from strawberry in Korea. Plant Pathol J. 2013;29:317-322. https://doi.org/10.5423/PPJ.NT.12.2012.0188
  48. Akgul DS, Awan QN, Guler PG, et al. First report of anthracnose and stem end rot diseases caused by Colletotrichum gloeosporioides and Neofusicoccum australe on avocado fruits in Turkey. Plant Dis. 2016;100:1792.
  49. Phoulivong S, Cai L, Chen H, et al. Colletotrichum gloeosporioides is not a common pathogen on tropical fruits. Fungal Divers. 2010;44:33-43. https://doi.org/10.1007/s13225-010-0046-0
  50. Sharma G, Kumar N, Weir BS, et al. The ApMat marker can resolve Colletotrichum species: a case study with Mangifera indica. Fungal Divers. 2013;61:117-138. https://doi.org/10.1007/s13225-013-0247-4
  51. Liu F, Weir BS, Damm U, et al. Unravelling Colletotrichum species associated with Camellia:employing ApMat and GS loci to resolve species in the C. gloeosporioides complex. Pers - Int Mycol J. 2015;35:63-86. https://doi.org/10.3767/003158515X687597
  52. Afanador-Kafuri L, Gonzalez A, Ga-nan L, et al. Characterization of the Colletotrichum species causing anthracnose in Andean blackberry in Colombia. Plant Dis. 2014;98:1503-1513. https://doi.org/10.1094/PDIS-07-13-0752-RE
  53. Velho AC, Alaniz S, Casanova L, et al. New insights into the characterization of Colletotrichum species associated with apple diseases in southern Brazil and Uruguay. Fungal Biol. 2015;119:229-244. https://doi.org/10.1016/j.funbio.2014.12.009

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  6. Multilocus identification and thiophanate‐methyl sensitivity of Colletotrichum gloeosporioides species complex associated with fruit with symptoms and symptomless leaves of mango vol.69, pp.6, 2018, https://doi.org/10.1111/ppa.13195
  7. Colletotrichum species causing anthracnose on avocado fruit in Mexico: Current status vol.69, pp.8, 2018, https://doi.org/10.1111/ppa.13234
  8. First Report of Anthracnose Caused by Colletotrichum fructicola on Tea in Taiwan vol.105, pp.3, 2018, https://doi.org/10.1094/pdis-06-20-1288-pdn
  9. Diversity of Colletotrichum Species Associated with Anthracnose Disease in Tropical Fruit Crops-A Review vol.11, pp.4, 2021, https://doi.org/10.3390/agriculture11040297
  10. Pest categorisation of Colletotrichum fructicola vol.19, pp.8, 2018, https://doi.org/10.2903/j.efsa.2021.6803