OnlineFirst Articles
Research Papers

Diversity of Colletotrichum species on strawberry (Fragaria × ananassa) in Germany

PDF Suppl.
  • Christiane Rose,
  • Ulrike DAMM
Christiane Rose
Hochschule Geisenheim University, Von-Lade-Straße 1, D-65366 Geisenheim, Germany
Ulrike DAMM
Senckenberg Museum of Natural History Görlitz, PF 300 154, 02806 Görlitz
DOI: https://doi.org/10.36253/phyto-15094

Published 2024-07-17

Keywords

  • Anthracnose,
  • Colletotrichum acutatum,
  • C. dematium,
  • pathogenicity,
  • multi-locus phylogeny

How to Cite

[1]
C. ROSE and U. DAMM, “Diversity of Colletotrichum species on strawberry (Fragaria × ananassa) in Germany”, Phytopathol. Mediterr., pp. 155–178, Jul. 2024.

Copyright (c) 2024 Christiane Rose, Ulrike Damm

Creative Commons License

This work is licensed under a Creative Commons Attribution 4.0 International License.

Funding data

Crossref
Scopus
Google Scholar
Europe PMC

Abstract

Anthracnose caused by Colletotrichum species is an important disease of strawberries (Fragaria × ananassa), but the species causing this disease in Germany have not been investigated based on modern systematics. By using multi-locus phylogenetic analyses (ITS, act, gapdh, chs-1, his3, tub2), 58 Colletotrichum isolates from previous and recent collections, obtained mainly from fruit anthracnose of cultivated strawberries in Germany, were identified or re-identified as C. fioriniae, C. godetiae and C. nymphaeae (C. acutatum species complex) as well as C. anthrisci and C. lineola (C. dematium complex). Colletotrichum nymphaeae was dominant; most of the isolates belonged to one clonal lineage that occurs on strawberries throughout Europe, the United States of America, and some African and Asian countries. One of the other two haplotypes was distantly related and only represented by recently collected material. All other species, each of one haplotype, had only been isolated once or twice from German strawberries. This is the first report of C. anthrisci in Germany and for the genus Fragaria worldwide; all the other isolated fungi are newly reported for this genus in Germany. Comparisons of morphological characteristics of the species identified demonstrate that these features are of limited use for identification, even to species complex level. In pathogenicity tests, all five species caused anthracnose symptoms on ripe fruit of Fragaria × ananassa ‘Asia’.

PDF Suppl.

Downloads

Download data is not yet available.

Metrics

Metrics Loading ...

References

  1. Anonymous, 2011. Amtsblatt der Europäischen Union 2011: Official Journal of the European Union. https://eur-lex.europa.eu/legal-content/DE/TXT/PDF/?uri=CELEX: 32011R0543&from=PT
  2. Baroncelli R., Zapparata A., Sarrocco S., Sukno S.A., Lane C.R., … Sreenivasaprasad S., 2015. Molecular diversity of anthracnose pathogen populations associated with UK strawberry production suggests multiple introductions of three different Colletotrichum species. PLoS ONE 10(6): e0129140. https://doi.org/10.1371/journal.pone.0129140
  3. Bien S., Damm U., 2020. Prunus trees in Germany – a hideout of unknown fungi? Mycological Progress 19: 667–690. https://doi.org/10.1007/s11557-020-01586-4
  4. Bobev S.G., Zveibil A., Freeman S., 2002. First report of Colletotrichum acutatum on strawberry in Bulgaria. Plant Disease 86: 1178. https://doi.org/10.1094/PDIS.2002.86.10.1178A
  5. Brooks A.N., 1931. Anthracnose of strawberry caused by Colletotrichum fragariae, n. sp. Phytopathology 21 (7): 739–744.
  6. Bustamante M.I., Osorio-Navarro C., Fernández Y., Bourret T.B., Zamorano A., Henríquez-Sáez J.L., 2022. First record of Colletotrichum anthrisci causing anthracnose on avocado fruits in Chile. Pathogens 11: 1204. https://doi.org/10.3390/pathogens11101204
  7. Carbone I., 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
  8. Chen Y., Fu D., Wang W., Gleason M.L., Zhang R., … Sun G., 2022. Diversity of Colletotrichum species causing apple bitter rot and Glomerella leaf spot in China. Journal of Fungi 8, 740. https://doi.org/10.3390/jof8070740
  9. Chung P.C., Wu H.Y., Wang Y.W., Ariyawansa H.A., Hu H.P., ... Chung C.L., 2020. Diversity and pathogenicity of Colletotrichum species causing strawberry anthracnose in Taiwan and description of a new species, Colletotrichum miaoliense sp. nov. Scientific Reports 10: 14664. https://doi.org/10.1038/s41598-020-70878-2
  10. Crous P.W., Groenewald J.Z., Risede J.M., Hywel-Jones N.L., 2004. Calonectria species and their Cylindrocladium anamorphs: species with sphaeropedunculate vesicles. Studies in Mycology 50: 415–430. https://doi.org/10.3114/sim.55.1.213
  11. Crous P.W., Verkleij G.J.M., Groenewald J.Z., Houbraken J., 2019. Fungal biodiversity. Westerdijk Laboratory Manual Series 1. Westerdijk Fungal Biodiversity Institute, Utrecht, The Netherlands.
  12. Damm U., Cannon P.F., Woudenberg J.H.C., Crous P.W., 2012a. The Colletotrichum acutatum species complex. Studies in Mycology 73: 37–113. https://doi.org/10.3114/sim0010
  13. Damm U., Cannon P.F., Woudenberg J.H.C., Johnston P.R., Weir B., … Crous P.W., 2012b. The Colletotrichum boninense species complex. Studies in Mycology 73: 1–36. https://doi.org/10.3114/sim0002
  14. Damm U., Crous P.W., Fourie P.H., 2007. Botryosphaeriaceae as potential pathogens of Prunus species in South Africa, with descriptions of Diplodia africana and Lasiodiplodia plurivora spp. nov. Mycologia 99: 664–680. https://doi.org/10.3852/mycologia.99.5.664
  15. 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. https://doi.org/10.3767/003158508X324227
  16. Damm U., O’Connell R.J., Crous P.W., Groenewald J.Z., 2014. The Colletotrichum destructivum species complex – hemibiotrophic pathogens of forage and field crops. Studies in Mycology 79: 49–84. https://doi.org/10.1016/j.simyco.2014.09.003
  17. Damm U., Sato T., Alizadeh A., Groenewald J.Z., Crous P.W., 2019. The Colletotrichum draecaenophilum, C. magnum and C. orchidearum species complexes. Studies in Mycology 92: 1–46. https://doi.org/10.1016/j.simyco.2018.04.001
  18. Damm U., Sun Y.C., Huang C.J., 2020. Colletotrichum eriobotryae sp. nov. and C. nymphaeae, the anthracnose pathogens of loquat fruit in central Taiwan, and their sensitivity to azoxystrobin. Mycological Progress 19: 367–380. https://doi.org/10.1007/s11557-020-01565-9
  19. Damm U., Woudenberg J.H.C., Cannon P.F., Crous P.W., 2009. Colletotrichum species with curved conidia from herbaceous hosts. Fungal Diversity 39: 45–87. http://www.fungaldiversity.org /fdp/sfdp/FD39-3.pdf
  20. Dämmrich F., Gminder A., Hardtke H.J., Karasch P., Schmidt M., Wehr K., 2023. Datenbank der Pilze Deutschlands, Deutsche Gesellschaft für Mykologie e. V. http://www.pilze-deutschland.de/. Retrieved December 27 2023.
  21. Debode J., Van Hemelrijck W., Baeyen S., Creemers P., Heungens K., Maes M., 2009. Quantitative detection and monitoring of Colletotrichum acutatum in strawberry leaves using real-time PCR. Plant Pathology 58: 504–514. https://doi.org/10.1111/j.1365-3059.2008.01987.x
  22. Denoyes B., Baudry A., 1995. Species identification and pathogenicity study of French Colletotrichum strains isolated from strawberry using morphological and cultural characteristics. Phytopathology 85: 53–57. https://doi.org/10.1094/Phyto-85-53
  23. Farr D.F., Rossman A.Y., 2024. Fungal Databases, U.S. National Fungus Collections, ARS. USDA. http://nt.ars-grin.gov/fungaldatabases/. Retrieved April 23 2024.
  24. Gan P., Nakata N., Suzuki T., Shirasu K., 2017. Markers to differentiate species of anthracnose fungi identify Colletotrichum fructicola as the predominant virulent species in strawberry plants in Chiba Prefecture of Japan. Journal of General Plant Pathology 83: 14–22. https://doi.org/10.1007/s10327-016-0689-0
  25. Gardes M., Bruns T.D., 1993. ITS primers with enhanced specificity for basidiomycetes - application to the identification of mycorrhizae and rusts. Molecular Ecology 2: 113–118. https://doi.org/10.1111/j.1365-294X.1993.tb00005.x
  26. Garrido C., Carbú M., Fernández-Acero F.J., Budge G., Vallejo I., … Cantoral J. M., 2008. Isolation and pathogenicity of Colletotrichum spp. causing anthracnose of strawberry in south west Spain. European Journal of Plant Pathology 120: 409–415. https://doi.org/10.1007/s10658-007-9224-7
  27. Glass N.L., Donaldson G., 1995. Development of primer sets designed for use with PCR to amplify conserved genes from filamentous ascomycetes. Applied and Environmental Microbiology 61: 1323–1330. https://doi.org/10.1128/aem.61.4.1323-1330.1995
  28. Grammen A., Wenneker M., Van Campenhout J., Pham K.T.K., Van Hemelrijck W., … Keulemans W., 2019. Identification and pathogenicity assessment of Colletotrichum isolates causing bitter rot of apple fruit in Belgium. European Journal of Plant Pathology 153, 47–63. https://doi.org/10.1007/s10658-018-1539-z
  29. Guerber J.C., Liu B., Correll J.C., 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
  30. Guindon S., Dufayard J.-F., Lefort V., Anisimova M., Hordijk W., Gascuel O., 2010. New algorithms and methods to estimate Maximum-Likelihood phylogenies: assessing the performance of PhyML 3.0. Systematic Biology 59: 307–321. https://doi.org/10.1093/sysbio/ syq010
  31. Han Y.C., Zeng X.G., Xiang F.Y., Ren L., Chen F.Y., Gu Y.C., 2016. Distribution and characteristics of Colletotrichum spp. associated with anthracnose of strawberry in Hubei, China. Plant Disease 100: 996–1006. https://doi.org/10.1094/PDIS-09-15-1016-RE
  32. Hardigan M.A., Poorten T.J., Acharya C.B., Cole G.S., Hummer K.E., … Knapp S.J., 2018. Domestication of temperate and coastal hybrids with distinct ancestral gene selection in octoploid strawberry. The Plant Genome 11(3): 1–11. https://doi.org/10.3835/plantgenome2018.07.0049
  33. Hillis D.M., Bull J.J., 1993. An empirical test of bootstrapping as a method for assessing confidence in phylogenetic analysis. Systematic Biology 42: 182–192. https://doi.org/10.1093/sysbio/42.2.182
  34. Hoang D.T., Chernomor O., von Haeseler A., Minh B.Q., Vinh L.S., 2018. UFBoot2: improving the ultrafast bootstrap approximation. Molecular Biology and Evolution 35: 518–522. https://doi.org/10.1093/ molbev/msx281
  35. Howard C.M., Maas J.L., Chandle C.K., Albregts E.E., 1992. Anthracnose of strawberry caused by the Colletotrichum complex in Florida. Plant Disease 76: 976–981. https://doi.org/10.1094/PD-76-0976
  36. Jayawardena R.S., Huang J.K., Jin B.C., Yan J.Y., Li X., … Zhang G.Z., 2016. An account of Colletotrichum species associated with strawberry anthracnose in China based on morphology and molecular data. Mycosphere 7: 1147–1163. https://doi.org/10.5943/mycosphere/si/2c/6
  37. Kalyaanamoorthy S., Minh B.Q., Wong T.K.F., von Haeseler A., Jermiin L.S., 2017. Fast model selection for accurate phyloge netic estimates. Nature Methods 14: 587–589. https://doi.org/10.1038/nmeth. 4285
  38. Karimi K., Ahari A.B., Arzanlou M., Amini J., Pertot I., Rota-Stabelli O., 2017. Application of the consolidated species concept to identify the causal agent of strawberry anthracnose in Iran and initial molecular dating of the Colletotrichum acutatum species complex. European Journal of Plant Pathology 147: 375–387. https://doi.org/10.1007/s10658-016-1009-4
  39. Konno M., Iwamoto S., Seiwa K., 2011. Specialization of a fungal pathogen on host tree species in a cross-inoculation experiment. Journal of Ecology 99: 1394–1401. https://doi.org/10.1111/ j.1365-2745.2011.01869.x
  40. Laun N., Fried A., 1996. Anthraknose bei Erdbeeren - ein neues Pflanzenschutzproblem? Rheinische Monatsschrift 4/96: 232–235.
  41. Lehari G., 2002. Erdbeeren. Sorten und Anbau, Fitness und Gesundheit, feine Rezepte. Stuttgart (Hohenheim): Ulmer (Garten-fit).
  42. Liu F., Ma Z.Y., Hou L.W., Diao Y.Z., Wu W.P., … Cai L., 2022. Updating species diversity of Colletotrichum, with a phylogenomic overview. Studies in Mycology 101: 1–56. https://doi.org/10.3114/sim.2022.101.01
  43. MacKenzie S.J., Peres N.A., Barquero M.P., Arauz L.F., Timmer L.W., 2009. Host range and genetic relatedness of Colletotrichum acutatum isolates from fruit crops and leatherleaf fern in Florida. Phytopathology 99: 620–631. https://doi.org/10.1094/PHYTO-99-5-0620
  44. Marcelino J., Giordano R., Gouli S., Gouli V., Parker B.L., … Cesnik R., 2008. Colletotrichum acutatum var. fiori- (teleomorph: Glomerella acutata var. fioriniae var. nov.) infection of a scale insect. Mycologia 100: 353–374. doi: 10.3852/07-174R
  45. Minh B.Q., Nguyen M.A.T., von Haeseler A., 2013. Ultrafast approximation for phylogenetic bootstrap. Molecular Biology and Evolution 30: 1188–1195. https://doi.org/10.1093/molbev/mst024
  46. Moriwaki J., Sato T., Tsukiboshi T., 2003. Morphological and molecular characterization of Colletotrichum boninense sp. nov. from Japan. Mycoscience 44: 47–53. https://doi.org/10.1007/S10267-002-0079-7
  47. Nam M.H., Park M.S., Lee H.D., Yu S.H., 2013. Taxonomic reevaluation of Colletotrichum gloeosporioides isolated from strawberry in Korea. The Plant Pathology Journal 29: 317–322. https://doi.org/10.5423/PPJ.NT.12.2012.0188
  48. Nguyen L.-T., Schmidt H.A., von Haeseler A., Minh B.Q., 2015. IQ-TREE: A fast and effective stochastic algorithm for estimating maximum likelihood phylogenies. Molecular Biology and Evolution 32: 268–274. https://doi.org/10.1093/molbev/msu300
  49. Nilsson U., Carlson-Nilsson U., Svedelius G., 2005. First report of anthracnose fruit rot caused by Colletotrichum acutatum on strawberry in Sweden. Plant Disease 89: 1242. https://doi.org/10.1094/PD-89-1242C
  50. Nirenberg H.I., 1976. Untersuchungen über die morphologische und biologische Differenzierung in der Fusarium-Sektion Liseola. Mitteilungen aus der Biologischen Bundesanstalt für Land- und Forstwirtschaft Berlin-Dahlem 169: 1–117.
  51. Nirenberg H.I., Feiler U., Hagedorn G., 2002. Description of Colletotrichum lupini comb. nov. in modern terms. Mycologia 94: 307–320. https://doi.org/10.2307/3761809
  52. O’Donnell K., Cigelnik E., 1997. Two divergent intragenomic rDNA ITS2 types within a monophyletic lineage of the fungus Fusarium are nonorthologous. Molecular Phylogenetics and Evolution 7: 103–116. https://doi.org/10.1006/mpev.1996.0376
  53. Rambaut A., 2002. Sequence Alignment Editor. Version 2.0. University of Oxford, Oxford, UK.
  54. Rayner R.W., 1970. A mycological colour chart. Commonwealth Mycological Institute, Kew, UK. ISBN 0851980260
  55. Smith B.J., Black L.L., 1986. First report of Colletotrichum acutatum on strawberry in the United States. Plant Disease 70: 1074.
  56. Sreenivasaprasad S., Talhinhas P., 2005. Genotypic and phenotypic diversity in Colletotrichum acutatum, a cosmopolitan pathogen causing anthracnose on a wide range of hosts. Molecular Plant Pathology 6(4): 361–378 https://doi.org/10.1111/j.1364-3703.2005.00291.x
  57. Statistisches Bundesamt, 2023. Obst, Gemüse und Gartenbau. Betriebe, Anbauflächen, Erträge und Erntemengen von Gemüse. Betriebe, Anbauflächen, Erträge und Erntemengen von Gemüse und Erdbeeren 2022. Statistisches Bundesamt.
  58. Sundelin T., Schiller M., Lübeck M., Jensen D.F., Paaske K., Petersen B.D., 2005. First report of anthracnose fruit rot caused by Colletotrichum acutatum on strawberry in Denmark. Plant Disease 89: 432. https://doi.org/10.1094/PD-89-0432B
  59. Swofford D.L., 2003. PAUP*. Phylogenetic analysis using parsimony (* and other methods). Version 4.0b 10. Sinauer Associates, Sunderland. https://doi.org/10.1111/j.0014-3820.2002.tb00191.x
  60. Talhinhas P., Baroncelli R., 2021. Colletotrichum species and complexes: geographic distribution, host range and conservation status. Fungal Diversity 110: 109–198. https://doi.org/10.1007/s13225-021-00491-9
  61. Talhinhas P., Baroncelli R., 2023. Hosts of Colletotrichum. Mycosphere 14: 158–261, https://doi.org/10.5943/mycosphere/14/si2/4
  62. Trifinopoulos J., Nguyen L.T., von Haeseler A., Minh B.Q., 2016. W-IQ-TREE: a fast online phylogenetic tool for maximum likelihood analysis. Nucleic Acids Research 44(W1): W232–W235. https://doi.org/10.1093/nar/gkw256
  63. Tsvetkova Y.V., Kuznetsova A.A., 2022. Detection of anthracnose in strawberry and methods of etiological diagnosis. Doklady Biological Sciences 507: 473–484. https://doi.org/10.1134/S0012496622060229
  64. Wang N.Y., Forcelini B.B., Peres N.A., 2019. Anthracnose fruit and root necrosis of strawberry are caused by a dominant species within the Colletotrichum acutatum species complex in the United States. Phytopathology 109: 1293–1301. https://doi.org/10.1094/PHYTO-12-18-0454-R
  65. Weir B., Damm U., Johnston P.R., 2012. The Colletotrichum gloeosporioides species complex. Studies in Mycology 73: 115–213. https://doi.org/10.3114/sim0011
  66. White T.J., Bruns T., Lee S., Taylor J., 1990. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: PCR Protocols: a Guide to Methods and Applications (Innis MA, Gelfand DH, Sninsky JJ, White TJ, ed). Academic Press, San Diego, USA. 315–322. http://doi.org/10.1016/B978-0-12-372180-8.50042-1
  67. Woudenberg J.H.C., Aveskamp M.M., Gruyter J. de, Spiers A.G., Crous P.W., 2009. Multiple Didymella teleomorphs are linked to the Phoma clematidina morphotype. Persoonia 22: 56–62. https://doi.org/10.3767/003158509X427808
  68. Zapata M., Rodríguez-Serrano E., Castro J.F., Santelices C., Carrasco-Fernández J., … Palfner G., 2024. Novel species and records of Colletotrichum associated with native woody plants in south-central Chile. Mycological Progress 23: 18. https://doi.org/10.1007/s11557-024-01956-2
  69. Zhang Q., Nizamani M.M., Feng Y., Yang Y.Q., Jayawardena R.S., … Li C., 2023a. Genome-scale and multi-gene phylogenetic analyses of Colletotrichum spp. host preference and associated with medicinal plants. Mycosphere 14(2): 1–106. https://doi.org/10.5943/mycosphere/14/si2/1
  70. Zhang YX, Chen JW, Manawasinghe IS, Lin YH, Jayawardena RS, … Xiang MM., 2023b. Identification and characterization of Colletotrichum species associated with ornamental plants in Southern China. Mycosphere 14(2): 262–302. https://doi.org/10.5943/mycosphere/14/si2/5