Skip to main content
Log in

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

  • Published:
European Journal of Plant Pathology Aims and scope Submit manuscript

Abstract

Anthracnose caused by Colletotrichum spp. is one of main strawberry diseases worldwide. The disease recently arrived in Iran and become epidemic in the Kurdistan province. A combination of morphological, molecular and pathogen-host interaction approaches (referred to the consolidated species concept) were applied to isolates from symptomatic strawberry tissues collected in Iran. Multi-gene phylogenetic analysis based on ITS-rDNA, beta-tubulin (TUB2) and glyceraldehyde-3-phosphate dehydrogenase (GAPDH) identified the species as the S5 clade of Colletotrichum nymphaeae. No significant intraspecies variation was observed in terms of morphology and pathogenicity. No significant genetic variation was observed among the isolates using inter simple sequence repeat analysis (ISSR) and primer pair combination of ERIC1/BOX and ERIC2/BOX fingerprinting markers. Based on the results of this study, it can be postulated that the C. nymphaeae population in Iran established itself from a single origin due to a founder effect. More generally, molecular dating based on relaxed clocks indicates co-radiation of C. nymphaeae S5 and strawberry plants and suggests high reciprocal specificity between the host and pathogen.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Armengol, J., Vicent, A., Leo’n,M., Berbegal, M., Abad-Campos, P., & García-Jiménez, J. (2010). Analysis of population structure of Rosellinia necatrix on Cyperus esculentus by mycelial compatibility and inter-simple sequence repeats (ISSR). Plant Pathology, 59, 179–185.

  • Arzanlou, M., Bakhshi, M., Karimi, K., & Torbati, M. (2015). Multigene phylogeny reveals three new records of Colletotrichum spp. and several new host records for the mycobiota of Iran. Journal of Plant Protection Research, 55(2), 198–211.

    Google Scholar 

  • Ayoubi, N., & Soleimani, J. (2013). Occurrence of strawberry anthracnose disease caused by Colletotrichum acutatum in Kurdistan province. 1th Iranian mycological congress. 3–5 September 2013. Rasht, Iran: University of Guilan.

    Google Scholar 

  • Baroncelli, R., Zapparata, A., Sarrocco, S., Sukno, S. A., Lane, C. R., Thon, M. R., Vannacci, G., Holub, E., & 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.

    Article  PubMed  PubMed Central  Google Scholar 

  • Bernstein, B., Zehr, E. I., Dean, R. A., & Shabi, E. (1995). Characteristics of Colletotrichum from peach, apple, pecan, and other hosts. Plant Disease, 79, 478–482.

    Article  Google Scholar 

  • Brown, A. E., Sreenivasaprasad, S., & Timmer, L. W. (1996). Molecular characterization of slow-growing orange and key lime anthracnose strains of Colletotrichum from citrus as C. acutatum. Phytopathology, 86, 523–527.

    Article  CAS  Google Scholar 

  • Buddie, A. G., Martínez-Culebras, P., Bridge, P. D., Garcia, M. D., Querol, A., Cannon, P. F., & Monte, E. (1999). Molecular characterization of Colletotrichum strains derived from strawberry. Mycological Research, 103(4), 385–394.

    Article  CAS  Google Scholar 

  • Cai, L., Hyde, K. D., Taylor, P. W. J., Weir, B. S., Waller, J., Abang, M. M., Zhang, J. Z., Yang, Y. L., Phoulivong, S., Liu, Z. Y., Prihastuti, H., Shivas, R. G., McKenzie, E. H. C., & Johnston, P. R. (2009). A polyphasic approach for studying Colletotrichum. Fungal Diversity, 39, 183–204.

    Google Scholar 

  • Curry, K. J., Abril, M., Avant, J. B., & Smith, B. J. (2002). Strawberry anthracnose: Histopathology of Colletotrichum acutatum and C. fragariae. Phytopathology, 92, 1055–1063.

    Article  PubMed  Google Scholar 

  • 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.

  • Damm, U., Cannon, P. F., Woudenberg, J. H. C., & Crous, P. W. (2012). The Colletotrichum acutatum species complex. Studies in Mycology, 73, 37–114.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Denoyes-Rothan, B., Guérin, G., Délye, C., Smith, B., Minz, D., Maymon, M., & Freeman, S. (2003). Genetic diversity and pathogenic variability among isolates of Colletotrichum species from strawberry. Phytopathology, 93, 219–228.

    Article  CAS  PubMed  Google Scholar 

  • Drummond, A. J., & Rambaut, A. (2007). BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evolutionary Biology, 7, 214.

    Article  PubMed  PubMed Central  Google Scholar 

  • Faedda, R., Agosteo, G. E., Schena, L., Mosca, S., Frisullo, S., Magnano, d. S. L. G., & Cacciola, S. O. (2011). Colletotrichum clavatum sp. nov. identified as the causal agent of olive anthracnose in Italy. Phytopathologia Mediterranea, 50, 283–302.

    CAS  Google Scholar 

  • Forster, H., & Adaskaveg, J. E. (1999). Identification of subpopulations of Colletotrichum acutatum and epidemiology of almond anthracnose in California. Phytopathology, 89(11), 1056–1065.

    Article  CAS  PubMed  Google Scholar 

  • Freeman, S., & Katan, T. (1997). Identification of Colletotrichum species responsible for anthracnose and root necrosis of strawberry in Israel. Phytopathology, 87, 516–521.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Hall, T. A. (1999). BioEdit: a user-friendly biological sequence alignment editor and analysis program for windows 95/98/NT. Nucleic Acids Symposium Series, 41, 95–98.

    CAS  Google Scholar 

  • Hantula, J., Lilja, A., & Parikka, P. (1997). Genetic variation and host specificity of Phytophthora cactorum isolated in Europe. Mycological Research, 101, 565–572.

    Article  Google Scholar 

  • Howard, C. M., Maas, J. L., Chandler, C. K., & Albregts, E. E. (1992). Anthracnose of strawberry caused by the Colletotrichum complex in Florida. Plant Disease, 76, 976–981.

    Article  Google Scholar 

  • 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 Diversity, 39, 147–182.

    Google Scholar 

  • Johnston, R. P., & Jones, D. (1997). Relationships among Colletotrichum isolates from fruit-rots assessed using rDNA sequences. Mycologia, 89(3), 420–430.

    Article  CAS  Google Scholar 

  • Kasuga, T., White, T. J., & Taylor, J. W. (2002). Estimation of nucleotide substitution rates in Eurotiomycete fungi. Molecular Biology and Evolution, 19(12), 2318–2324.

    Article  CAS  PubMed  Google Scholar 

  • Kück, P., & Meusemann, K. (2010). FASconCAT: Convenient handling of data matrices. Molecular Phylogenetics and Evolution, 56, 1115–1118.

    Article  PubMed  Google Scholar 

  • Lardner, R., Johnston, P. R., Plummer, K. M., & Pearson, M. N. (1999). Morphological and molecular analysis of Colletotrichum acutatum sensu lato. Mycological Research, 103, 275–285.

    Article  Google Scholar 

  • Liyanage, H. D., McMillan Jr., R. T., & Kistler, H. C. (1992). Two genetically distinct populations of Colletotrichum gloeosporioides from citrus. Phytopathology, 82, 1371–1376.

    Article  CAS  Google Scholar 

  • Mahmodi, F., Kadir, J. B., Puteh, A., Pourdad, S. S., Nasehi, A., & Soleimani, N. (2014). Genetic Diversity and Differentiation of Colletotrichum spp. Isolates Associated with Leguminosae Using Multigene Loci. RAPD and ISSR. Plant Pathology Journal, 30(1), 10–24.

    Article  CAS  PubMed  Google Scholar 

  • Mahuku, G. S., Henrı’quez, M. A., Mun˜ oz, J., & Buruchara, R. (2002). Molecular markers dispute the existence of the Afro-Andean group of the bean angular leaf spot pathogen, Phaeoisariopsis griseola. Phytopathology, 92, 580–589.

  • Möller, E. M., Bahnweg, G., & Geiger, H. H. (1992). A simple and efficient protocol for isolation of high molecular weight DNA from filamentous fungi, fruit bodies, and infected plant tissues. Nucleic Acids Research, 20(22), 6115–6116.

    Article  PubMed  PubMed Central  Google Scholar 

  • Nasehi, A., Kadir, J., Rashid, T. S., Awla, H. K., Golkhandan, E., & Mahmodi, F. (2016). Occurrence of anthracnose fruit rot caused by Colletotrichum nymphaeae on pepper (Capsicum annuum) in Malaysia. Plant Disease. doi:10.1094/PDIS-08-15-0876-PDN.

    Google Scholar 

  • Nirenberg, H. I., Feiler, U., & Hagedorn, G. (2002). Description of Colletotrichum lupini comb.nov. in modern terms. Mycologia, 94, 307–320.

    Article  PubMed  Google Scholar 

  • Njuguna, W., Liston, A., Cronn, R., Ashman, T.-L., & Bassil, N. (2013). Insights into phylogeny, sex function and age of Fragaria based on whole chloroplast genome sequencing. Molecular Phylogenetics and Evolution, 66, 17–29.

    Article  PubMed  Google Scholar 

  • Nylander, J. A. A. (2004). MrModeltest v2. Program distributed by the author. Evolutionary Biology Centre: Uppsala University.

    Google Scholar 

  • O’Donnell, K., & Cigelnik, E. (1997). Two divergent intragenomic rDNA ITS2 types within a monophyletic lineage of the fungus Fusarium are non orthologous. Molecular Phylogenetics and Evolution, 7, 103–116.

    Article  PubMed  Google Scholar 

  • Photita, W., Taylor, P. W. J., Ford, R., Hyde, K. D., & Lumyong, S. (2005). Morphological and molecular characterization of Colletotrichum species from herbaceous plants in Thailand. Fungal Diversity, 18, 117–133.

    Google Scholar 

  • Quaedvlieg, W., Binder, M., Groenewald, J. Z., Summerell, B. A., Carnegie, A. J., Burgess, T. I., & Crous, P. W. (2014). Introducing the Consolidated Species Concept to resolve species in the Teratosphaeriaceae. Persoonia, 33, 1–40.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ratanacherdchai, K., Wang, H. K., Lin, F. C., & Soytong, K. (2010). ISSR for comparison of cross-inoculation potential of Colletotrichum capsici causing chilli anthracnose. African Journal of Microbiology Research, 4, 76–83.

    CAS  Google Scholar 

  • Ronquist, F., & Huelsenbeck, J. P. (2003). MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics, 19, 1572–1574.

    Article  CAS  PubMed  Google Scholar 

  • Shivas, R. G., & Tan, Y. P. (2009). A taxonomic re-assessment of Colletotrichum acutatum, intro-ducing C. fioriniae comb. et stat. nov. and C. simmondsii sp. nov. Fungal Diversity, 39, 111–122.

    Google Scholar 

  • Simmonds, J. H. (1965). A study of the species of Colletotrichum causing ripe fruit rots in Queensland. Queensland Journal of Agricultural and Animal Science, 22, 437–459.

    Google Scholar 

  • Smith, B. J. (2008). Epidemiology and pathology of strawberry anthracnose: a north American perspective. Hortscience, 43(1), 69–73.

    Google Scholar 

  • Smith, H., Wingfield, M. J., Crous, P. W., & Coutinho, T. A. (1996). Sphaeropsis sapinea and Botryosphaeria dothidea endophytic in Pinus spp. and Eucalyptus spp. in South Africa. South African Journal of Botany, 62, 86–88.

    Article  Google Scholar 

  • 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, 361–378.

    Article  CAS  PubMed  Google Scholar 

  • Sreenivasaprasad, S., Mills, P. R., & Brown, A. E. (1994). Nucleotide sequence of the rDNA spacer 1 enables identification of isolates of Colletotrichum as C. acutatum. Mycological Research, 98, 186–188.

    Article  CAS  Google Scholar 

  • Staden, R. (1996). The staden sequence analysis package. Molecular Biotechnology, 5(3), 233–241.

    Article  CAS  PubMed  Google Scholar 

  • 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. 1–27). Wallingford: CAB International.

    Google Scholar 

  • Talhinhas, P., Sreenivasaprasad, S., Neves-Martin, J., & Oliveira, H. (2005). Molecular and phenotypic analyses reveal association of diverse Colletotrichum acutatum groups and a low level of C. gloeosporioides with olive anthracnose. Applied and Environmental Microbiology, 71, 2987–2998.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tehranifar, A., & Sarsaefi, M. (2002). Strawberry growing in Iran. Acta Horticulturae, 567, 547–549.

    Article  Google Scholar 

  • Ureña-Padilla, A. R., MacKenzie, S. J., Bowen, B. W., & Legard, D. E. (2002). Etiology and population genetics of Colletotrichum spp. causing crown and fruit rot of strawberry. Phytopathology, 92, 1245–1252.

    Article  PubMed  Google Scholar 

  • van der Aa, H. A. (1978). A leaf spot of Nymphaea alba in the Netherlands. Netherlands Journal of Plant Pathology, 84, 109–115.

    Article  Google Scholar 

  • Velho, A. C., Stadnik, M. J., Casanova, L., Mondino, P., & Alaniz, S. (2014). First report of Colletotrichum nymphaeae causing apple bitter rot in southern Brazil. Plant Disease Note, 98(4), 56.

    Google Scholar 

  • Versalovic, J., Koeuth, T., & Lupski, J. R. (1991). Distribution of repetitive DNA sequences in eubacteria and application to fingerprinting of bacterial genomes. Nucleic Acids Research, 19, 6823–6831.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Versalovic, J., Schneider, M., de Bruijn, F. J., & Lupski, J. R. (1994). Genomic fingerprinting of bacteria using repetitive sequence based polymerase chain reaction. Methods in Molecular and Cellular Biology, 5(1), 25–40.

    CAS  Google Scholar 

  • White, T. J., Bruns, T., & Taylor, J. (1990). Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In M. A. Innis, D. H. Gelfand, J. J. Sninsky, & J.W. White (Eds.), A guide to molecular methods and applications (pp. 482). New York: Academic Press, USA.

  • Whitelaw-Weckert, M. A., Curtin, S. J., Huang, R., Steel, C. C., Blanchard, C. L., & Roffey, P. E. (2007). Phylogenetic relationships and pathogenicity of Colletotrichum acutatum isolates from grape in subtropical Australia. Plant Pathology, 56, 448–463.

    Article  CAS  Google Scholar 

  • Yamagishi, N., Ishiyama, Y., Ogiso, H., Sato, T., & Tosa, Y. (2015). Life cycle and control of Colletotrichum nymphaeae, the causal agent of celery stunt anthracnose. Journal of General Plant Pathology, 81(4), 279–286.

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The authors would like to thank the research deputy of the University of Tabriz in Iran and the Fondazione Edmund Mach in Italy for financial support.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Mahdi Arzanlou.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Karimi, K., Babai Ahari, A., Arzanlou, M. et al. 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. Eur J Plant Pathol 147, 375–387 (2017). https://doi.org/10.1007/s10658-016-1009-4

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10658-016-1009-4

Keywords

Navigation