Journal of General Plant Pathology

, Volume 78, Issue 5, pp 316–330 | Cite as

Colletotrichum carthami comb. nov., an anthracnose pathogen of safflower, garland chrysanthemum and pot marigold, revived by molecular phylogeny with authentic herbarium specimens

  • Seiji Uematsu
  • Koji Kageyama
  • Jouji Moriwaki
  • Toyozo SatoEmail author
Fungal Diseases


Authentic herbarium specimens of Gloeosporium carthami and G. chrysanthemi as well as live Colletotrichum strains from Carthamus tinctorius, Chrysanthemum coronarium var. spatiosum, and Calendula officinalis were judged to be conspecific based on morphological and molecular phylogenetic analyses. Representative strains from three asteraceous plants were demonstrated by inoculation tests to possess specific pathogenicity to the host plants. We propose a new combination, Colletotrichum carthami, for the anthracnose pathogen of the asteraceous plants, designating our specimen of G. carthami as its epitype. We characterize the species, which differs from the closely related Colletotrichum simmondsii in its pathogenicity and molecular characteristics.


Gloeosporium chrysanthemi Epitype β-Tubulin-2 gene Carthamus tinctorius Chrysanthemum coronarium var. spatiosum Calendula officinalis 



This work was sponsored by research grants from the NIAS Genebank Project in 2003 and Research and Development Projects for Application in Promoting New Policy of Agriculture, Forestry and Fisheries, Japan. We are grateful to Professor Dr. Hideki Takahashi, Hokkaido University Museum, for loaning herbarium specimens of G. carthami and G. chrysanthemi; Dr. Toshihiro Kajiwara for providing valuable suggestions and encouragement; Mr. Hiroei Kanno, Miyagi Prefectural Government, for providing the fungal strain from garland chrysanthemum, Dr. Urlike Damm, Centraalbureau voor Schimmelcultures, for sharing information on the phylogenetic placement of C. carthami; Dr. Kei Sugawara, Yamagata Prefectural Agricultural Technique Improvement Research Office, for the gift of safflower seeds; Dr. Tomiichi Takeda, Yamagata General Agricultural Research Center, for help with the collection of fungal materials; Ms. Kayoko Otsubo for technical support; Ms. Miki Kato, Mr. Haruhiko Kagawa, Mr. Yoshiyuki Ebihara, and Mr. Yoshihiko Kanegae of Chiba Prefectural Agriculture and Forestry Research Center and Ms. Silvia M. Kato of Assoiacao dos Floricultores da Regiao Dutra, Brasil, for assistance in morphological observation and inoculations.


  1. Cullen DW, Lees AK, Toth IK, Duncan JM (2002) Detection of Colletotrichum coccodes from soil and potato tubers by conventional and quantitative real-time PCR. Plant Pathol 51:281–292CrossRefGoogle Scholar
  2. Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791CrossRefGoogle Scholar
  3. Fukui T (1916) Some fungi on the useful plants in Japan (in Japanese). J Scient Agric Soc Tokyo 166:381–383Google Scholar
  4. Fujinaga M, Yamagishi N, Ogiso H, Takeuchi J, Moriwaki J, Sato T (2011) First report of celery stunt anthracnose caused by Colletotrichum simmondsii in Japan. J Gen Plant Pathol 77:243–247CrossRefGoogle Scholar
  5. Glass NL, Donaldson GC (1995) Development of primer sets designed for use with the PCR to amplify conserved genes form filamentous ascomycetes. Appl Environ Microbiol 61:1323–1330PubMedGoogle Scholar
  6. Guerber JC, Correll JC (2001) Characterization of Glomerella acutata, the teleomorph of Colletotrichum acutatum. Mycologia 93:216–229CrossRefGoogle Scholar
  7. Guerber JC, Liu B, Correll JC, Johnston PR (2003) Characterization of diversity in Colletotrichum acutatum sensu lato by sequence analysis of two gene introns, mtDNA and intron RFLPs, and mating compatibility. Mycologia 95:872–895PubMedCrossRefGoogle Scholar
  8. Hemmi T (1919) Vorläufige mitteilung ueber eine anthraknose von Carthamus tinctorius (in German). Ann Phytopathol Soc Jpn 1:1–11CrossRefGoogle Scholar
  9. Hotta M, Ogata K, Nitta A, Hoshikawa K, Yanagi M, Yamazaki K (eds) (1989) Useful plants of the world (in Japanese). Heibonsha Co, Tokyo, pp 191–192, 221–222, 259–260Google Scholar
  10. Johnston PR, Jones D (1997) Relationships among Colletotrichum isolates from fruit-rots assessed using rDNA sequences. Mycologia 89:420–430CrossRefGoogle Scholar
  11. Kanagawa T (2003) Bias and artifacts in multitemplate polymerase chain reactions (PCR). J Biosci Bioeng 96:317–323PubMedGoogle Scholar
  12. Kim WG, Moon YG, Cho WD, Park SD (1999) Anthracnose of safflower caused by Colletotrichum acutatum. Plant Pathol J 15:62–67Google Scholar
  13. Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120PubMedCrossRefGoogle Scholar
  14. Kwon JH, Kang SW, Kim HK, Park CS (1998) Safflower (Carthamus tinctorius L.) anthracnose caused by Colletotrichum acutatum in Korea (in Korean). Korean J Plant Pathol 14:651–653Google Scholar
  15. Lardner R, Johnston PR, Plummer KM, Pearson MN (1999) Morphological and molecular analysis of Colletotrichum acutatum sensu lato. Mycol Res 103:275–285CrossRefGoogle Scholar
  16. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948PubMedCrossRefGoogle Scholar
  17. Li M, Asano T, Suga H, Kageyama K (2011) A multiplex PCR for the detection of Phytophthora nicotianae and P. cactorum, and a survey of their occurrence in strawberry production areas of Japan. Plant Dis 95:1270–1278CrossRefGoogle Scholar
  18. Li W, Song S, Brlansky RH, Hartung JS (2007) Genetic diversity of citrus bacterial canker pathogens preserved in herbarium specimens. Proc Natl Acad Sci USA 104:18427–18432PubMedCrossRefGoogle Scholar
  19. Nakata K, Takimoto S (1928) Anthracnose of crown daisy, Glebionis coronaria (L.) Cass. ex Spach. In: descriptive catalogue of the Korean fungi (in Japanese). Ann Agric Expt Stat 15:87 (Gov Chosen)Google Scholar
  20. Numata I, Enjoji S, Urabe Y, Shoji H (1958) Anthracnose of Calendula officinalis (new disease) (abstract in Japanese). Ann Phytopathol Soc Jpn 23:21Google Scholar
  21. O’Donnell K, Cigelnik E (1997) Two divergent intragenomic rDNA ITS2 types within a monophyletic lineage of the fungus Fusarium are nonorthologous. Mol Phylogenet Evol 7:103–116PubMedCrossRefGoogle Scholar
  22. O’Gorman DT, Sholberg PL, Stokes SC, Ginns J (2008) DNA sequence analysis of herbarium specimens facilitates the revival of Botrytis mali, a postharvest pathogen of apple. Mycologia 100:227–235PubMedCrossRefGoogle Scholar
  23. Ristaino JB, Groves CT, Parra GR (2001) PCR amplification of the Irish potato famine pathogen from historic specimens. Nature 411:695–697PubMedCrossRefGoogle Scholar
  24. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425PubMedGoogle Scholar
  25. Sato T, Ueda S, Iijima A, Tezuka N (1996) Re-identification of pathogens of anemone and prune anthracnose. Ann Phytopathol Soc Jpn 62:170–174CrossRefGoogle Scholar
  26. Sato T, Uematsu S, Mizoguchi H, Kiku T, Miura T (1997) Anthracnose of prairie gentian and loquat caused by Colletotrichum acutatum. Ann Phytopathol Soc Jpn 63:16–20CrossRefGoogle Scholar
  27. Sawada K (1943) Descriptive catalogue of the Formosan fungi Part VIII-119. Anthracnose fungus of crown daisy, Glebionis coronaria (in Japanese). Rep Govt Res Inst Dep Agric, Formosa 85:81–82Google Scholar
  28. Shivas RG, Tan YP (2009) A taxonomic re-assessment of Colletotrichum acutatum, introducing C. fioriniae comb. et stat. nov. and C. simmondsii sp. nov. Fungal Divers 39:111–122Google Scholar
  29. Sreenivasaprasad S, Talhinhas P (2005) Genotypic and phenotypic diversity in Colletotrichum acutatum, a cosmopolitan pathogen causing anthracnose on a wide range of hosts. Mol Plant Pathol 6:361–378PubMedCrossRefGoogle Scholar
  30. Swofford DL (2002) PAUP*: Phylogenetic analysis using parsimony (*and other methods) ver. 4.0 beta 10. Sinauer, SunderlandGoogle Scholar
  31. Takimoto S (1924) Anthracnose of crown daisy, Glebionis coronaria (in Japanese). Nihon-engei-zasshi 36(9):27–28Google Scholar
  32. Tanaka T (1917) New Japanese fungi, notes and translations—I. Mycologia 9:167–172CrossRefGoogle Scholar
  33. Talhinhas P, Sreenivasaprasad S, Neves-Martins J, Oliveira H (2002) Genetic and morphological characterization of Colletotrichum acutatum causing anthracnose of lupins. Phytopathology 92:986–996PubMedCrossRefGoogle Scholar
  34. Talhinhas P, Sreenivasaprasad S, Neves-Martins 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. Appl Environ Microbiol 71:2987–2998PubMedCrossRefGoogle Scholar
  35. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The Clustal X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucl Acids Res 25:4876–4882PubMedCrossRefGoogle Scholar
  36. Ueda I, Kajiwara T (1968) Anthracnose of asteraceous plants (abstract in Japanese). Ann Phytopathol Soc Jpn 34:371Google Scholar
  37. Uematsu S, Kato SM, Moriwaki J, Sato T, Ebihara Y (2004) Anthracnose of Calendula officinalis, Chrysanthemum coronarium var. spatiosum and Carthamus tinctorius caused by Colletotrichum acutatum (abstract in Japanese). Ann Phytopathol Soc Jpn 70:47Google Scholar
  38. Víchová J, Vejražka K, Cholastová T, Pokorný R, Hrudová E (2011) Colletotrichum simmondsii causing anthracnose on safflower in the Czech Republic. Plant Dis 95:79CrossRefGoogle Scholar
  39. Vinnere O, Fatehi J, Wright SAI, Gerhardson B (2002) The causal agent of anthracnose of Rhododendron in Sweden and Latvia. Mycol Res 106:60–69CrossRefGoogle Scholar
  40. von Arx JA (1957) Die arten der gattung Colletotrichum Cda (in German). Phytopathol Z 29:413–468Google Scholar
  41. White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols: A guide to methods and applications. Academic Press, San Diego, pp 315–322Google Scholar

Copyright information

© The Phytopathological Society of Japan and Springer 2012

Authors and Affiliations

  • Seiji Uematsu
    • 1
  • Koji Kageyama
    • 2
  • Jouji Moriwaki
    • 3
  • Toyozo Sato
    • 4
    Email author
  1. 1.Southern Prefectural Horticulture InstituteChiba Prefectural Agriculture and Forestry Research CenterTateyamaJapan
  2. 2.River Basin Research CenterGifu UniversityGifuJapan
  3. 3.Horticultural Research InstituteToyama Prefectural Agricultural, Forestry & Fisheries Research CenterTonamiJapan
  4. 4.National Institute of Agrobiological SciencesTsukubaJapan

Personalised recommendations