Cerato-Ulmin, a Toxin Produced by the Pathogens of the Dutch Elm Disease

  • Giovanni Del Sorbo
  • Aniello Scala
  • Felice Scala
  • Stefania Tegli


Dutch elm disease (DED) is a destructive disease of both native European and North American elms. DED was first noticed in 1919 by the Dutch Phytopathological Service, when it was spread over large areas of Belgium, The Netherlands and part of Northern France. A few years later, the disease was described by Spierenburg (1921, 1922). The anamorphic stage of the causal agent was described as Graphium ulmi (Schwarz, 1922), and the sexual form as Ceratostomella ulmi (Buisman, 1932). The disease was named “Dutch” by some German and English researchers in recognition of the scientific studies made by the Dutch authors in the twenties (Holmes and Heybroek, I990). The pathogen was then named Ceratocystis ulmi (Buisman) C. Moreau and Ophiostoma ulmi (Buisman) Nannfeldt, and maintained these names for a long time.


Colony Morphology Aerial Hypha Schizophyllum Commune Cryphonectria Parasitica Hydrophobin Gene 
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  1. Bowden, C.G., Hintz, W.E., Jeng, R., Hubbes, M., and Horgen, P.A., 1994, Isolation and characterization of the cerato-ulmin toxin gene of the Dutch elm disease pathogen, Ophiostoma ulmi, Curr. Genet. 25: 323–329.PubMedCrossRefGoogle Scholar
  2. Bowden, C.G., Smalley, E., Guries, R.P., Hubbes, M., Temple, B., and Horgen, P.A., 1996, Lack of association between cerato-ulmin production and virulence in Ophiostoma novo-ulmi, Mol. Plant-Microbe Interact. 8: 556–564.CrossRefGoogle Scholar
  3. Brasier, C.M., Takai, S., Nordin, J.H., and Richards, W.C., 1990, Differences in cerato-ulmin production between the EAN, NAN and non aggressive subgroups of Ophiostoma ulmi, Plant Pathol. 39: 231–236.CrossRefGoogle Scholar
  4. Brasier, C.M., 1991, Ophiostoma novo-ulmi sp. nov. causative agent of the current Dutch elm disease epidemics, Mycopathologia 115: 151–161.Google Scholar
  5. Brasier, C.M. and Mehrotra, M.D., 1995, Ophiostoma himal-ulmi sp. nov., a new species of Dutch elm disease fungus endemic to the Himalayas, Mycol. Res. 99: 205–215.Google Scholar
  6. Brasier, C.M., Kirk, S.A., and Tegli, S., 1995, Naturally occurring non cerato-ulmin producing mutants of Ophiostoma novo-ulmi are pathogenic but lack aerial mycelium, Mycol. Res. 99: 436–440.CrossRefGoogle Scholar
  7. Brasier, C. M., Kirk, S. A., Pipe, N. D., and Buck, K. W., 1998, Rare interspecific hybrids in natural populations of the Dutch elm disease pathogens Ophiostoma ulmi and O. novo-ulmi, Mycol. Res. 102: 45–57.CrossRefGoogle Scholar
  8. Brotzman, H.G., and Campana, R.J., 1968, Viability in vitro of the smallest spores of Ceratocystis ulmi following centrifugation and microinfiltration, Phytopathology 58: 398.Google Scholar
  9. Buisman, C.J., 1932, Ceratostomella ulmi, de geskachtlijke vorm van Graphium ulmi Schwarz, Tijdschrift over Plantenziekten 38: 1–5.Google Scholar
  10. Vocht, M.L., Reviakine, I., Wosten, H.A., Brisson, A., Wessels, J.G., and Robillard, G.T., 2000, Structural and functional role of the disulfide bridges in the hydrophobin SC3, J. Biol. Chem. 275: 28428–28432.PubMedCrossRefGoogle Scholar
  11. Sorbo, G., Scala, F., Parrella, G., Lorito, M., Ruocco, M., and Scala, A., 2000, Functional expression of the gene cu, encoding the phytotoxic hydrophobin cerato-ulmin, enables Ophiostoma quercus, a non-pathogen on elm, to cause symptoms of Dutch elm disease, Mol. Plant-Microbe Interact. 13: 43–53.PubMedCrossRefGoogle Scholar
  12. Dons, J.J., Springer, J., Vries, S.C., and Wessels, J.G., 1984, Molecular cloning of a gene abundantly expressed during fruiting body initiation in Schizophyllum commune, J. Bacteriol. 157: 802–808.PubMedGoogle Scholar
  13. Doss, R.P., Potter, S.W., Chastagner, G.A., and Christian, J.K.,1993, Adhesion of nongerminated Botrytis cinerea conidia to several substrata, Appl. Environm. Microbiol. 59: 1786–1791.Google Scholar
  14. Et-Touil, A., Brasier, C.M., and Bemier, L., 1999, Localization ofa pathogenicity gene in Ophiostoma novo-ulmi and evidence that it may be introgressed from O. ulmi, Mol. Plant-Microbe Interact. 12: 6–15.CrossRefGoogle Scholar
  15. Gurr, S.J., Unkles, S. E., and Kinghorn, J.R. 1987. The structure and organization of nuclear genes of filamentous fungi, in: Gene Structure in Eukaryotic Microbes, J.R. Kinghorn, ed., IRL Press, Oxford, U.K., pp. 93–139.Google Scholar
  16. Holmes, W., and Heybroek, H.M., 1990, Dutch Elm Disease-The Early Papers: Selected Works of Seven Dutch Women Phytopathologists, APS Press, St. Paul, MN, USA.Google Scholar
  17. Kershaw, M.J., and Talbot, N.J., 1998, Hydrophobins and repellents: proteins with fundamental roles in fungal morphogenesis, Fungal Genet. Biol. 23: 18–33.PubMedCrossRefGoogle Scholar
  18. Klein, P., Kanehisa, M., and DeLisi, C., 1985, The detection and classification of membrane-spanning proteins, Biochim. Biophys. Acta,815: 468.Google Scholar
  19. Martin, F., Laurent, P., Carvalho, D., Burgess, T., Murphy, P., Nehis, U., and Tagu, D., 1995, Fungal gene expression during ectomycorrhiza formation, Can. J. Bot. 73 (suppl. 1): S541–S547.CrossRefGoogle Scholar
  20. McCabe, P.M., and Alfen, N.K., 1999, Secretion of cryparin, a fungal hydrophobin, Appl. Environ. Microbiol. 65: 5431–5435.PubMedGoogle Scholar
  21. McCabe, P.M., Pfeiffer, P., and Alfen, N.K., 1999, The influence of dsRNA viruses on the biology of plant pathogenic fungi, Trends Microbiol. 7: 377–381.PubMedCrossRefGoogle Scholar
  22. Nuske, J., and Fritsche, W., 1989, Phaseolotoxin production by Pseudomonas syringae pv. phaseolicola: the influence of temperature, J. Basic Microbiol. 29: 441–447.PubMedCrossRefGoogle Scholar
  23. Ouellette, G.B., and Gagnon, C., 1960, Formation of microendospores in Ceratocystis ulmi (Buism.)C. Moreau, Can. J. Bot. 38: 235–241.CrossRefGoogle Scholar
  24. Padgett, R.A., Grabowski, P.J., Konarska, M.M., Seiler, S., and Sharp, P.A., 1986, Splicing of messenger RNA precursors, Annu. Rev. Biochem. 55: 1119–1150.PubMedCrossRefGoogle Scholar
  25. Pipe, N.D., Buck, K.W., and Brasier, C.M., 1997, Comparison of the cerato-ulmin (cu) gene sequences of the Himalayan Dutch elm diease fungus Ophiostoma hima!-ulmi with those of O. u/mi and O. novo-ulmi suggests that the cu gene of O. novo-ulmi is unlikely to have been acquired recently from O. himal-ulmi, Mycol. Res. 101: 415–421.CrossRefGoogle Scholar
  26. Pipe, N.D., Brasier, C.M., and Buck, K.W., 2000, Two natural cerato-ulmin (CU)-deficient mutants of Ophiostoma novo-ulmi: one has an introgressed O. u/mi cu gene, the other has an O. novo-ulmi cu gene with a mutation in an intron splice consensus sequence, Mol. PL Pathol. 1: 379–382.CrossRefGoogle Scholar
  27. Richards, W.C., and Takai, S., 1984, Characterization of the toxicity ofcerato-ulmin, the toxin of Dutch elm disease, Can. J Pl. Pathol. 6: 291–298.CrossRefGoogle Scholar
  28. Richards, W.C., and Takai, S., 1988, Production of cerato-ulmin in white elm following artificial inoculation with Ceratocystis ulmi, Physiol. Mol. Pl. Pathol. 33: 279–285.CrossRefGoogle Scholar
  29. Richards, W.C., 1993, Cerato-ulmin: a unique wilt toxin of instrumental significance in the development of Dutch elm disease, in: Dutch Elm Disease Research: Cellular and Molecular Approaches, M.B. Sticklen and J.L. Sherald, eds., Springer-Verlag, New York.Google Scholar
  30. Scala, A., Tegli, S., Comparini, C., Mittempergher, L., Scala, F., and Del Sorbo, G., 1994, Influence of fungal inoculum on cerato-ulmin production; purification of cerato-ulmin and detection in elm sucker cuttings, Petria 4: 57–67.Google Scholar
  31. Scala, A., Pattuelli, M., Coppola, L., Guastini, M., Tegli, S., Del Sorbo, G., Mittempergher, L., and Scala, F., 1997a, Dutch elm disease progression and quantitative determination of cerato-ulmin in leaves, stems and branches of elms inoculated with Ophiostoma novo-ulmi and O. ulmi, Physiol, Mol. PL Pathol. 50: 349–360.CrossRefGoogle Scholar
  32. Scala, F., Bertelli, E., Coppola, L., Del Sorbo, G., Tegli, S., and Scala, A., 1997b, Comparative determination of ceratoulmin on cell surface and in mycelial extracts of pathogenic and non-pathogenic Ophiostoma species, Mycol. Res. 101: 829–834.CrossRefGoogle Scholar
  33. Scheffer, R.J., Liem, J.I., and Elgersma, D.D., 1987, Production in vitro of phytotoxic compounds by non-aggressive and aggressive isolates of Ophiostoma ulmi, the Dutch elm disease pathogen, Physiol. Mol. Pl. Pathol. 30: 321–335.CrossRefGoogle Scholar
  34. Schuren, F.H.J., and Wessels, J.G.H., 1990, Two genes specifically expressed in fruiting dikaryons of Schizophyllum commune: homologies with a gene not regulated by mating type genes, Gene 90: 199–205.PubMedCrossRefGoogle Scholar
  35. Schwarz, M.B., 1922, Das zweigsterben der Ulmen, Trauerweiden und Pfirsichbaume, ein vergleichend-pathologischeStudie, Doctor’s disseration, University of Utrecht (reported in Holmes and Heibroek, cited op.).Google Scholar
  36. Segers, G.C., Hamada, W., Oliver, R.P., and Spanu, P.D., 1999, Isolation and characterisation of five different hydrophobin-encoding cDNAs from the fungal tomato pathogen Cladosporium fulvum, Mol. Gen. Genet. 261: 644–652.PubMedCrossRefGoogle Scholar
  37. Spierenburg, D., 1921, Een onbekende ziekte in de iepen Plantenziektenkundinge Waarnemingen I. Mededelingen 18 van den Phytopathologischen Dienst, 3–10.Google Scholar
  38. Spierenburg, D., 1922, Een onbekende ziekte in de iepen Plantenziektenkundinge Waarnemingen III. Verslagen en Mededelingen van den Phytopathologischen Dienst te Wageningen 24: 1–31.Google Scholar
  39. Leger, R.J., Staples, R.C., and Roberts, D.W., 1992, Cloning and regulatory analysis of starvation-stress gene ssgA, encoding a hydrophobin-like protein from the entomopathogenic fungus Metarhizium anisopliae, Gene 120: 119–124.CrossRefGoogle Scholar
  40. Stevenson, K.J., Slater, J.A., and Takai, S., 1979, Cerato-ulmin: a wilting toxin of Dutch elm disease fungus, Phytochemistry 18: 235–238.CrossRefGoogle Scholar
  41. Stringer, M.A., and Timberlake, W.E., 1993, Cerato-ulmin, a toxin involved in Dutch elm disease, is a fungal hydrophobin, The Plant Cell 5: 145–146.PubMedGoogle Scholar
  42. Sutherland, M.L., and Brasier, C.M., 1995, Effect of d-factors on in vitro cerato-ulmin production by the Dutch elm disease pathogen Ophiostoma novo-ulmi, Mycol. Res. 99: 1211–1217.CrossRefGoogle Scholar
  43. Takai, S., 1974, Pathogenicity and cerato-ulmin production in Ceratocystis ulmi, Nature 252: 124–126.PubMedCrossRefGoogle Scholar
  44. Takai, S., 1978, Cerato-ulmin, a wilting toxin of Ceratocystis ulmi: cultural factors affecting cerato-ulmin production by the fungus, J. Phytopathol. 91: 147–158.CrossRefGoogle Scholar
  45. Takai, S. and Richards, W.C., 1978, Cerato-ulmin, a wilting toxin of Ceratocystis ulmi: isolation and some properties of cerato-ulmin from the culture of C. ulmi. Phytopathologische Zeitschrift 91: 129–146.CrossRefGoogle Scholar
  46. Takai, S., Richards, W.C., Hiratsuka, Y., and Stevenson, K.J., 1979, Cerato-ulmin, a semi pathotoxin of Ceratocystis ulmi, in: Recognition and Specificity in Plant Host-Parasite Interactions, J.M. Daly and I. Uritani, eds., Japan Science Society Press, Tokyo.Google Scholar
  47. Takai, S., Richards, W.C., and Stevenson, K.J., 1983, Evidence for the involvement of cerato-ulmin, the Ceratocystis ulmi toxin, in the development of Dutch elm disease, Physiol. PI. Pathol. 23: 275–280.CrossRefGoogle Scholar
  48. Takai, S., and Hiratsuka, Y., 1984, Scanning electron microscope observations of internal symptoms of white elm following Ceratocystis ulmi infection and cerato-ulmin treatment, Can. J. Bot. 62: 1365–1371.CrossRefGoogle Scholar
  49. Talbot, N.J., Kershaw, M.J., Wakley, G.E., Devries, O.M.H., Wessels, J.G.H., and Hamer, J.E., 1996, MPG1 encodes a fungal hydrophobin involved in surface interactions during infection-related development of Magnaporthe grisea, The Plant Cell 8: 985–999.PubMedGoogle Scholar
  50. Talbot, N.J., 1999, Fungal biology. Coming up for air and sporulation, Nature 398: 295–296.PubMedCrossRefGoogle Scholar
  51. Tegli, S., Comparini, C., Giannetti, C., and Scala, A., I994a, Effect of temperature on growth and cerato-ulmin production of Ophiostoma novo-ulmi and O. ulmi, Mycol. Res. 98: 408–412.Google Scholar
  52. Tegli, S., Comparini, C., Giannetti, C., and Scala, A., 1994b, Effect of cerato-ulmin on survival of in vitro elm callus and cells, Giornale Botanico Italiano 127: 190–191.Google Scholar
  53. Tegli, S., and Scala, A., 1996, Isolation and characterization of non cerato-ulmin producing laboratory induced mutants of Ophiostoma novo-ulmi, Mycol. Res. 100: 661–668.CrossRefGoogle Scholar
  54. Temple, B., Horgen, P.A., Bernier, L., and Hintz, W.E., 1997, Cerato-ulmin, a hydrophobin secreted by the causal agents of Dutch elm disease, is a parasitic fitness factor, Fungal Genet. Biol. 22: 39–53.PubMedCrossRefGoogle Scholar
  55. Thompson, J.D., Higgins, D.G., and Gibson T.J., 1994, CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice, Nucl. Acids Res. 22: 4673–4680.PubMedCrossRefGoogle Scholar
  56. Van Wetter, M.A., Schuren, F.H.J., Schuurs, T.A., and Wessels, J.G.H., 1996, Targeted mutation of the Sc3 hydrophobin gene of Schizophyllum commune affects formation of aerial hyphae, FEMS Microbiol. Lett. 140: 265–269.CrossRefGoogle Scholar
  57. Wessels, J.G.H., De Vries, O.M.H., Asgerirsdottir, S.A., and Schuren, F.H.J., 1991, Hydrophobin genes involved in formation of aerial hyphae and fruit bodies in Schizophyllum, The Plant Cell 3: 793–799.PubMedGoogle Scholar
  58. Wessels, J.G.H., 1992, Gene expression during fruiting in Schizophyllum commune, Mycol. Res. 96: 609–620.CrossRefGoogle Scholar
  59. Wessels, J.G.H., 1997, Hydrophobins: proteins that change the nature of the fungal surface, Adv. Microbial Physiol. 38: 1–45.CrossRefGoogle Scholar
  60. Wessels, J.G., 1999, Fungi in their own right, Fungal Genet. Biol. 27: 134–145.PubMedCrossRefGoogle Scholar
  61. Wosten, H.A., Wetter, M.A., Lugones, L.G., Mei, H.C., Busscher, H.J., and Wessels, J.G., 1999, How a fungus escapes the water to grow into the air, Curr. Biol. 9: 85–88.PubMedCrossRefGoogle Scholar
  62. Wosten, H.A., and De Vocht, M.L., 2000, Hydrophobins, the fungal coat unravelled, Biochim. Biophys. Acta 1469: 79–86.Google Scholar
  63. Wu, W.D., Jeng, R.S., and Hubbes, M., 1989, Toxic effects of elm phytoalexin mansonones on Ophiostoma ulmi, the causal agent of Dutch elm disease, Eur. J. For. Pathol. 19: 343–357.CrossRefGoogle Scholar
  64. Yaguchi, M., Pusztai-Carey, M., Roy, C., Surewicz, W.K., Carey, P.R., Stevenson, K.J., Richards, W.C., and Takai, S.,1993, Amino-acid sequence and spectroscopic studies of Dutch elm disease toxin, cerato-ulmin, in: Dutch Elm Disease Research: Cellular and Molecular Approaches S.J.L., Sticklen M.B., ed., Springer-Verlag, New-York.Google Scholar
  65. Zentmyer, G.A., 1942, Toxin formation by Ceratostomella ulmi, Science 95: 512–513.PubMedCrossRefGoogle Scholar
  66. Zhang, L., Villalon, D., Sin, Y., Kazmierczak, P., and Van Alfen, N.K., 1994, Virus-associated down-regulation of the gene encoding cryparin, an abundant cell surface protein of the chestnut blight fungus Cryphonectria parasitica, Gene 139: 59–64.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2002

Authors and Affiliations

  • Giovanni Del Sorbo
    • 1
  • Aniello Scala
    • 2
  • Felice Scala
    • 1
  • Stefania Tegli
    • 2
  1. 1.Department Ar.Bo.Pa.Ve., Section of Plant PathologyUniversity of NaplesPortici (NA)Italy
  2. 2.Department of Agricultural Biotechnology, Section of Plant PathologyUniversity of FlorenceFlorenceItaly

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