Antonie van Leeuwenhoek

, Volume 65, Issue 3, pp 257–262 | Cite as

Molecular communication between host plant and the fungal tomato pathogenCladosporium fulvum

  • Pierre J. G. M. de Wit
  • Matthieu H. A. J. Joosten
  • Guy Honée
  • Jos P. Wubben
  • Guido F. J. M. van den Ackerveken
  • H. W. J. van den Broek


Host genotype specificity in interactions between biotrophic fungal pathogens and plants in most cases complies with the gene-for-gene model. Success or failure of infection is determined by absence or presence of complementary genes, avirulence and resistance genes, in the pathogen and the host plant, respectively. Resistance, expressed by the induction of a hypersensitive response followed by other defence responses in the host, is envisaged to be based on recognition of the pathogen, mediated through direct interaction between products of avirulence genes of the pathogen (the so-called race-specific elicitors) and receptors in the host plant, the putative products of resistance genes. The interaction between the biothrophic fungusCladosporium fulvum and its only host tomato is a model system to study fungus-plant gene-for-gene relationships. Here we report on isolation, characterization and biological function of putative pathogenicity factors ECP1 and ECP2 and the race-specific elicitors AVR4 and AVR9 ofC. fulvum and cloning and regulation of their encoding genes. Disruption ofecp1 andecp2 genes has no clear effect on pathogenicity ofC. fulvum. Disruption of theavr9 gene, which codes for the race-specific 28 amino acid AVR9 elicitor, in wild type avirulent races, leads to virulence on tomato genotypes carrying the complementary resistance geneCf9. The avirulence geneavr4 encodes a 105 amino acid race-specific elicitor. A single basepair change in the avirulence geneavr4 leads to virulence on tomato genotypes carrying theCf4 resistance gene.

Key words

pathogenicity genes avirulence genes race-specific elicitors resistance genes hypersensitive response host defense responses 


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  1. Bazan JF (1993) Emerging families of cytokines and receptors. Curr. Biol. 3: 603–606PubMedGoogle Scholar
  2. Danhash N, Wagemakers CAM, Van Kan JAL & De Wit PJGM (1993) Molecular characterization of four chitinase cDNAs obtained fromCladosporium fulvum-infected tomato. Plant Mol. Biol. 22: 1017–1029PubMedGoogle Scholar
  3. De Wit PJGM (1992) Molecular characterization of gene-for-gene systems in plant-fungus interactions and the application of avirulence genes in control of plant pathogens. Ann. Rev. Phytopathol. 30: 391–418Google Scholar
  4. De Wit PJGM & Spikman G (1982) Evidence for the occurrence of race and cultivar-specific elicitors of necrosis in intercellular fluids of compatible interactions ofCladosporium fulvum and tomato. Physiol. Plant Pathol. 21: 1–11Google Scholar
  5. De Wit PJGM & Van der Meer FE (1986) Accumulation of the pathogenesis-related tomato leaf protein P14 as an early indicator of incompatibility in the interaction betweenCladosporium fulvum (syn.Fulvia fulva) and tomato. Physiol. Mol. Plant Pathol. 28: 203–214Google Scholar
  6. De Wit PJGM, Hofman JE, Velthuis GCM & Ku〈cacute〉 JA (1985) Isolation and characterization of an elicitor of necrosis isolated from intercellular fluids of compatible interactions ofCladosporium fulvum (syn.Fulvia fulva) and tomato. Plant Physiol. 77: 642–47Google Scholar
  7. De Wit PJGM, Van den Ackerveken GFJM, Joosten MHAJ & Van Kan JAL (1989) Apoplastic proteins involved in communication between tomato and fungal pathogenCladosporium fulvum. In: Lugtenberg BJJ (Ed) Signal Molecules in Plants and Plant-Microbe Interactions (pp 273–280). Springer-Verlag, BerlinGoogle Scholar
  8. Flor HH (1942) Inheritance of pathogenicity inMelampsora lini. Phytopathology 32: 653–669Google Scholar
  9. Flor HH (1971) Current status of the gene-for-gene concept. Ann. Rev. Phytopathol. 9: 275–296Google Scholar
  10. Hammond-Kosack K, Oliver RP, Harrison K, Ashfield T & Jones JDG (1993) Studies on the mechanism by which tomato Cf (Cladosproium fulvum) resistance genes activate plant defence. In: Nester EW and Verma DPS (Eds) Advances in Molecular Genetics of Plant-Microbe Interactions, Vol 2 (pp 457–461). Kluwer Academic, DordrechtGoogle Scholar
  11. Higgins VJ & De Wit PJGM (1985) Use of race- and cultivar-specific elicitors from intercellular fluids for characterizing races ofCladosporium fulvum and resistant tomato cultivars. Phytopathology 75: 695–99Google Scholar
  12. Joosten MHAJ & De Wit PJGM (1988) Isolation, purification and preliminary characterization of a protein specific for compatibleCladosporium fulvum-tomato interactions. Physiol. Mol. Plant Pathol. 33: 241–253Google Scholar
  13. Joosten MHAJ & De Wit PJGM (1989) Identification of several pathogenesis-related proteins in tomato leaves inoculted withCladosporium fulvum (syn.Fulvia fulva) as 1,3-β-glucanases and chitinases. Plant Physiol. 89: 945–951Google Scholar
  14. Joosten MHAJ, Cozijnsen AJ & De Wit PJGM (1994) Host resistance to a fungal tomato pathogen lost by a single base-pair change in an avirulence gene. Nature 367: 384–386PubMedGoogle Scholar
  15. Keen NT (1990) Gene-for-gene complementarity in plant-pathogen interactions. Ann. Rev. Phytopathol. 24: 447–463Google Scholar
  16. Lindhout P, Korta W, Cislik M, Vos I & Gerlagh T (1989) Further identification of races ofCladosporium fulvum (Fulvia fulva) on tomato originating from the Netherlands, France and Poland. Neth. J. Plant Pathol. 95: 143–48Google Scholar
  17. Marmeisse R, Van den Ackerveken GFJM, Goosen T, De Wit PJGM & Van den Broek HWJ (1993) Disruption of the avirulence geneavr9 inCladosporium fulvum causes virulence on tomato genotypes with the complementary resistance gene Cf9. Mol. Plant-Microbe Interact. 6: 412–417Google Scholar
  18. Marmeisse R, Van den Ackerveken GFJM, Goosen T, De Wit PJGM & Van den Broek HWJ (1994) The in planta inducedecp2 gene of the tomato pathogenCladosporium fulvum is not essential for pathogenicity. Curr. Genet., in pressGoogle Scholar
  19. Peever TL & Higgins VJ (1989) Electrolyte leakage, lipoxygenase, and lipid peroxidation induced in tomato leaf tissue by specific and nonspecific elicitors fromCladosporium fulvum. Plant Physiol. 90: 867–75Google Scholar
  20. Rodrigo I, Vera P & Conejero V (1989) Degradation of tomato pathogenesis-related proteins by an endogeneous 37-kDa aspartyl endoproteinase. Eur. J. Biochem. 184: 663–669PubMedGoogle Scholar
  21. Scholtens-Toma IMJ & De Wit PJGM (1988) Purification and primary structure of a necrosis inducing peptide from the apoplastic fluids of tomato infected withCladosporium fulvum (syn.Fulvia fulva). Physiol. Mol. Plant Pathol. 33: 59–67Google Scholar
  22. Scholtens-Toma IMJ, De Wit GJM & De Wit PJGM (1989) Characterization of elicitor activities of apoplastic fluids isolated from tomato lines infected with new races ofCladosporium fulvum. Neth. J. Plant Pathol. 95: 161–68Google Scholar
  23. Van den Ackerveken GFJM, Van Kan JAL & De Wit PJGM (1992) Molecular analysis of the avirulence geneavr9 ofCladosporium fulvum fully supports the gene-for-gene hypothesis. Plant J. 2: 359–366PubMedGoogle Scholar
  24. Van den Ackerveken GFJM, Van Kan JAL, Joosten MHAJ, Muisers JM, Verbakel HM & De Wit PJGM (1993a) Isolation and characterization of two putative pathogenicity genes ofCladosporium fulvum Mol. Plant-Microbe Interact. 6: 210–215Google Scholar
  25. Van den Ackerveken GFJM, Vossen P & De Wit PJGM (1993b) The AVR9 race-specific elicitor ofCladosporium fulvum is processed by endogenous and plant proteases. Plant Physiol. 103: 91–96PubMedGoogle Scholar
  26. Van den Ackerveken GFJM, Dunn RM, Cozijnsen TJ, Vossen P, Van den Broek HWJ & De Wit PJGM (1994) Nitrogen limitation induces expression of the avirulence geneavr9 inCladosporium fulvum. Mol. Gen. Genet. 243: 277–285PubMedGoogle Scholar
  27. Van Kan JAL, Van den Ackerveken GFJM & De Wit PJGM (1991) Cloning and characterization of cDNA of avirulence geneavr9 of the fungal pathogenCladosporium fulvum, causal agent of tomato leaf mold. Mol. Plant-Microbe Interact. 4: 52–59PubMedGoogle Scholar
  28. Van Kan JAL, Joosten MHAJ, Wagemakers CAM, Van den Berg-Velthuis GCM & De Wit PJGM (1992) Differential accumulation of mRNAs encoding extracellular and intracellular PR proteins in tomato induced by virulent and avirulent races ofCladosporium fulvum. Plant Mol. Biol. 20: 513–527PubMedGoogle Scholar
  29. Vera-Estrella R, Blumwald E & Higgins VJ (1993) Effect of specific elicitors ofCladosporium fulvum on tomato suspension cells. Plant Physiol. 99: 1208–1215Google Scholar
  30. Wubben JP, Joosten MHAJ & De Wit PJGM (1994) Expression and localization of two in planta induced extracellular proteins of the fungal tomato pathogenCladosporium fulvum, submittedGoogle Scholar

Copyright information

© Kluwer Academic Publishers 1994

Authors and Affiliations

  • Pierre J. G. M. de Wit
    • 1
  • Matthieu H. A. J. Joosten
    • 1
  • Guy Honée
    • 1
  • Jos P. Wubben
    • 1
  • Guido F. J. M. van den Ackerveken
    • 2
    • 1
  • H. W. J. van den Broek
    • 3
    • 1
  1. 1.Department of PhytopathologyWageningen Agricultural UniversityWageningenThe Netherlands
  2. 2.Intitut de Sciences VégétalesCentre National de la Recherche ScientifiqueGif-sur-YvetteFrance
  3. 3.Department of GeneticsWageningen Agricultural UniversityWageningenThe Netherlands

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