The biotrophic fungus Cladosporium fulvum circumvents Cf-4-mediated resistance by producing unstable AVR4 elicitors.

The avirulence gene Avr4 conditions avirulence of the biotrophic fungus Cladosporium fulvum on tomato genotypes carrying resistance gene Cf-4 (MM-Cf4). Strains of the fungus that circumvent Cf-4-specific resistance show various single point mutations in the coding region of the Avr4 gene. Similar to expression of the Avr4 gene, expression of the various virulent avr4 alleles is specifically induced during pathogenesis. Polyclonal antibodies raised against the AVR4 elicitor, however, did not detect AVR4 isoforms in MM-Cf4 plants infected by the different virulent strains, indicating that these isoforms are unstable. To analyze whether the AVR4 isoforms still possess specific elicitor activity, the avr4 alleles were expressed in MM-Cf4 plants by using the potato virus X (PVX)-based expression system. Inoculation with PVX::Avr4 resulted in the development of spreading lesions, eventually leading to plant death, whereas the various PVX::avr4 derivatives induced symptoms ranging from severe necrosis to no lesions at all. We conclude that instability of the AVR4 isoforms that are produced by virulent strains is a crucial factor in circumvention of Cf-4-mediated resistance.

Host resistance to a fungal tomato pathogen lost by a single base-pair change in an avirulence gene.

Host genotype specificity in interactions between biotrophic 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 host plant, respectively. Resistance, expressed by the induction of a hypersensitive response in the host, is envisaged to be based on recognition of the pathogen, mediated through direct interaction between products of pathogen avirulence genes (the so-called race-specific elicitors) and receptors in the host plant, the putative products of resistance genes. The interaction between the biotrophic fungus Cladosporium fulvum and its only host, tomato (Lycopersicon esculentum), is a well-established model system for studying fungus-plant gene-for-gene relationships. Here we report the isolation of race-specific elicitor AVR4 of C. fulvum and the cloning of its encoding avirulence gene. We present evidence that, in nature, a single base-pair change in this avirulence gene leads to virulence of races previously avirulent on tomato genotypes carrying the complementary Cf4 resistance gene.