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

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Abstract
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.