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The Cladosporium fulvum Virulence Protein Avr2 Inhibits Host Proteases Required for Basal Defense^[W],[OA]

^a Laboratory of Phytopathology, Wageningen University, 6709 PD Wageningen, The Netherlands
^b Centre for BioSystems Genomics, 6700 AB Wageningen, The Netherlands
^c Department of Plant Pathology, North Dakota State University, Fargo, North Dakota 58105
^d U.S. Department of Agriculture–Agricultural Research Service, Northern Crop Science Laboratory, Fargo, North Dakota 58105
^e TI Food and Nutrition, 6700 AN Wageningen, the Netherlands
^f Centre for Molecular and Biomolecular Informatics, Nijmegen Centre for Molecular Life Sciences, Radboud University Medical Centre, 6500 HB Nijmegen, The Netherlands
^g Laboratory of Biochemistry, Wageningen University, 6703 HA Wageningen, The Netherlands

³ Address correspondence to bart.thomma{at}wur.nl.

Cladosporium fulvum (syn. Passalora fulva) is a biotrophic fungal pathogen that causes leaf mold of tomato (Solanum lycopersicum). During growth in the apoplast, the fungus establishes disease by secreting effector proteins, 10 of which have been characterized. We have previously shown that the Avr2 effector interacts with the apoplastic tomato Cys protease Rcr3, which is required for Cf-2–mediated immunity. We now show that Avr2 is a genuine virulence factor of C. fulvum. Heterologous expression of Avr2 in Arabidopsis thaliana causes enhanced susceptibility toward extracellular fungal pathogens, including Botrytis cinerea and Verticillium dahliae, and microarray analysis showed that Avr2 expression triggers a global transcriptome reflecting pathogen challenge. Cys protease activity profiling showed that Avr2 inhibits multiple extracellular Arabidopsis Cys proteases. In tomato, Avr2 expression caused enhanced susceptibility toward Avr2-defective C. fulvum strains and also toward B. cinerea and V. dahliae. Cys protease activity profiling in tomato revealed that, in this plant also, Avr2 inhibits multiple extracellular Cys proteases, including Rcr3 and its close relative Pip1. Finally, silencing of Avr2 significantly compromised C. fulvum virulence on tomato. We conclude that Avr2 is a genuine virulence factor of C. fulvum that inhibits several Cys proteases required for plant basal defense.

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