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ARS Home » Plains Area » Fargo, North Dakota » Edward T. Schafer Agricultural Research Center » Sugarbeet and Potato Research » Research » Publications at this Location » Publication #227230

Title: The Cladosporium fulvum virulence protein Avr2 inhibits host proteases require for basal defense

item VAN ESSE, H
item Bolton, Melvin

Submitted to: The Plant Cell
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 7/8/2008
Publication Date: 7/25/2008
Citation: van Esse, H.P., van't Klooster, J.W., Bolton, M.D., Yadeta, K.A., Van Baarlen, P., Boeren, S., Vervoort, J., de Wit, P.J.G.M., Thomma, B.P.H.J. 2008. The Cladosporium fulvum Virulence Protein Avr2 Inhibits Host Proteases Required for Basal Defense. The Plant Cell. 20:1948-1963.

Interpretive Summary: Plant pathogens produce molecules called “effector proteins” that are critical for causing disease on their plant hosts. Understanding effector protein function is important for studying pathogen biology and to learn how pathogens cause disease. The fungus Cladosporium fulvum causes leaf mold disease of tomato and is a model organism for studying effector protein function. In earlier work it was shown that the effector protein Avr2 binds to the tomato protein Rcr3. The binding of Rcr3 by Avr2 triggers immunity to C. fulvum when tomato plants have the resistance gene Cf-2. In the current study, it is shown that Avr2 function is required for full virulence of the pathogen. Expression of Avr2 in the plant species Arabidopsis thaliana and in tomato caused them to become more susceptible to other pathogens. Even with no pathogen present, expression of Avr2 in these plant species caused them to induce the expression of genes typically expressed after pathogen inoculation. Besides binding to Rcr3, this study shows that Avr2 binds other tomato proteins similar to Rcr3 and by doing so, results in their inactivation. Silencing of the Avr2 gene in C. fulvum reduces its ability to cause disease, suggesting that the inactivation of these tomato proteins is an important aspect of leaf mold disease.

Technical Abstract: Cladosporium fulvum (syn. Passalora fulva) is a biotrophic fungal pathogen that causes leaf mold of tomato. During growth in the apoplast, the fungus secretes effector proteins enabling it to establish disease. For most of these effectors, cognate C. fulvum resistance (Cf) loci have been identified that monitor the presence or the activity of the effector protein and mediate an immune response in tomato. We have previously shown that the Avr2 effector interacts with the apoplastic tomato cysteine 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 leads to enhanced susceptibility towards a number of extracellular fungal pathogens that include Botrytis cinerea and Verticillium dahliae, and microarray analysis of unchallenged plants showed that Avr2 expression triggers a global transcription pattern reflecting pathogen challenge. Cysteine protease activity profiling showed that Avr2 inhibits multiple extracellular Arabidopsis cysteine proteases. In tomato, Avr2 expression resulted in enhanced susceptibility not only towards natural Avr2-defective C. fulvum strains, but also towards B. cinerea and V. dahliae. Cysteine protease activity profiling in tomato revealed that also in this plant Avr2 inhibits multiple extracellular cysteine proteases, including Rcr3 and its close relative Pip1. Finally, silencing of the Avr2 gene in C. fulvum significantly compromised its virulence on tomato. We conclude that Avr2 is a genuine virulence factor of C. fulvum that inhibits several cysteine proteases required for plant basal defense in tomato. Moreover, heterologous expression in Arabidopsis and tomato enhances virulence of additional pathogens.