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Transcriptome Sequencing Uncovers the Avr5 Avirulence Gene of the Tomato Leaf Mold Pathogen Cladosporium fulvum

August 2014 , Volume 27 , Number  8
Pages  846 - 857

Carl H. Mesarich,1 Scott A. Griffiths,1 Ate van der Burgt,1 Bilal Ökmen,1 Henriek G. Beenen,1 Desalegn W. Etalo,2 Matthieu H. A. J. Joosten,1 and Pierre J. G. M. de Wit1,3

1Laboratory of Phytopathology, and 2Laboratory of Plant Physiology, Wageningen University, Droevendaalsesteeg 1, 6708 PB Wageningen, The Netherlands; 3Centre for BioSystems Genomics, P.O. Box 98, 6700 AB Wageningen, The Netherlands

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Accepted 19 March 2014.

The Cf-5 gene of tomato confers resistance to strains of the fungal pathogen Cladosporium fulvum carrying the avirulence gene Avr5. Although Cf-5 has been cloned, Avr5 has remained elusive. We report the cloning of Avr5 using a combined bioinformatic and transcriptome sequencing approach. RNA-Seq was performed on the sequenced race 0 strain (0WU; carrying Avr5), as well as a race 5 strain (IPO 1979; lacking a functional Avr5 gene) during infection of susceptible tomato. Forty-four in planta–induced C. fulvum candidate effector (CfCE) genes of 0WU were identified that putatively encode a secreted, small cysteine-rich protein. An expressed transcript sequence comparison between strains revealed two polymorphic CfCE genes in IPO 1979. One of these conferred avirulence to IPO 1979 on Cf-5 tomato following complementation with the corresponding 0WU allele, confirming identification of Avr5. Complementation also led to increased fungal biomass during infection of susceptible tomato, signifying a role for Avr5 in virulence. Seven of eight race 5 strains investigated escape Cf-5-mediated resistance through deletion of the Avr5 gene. Avr5 is heavily flanked by repetitive elements, suggesting that repeat instability, in combination with Cf-5-mediated selection pressure, has led to the emergence of race 5 strains deleted for the Avr5 gene.

© 2014 The American Phytopathological Society