New races with unique mutations in avirulence genes overcoming tomato Cf resistance genes in a Japanese population of Cladosporium fulvum

Leaf mold of tomato is caused by the biotrophic fungus Cladosporium fulvum which complies with the gene-for-gene system indicating that each dominant pathogen avirulence (Avr) gene product is recognized by the product of a corresponding dominant host C. fulvum (Cf) resistance gene. As a result of selection pressure imposed by Cf genes often, pathogenic races developed adapted to the introduced Cf resistance genes. The fungus has been reported to occur on tomato in Japan since the 1920s. Initially only race 0, unable to overcome any of the known Cf genes, was reported. However, during the last two decades Cf resistance genes have been introduced and new races evolved adapted to corresponding Cf genes. Here we determined the virulence spectrum of 123 C. fulvum strains collected from different parts of Japan and sequenced their avirulence (Avr) genes to get detailed information on the molecular basis of adaptation to the different Cf genes. Ten races of C. fulvum were identified of which races 9, 2.9, 4.9 and 4.9.11 occur in Japan only. The Avr genes of these races contain unique mutations causing adaptation to Cf genes including (i) frameshift mutations and (ii) transposon insertions in Avr2, (iii) point mutations in Avr4 and Avr4E, and (iv) deletion of Avr4E and Avr9. It is concluded that molecular mechanisms of adaptation to different Cf genes in an isolated C. fulvum population in Japan are unique but follow similar patterns as those observed in other parts of the world.