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Allelic Variation in the Effector Genes of the Tomato Pathogen Cladosporium fulvum Reveals Different Modes of Adaptive Evolution

October 2007 , Volume 20 , Number  10
Pages  1,271 - 1,283

Ioannis Stergiopoulos,1 Maarten J. D. De Kock,1,2 Pim Lindhout,2 and Pierre J. G. M. De Wit1

1Laboratory of Phytopathology, Wageningen University & Research Centre, Binnenhaven 5, 6709 PD Wageningen, The Netherlands; 2Laboratory of Plant Breeding, Wageningen University & Research Centre, Droevendaalsesteeg 1, 6708 PB Wageningen, The Netherlands

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Accepted 14 June 2007.

The allelic variation in four avirulence (Avr) and four extracellular protein (Ecp)--encoding genes of the tomato pathogen Cladosporium fulvum was analyzed for a worldwide collection of strains. The majority of polymorphisms observed in the Avr genes are deletions, point mutations, or insertions of transposon-like elements that are associated with transitions from avirulence to virulence, indicating adaptive evolution of the Avr genes to the cognate C. fulvum resistance genes that are deployed in commercial tomato lines. Large differences in types of polymorphisms between the Avr genes were observed, especially between Avr2 (indels) and Avr4 (amino-acid substitutions), indicating that selection pressure favors different types of adaptation. In contrast, only a limited number of polymorphisms were observed in the Ecp genes, which mostly involved synonymous modifications. A haplotype network based on the polymorphisms observed in the effector genes revealed a complex pattern of evolution marked by reticulations that suggests the occurrence of genetic recombination in this presumed asexual fungus. This, as well as the identification of strains with identical polymorphisms in Avr and Ecp genes but with opposite mating-type genes, suggests that development of complex races can be the combined result of positive selection and genetic recombination.

Additional keywords: haplotype variation, single nucleotide polymorphisms (SNP).

© 2007 The American Phytopathological Society