9Natural plant populations encounter strong pathogen pressure and defense-associated genes are 2 0 known to be under different selection pressure dependent on the pressure by the pathogens. Here 2 1 we use wild tomato Solanum chilense populations to investigate natural resistance against 2 2 Cladosporium fulvum, a well-known pathogenic fungus of domesticated tomatoes. We show that 2 3 populations of S. chilense differ in resistance against the pathogen. Next, we explored the 2 4underlying molecular processes in a species wide-context. Then, focusing on recognition of the 2 5 two prominent avirulence factors secreted by C. fulvum (Avr4 and Avr9) in central and northern 2 6 populations of S. chilense we observed high complexity in the cognate homologues of 2 7Cladosporium resistance (Hcr9) locus underlying the recognition of these effectors. Presence of 2 8 canonical genomic regions coding for Cf-4 and Cf-9, two major dominant resistance genes in the 2 9Hcr9 locus recognizing Avr4 and Avr9, respectively, does not meet prediction from Avr 3 0 response phenotypes. We find both genes in varying fractions of the plant populations and we 3 1show possible co-existence of two functionally active resistance genes, previously thought to be 3 2 allelic. Additionally, we observed the complete local absence of recognition of additional Avr 3 3 proteins of C. fulvum. In the southern populations we attribute this to changes in the coregulatory 3 4 network. As a result of loss of pathogen pressure or adaptation to extreme climatic conditions. 5This may ultimately explain the observed pathogen susceptibility in the southern populations. 6This work puts major gene mediated disease resistance in an ecological context. 3 7 3 8 3 9
Natural plant populations encounter strong pathogen pressure and defence-associated genes are known to be under selection dependent on the pressure by the pathogens. Here, we use populations of the wild tomato Solanum chilense to investigate natural resistance against Cladosporium fulvum , a well-known ascomycete pathogen of domesticated tomatoes. Host populations used are from distinct geographical origins and share a defined evolutionary history. We show that distinct populations of S. chilense differ in resistance against the pathogen. Screening for major resistance gene-mediated pathogen recognition throughout the whole species showed clear geographical differences between populations and complete loss of pathogen recognition in the south of the species range. In addition, we observed high complexity in a homologues of Cladosporium resistance ( Hcr ) locus, underlying the recognition of C. fulvum, in central and northern populations. Our findings show that major gene-mediated recognition specificity is diverse in a natural plant-pathosystem. We place major gene resistance in a geographical context that also defined the evolutionary history of that species. Data suggest that the underlying loci are more complex than previously anticipated, with small-scale gene recombination being possibly responsible for maintaining balanced polymorphisms in the populations that experience pathogen pressure.
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