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Hörger, Anja Christina (2011): Evolution of disease resistance genes in wild tomato species. Dissertation, LMU München: Faculty of Biology
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Abstract

The coevolutionary arms race between hosts and pathogens is often described as a recurrent struggle for increased resistance in hosts and evasion of recognition by pathogens. These coevolutionary dynamics dominated by balancing selection lead to the maintenance of allelic diversity at genes involved in interactions between hosts and pathogens. In plant-pathogen interactions, the current paradigm posits that the specific defence response is activated upon recognition of a specific pathogen effector through the corresponding resistance (R) gene in the host. Numerous studies demonstrated that balancing selection acts on these R genes. However, little is known about the evolutionary mechanisms shaping other molecules not directly involved in pathogen recognition, but nevertheless playing an important role in defence signal activation. In this thesis I investigate the evolutionary forces acting at these genes in wild tomato species (Solanum sp.). First, I focus on Rcr3, a ‘guardee’, i.e. target of pathogen effectors secreted by the fungus Cladosporium fulvum and the oomycete Phytophthora infestans in tomato plants. Specific activation of the defence response occurs when R genes (the ‘guards’) sense the modification of the ‘guardee’ by pathogen effectors (‘Guard-Hypothesis’). These interactions between effector, ‘guardee’ and ‘guard’, are expected to favour contrasting evolutionary forces acting on the guardee. I study the pattern of sequence evolution and functional consequences of natural sequence variation on host resistance and show that the evolution of Rcr3 is characterized by gene duplication, gene conversion and balancing selection in wild tomato species. Investigating the functional characteristics of 54 natural variants through in vitro and in planta assays, I reveal differences in the strength of the defence response, but not in pathogen recognition specificity. These results suggest that functional diversity may be maintained at the ‘guardee’ (Rcr3) through the coevolution with its ‘guard’ because natural selection favours improved transduction of the defence signal or avoidance of auto-immune response. Second, I study the pattern of polymorphism in one population of the wild tomato species S. peruvianum at five genes (Pto, Fen, Rin4, Prf and Pfi) involved in a common defence signalling network. This network contributes to resistance against the bacterium Pseudomonas syringae. Two of these genes, Pto and Pfi, exhibit a signature of balancing selection but only Pto is known to directly interact with pathogen ligands in pathogen recognition. Pfi however was found to function further ‘downstream’ in the network. These results suggest that pathogens may target genes at different positions of the resistance networks to manipulate or nullify host resistance. I further investigate the evolution of these two genes in three recently diverged sister species (S. peruvianum, S. corneliomulleri and S. chilense) using a species wide sampling approach. Both genes exhibit trans-species polymorphism, but it is shown that at the Pto gene this is most likely due to recent introgression of favourable alleles, where Pfi1 exhibits ancestral trans-species polymorphism. Interestingly, Pfi shows signature of enhanced divergence between species, suggesting that this gene may represent a potential example of Dobzhansky-Muller incompatibility. Altogether, these results suggest that coevolution occurs not only at genes of interaction between hosts and pathogens, but as well at genes indirectly involved in recognition (guardees) or signal transduction. Understanding the evolution of the plant immune system requires therefore extending the scope of functional and population genetics studies to signalling molecules in defence networks.