Host Jump Enabling Factors in a Fungal/Grass Pathosystem

Smut fungi are biotrophic pathogens which infect mainly grasses, among them important cereal crop plants like barley, wheat, corn, sorghum, sugarcane and forage grasses. The so far 1200 smut fungi species identified show relatively strict host specificity and can infect in sum up to 4000 different plant species. The host range of a pathogen is likely a product of the acquisition of novel or adapted virulence factors (like small secreted proteins, so called effectors) or/and loss of avirulence factors (avr- Genes). On the host side the lack of restricting molecules like for example specific R- genes that would lead to strict defense responses or quantitative traits that in sum would lead to resistance can limit the host range of the pathogen. We identified interspecific mate pairs between Ustilago bromivora and different other grass-infecting but not Brachypodium infecting smuts which are able to cause infection symptoms and full completion of their lifecycle as hybrids on the model grass Brachypodium distachyon..This finding is the basis to dissect exemplary the molecular basis of host jump enabling factors by the employment of a genetic backcross approach assisted with comparative genomic approaches. Host jump events caused severe damage in the past and will also be in the future a constant threat to crops. Beside their economic importance an understanding of the molecular basis will have also impact on our view on evolutionary aspects of the ~1200 smuts and maybe beyond.

Smut fungi form a group of over 1200 species infecting as biotrophic pathogens mainly grass hosts, among them important crops like maize, sorghum and barley. One commonality among smuts is, that their sexual cycle is closely linked with infectivity. Infection mostly occurs at the early seedling stage of the respective host plant. After penetrating the plant, the dikaryotic pathogen grows biotrophically inter- and intracellularly in its host and macroscopic symptoms are usually exclusively limited to the inflorescences. The mating of compatible mating partners in smuts is controlled by a pheromone receptor system which provides specificity. Nevertheless it has been previously shown that interspecific mating occurs frequently under in vitro conditions. We found that the two smut fungi, Ustilago bromivora and Ustilago hordei can infect as hybrids the U. bromivora host grass Brachypodium spec.. By systematic backcrossings with U. hordei over four generations and sequencing of still infecting hybrid backcrosses and not anymore infecting hybrid backcrosses, we identified, that the virulence of U. bromivora is linked to many loci in a quantitative manner. This means that different combinations of virulence factors encoding regions led to infection symptoms and that single factors had small contributions to virulence that sum up to enable the fungus to complete its lifecycle. We proceeded in our study to further focus on the functional characterization of conserved effectors with virulence function and identified a ROS-burst inhibiting effector Rip1 targeting a conserved plant lipoxygenase which acts as a susceptibility factor.