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Exploring the molecular mechanisms that drive rapid evolutionary adaptations in the “one-speed" genome of the phytopathogenic barley powdery mildew fungus

Subject Area Evolution and Systematics of Plants and Fungi
Term from 2015 to 2024
Project identifier Deutsche Forschungsgemeinschaft (DFG) - Project number 274444799
 
Powdery mildews are obligate biotrophic ascomycete phytopathogens that are subject to rapid adaptation in the context of the co-evolutionary warfare with their respective host plants. The barley powdery mildew pathogen, Blumeria graminis f.sp. hordei (Bgh), serves as a model system for these fungi. In the previous funding period of this Priority Programme, we greatly improved the Bgh reference genome to enable the tracking of genomic alterations that occur in the course of experimental evolution pursued with this fungus. This approach revealed a dynamic “one-speed” genome, which differs fundamentally in its architecture and its (co-)evolutionary pattern from the so-called “two-speed” genomes described for several other filamentous phytopathogens. A key feature of the Bgh genome is the occurrence of evenly and genome-wide dispersed transposable elements (TEs), which experienced recent and massive proliferation and are in part still transcriptionally active. We further performed experimental evolution and selected a Bgh isolate that became partially virulent on otherwise highly resistant barley mlo genotypes. The incomplete mlo virulence of this isolate is apparently associated with a fitness penalty that results in reduced virulence on susceptible wild-type (Mlo) barley genotypes. In the current funding period of the Priority Programme we propose to explore the seemingly pivotal role of TEs as drivers of rapid evolutionary adaptation in powdery mildew fungi. The unique genome architecture, the high proportion of TEs and their retained transcriptional activity renders Bgh an exquisite experimental system to study the biological relevance of these elements in this context. To this end, we will carefully inspect whether and how the observed copy number variation of effector gene candidates between Bgh isolates is linked to TE activity. We will further analyze the expression profiles of selected (transcriptionally active) TEs under various stress conditions and upon the experimental relief of epigenetic marks, which is presumed to create an artificial TE burst. In addition, we will assess the epigenetic landscape of Bgh, which is supposedly linked to the control of TE transcription, by studying DNA methylation and histone marks at a genome-wide level and by surveying small RNA (sRNA) expression. We will finally study whether an experimentally induced TE burst will accelerate the evolutionary adaptation of Bgh to otherwise inaccessible plant environments. Taken together, these experimental approaches promise to unravel how and to which extent TEs indeed contribute to the rapid evolutionary adaptation of Bgh.
DFG Programme Priority Programmes
 
 

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