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

PA 861/14-2

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.

Publications

• Frantzeskakis, L., Di Pietro, A., Rep, M., Schirawski, J., Wu, C.‐H. and Panstruga, R. (2020) Rapid evolution in plant–microbe interactions – a molecular genomics perspective. New Phytol. 2020 Feb;225(3):1134-1142. DOI: 10.1111/nph.15966
  
  
• Stefan Kusch, Márk Z. Németh, Niloofar Vaghefi, Heba M. M. Ibrahim, Ralph Panstruga, and Levente Kiss (2020) A Short-Read Genome Assembly Resource for Leveillula taurica Causing Powdery Mildew Disease of Sweet Pepper (Capsicum annuum). Molecular Plant-Microbe Interactions. DOI: 10.1094/MPMI-02-20-0029-A
  
  
• Mirna Barsoum, Stefan Kusch, Lamprinos Frantzeskakis, Ulrich Schaffrath, and Ralph Panstruga (2020) UV mutagenesis coupled with next-generation sequencing as a method for functional interrogation of powdery mildew genomes. Molecular Plant-Microbe Interactions. DOI: 10.1094/MPMI-02-20-0035-TA
  
  
• Isabel ML Saur, Saskia Bauer, Barbara Kracher, Xunli Lu, Lamprinos Franzeskakis, Marion C Müller, Björn Sabelleck, Florian Kümmel, Ralph Panstruga, Takaki Maekawa, Paul Schulze-Lefert (2019) Multiple pairs of allelic MLA immunereceptor-powdery mildew AVRA effectors argue for a direct recognition mechanism. eLife, 8:e44471. DOI: 10.7554/eLife.44471
  
  
• Mirna Barsoum, Björn Sabelleck, Pietro D. Spanu and Ralph Panstruga (2019) Rumble in the Effector Jungle: Candidate Effector Proteins in Interactions of Plants with Powdery Mildew and Rust Fungi. Critical Reviews in Plant Sciences, 38:4, 255-279, DOI: 10.1080/07352689.2019.1653514
  
  
• Lamprinos Frantzeskakis, Márk Z. Németh, Mirna Barsoum, Stefan Kusch, Levente Kiss, Susumu Takamatsu, Ralph Panstruga (2019) The Parauncinula polyspora Draft Genome Provides Insights into Patterns of Gene Erosion and Genome Expansion in Powdery Mildew Fungi. mBio Sep 2019, 10 (5) e01692-19, DOI: 10.1128/mBio.01692-19
  
  
• Pennington, H. G., Jones, R., Kwon, S., Bonciani, G., Thieron, H., Chandler, T., Luong, P., Morgan, S., Przydacz, Bozkurt, T. O., Bowden, S., Craze, M., Wallington, E., Garnett, J., Kwaaitaal, M., Panstruga, R., Cota, E. and Spanu, P. D. S. (2019) The fungal ribonuclease-like effector protein CSEP0064/BEC1054 represses plant immunity and interferes with degradation of host ribosomal RNA. PLoS Pathog. 15(3):e1007620. DOI: 10.1371/journal.ppat.1007620
  
  
• Stefan Kusch, Lamprinos Frantzeskakis, Hannah Thieron, Ralph Panstruga (2018) Small RNAs from cereal powdery mildew pathogens may target host plant genes. Fungal Biology, Volume 122, Issue 11:1050-1063. DOI:10.1016/j.funbio.2018.08.008
  
  
• Lamprinos Frantzeskakis, Stefan Kusch, Ralph Panstruga (2018) The need for speed: compartmentalized genome evolution in filamentous phytopathogens. Molecular Plant Pathology, 20 (1), 3–7. DOI: 10.1111/mpp.12738
  
  
• Frantzeskakis, L., von Dahlen, J.K., Panstruga, R., and Rose, L.E. (2018) Rapid evolution in the tug-of-war between microbes and plants. New Phytologist 219: 12-14. DOI: 10.1111/nph.15220
  
  
• Frantzeskakis, L., Kracher, B., Kusch, S., Yoshikawa-Maekawa, M., Bauer, S., Pedersen, C., Spanu, P. D., Maekawa, T., Schulze-Lefert, P., and Panstruga, R. (2018) Signatures of host specialization and a recent transposable element burst in the dynamic one-speed genome of the fungal barley powdery mildew pathogen. BMC Genomics 19: 381 DOI: 10.1186/s12864-018-4750-6
  
  
• Thordal-Christensen, H., Birch, P. R. J., Spanu, P. D., and Panstruga, R. (2018) Why did filamentous plant pathogens evolve the potential to secrete hundreds of effectors to enable disease? Molecular Plant Pathology 19: 781-785. DOI: 10.1111/mpp.12649

• Spanu, P. D., Panstruga, R. (2017) Editorial: Biotrophic Plant-Microbe Interactions. Frontiers in Plant Science 8: 192. DOI: 10.3389/fpls.2017.00192
  
  
• Bindschedler LV, Panstruga R, Spanu PD (2016) Mildew-Omics: How Global Analyses Aid the Understanding of Life and Evolution of Powdery Mildews. Frontiers in Plant Science 7:123. DOI: 10.3389/fpls.2016.00123