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

白粉病是专性生体营养型子囊菌植物病原体，在与各自宿主植物的共同进化战争中经历快速适应。大麦白粉病病原体，大麦白粉病菌大麦专化型（Blumeria graminis f.sp.hordei，Bgh），作为这些真菌的模式系统。在该优先计划的上一个资助期内，我们大大改进了BGH参考基因组，以便能够跟踪这种真菌在实验进化过程中发生的基因组改变。这种方法揭示了一个动态的“单速”基因组，它的结构和（共）进化模式从根本上不同于其他几种丝状植物病原体所描述的所谓的“双速”基因组。Bgh基因组的一个关键特征是出现了均匀和全基因组分散的转座因子（TE），这些转座因子经历了最近的大规模增殖，并且部分仍具有转录活性。我们进一步进行了实验进化，并选择了一个BGH分离，成为部分毒力，否则高抗大麦mlo基因型。该分离株的不完全MLO毒力显然与导致易感野生型（MLO）大麦基因型毒力降低的适应性罚分相关。在优先计划的当前资助期间，我们建议探索TEs作为白粉病真菌快速进化适应的驱动因素的看似关键的作用。独特的基因组结构，高比例的TE及其保留的转录活性，使BGH一个精致的实验系统，研究这些元素在这种情况下的生物学相关性。为此，我们将仔细检查是否以及如何观察到的Bgh分离株之间的候选效应基因的拷贝数变异与TE活动。我们将进一步分析所选（转录活性）TE在各种应激条件下的表达谱，并在实验上减轻表观遗传标记，这被认为是创造一个人工TE爆发。此外，我们将通过研究全基因组水平的DNA甲基化和组蛋白标记以及通过调查小RNA（sRNA）表达来评估Bgh的表观遗传景观，这被认为与TE转录的控制有关。最后，我们将研究实验诱导的TE突发是否会加速BGH的进化适应，否则无法进入植物环境。总之，这些实验方法有望揭示TE如何以及在多大程度上确实有助于BGH的快速进化适应。

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.