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

白粉病是专性生物营养性子囊菌植物病原体，在与各自寄主植物的共同进化战中迅速适应。大麦白粉病病原菌Blumeria graminis f.sp。hordei （Bgh）作为这些真菌的模型系统。在该优先计划的前期资助期内，我们极大地改进了Bgh参考基因组，使其能够跟踪这种真菌在实验进化过程中发生的基因组变化。这种方法揭示了一个动态的“单速”基因组，它的结构和（共同）进化模式与其他几种丝状植物病原体的所谓“双速”基因组有着根本的不同。Bgh基因组的一个关键特征是出现均匀且全基因组范围内的分散转座因子（te），这些因子最近经历了大量增殖，并且部分仍具有转录活性。我们进一步进行了实验进化，并选择了一种Bgh分离物，该分离物对其他高度抗性的大麦mlo基因型具有部分毒性。该分离物的不完全mlo毒力显然与适应度惩罚有关，适应度惩罚导致对易感野生型（mlo）大麦基因型的毒力降低。在优先计划的当前资助期内，我们建议探索te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成为研究这些元件在这种情况下的生物学相关性的一个精美的实验系统。为此，我们将仔细检查在Bgh分离株之间观察到的效应候选基因拷贝数变化是否以及如何与TE活性相关。我们将进一步分析选择的（转录活性的）TE在各种胁迫条件下的表达谱，并在实验中释放表观遗传标记，这被认为是造成人工TE爆发的原因。此外，我们将通过在全基因组水平上研究DNA甲基化和组蛋白标记以及测量小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。我们将最终研究实验诱导的TE爆发是否会加速Bgh对其他难以进入的植物环境的进化适应。综上所述，这些实验方法有望揭示te如何以及在多大程度上促进了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.