How do plant pathogens adapt to novel host groups? Divergent genome evolution after a host jump in the plant parasitic oomycete Hyaloperonospora crispula and its sister species Hyaloperonospora arabidopsidis.

高度特化的植物生物营养微生物可以在一定频率上感染非宿主物种。偶尔，这会产生适应性和新的病原体谱系。在许多病原体群体中，包括严重的作物病原体，经常特化到遥远的宿主群体。面对宿主跳跃相关的破坏性流行病风险，我们仍然缺乏对宿主跳跃的门户和边界以及以下适应过程的深刻了解。卵菌透明operonospora crispula （Hpc）是分析遥远宿主群体适应分子机制的理想候选菌。它是唯一一种在透明膜孢子属中适应非十字花科宿主的物种。我推测宿主跳跃后，Hpc在基因含量和基因调控方面发生了根本性的变化，这些变化在很大程度上反映了对新宿主的适应特性。在提议的奖学金期间，我的目标是确定Hpc对这种新型主群的分子需求和宿主特异性的后果。我将分析Hpc的基因组和转录组，并将其与感染十字花科植物的姐妹物种拟南芥（Hpa）进行比较，Hpa是模式植物拟南芥（Arabidopsis thaliana）的一种成熟的模式寄生虫。5个亲缘关系较远的疫霉种的数据将作为外群。对Hpc基因组进行基因获得和丢失、基因家族的兴起和衰落、非编码基因组特征和选择特征的调查。除了一组保守的毒力相关基因外，这种方法还可能揭示新的效应类，这些效应类代表了宿主特化的有希望的候选基因。为了分析多态性和替换率，我将对东英格兰Reseda上的Hpc种群进行取样。为了进一步研究宿主植物特异性基因在Hpc中的表达，将使用Illumina HiSeq2000对感染的植物材料进行RNAseq检测。最后，我将利用丁香假单胞菌的细菌3型分泌系统，分析约10个宿主特化候选基因对拟南芥对木黄霉毒力的影响。这包括具有加速进化速率的基因、缺失/存在多态性、寄主植物之间的差异转录以及扩展/收缩基因家族。总之，本项目旨在了解宿主跳跃后寄生虫宿主特化的适应性进化机制。它研究了专性生物营养卵菌Hpc与其姊妹种Hpa的基因组，转录和分子特征。建立了Hpc种群的野生型集合。因此，它突出了对适应新宿主后基因组结构和基因表达变化的基本见解，并可能成为科学家推进农业生态系统中植物防御策略的关键资源。最后，它将为拟南芥hpa -拟南芥病理系统的广泛免疫和病理研究带来新的工具和视角。

Highly specialized plant-biotrophic microbes can infect non-host species at some frequency. Occasionally, this gives rise to adaptation and novel pathogen lineages. In many pathogen groups, including severe crop pathogens, specialization to distant host groups is frequent. Facing host jump-related risks for devastating pandemics we still lack profound knowledge of gateways and borders for host jumps and the following adaptive processes. The oomycete Hyaloperonospora crispula (Hpc) is an ideal candidate to analyze molecular mechanisms of adaptation to distant host groups. It is the only species in the Hyaloperonospora genus that adapted to non-crucifer hosts of the genus Reseda. I hypothesize that after the host jump, Hpc underwent fundamental changes in gene content and gene regulation and that these changes largely reflect adaptive traits towards the novel host group. During the proposed fellowship I aim to identify molecular requirements and consequences of host specificity of Hpc to this novel host group. I will analyze the genome and transcriptome of Hpc in comparison to its crucifer-infecting sister species H. arabidopsidis (Hpa), a well-established model parasite of the model plant Arabidopsis thaliana. Data of 5 distantly related Phytophthora species will serve as an outgroup. The genome of Hpc will be surveyed for gene gain and loss, gene family rise and fall, non-coding genomic features and signatures of selection. Besides the set of conserved virulence-related genes this approach will potentially disclose novel effector classes that represent promising candidate genes of host specialization. To analyze rates of polymorphisms and substitutions I will sample populations of Hpc on Reseda from East England. To further survey host plant-specific gene expression in Hpc, RNAseq will be performed on infected plant material using Illumina HiSeq2000. Finally, I will analyse ~10 host specialization candidate genes for their effect on virulence in A. thaliana versus R. luteola using the bacterial type-three secretion system of Pseudomonas syringae. This includes genes with accelerated evolutionary rates, absence/presence polymorphisms, differential transcription between host plants, and expanded/retracted gene families. In summary, this project aims to understand mechanisms of adaptive evolution that are involved in host specialization of a parasite following a host jump. It studies genomic, transcriptional and molecular features of the obligate biotrophic oomycete Hpc in comparison to its sister species Hpa. It establishes a wild type collection of Hpc populations. Thereby, it highlights fundamental insights into changes of genome structure and gene expression after adaption to a novel host group and could become a key resource for scientists to advance our plant defense strategies in agro-ecosystems. Finally, it will bring new tools and perspectives to the extensive immunity and pathology research taking place on the Hpa-Arabidopsis pathosystem.