The role of recombination in rapid adaptive evolution of fungal plant pathogens: Integrating demographic models, inferences of natural selection and population recombination maps

病原体与其宿主之间的对抗性共同进化可以推动双方的快速适应性变化。在这个项目中，我们的目标是了解驱动两种密切相关的真菌植物病原菌小麦发酵斑孢菌（栽培小麦的病原体）和阿达比利亚发酵斑孢菌（野草的病原体）快速适应的潜在机制。这两个物种不仅在寄主和环境（农业生态系统与天然草地）方面不同，而且在有效种群规模方面也不同。我们之前已经表明，尽管对麦田中的病原体施加了强大的定向选择压力，但小麦小麦的有效种群规模明显更高。在 SPP1819 的第一阶段，我们比较了多态性和趋异模式，以模拟小麦基因组中适应度效应的分布，并推断由选择固定的适应性突变的比例 α 以及总体适应率 ωA。与此同时，我们使用序列进化的密码子模型来检测在平衡选择下进化的基因，并推断作用于每个基因的纯化选择的强度。我们进一步将适应测量与重组率、转座元件含量、基因密度和蛋白质大小等不同参数相关联。基于 α 和 ωA，我们发现适应性进化总体上在小麦小麦的蛋白质进化中发挥着重要作用，特别是影响编码假定毒力因子的基因。我们还报告了重组对适应率以及普遍背景选择的强烈影响。在SPP的第二阶段，我们将进一步评估重组对快速适应性进化的影响。我们将通过使用复合似然比 (CLR) 统计推断小麦小麦和阿尔达比利亚基因组中选择性扫描的分布来实现这一点。在这个项目中，我们建议开发新的群体遗传模型，该模型考虑到两种植物病原体物种的人口统计学，并包括推断的遗传参数和基因座特异性重组率，以推断真菌基因组选择性扫描的图谱。这将使我们能够比较两个物种的扫描分布和适应性进化的速率。最后，该项目将通过对位于扫描基因组区域的选定候选基因进行功能分析来研究快速适应性进化的重要生物学意义。总之，该项目将为植物病原体快速适应性进化机制提供新的见解，特别是重组率变化的作用。 我们最终将识别并描述那些在这些重要的植物病原体中经历了最近快速适应性进化的基因的作用。

Antagonistic co-evolution between pathogens and their hosts can drive rapid adaptive changes in both partners. In this project we aim to understand the underlying mechanisms that drive rapid adaptation in two closely related fungal plant pathogenic species Zymoseptoria tritici (pathogen of cultivated wheat) and Zymoseptoria ardabiliae (pathogen of wild grasses). These two species differ not only in terms of host and environment (agro-ecosystem versus natural grassland) but also in terms of effective population size. We have previously shown that the effective population size is significantly higher in Z. tritici in spite of the strong directional selection pressure imposed to the pathogen in the wheat field. In the first phase of the SPP1819 we compared patterns of polymorphism and divergence to model the distribution of fitness effects across the genome of Z. tritici and to infer the proportion of adaptive mutations fixed by selection, α, as well as the overall rate of adaptation, ωA. In parallel, we used codon models of sequence evolution to detect genes evolving under balancing selection and to infer the strength of purifying selection acting on each gene. We furthermore correlated measures of adaptation with different parameters among others recombination rate, transposable element content, gene density and protein size. Based on α and ωA we find that adaptive evolution overall plays a strong role in protein evolution in Z. tritici and in particular affects genes encoding putative virulence factors. We also report a strong effect of recombination on the rate of adaptation, as well as pervasive background selection. In the second phase of the SPP we will further assess the impact of recombination on rapid adaptive evolution. We will do this by inferring the distribution of selective sweeps throughout the genome of Z. tritici and Z. ardabiliae using composite likelihood ratio (CLR) statistics. In this project we propose to develop new population genetic models that take the demography of the two plant pathogens species into account and include inferred genetic parameters and locus-specific recombination rates to infer maps of selective sweeps across the fungal genomes. This will allow us to compare the distribution of sweeps in the two species and rates of adaptive evolution. Finally, the project will investigate the underlining biological implications of rapid adaptive evolution by conducting functional analyses of selected candidate genes located in swept genome regions. In summary this project will provide novel insight into mechanisms of rapid adaptive evolution of plant pathogens, in particular the role of recombination rate variation. We will finally identify and describe the role of those genes that have experienced recent rapid adaptive evolution in these important plant pathogens.