The basal ascomycetes in genus Taphrina have strict host specificity and coevolution with their host plants, making them appealing models for studying the genomic basis of ecological divergence and host adaption. We therefore performed genome sequencing and comparative genomics of different Taphrina species with distinct host ranges to reveal their evolution. We identified frequent chromosomal rearrangements and highly dynamic lineage‐specific (LS) genomic regions in Taphrina genomes. The LS regions occur at the flanking regions of chromosomal breakpoints, and are greatly enriched for DNA repeats, non‐core genes, and in planta up‐regulated genes. Furthermore, we identified hundreds of candidate secreted effector proteins (CSEPs) that are commonly organized in gene clusters that form distinct AT‐rich isochore‐like regions. Nearly half of the CSEPs constitute two novel superfamilies with modular structures unique to Taphrina. These CSEPs are commonly up‐regulated during infection, enriched in the LS regions, evolved faster, and underwent extensive gene gain and loss in different species. In addition to displaying signatures of positive selection, functional characterization of selected CSEP genes confirmed their roles in suppression of plant defence responses. Overall, our results showed that extensive chromosomal rearrangements and rapidly evolving CSEP superfamilies play important roles in speciation and host adaptation in the early‐branching ascomycetous fungi.

中文翻译：

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广泛的染色体重排和新型效应超家族的快速进化有助于基础子囊菌真菌的宿主适应和物种形成。


Taphrina属的基础子囊菌具有严格的寄主特异性并与其寄主植物共同进化，使其成为研究生态分化和寄主适应的基因组基础的有吸引力的模型。因此，我们对具有不同宿主范围的不同Taphrina物种进行了基因组测序和比较基因组学，以揭示它们的进化。我们在Taphrina基因组中发现了频繁的染色体重排和高度动态的谱系特异性 (LS) 基因组区域。 LS 区域出现在染色体断点的侧翼区域，并且非常富含 DNA 重复、非核心基因和植物上调基因。此外，我们还发现了数百种候选分泌效应蛋白（CSEP），它们通常组织在基因簇中，形成独特的富含 AT 的等孔样区域。近一半的 CSEP 构成了两个新颖的超家族，具有Taphrina独有的模块化结构。这些 CSEP 在感染过程中通常会上调，在 LS 区域富集，进化速度更快，并在不同物种中经历广泛的基因获得和损失。除了显示正选择的特征之外，选定的 CSEP 基因的功能表征还证实了它们在抑制植物防御反应中的作用。总的来说，我们的结果表明，广泛的染色体重排和快速进化的 CSEP 超家族在早期分支子囊菌真菌的物种形成和宿主适应中发挥着重要作用。