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子超家族的快速进化有助于基底子囊性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和与其寄主植物的共进化特性，使其成为研究生态多样性和寄主适应的基因组基础的有吸引力的模型。因此，我们进行了具有不同寄主范围的不同Taphrina物种的基因组测序和比较基因组学，以揭示其进化过程。我们在Taphrina中发现了频繁的染色体重排和高度动态的谱系特定（LS）基因组区域基因组。LS区位于染色体断裂点的侧翼区域，并且对于DNA重复序列，非核心基因以及植物上调基因而言，其含量大大丰富。此外，我们鉴定了数百种候选分泌的效应蛋白（CSEP），这些蛋白通常组织在基因簇中，形成独特的富含AT的等时线样区域。将近一半的CSEP组成了两个新颖的超家族，具有Taphrina独有的模块化结构。这些CSEP通常在感染过程中被上调，在LS区富集，进化更快，并且在不同物种中经历了广泛的基因增减。除了显示阳性选择的特征外，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。总体而言，我们的结果表明，广泛的染色体重排和快速发展的CSEP超家族在早期分支子囊菌真菌的物种形成和寄主适应中起重要作用。