Agriculture and Agri-Food Canada, Lethbridge, AB, Canada.
School of Biosciences, University of Birmingham, Institute of Microbiology and Infection, Edgbaston, Birmingham, UK.
BMC Biol. 2022 Oct 24;20(1):239. doi: 10.1186/s12915-022-01433-w.
In fungal plant pathogens, genome rearrangements followed by selection pressure for adaptive traits have facilitated the co-evolutionary arms race between hosts and their pathogens. Pyrenophora tritici-repentis (Ptr) has emerged recently as a foliar pathogen of wheat worldwide and its populations consist of isolates that vary in their ability to produce combinations of different necrotrophic effectors. These effectors play vital roles in disease development. Here, we sequenced the genomes of a global collection (40 isolates) of Ptr to gain insights into its gene content and genome rearrangements.
A comparative genome analysis revealed an open pangenome, with an abundance of accessory genes (~ 57%) reflecting Ptr's adaptability. A clear distinction between pathogenic and non-pathogenic genomes was observed in size, gene content, and phylogenetic relatedness. Chromosomal rearrangements and structural organization, specifically around effector coding genes, were detailed using long-read assemblies (PacBio RS II) generated in this work in addition to previously assembled genomes. We also discovered the involvement of large mobile elements associated with Ptr's effectors: ToxA, the gene encoding for the necrosis effector, was found as a single copy within a 143-kb 'Starship' transposon (dubbed 'Horizon') with a clearly defined target site and target site duplications. 'Horizon' was located on different chromosomes in different isolates, indicating mobility, and the previously described ToxhAT transposon (responsible for horizontal transfer of ToxA) was nested within this newly identified Starship. Additionally, ToxB, the gene encoding the chlorosis effector, was clustered as three copies on a 294-kb element, which is likely a different putative 'Starship' (dubbed 'Icarus') in a ToxB-producing isolate. ToxB and its putative transposon were missing from the ToxB non-coding reference isolate, but the homolog toxb and 'Icarus' were both present in a different non-coding isolate. This suggests that ToxB may have been mobile at some point during the evolution of the Ptr genome which is contradictory to the current assumption of ToxB vertical inheritance. Finally, the genome architecture of Ptr was defined as 'one-compartment' based on calculated gene distances and evolutionary rates.
These findings together reflect on the highly plastic nature of the Ptr genome which has likely helped to drive its worldwide adaptation and has illuminated the involvement of giant transposons in facilitating the evolution of virulence in Ptr.
在真菌植物病原体中，基因组重排后伴随着适应性特征的选择压力，促进了宿主与病原体之间的共同进化军备竞赛。禾旋孢腔菌（Ptr）最近作为一种世界性的小麦叶部病原体出现，其种群由在产生不同坏死效应子组合能力上存在差异的分离株组成。这些效应子在疾病发展中起着至关重要的作用。在这里，我们对全球范围内（40 个分离株）的 Ptr 进行了基因组测序，以深入了解其基因组成和基因组重排。
比较基因组分析显示，一个开放的泛基因组存在丰富的附加基因（~57%），反映了 Ptr 的适应性。致病性和非致病性基因组在大小、基因组成和系统发育关系上有明显的区别。使用本研究中生成的长读长组装（PacBio RS II）以及以前组装的基因组，详细描述了染色体重排和结构组织，特别是围绕效应子编码基因的结构组织。我们还发现了与 Ptr 效应子相关的大型移动元件的参与：编码坏死效应子的基因 ToxA 被发现作为一个单一拷贝存在于一个 143kb 的“星际飞船”转座子（称为“地平线”）中，该转座子具有明确的靶位点和靶位点重复。“地平线”在不同的分离株中位于不同的染色体上，表明其具有移动性，而先前描述的 ToxhAT 转座子（负责 ToxA 的水平转移）嵌套在这个新发现的“星际飞船”中。此外，编码黄化效应子的基因 ToxB 聚集在一个 294kb 的元件上的三个拷贝中，该元件可能是产毒分离株中的另一个潜在的“星际飞船”（称为“伊卡洛斯”）。ToxB 及其潜在的转座子在非编码参考分离株中缺失，但同源基因 toxb 和“伊卡洛斯”都存在于另一个非编码分离株中。这表明，在 Ptr 基因组的进化过程中，ToxB 可能具有移动性，这与 ToxB 垂直遗传的当前假设相矛盾。最后，根据计算的基因距离和进化率，Ptr 的基因组结构被定义为“单区室”。
这些发现共同反映了 Ptr 基因组的高度可塑性，这可能有助于推动其在全球范围内的适应，并阐明了巨型转座子在促进 Ptr 毒力进化中的作用。
