Repetitive Elements Contribute to the Diversity and Evolution of Centromeres in the Fungal Genus Verticillium
Repetitive Elements Contribute to the Diversity and Evolution of Centromeres in the Fungal Genus Verticillium
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DOI：
10.1128/mbio.01714-20
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发表时间：
2020-09-01
期刊：
影响因子：
6.4
通讯作者：
Thomma, Bart P. H. J.
中科院分区：
文献类型：
--
作者：
Seidl, Michael F.;Kramer, H. Martin;Thomma, Bart P. H. J.
着丝粒是染色体区域，在有丝分裂和减数分裂过程中对染色体分离至关重要，着丝粒形成失败会导致染色体异常。尽管有这种保守的功能，着丝粒在物种之间甚至在物种内都有显著的差异。到目前为止，对真菌着丝粒的组织和进化的系统研究仍然很少。在这项研究中，我们鉴定了黄萎病菌属10种真菌中的着丝粒，并描述了它们的组织和进化。着丝粒特异性组蛋白CenH3(ChIP-seq)和染色质构象捕获(Hi-C)的染色质免疫沉淀和高通量测序鉴定了8个保守的、大的(类似于150-kb)、AT-和富含重复的区域着丝粒，它们嵌入在植物病原菌大丽轮枝菌的异染色质中。使用Hi-C，我们类似地在其他黄萎菌物种中发现了富含重复的着丝粒。值得注意的是，在一些但不是所有的黄萎菌物种中，单个退化的长末端重复序列(LTR)反转录转座子与着丝粒区域密切相关。在黄萎病的进化过程中发生了广泛的染色体重排，其中一些重排可能与着丝粒有关，这表明着丝粒对染色体进化有贡献。着丝粒的大小和组织在物种之间有很大的差异，着丝粒的大小被发现与全基因组重复内容相关。总体而言，我们的研究强调了重复元件对黄萎病菌属着丝粒的多样性和快速进化的贡献。黄萎病是由频繁的染色体重排进化而来的，这有助于基因组的可塑性。着丝粒在有丝分裂和减数分裂过程中对染色体的分离起着丝粒作用，着丝粒功能失效会导致染色体异常。在这里，我们使用了一系列实验技术来鉴定和描述每一种黄萎病菌的着丝粒。有趣的是，我们可以强烈地将单个重复元件与一些黄萎菌物种的着丝粒联系起来。着丝粒中该元件的存在与着丝粒大小增加和全基因组重复扩增相一致。总而言之，我们的发现表明，在一组密切相关的真菌物种中，重复元件在着丝粒的功能、组织和快速进化中发挥了作用。
Centromeres are chromosomal regions that are crucial for chromosome segregation during mitosis and meiosis, and failed centromere formation can contribute to chromosomal anomalies. Despite this conserved function, centromeres differ significantly between and even within species. Thus far, systematic studies into the organization and evolution of fungal centromeres remain scarce. In this study, we identified the centromeres in each of the 10 species of the fungal genus Verticillium and characterized their organization and evolution. Chromatin immunoprecipitation of the centromere-specific histone CenH3 (ChIP-seq) and chromatin conformation capture (Hi-C) followed by high-throughput sequencing identified eight conserved, large (similar to 150-kb), AT-, and repeat-rich regional centromeres that are embedded in heterochromatin in the plant pathogen Verticillium dahliae. Using Hi-C, we similarly identified repeat-rich centromeres in the other Verticillium species. Strikingly, a single degenerated long terminal repeat (LTR) retrotransposon is strongly associated with centromeric regions in some but not all Verticillium species. Extensive chromosomal rearrangements occurred during Verticillium evolution, of which some could be linked to centromeres, suggesting that centromeres contributed to chromosomal evolution. The size and organization of centromeres differ considerably between species, and centromere size was found to correlate with the genome-wide repeat content. Overall, our study highlights the contribution of repetitive elements to the diversity and rapid evolution of centromeres within the fungal genus Verticillium.IMPORTANCE The genus Verticillium contains 10 species of plant-associated fungi, some of which are notorious pathogens. Verticillium species evolved by frequent chromosomal rearrangements that contribute to genome plasticity. Centromeres are instrumental for separation of chromosomes during mitosis and meiosis, and failed centromere functionality can lead to chromosomal anomalies. Here, we used a combination of experimental techniques to identify and characterize centromeres in each of the Verticillium species. Intriguingly, we could strongly associate a single repetitive element to the centromeres of some of the Verticillium species. The presence of this element in the centromeres coincides with increased centromere sizes and genome-wide repeat expansions. Collectively, our findings signify a role of repetitive elements in the function, organization, and rapid evolution of centromeres in a set of closely related fungal species.