Repetitive DNA sequences, including transposable elements (TEs) and tandemly repeated satellite DNA (satDNAs), collectively called the “repeatome”, are found in high proportion in organisms across the Tree of Life. Grasshoppers have large genomes, averaging 9 Gb, that contain a high proportion of repetitive DNA, which has hampered progress in assembling reference genomes. Here we combined linked-read genomics with transcriptomics to assemble, characterize, and compare the structure of repetitive DNA sequences in four chromosomal races of the morabine grasshopper Vandiemenella viatica species complex and determine their contribution to genome evolution. We obtained linked-read genome assemblies of 2.73–3.27 Gb from estimated genome sizes of 4.26–5.07 Gb DNA per haploid genome of the four chromosomal races of V. viatica. These constitute the third largest insect genomes assembled so far. Combining complementary annotation tools and manual curation, we found a large diversity of TEs and satDNAs, constituting 66 to 75% per genome assembly. A comparison of sequence divergence within the TE classes revealed massive accumulation of recent TEs in all four races (314–463 Mb per assembly), indicating that their large genome sizes are likely due to similar rates of TE accumulation. Transcriptome sequencing showed more biased TE expression in reproductive tissues than somatic tissues, implying permissive transcription in gametogenesis. Out of 129 satDNA families, 102 satDNA families were shared among the four chromosomal races, which likely represent a diversity of satDNA families in the ancestor of the V. viatica chromosomal races. Notably, 50 of these shared satDNA families underwent differential proliferation since the recent diversification of the V. viatica species complex. This in-depth annotation of the repeatome in morabine grasshoppers provided new insights into the genome evolution of Orthoptera. Our TEs analysis revealed a massive recent accumulation of TEs equivalent to the size of entire Drosophila genomes, which likely explains the large genome sizes in grasshoppers. Despite an overall high similarity of the TE and satDNA diversity between races, the patterns of TE expression and satDNA proliferation suggest rapid evolution of grasshopper genomes on recent timescales.

中文翻译：

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莫拉宾蚱蜢基因组的比较分析揭示了高度丰富的转座元件和快速增殖的卫星DNA重复序列


重复 DNA 序列，包括转座元件 (TE) 和串联重复卫星 DNA (satDNA)，统称为“重复组”，在生命之树的生物体中含量很高。蚱蜢的基因组很大，平均为 9 Gb，其中包含高比例的重复 DNA，这阻碍了参考基因组组装的进展。在这里，我们将链接读取基因组学与转录组学结合起来，组装、表征和比较莫拉宾蚱蜢 Vandiemenella viatica 物种复合体的四个染色体种族中重复 DNA 序列的结构，并确定它们对基因组进化的贡献。我们从 V. viatica 四个染色体种族的每个单倍体基因组的估计基因组大小 4.26-5.07 Gb DNA 中获得了 2.73-3.27 Gb 的链接读取基因组组装。这些构成了迄今为止组装的第三大昆虫基因组。结合互补的注释工具和手动管理，我们发现了 TE 和 satDNA 的多样性，占每个基因组组装的 66% 至 75%。 TE 类别内序列差异的比较显示，所有四个种族中最近 TE 的大量积累（每次组装 314-463 Mb），表明它们的基因组大小可能是由于相似的 TE 积累率所致。转录组测序显示，生殖组织中的 TE 表达比体细胞组织中的 TE 表达更偏向，这意味着配子发生过程中的转录是允许的。在 129 个 satDNA 家族中，有 102 个 satDNA 家族在四个染色体种族之间共享，这可能代表了 V. viatica 染色体种族祖先中 satDNA 家族的多样性。值得注意的是，自从 V. viatica 物种复合体最近多样化以来，其中 50 个共享 satDNA 家族经历了差异增殖。 对莫拉宾蚱蜢重复组的深入注释为直翅目基因组进化提供了新的见解。我们的 TE 分析显示，最近 TE 的大量积累相当于整个果蝇基因组的大小，这可能解释了蚱蜢基因组的大小。尽管种族之间的 TE 和 satDNA 多样性总体上高度相似，但 TE 表达和 satDNA 增殖的模式表明蚱蜢基因组在最近的时间尺度上快速进化。