Department of Molecular Biology and Genetics, Cornell University, Ithaca, New York 14853, USA
Genome Res. 2024 Jun 25;34(5):711-724. doi: 10.1101/gr.278062.123.
The piRNA pathway is a highly conserved mechanism to repress transposable element (TE) activity in the animal germline via a specialized class of small RNAs called piwi-interacting RNAs (piRNAs). piRNAs are produced from discrete genomic regions called piRNA clusters (piCs). Although the molecular processes by which piCs function are relatively well understood in , much less is known about the origin and evolution of piCs in this or any other species. To investigate piC origin and evolution, we use a population genomic approach to compare piC activity and sequence composition across eight geographically distant strains of with high-quality long-read genome assemblies. We perform annotations of ovary piCs and genome-wide TE content in each strain. Our analysis uncovers extensive variation in piC activity across strains and signatures of rapid birth and death of piCs. Most TEs inferred to be recently active show an enrichment of insertions into old and large piCs, consistent with the previously proposed "trap" model of piC evolution. In contrast, a small subset of active LTR families is enriched for the formation of new piCs, suggesting that these TEs have higher proclivity to form piCs. Thus, our findings uncover processes leading to the origin of piCs. We propose that piC evolution begins with the emergence of piRNAs from individual insertions of a few select TE families prone to seed new piCs that subsequently expand by accretion of insertions from most other TE families during evolution to form larger "trap" clusters. Our study shows that TEs themselves are the major force driving the rapid evolution of piCs.
piRNA 通路是一种高度保守的机制，通过一类称为 piwi 相互作用 RNA（piRNAs）的特殊小 RNA 来抑制动物生殖系中转座元件（TE）的活性。piRNAs 是从离散的基因组区域（称为 piRNA 簇，piCs）产生的。虽然 piCs 发挥作用的分子过程在 中相对较好理解，但关于 piCs 在该物种或任何其他物种中的起源和进化知之甚少。为了研究 piC 的起源和进化，我们使用群体基因组学方法比较了具有高质量长读长基因组组装的八个地理上遥远的 菌株之间的 piC 活性和序列组成。我们在每个菌株中进行了卵巢 piC 和全基因组 TE 含量的注释。我们的分析揭示了菌株间 piC 活性的广泛变化和 piC 快速诞生和死亡的特征。最近推断为活跃的大多数 TEs 显示插入到旧的和大的 piCs 中的富集，与先前提出的 piC 进化“陷阱”模型一致。相比之下，一小部分活跃的 LTR 家族富含新的 piCs 的形成，这表明这些 TEs 具有更高的形成 piCs 的倾向。因此，我们的发现揭示了导致 piC 起源的过程。我们提出，piC 进化始于少数几个易于产生新 piCs 的 TE 家族的单个插入产生 piRNAs，随后通过进化过程中来自大多数其他 TE 家族的插入积累来扩展，形成更大的“陷阱”簇。我们的研究表明，TE 本身是推动 piCs 快速进化的主要力量。
