Institute of Evolutionary Biology, University of Edinburgh, Edinburgh, United Kingdom.
Josephine Bay Paul Center for Comparative Molecular Biology and Evolution, Marine Biological Laboratory, Woods Hole, MA, USA.
Mol Biol Evol. 2021 Oct 27;38(11):5005-5020. doi: 10.1093/molbev/msab225.
Penelope-like elements (PLEs) are an enigmatic clade of retrotransposons whose reverse transcriptases (RTs) share a most recent common ancestor with telomerase RTs. The single ORF of canonical endonuclease (EN)+ PLEs encodes RT and a C-terminal GIY-YIG EN that enables intrachromosomal integration, whereas EN- PLEs lack EN and are generally restricted to chromosome termini. EN+ PLEs have only been found in animals, except for one case of horizontal transfer to conifers, whereas EN- PLEs occur in several kingdoms. Here, we report a new, deep-branching PLE clade with a permuted domain order, whereby an N-terminal GIY-YIG EN is linked to a C-terminal RT by a short domain with a characteristic CxC motif. These N-terminal EN+ PLEs share a structural organization, including pseudo-LTRs and complex tandem/inverted insertions, with canonical EN+ PLEs from Penelope/Poseidon, Neptune, and Nematis clades, and show insertion bias for microsatellites, but lack canonical hammerhead ribozyme motifs. However, their phylogenetic distribution is much broader. The Naiads, found in numerous invertebrate phyla, can reach tens of thousands of copies per genome. In spiders and clams, Naiads independently evolved to encode selenoproteins containing multiple selenocysteines. Chlamys, which lack the CCHH motif universal to PLE ENs, occur in green algae, spike mosses (targeting ribosomal DNA), and slime molds. Unlike canonical PLEs, RTs of N-terminal EN+ PLEs contain the insertion-in-fingers domain (IFD), strengthening the link between PLEs and telomerases. Additionally, we describe Hydra, a novel metazoan C-terminal EN+ clade. Overall, we conclude that PLE diversity, taxonomic distribution, and abundance are comparable with non-LTR and LTR-retrotransposons.
类彭蠡海胆元件（PLEs）是一类神秘的逆转录转座子，其逆转录酶（RT）与端粒酶 RT 具有最近的共同祖先。典型内切酶（EN）+ PLEs 的单个 ORF 编码 RT 和 C 末端 GIY-YIG EN，使染色体内整合成为可能，而 EN- PLEs 缺乏 EN，通常局限于染色体末端。EN+ PLEs 仅在动物中发现，除了一个水平转移到松柏类植物的例子外，而 EN- PLEs 则存在于几个王国中。在这里，我们报告了一个新的、深分支的 PLE 类群，其结构域排列发生了置换，即 N 端 GIY-YIG EN 通过一个具有特征 CxC 基序的短结构域与 C 端 RT 相连。这些 N 端 EN+ PLEs 具有与 Penelope/Poseidon、Neptune 和 Nematis 类群的典型 EN+ PLEs 相似的结构组织，包括假 LTRs 和复杂串联/反向插入，并且显示出对微卫星的插入偏向，但缺乏典型的锤头核酶基序。然而，它们的系统发育分布要广泛得多。Naiads 存在于许多无脊椎动物门中，每个基因组可以达到数万份拷贝。在蜘蛛和蛤中，Naiads 独立进化为编码含有多个硒代半胱氨酸的硒蛋白。Chlamys 缺乏 PLE EN 通用的 CCHH 基序，存在于绿藻、刺叶苔科植物（靶向核糖体 DNA）和粘菌中。与典型的 PLE 不同，N 端 EN+ PLEs 的 RT 含有插入指结构域（IFD），加强了 PLEs 与端粒酶之间的联系。此外，我们描述了 Hydra，一种新型后生动物 C 端 EN+ 类群。总的来说，我们得出结论，PLE 的多样性、分类分布和丰度与非 LTR 和 LTR-逆转录转座子相当。
