Retrotransposons are "copy-and-paste" insertional mutagens that substantially contribute to mammalian genome content. Retrotransposons often carry long terminal repeats (LTRs) for retrovirus-like reverse transcription and integration into the genome. We report an extraordinary impact of a group of LTRs from the mammalian endogenous retrovirus-related ERVL retrotransposon class on gene expression in the germline and beyond. In mouse, we identified more than 800 LTRs from ORR1, MT, MT2, and MLT families, which resemble mobile gene-remodeling platforms that supply promoters and first exons. The LTR-mediated gene remodeling also extends to hamster, human, and bovine oocytes. The LTRs function in a stagespecific manner during the oocyte-to-embryo transition by activating transcription, altering protein-coding sequences, producing noncoding RNAs, and even supporting evolution of new protein-coding genes. These functions result, for example, in recycling processed pseudogenes into mRNAs or lncRNAs with regulatory roles. The functional potential of the studied LTRs is even higher, because we show that dormant LTR promoter activity can rescue loss of an essential upstream promoter. We also report a novel protein-coding gene evolution-D6Ertd527e-in which an MT LTR provided a promoter and the 5

Over a half of mammalian genomes is occupied by repetitive elements whose ability to provide functional sequences, move into new locations, and recombine underlies the so-called genome plasticity. At the same time, mobile elements exemplify selfish DNA, which is expanding in the genome at the expense of the host. The selfish generosity of mobile genetic elements is in the center of research interest as it offers insights into mechanisms underlying evolution and emergence of new genes. In terms of numbers, with over 20,000 in count, protein-coding genes make an outstanding >2 % minority. This number is exceeded by an ever-growing list of genes producing long non-coding RNAs (lncRNAs), which do not encode for proteins. LncRNAs are a dynamically evolving population of genes. While it is not yet clear what fraction of lncRNAs represents functionally important ones, their features imply that many lncRNAs emerge at random as new non-functional elements whose functionality is acquired through natural selection. Here, we explore the intersection of worlds of mobile genetic elements (particularly retrotransposons) and lncRNAs. In addition to summarizing essential features of mobile elements and lncRNAs, we focus on how retrotransposons contribute to lncRNA evolution, structure, and function in mammals.

The oocyte-to-embryo transition (OET) transforms a differentiated gamete into pluripotent blastomeres. The accompanying maternal-zygotic RNA exchange involves remodeling of the long non-coding RNA (lncRNA) pool. Here, we used next generation sequencing and de novo transcript assembly to define the core population of 1,600 lncRNAs expressed during the OET (lncRNAs). Relative to mRNAs, OET lncRNAs were less expressed and had shorter transcripts, mainly due to fewer exons and shorter 5′ terminal exons. Approximately half of OET lncRNA promoters originated in retrotransposons suggesting their recent emergence. Except for a small group of ubiquitous lncRNAs, maternal and zygotic lncRNAs formed two distinct populations. The bulk of maternal lncRNAs was degraded before the zygotic genome activation. Interestingly, maternal lncRNAs seemed to undergo cytoplasmic polyadenylation observed for dormant mRNAs. We also identified lncRNAs giving rise to trans-acting short interfering RNAs, which represent a novel lncRNA category. Altogether, we defined the core OET lncRNA transcriptome and characterized its remodeling during early development. Our results are consistent with the notion that rapidly evolving lncRNAs constitute signatures of cells-of-origin while a minority plays an active role in control of gene expression across OET. Our data presented here provide an excellent source for further OET lncRNA studies.