Abstract
Transposable elements are driving forces for establishing genetic innovations such as transcriptional regulatory networks in eukaryotic genomes. Here, we describe a silencer situated in the last 300 bp of the Mos1 transposase open reading frame (ORF) which functions in vertebrate and arthropod cells. Functional silencers are also found at similar locations within three other animal mariner elements, i.e. IS630-Tc1-mariner (ITm) DD34D elements, Himar1, Hsmar1 and Mcmar1. These silencers are able to impact eukaryotic promoters monitoring strong, moderate or low expression as well as those of mariner elements located upstream of the transposase ORF. We report that the silencing involves at least two transcription factors (TFs) that are conserved within animal species, NFAT-5 and Alx1. These cooperatively act with YY1 to trigger the silencing activity. Four other housekeeping transcription factors (TFs), neuron restrictive silencer factor (NRSF), GAGA factor (GAF) and GTGT factor (GTF), were also found to have binding sites within mariner silencers but their impact in modulating the silencer activity remains to be further specified. Interestingly, an NRSF binding site was found to overlap a 30 bp motif coding a highly conserved PHxxYSPDLAPxD peptide in mariner transposases. We also present experimental evidence that silencing is mainly achieved by co-opting the host Polycomb Repressive Complex 2 pathway. However, we observe that when PRC2 is impaired another host silencing pathway potentially takes over to maintain weak silencer activity. Mariner silencers harbour features of Polycomb Response Elements, which are probably a way for mariner elements to self-repress their transcription and mobility in somatic and germinal cells when the required TFs are expressed. At the evolutionary scale, mariner elements, through their exaptation, might have been a source of silencers playing a role in the chromatin configuration in eukaryotic genomes.
Highlights
Almost all eukaryotic genomes contain transposable elements (TEs)
As the regulation of chromatin configuration by polycomb is an important regulator of animal development, our findings open the possibility that mariner silencers might have been exapted during animal evolution to participate in certain regulation pathways of their hosts
Since some of the transcription factors (TFs) involved in mariner silencer activity play a role at different stages of nervous system development and neuron differentiation, it might be possible that mariner transposons can be active during some steps of cell differentiation
Summary
Almost all eukaryotic genomes contain transposable elements (TEs). Some of these, known as DNA transposons, move by a simple ‘cut-and-paste’ mechanism removing DNA from one site and inserting it into a new target site. DNA segments derived from TEs that were exapted or inactivated over time by accumulation of mutations appear as remnants of repeated sequences of various ages While they are rare, active TEs are still present in the genome of extant species in which de novo insertions can generate genetic variations. In multicellular eukaryotes TE insertions must occur within the germinal lineage or during early development in order to be transmitted to the following generations This leads to the suggestion that transposition into somatic cells had no value for the TEs or their host. In the early 1980’s evidence began to accumulate showing that somatic TE activity (i.e. single excision or excision followed by re-insertion) occurred at high frequency in animal taxa This was first shown for a DNA transposon, Tc1 in the worm Caenorhabditis elegans [4]. All of these somatic transpositions occurred in primordial cells associated with neuron-related lineages during embryonic or metamorphic development
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