Abstract
Transposable elements (TEs) are abundant in mammalian genomes and appear to have contributed to the evolution of their hosts by providing novel regulatory or coding sequences. We analyzed different regions of long intergenic non-coding RNA (lincRNA) genes in human and mouse genomes to systematically assess the potential contribution of TEs to the evolution of the structure and regulation of expression of lincRNA genes. Introns of lincRNA genes contain the highest percentage of TE-derived sequences (TES), followed by exons and then promoter regions although the density of TEs is not significantly different between exons and promoters. Higher frequencies of ancient TEs in promoters and exons compared to introns implies that many lincRNA genes emerged before the split of primates and rodents. The content of TES in lincRNA genes is substantially higher than that in protein-coding genes, especially in exons and promoter regions. A significant positive correlation was detected between the content of TEs and evolutionary rate of lincRNAs indicating that inserted TEs are preferentially fixed in fast-evolving lincRNA genes. These results are consistent with the repeat insertion domains of LncRNAs hypothesis under which TEs have substantially contributed to the origin, evolution, and, in particular, fast functional diversification, of lincRNA genes.
Highlights
Genomes have been perceived mostly as repositories of protein-coding genes
The lowest fraction of TE-derived sequences (TES) was found in the predicted core promoter regions (100 bp upstream regions), and the highest fraction of TES was observed in introns, whereas exonic sequences showed intermediate densities of TES (Figure 1A)
In the exons and the core promoter regions of long intergenic non-coding RNA (lincRNA) genes, the fractions of TES are substantially and statistically significantly (P < 10−5 according to the Fisher exact test) higher than in the respective regions of protein-coding genes
Summary
Genomes have been perceived mostly as repositories of protein-coding genes. This might be largely true in the case of viruses, prokaryotes, and unicellular eukaryotes, numerous recent studies on the genomes of multicellular eukaryotes, animals, have revealed a vast non-coding RNome, i.e., numerous genes encoding various classes of non-coding RNAs (ncRNAs) (Carninci et al, 2005; Mattick and Makunin, 2006; Ponting et al, 2009; Derrien et al, 2012; Amaral et al, 2013). The total number of genes for ncRNAs that are expressed from a mammalian genome seems to exceed the number of protein-coding genes several fold (Mattick and Makunin, 2006; Amaral et al, 2013). Among many distinct classes of ncRNAs, the long non-coding RNA (lncRNA) is probably the most enigmatic group. The definition of a lncRNA is based solely on the transcript size: lncRNAs are defined as ncRNAs longer than 200 nt (Mattick and Makunin, 2006; Ponting et al, 2009)
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