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Functional repeat‐derived RNAs often originate from retrotransposon‐propagated ncRNAs

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The human genome is scattered with repetitive sequences, and the ENCODE project revealed that 60–70% of the genomic DNA is transcribed into RNA. As a consequence, the human transcriptome contains a large portion of repeat‐derived RNAs (repRNAs). Here, we present a hypothesis for the evolution of novel functional repeat‐derived RNAs from non‐coding RNAs (ncRNAs) by retrotransposition. Upon amplification, the ncRNAs can diversify in sequence and subsequently evolve new activities, which can result in novel functions. Non‐coding transcripts derived from highly repetitive regions can therefore serve as a reservoir for the evolution of novel functional RNAs. We base our hypothetical model on observations reported for short interspersed nuclear elements derived from 7SL RNA and tRNAs, α satellites derived from snoRNAs and SL RNAs derived from U1 small nuclear RNA. Furthermore, we present novel putative human repeat‐derived ncRNAs obtained by the comparison of the Dfam and Rfam databases, as well as several examples in other species. We hypothesize that novel functional ncRNAs can derive also from other repetitive regions and propose Genomic SELEX as a tool for their identification. WIREs RNA 2014, 5:591–600. doi: 10.1002/wrna.1243 This article is categorized under: RNA Processing > 3' End Processing RNA Turnover and Surveillance > Turnover/Surveillance Mechanisms
Human genome is repetitive. (a) Composition of the human genome. 2.5 and 0.5% of the human genome is covered with coding exons and non‐coding RNA (ncRNA) exons, respectively. Repeats represent 51% of the genome while the unannotated regions amount to 46% of the genome. (b) Composition of the repetitive portion of the human genome. Repeats with the largest genome coverage are long interspersed nuclear elements (LINEs) (41%), followed by short interspersed nuclear elements (SINEs) (29%), long terminal repeats (LTRs) (18%), DNA transposons (6%), and satellite repeats (6%).
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Comparison of Dfam with Rfam reveals new relationships between repeat elements and non‐coding RNAs (ncRNAs). (a) For each repeat and ncRNA family found in Dfam and Rfam, respectively, an hidden Markov model (HMM) was constructed based on the corresponding seed alignments. These HMMs were then compared by literally aligning the states of both HMMs using dynamic programming. The best state alignment ending with the alignment of match state Mi and Mj can be obtained either from Mi−1Mj−1, Di−1Mj−1, Mi−1Dj−1, Mi−1Ij−1 or from Ii−1Mj−1. (b) Examples of novel relationships between repeat elements and ncRNAs. mir‐763 shows strong similarity with a MITE, mir‐4428 derives from long terminal repeats (LTRs). KCNQ1DN ncRNA is highly homologous to long interspersed nuclear elements (LINEs).
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Repeat‐derived RNAs (repRNAs) often originate from retrotransposed non‐coding RNAs (ncRNAs). Top: Upon retrotransposition, ncRNAs are highly amplified, and as they spread throughout the genome, they diversify in sequence (depicted as bands of different shades of the same color). Some copies evolve new functions (depicted as a band with a changed color) giving rise to new classes of repRNAs. Therefore, non‐coding transcripts derived from highly repetitive regions can be a rich reservoir for the evolution of novel functional RNAs. Bottom: Examples of repRNAs and their corresponding ancestor mastergenes. For detailed discussion, see text.
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RNA Turnover and Surveillance > Turnover/Surveillance Mechanisms
RNA Processing > 3′ End Processing

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