Exaptation of Protein Coding Sequences from Transposable Elements

Bowen, Nathan J.; Jordan, I. King

doi:10.1159/000107609

Cited by 26 publications

(18 citation statements)

References 60 publications

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“…The evolutionary process by which TE sequences are subverted for novel function by the host genome is known as "exaptation" (de Souza et al 2013). There is extensive literature demonstrating that TEs have contributed repeatedly and profoundly to the evolution of genome structure and function through the insertion of preformed sequence elements, both at the level of genomic DNA, e.g., transcription factor binding sites (Johnson et al 2006), splice sites (Sela et al 2010), enhancer elements (Huda et al 2011b), and promoters (Huda et al 2011a), and at the level of RNA, e.g., microRNA genes (Spengler et al 2014), recognition elements (Piriyapongsa and Jordan 2007), and protein-coding domains (Bowen and Jordan 2007).…”

Section: Te Sequences Are Abundantly Found In Lncrna Exonsmentioning

confidence: 99%

The RIDL hypothesis: transposable elements as functional domains of long noncoding RNAs

Johnson

Guigó

2014

RNA

268

231

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Our genome contains tens of thousands of long noncoding RNAs (lncRNAs), many of which are likely to have genetic regulatory functions. It has been proposed that lncRNA are organized into combinations of discrete functional domains, but the nature of these and their identification remain elusive. One class of sequence elements that is enriched in lncRNA is represented by transposable elements (TEs), repetitive mobile genetic sequences that have contributed widely to genome evolution through a process termed exaptation. Here, we link these two concepts by proposing that exonic TEs act as RNA domains that are essential for lncRNA function. We term such elements Repeat Insertion Domains of LncRNAs (RIDLs). A growing number of RIDLs have been experimentally defined, where TE-derived fragments of lncRNA act as RNA-, DNA-, and protein-binding domains. We propose that these reflect a more general phenomenon of exaptation during lncRNA evolution, where inserted TE sequences are repurposed as recognition sites for both protein and nucleic acids. We discuss a series of genomic screens that may be used in the future to systematically discover RIDLs. The RIDL hypothesis has the potential to explain how functional evolution can keep pace with the rapid gene evolution observed in lncRNA. More practically, TE maps may in the future be used to predict lncRNA function.

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Section: Te Sequences Are Abundantly Found In Lncrna Exonsmentioning

confidence: 99%

The RIDL hypothesis: transposable elements as functional domains of long noncoding RNAs

Johnson

Guigó

2014

RNA

268

231

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“…Transposable elements (TEs) are repetitive sequences that are able to move from one chromosomal location to another, often replicating themselves through DNA (class I) or RNA (class II, or retrotransposons) intermediates (Biemont and Vieira 2006;Bowen and Jordan 2007;Jurka et al 2007). TEs have been found in virtually all eukaryotic organisms, covering 3-80% of their genomes and considerably influencing evolutionary history, exon-intron Electronic supplementary material The online version of this article (doi:10.1007/s00439-009-0752-4) contains supplementary material, which is available to authorized users.…”

Section: Introductionmentioning

confidence: 99%

“…TEs have been found in virtually all eukaryotic organisms, covering 3-80% of their genomes and considerably influencing evolutionary history, exon-intron Electronic supplementary material The online version of this article (doi:10.1007/s00439-009-0752-4) contains supplementary material, which is available to authorized users. structure and regulation of gene expression (Biemont and Vieira 2006;Bowen and Jordan 2007;Hasler and Strub 2006;Jurka et al 2007). Human retrotransposons are represented by long terminal repeats (LTRs) and long and short interspersed nuclear elements (LINEs and SINEs) (Lander et al 2001).…”

Section: Introductionmentioning

confidence: 99%

Transposable elements in disease-associated cryptic exons

Vořechovský

2009

Hum Genet

110

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Transposable elements (TEs) make up a half of the human genome, but the extent of their contribution to cryptic exon activation that results in genetic disease is unknown. Here, a comprehensive survey of 78 mutation-induced cryptic exons previously identified in 51 disease genes revealed the presence of TEs in 40 cases (51%). Most TE-containing exons were derived from short interspersed nuclear elements (SINEs), with Alus and mammalian interspersed repeats (MIRs) covering >18 and >16% of the exonized sequences, respectively. The majority of SINE-derived cryptic exons had splice sites at the same positions of the Alu/MIR consensus as existing SINE exons and their inclusion in the mRNA was facilitated by phylogenetically conserved changes that improved both traditional and auxiliary splicing signals, thus marking intronic TEs amenable for pathogenic exonization. The overrepresentation of MIRs among TE exons is likely to result from their high average exon inclusion levels, which reflect their strong splice sites, a lack of splicing silencers and a high density of enhancers, particularly (G)AA(G) motifs. These elements were markedly depleted in antisense Alu exons, had the most prominent position on the exon-intron gradient scale and are proposed to promote exon definition through enhanced tertiary RNA interactions involving unpaired (di)adenosines. The identification of common mechanisms by which the most dynamic parts of the genome contribute both to new exon creation and genetic disease will facilitate detection of intronic mutations and the development of computational tools that predict TE hot-spots of cryptic exon activation.

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“…However, a large body of evidence indicates that sequences from these elements are routinely recruited as regulatory regions of host genes (Jordan et al 2003; Makalowski 2000; Rebollo et al 2012). Less frequently but also on many occasions, entire genes of mobile elements are captured to function in the host cells (Alzohairy et al 2013; Bowen and Jordan 2007; Rebollo, Romanish and Mager 2012). The telomerase, a key enzyme in the replication of eukaryotic linear chromosomes, that was derived from retroelements is one striking example (Gladyshev and Arkhipova 2011; Koonin 2006), and the much more recent capture of syncytins, essential placental proteins, from retroviruses is another (Dupressoir et al 2012).…”

Section: The Replicator Paradigmmentioning

confidence: 99%

Are viruses alive? The replicator paradigm sheds decisive light on an old but misguided question

Koonin

Starokadomskyy

2016

Studies in History and Philosophy of Science Part C: Studies in

115

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The question whether or not “viruses are alive” has caused considerable debate over many years. Yet, the question is effectively without substance because the answer depends entirely on the definition of life or the state of “being alive” that is bound to be arbitrary. In contrast, the status of viruses among biological entities is readily defined within the replicator paradigm. All biological replicators form a continuum along the selfishness-cooperativity axis, from the completely selfish to fully cooperative forms. Within this range, typical, lytic viruses represent the selfish extreme whereas temperate viruses and various mobile elements occupy positions closer to the middle of the range. Selfish replicators not only belong to the biological realm but are intrinsic to any evolving system of replicators. No such system can evolve without the emergence of parasites, and moreover, parasites drive the evolution of biological complexity at multiple levels. The history of life is a story of parasite-host coevolution that includes both the incessant arms race and various forms of cooperation. All organisms are communities of interacting, coevolving replicators of different classes. A complete theory of replicator coevolution remains to be developed, but it appears likely that not only the differentiation between selfish and cooperative replicators but the emergence of the entire range of replication strategies, from selfish to cooperative, is intrinsic to biological evolution.

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Exaptation of Protein Coding Sequences from Transposable Elements

Cited by 26 publications

References 60 publications

The RIDL hypothesis: transposable elements as functional domains of long noncoding RNAs

The RIDL hypothesis: transposable elements as functional domains of long noncoding RNAs

Transposable elements in disease-associated cryptic exons

Are viruses alive? The replicator paradigm sheds decisive light on an old but misguided question

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