Key Points
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The enzymatic machinery encoded by certain retrotransposons enables genes to duplicate via an RNA intermediate, a mechanism termed retroposition or retroduplication. In mammals, retroposition has produced thousands of gene copies, termed retrocopies.
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Retrocopies are expected to lack promoter sequences and were long regarded as pseudogenes with no functional relevance. However, cases of functional retrocopies, termed retrogenes, have accumulated in the literature, implying that retrocopies can be transcribed.
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Recent large-scale studies indicate that transcribed retrocopies are widespread. Retrocopies can become transcribed in various ways. For example, they can use promoters of other genes or retrotransposable elements in their vicinity, but they can (unexpectedly) also inherit promoters from their parental source genes.
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Retrocopies and retrogenes are frequently functionally transcribed in the testis, which is probably due to the permissive transcriptional state of chromatin during and after meiosis.
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Several 'out-of-the-X' autosomal retrogenes have been shown to functionally substitute their X-linked parental genes during and after meiotic sex-chromosome inactivation.
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Phylogenetic dating of out-of-the-X retrogenes in mammals has led to the reassessment of the age of our sex chromosomes.
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Detailed functional studies of young retrogenes have provided novel insights pertaining to the origin of new genes. For example, analyses of recent primate genes revealed that new gene functions can arise through changes in the localization of encoded proteins in the cell during evolution, whereas studies in Drosophila melanogaster uncovered the first example of a new gene with a behavioral phenotype.
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Studies of the process of retroposition have not only shed light on the origin of new genes, but have also provided other general insights pertaining to the evolution of mammalian genomes. For example, retrocopies have served as unique 'genomic archives' of mammalian transcriptomes, revealing extinct transcripts and gene expression activity during evolution.
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Gene copies originating from segmental duplication and retroposition have distinct features (such as the presence or absence of inherited regulatory sequences and introns) that profoundly influence their evolutionary fate. Studying RNA-based gene duplication is therefore a useful alternative to further enhance our understanding of the emergence of new genes and their functions.
Abstract
Gene copies that stem from the mRNAs of parental source genes have long been viewed as evolutionary dead-ends with little biological relevance. Here we review a range of recent studies that have unveiled a significant number of functional retroposed gene copies in both mammalian and some non-mammalian genomes. These studies have not only revealed previously unknown mechanisms for the emergence of new genes and their functions but have also provided fascinating general insights into molecular and evolutionary processes that have shaped genomes. For example, analyses of chromosomal gene movement patterns via RNA-based gene duplication have shed fresh light on the evolutionary origin and biology of our sex chromosomes.
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Acknowledgements
We apologize to colleagues whose work could not be discussed or cited owing to space constraints and/or the focus of this Review. We thank the members of the H.K. and M.L. laboratories for discussions. This work was supported by funds from the Swiss National Science Foundation, the European Research Council (STREP: 140404), and EMBO Young Investigator Grant (to H.K.), as well as the National Institutes of Health (R0IGM078070-01A1) (to M. L.).
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Glossary
- New gene
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A gene that originated recently during evolution.
- Parental gene
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Source of the mRNA that gives rise to a retroposed gene copy.
- Retrogene
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Expressed and functional retrocopy, usually with an intact ORF consistent with that of the parental gene.
- Gene fusion
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The fusion of adjacent genes into a single transcription unit, which is then termed a chimeric or fusion gene.
- Retroposition
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A mechanism that creates duplicate gene copies in new genomic positions through the reverse transcription of mRNAs from source genes (also known as RNA-based duplication or retroduplication).
- Retrocopy
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Gene copy that results from the process of retroposition (also termed retroposed gene copy or retroposed copy).
- L1 element
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A member of the long interspersed nuclear element (LINE) family of repeats. Provides the enzymatic machinery necessary for the process of retroposition in mammals.
- Retropseudogene
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Non-functional retrocopy, which usually carries frameshift-causing insertions or deletions and/or premature stop codons that preclude gene function.
- Subcellular adaptation
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A process by which a duplicate gene product evolves a new localization in the cell or localizes more specifically to one of the ancestral compartments under the influence of positive Darwinian selection.
- Domain shuffling
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Juxtaposition of one or more exons from two different genes that encode functional protein domains.
- Meiotic sex chromosome inactivation
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(MSCI). The transcriptional silencing of the X and Y chromosomes during the meiotic phase of spermatogenesis.
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Kaessmann, H., Vinckenbosch, N. & Long, M. RNA-based gene duplication: mechanistic and evolutionary insights. Nat Rev Genet 10, 19–31 (2009). https://doi.org/10.1038/nrg2487
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DOI: https://doi.org/10.1038/nrg2487
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