Transposable Elements: An Abundant and Natural Source of Regulatory Sequences for Host Genes

Transposable elements (TEs) are constitutive components of both eukaryotic and prokaryotic genomes. The role of TEs in the evolution of genes and genomes has been widely assessed over the past years in a variety of model and non-model organisms. Drosophila is undoubtedly among the most powerful model organisms used for the purpose of studying the role of transposons and their effects on the stability and evolution of genes and genomes. Besides their most intuitive role as insertional mutagens, TEs can modify the transcriptional pattern of host genes by juxtaposing new cis-regulatory sequences. A key element of TE biology is that they carry transcriptional control elements that fine-tune the transcription of their own genes, but that can also perturb the transcriptional activity of neighboring host genes. From this perspective, the transposition-mediated modulation of gene expression is an important issue for the short-term adaptation of physiological functions to the environmental changes, and for long-term evolutionary changes. Here, we review the current literature concerning the regulatory and structural elements operating in cis provided by TEs in Drosophila. Furthermore, we highlight that, besides their influence on both TEs and host genes expression, they can affect the chromatin structure and epigenetic status as well as both the chromosome’s structure and stability. It emerges that Drosophila is a good model organism to study the effect of TE-linked regulatory sequences, and it could help future studies on TE–host interactions in any complex eukaryotic genome.

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Sex and the TEs: transposable elements in sexual development and function in animals

Mobile DNA ◽

10.1186/s13100-019-0185-0 ◽

2019 ◽

Vol 10 (1) ◽

Cited By ~ 18

Author(s):

Corentin Dechaud ◽

Jean-Nicolas Volff ◽

Manfred Schartl ◽

Magali Naville

Keyword(s):

Transposable Elements ◽

Sexual Reproduction ◽

Dna Sequences ◽

Sexual Development ◽

Regulatory Sequences ◽

New Host ◽

Transpositional Activity ◽

Evolutionary Success ◽

And Function ◽

Host Genes

Abstract Transposable elements are endogenous DNA sequences able to integrate into and multiply within genomes. They constitute a major source of genetic innovations, as they can not only rearrange genomes but also spread ready-to-use regulatory sequences able to modify host gene expression, and even can give birth to new host genes. As their evolutionary success depends on their vertical transmission, transposable elements are intrinsically linked to reproduction. In organisms with sexual reproduction, this implies that transposable elements have to manifest their transpositional activity in germ cells or their progenitors. The control of sexual development and function can be very versatile, and several studies have demonstrated the implication of transposable elements in the evolution of sex. In this review, we report the functional and evolutionary relationships between transposable elements and sexual reproduction in animals. In particular, we highlight how transposable elements can influence expression of sexual development genes, and how, reciprocally, they are tightly controlled in gonads. We also review how transposable elements contribute to the organization, expression and evolution of sexual development genes and sex chromosomes. This underscores the intricate co-evolution between host functions and transposable elements, which regularly shift from a parasitic to a domesticated status useful to the host.

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Faculty Opinions recommendation of Origin of a substantial fraction of human regulatory sequences from transposable elements.

Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature ◽

10.3410/f.1012095.184370 ◽

2003 ◽

Author(s):

Marie-Angele Grandbastien

Keyword(s):

Transposable Elements ◽

Regulatory Sequences ◽

Substantial Fraction

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Role of Transposable Elements in Gene Regulation in the Human Genome

Life ◽

10.3390/life11020118 ◽

2021 ◽

Vol 11 (2) ◽

pp. 118

Author(s):

Arsala Ali ◽

Kyudong Han ◽

Ping Liang

Keyword(s):

Gene Regulation ◽

Transposable Elements ◽

Regulatory Sequences ◽

Rna Sequences ◽

Expression Of Genes ◽

Wide Range ◽

Lineage Specificity ◽

Regulatory Rnas ◽

Potential Factors ◽

Interspersed Repeats

Transposable elements (TEs), also known as mobile elements (MEs), are interspersed repeats that constitute a major fraction of the genomes of higher organisms. As one of their important functional impacts on gene function and genome evolution, TEs participate in regulating the expression of genes nearby and even far away at transcriptional and post-transcriptional levels. There are two known principal ways by which TEs regulate the expression of genes. First, TEs provide cis-regulatory sequences in the genome with their intrinsic regulatory properties for their own expression, making them potential factors for regulating the expression of the host genes. TE-derived cis-regulatory sites are found in promoter and enhancer elements, providing binding sites for a wide range of trans-acting factors. Second, TEs encode for regulatory RNAs with their sequences showed to be present in a substantial fraction of miRNAs and long non-coding RNAs (lncRNAs), indicating the TE origin of these RNAs. Furthermore, TEs sequences were found to be critical for regulatory functions of these RNAs, including binding to the target mRNA. TEs thus provide crucial regulatory roles by being part of cis-regulatory and regulatory RNA sequences. Moreover, both TE-derived cis-regulatory sequences and TE-derived regulatory RNAs have been implicated in providing evolutionary novelty to gene regulation. These TE-derived regulatory mechanisms also tend to function in a tissue-specific fashion. In this review, we aim to comprehensively cover the studies regarding these two aspects of TE-mediated gene regulation, mainly focusing on the mechanisms, contribution of different types of TEs, differential roles among tissue types, and lineage-specificity, based on data mostly in humans.

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Host Gene Regulation by Transposable Elements: The New, the Old and the Ugly

Viruses ◽

10.3390/v12101089 ◽

2020 ◽

Vol 12 (10) ◽

pp. 1089 ◽

Cited By ~ 2

Author(s):

Rocio Enriquez-Gasca ◽

Poppy A. Gould ◽

Helen M. Rowe

Keyword(s):

Gene Expression ◽

Gene Regulation ◽

Transposable Elements ◽

Essential Gene ◽

Expression Patterns ◽

Genetic Material ◽

Endogenous Retroviruses ◽

Host Gene ◽

New Genes ◽

Host Genes

The human genome has been under selective pressure to evolve in response to emerging pathogens and other environmental challenges. Genome evolution includes the acquisition of new genes or new isoforms of genes and changes to gene expression patterns. One source of genome innovation is from transposable elements (TEs), which carry their own promoters, enhancers and open reading frames and can act as ‘controlling elements’ for our own genes. TEs include LINE-1 elements, which can retrotranspose intracellularly and endogenous retroviruses (ERVs) that represent remnants of past retroviral germline infections. Although once pathogens, ERVs also represent an enticing source of incoming genetic material that the host can then repurpose. ERVs and other TEs have coevolved with host genes for millions of years, which has allowed them to become embedded within essential gene expression programmes. Intriguingly, these host genes are often subject to the same epigenetic control mechanisms that evolved to combat the TEs that now regulate them. Here, we illustrate the breadth of host gene regulation through TEs by focusing on examples of young (The New), ancient (The Old), and disease-causing (The Ugly) TE integrants.

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Regulation of transposable elements: Interplay between TE-encoded regulatory sequences and host-specifictrans-acting factors inDrosophila melanogaster

Molecular Ecology ◽

10.1111/mec.14259 ◽

2017 ◽

Vol 26 (19) ◽

pp. 5149-5159 ◽

Cited By ~ 8

Author(s):

Ana Marija Jakšić ◽

Robert Kofler ◽

Christian Schlötterer

Keyword(s):

Transposable Elements ◽

Regulatory Sequences

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Codon Usage by Transposable Elements and Their Host Genes in Five Species

Journal of Molecular Evolution ◽

10.1007/s00239-001-0059-0 ◽

2002 ◽

Vol 54 (5) ◽

pp. 625-637 ◽

Cited By ~ 21

Author(s):

Emmanuelle Lerat ◽

Pierre Capy ◽

Christian Biémont

Keyword(s):

Transposable Elements ◽

Codon Usage ◽

Host Genes

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Transposable elements as a potent source of diverse cis -regulatory sequences in mammalian genomes

Philosophical Transactions of the Royal Society B Biological Sciences ◽

10.1098/rstb.2019.0347 ◽

2020 ◽

Vol 375 (1795) ◽

pp. 20190347 ◽

Cited By ~ 14

Author(s):

Vasavi Sundaram ◽

Joanna Wysocka

Keyword(s):

Gene Regulation ◽

Transposable Elements ◽

Regulatory Networks ◽

Regulatory Elements ◽

Regulatory Function ◽

Specific Gene ◽

Regulatory Sequences ◽

Dependent Manner ◽

Unique Contribution ◽

Regulatory Potential

Eukaryotic gene regulation is mediated by cis -regulatory elements, which are embedded within the vast non-coding genomic space and recognized by the transcription factors in a sequence- and context-dependent manner. A large proportion of eukaryotic genomes, including at least half of the human genome, are composed of transposable elements (TEs), which in their ancestral form carried their own cis -regulatory sequences able to exploit the host trans environment to promote TE transcription and facilitate transposition. Although not all present-day TE copies have retained this regulatory function, the preexisting regulatory potential of TEs can provide a rich source of cis -regulatory innovation for the host. Here, we review recent evidence documenting diverse contributions of TE sequences to gene regulation by functioning as enhancers, promoters, silencers and boundary elements. We discuss how TE-derived enhancer sequences can rapidly facilitate changes in existing gene regulatory networks and mediate species- and cell-type-specific regulatory innovations, and we postulate a unique contribution of TEs to species-specific gene expression divergence in pluripotency and early embryogenesis. With advances in genome-wide technologies and analyses, systematic investigation of TEs' cis -regulatory potential is now possible and our understanding of the biological impact of genomic TEs is increasing. This article is part of a discussion meeting issue ‘Crossroads between transposons and gene regulation’.

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