Molecular domestication of transposable elements: From detrimental parasites to useful 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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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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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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Analysis of 3D genomic interactions identifies candidate host genes that transposable elements potentially regulate

Genome Biology ◽

10.1186/s13059-018-1598-7 ◽

2018 ◽

Vol 19 (1) ◽

Cited By ~ 9

Author(s):

Ramya Raviram ◽

Pedro P. Rocha ◽

Vincent M. Luo ◽

Emily Swanzey ◽

Emily R. Miraldi ◽

...

Keyword(s):

Transposable Elements ◽

Host Genes

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Hinfp is a guardian of the somatic genome by repressing transposable elements

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.2100839118 ◽

2021 ◽

Vol 118 (41) ◽

pp. e2100839118

Author(s):

Niraj K. Nirala ◽

Qi Li ◽

Prachi N. Ghule ◽

Hsi-Ju Chen ◽

Rui Li ◽

...

Keyword(s):

Dna Damage ◽

Transposable Elements ◽

Transposable Element ◽

Cancer Progression ◽

Genome Stability ◽

Genome Instability ◽

Tissue Growth ◽

Loss Of Function ◽

Element Mobilization ◽

Host Genes

Germ cells possess the Piwi-interacting RNA pathway to repress transposable elements and maintain genome stability across generations. Transposable element mobilization in somatic cells does not affect future generations, but nonetheless can lead to pathological outcomes in host tissues. We show here that loss of function of the conserved zinc-finger transcription factor Hinfp causes dysregulation of many host genes and derepression of most transposable elements. There is also substantial DNA damage in somatic tissues of Drosophila after loss of Hinfp. Interference of transposable element mobilization by reverse-transcriptase inhibitors can suppress some of the DNA damage phenotypes. The key cell-autonomous target of Hinfp in this process is Histone1, which encodes linker histones essential for higher-order chromatin assembly. Transgenic expression of Hinfp or Histone1, but not Histone4 of core nucleosome, is sufficient to rescue the defects in repressing transposable elements and host genes. Loss of Hinfp enhances Ras-induced tissue growth and aging-related phenotypes. Therefore, Hinfp is a physiological regulator of Histone1-dependent silencing of most transposable elements, as well as many host genes, and serves as a venue for studying genome instability, cancer progression, neurodegeneration, and aging.

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Chromosomal distribution of the retroelements Rex 1, Rex 3 and Rex 6 in species of the genus Harttia and Hypostomus (Siluriformes: Loricariidae)

Neotropical Ichthyology ◽

10.1590/1982-0224-20190010 ◽

2019 ◽

Vol 17 (2) ◽

Cited By ~ 4

Author(s):

Josiane B. Traldi ◽

Roberto L. Lui ◽

Juliana de F. Martinez ◽

Marcelo R. Vicari ◽

Viviane Nogaroto ◽

...

Keyword(s):

Transposable Elements ◽

Physical Mapping ◽

Genome Organization ◽

Chromosomal Rearrangements ◽

Chromosome Mapping ◽

Chromosomal Evolution ◽

Chromosomal Distribution ◽

Chromosome Markers ◽

Molecular Domestication

ABSTRACT The transposable elements (TE) have been widely applied as physical chromosome markers. However, in Loricariidae there are few physical mapping analyses of these elements. Considering the importance of transposable elements for chromosomal evolution and genome organization, this study conducted the physical chromosome mapping of retroelements (RTEs) Rex1, Rex3 and Rex6 in seven species of the genus Harttia and four species of the genus Hypostomus, aiming to better understand the organization and dynamics of genomes of Loricariidae species. The results showed an intense accumulation of RTEs Rex1, Rex3 and Rex6 and dispersed distribution in heterochromatic and euchromatic regions in the genomes of the species studied here. The presence of retroelements in some chromosomal regions suggests their participation in various chromosomal rearrangements. In addition, the intense accumulation of three retroelements in all species of Harttia and Hypostomus, especially in euchromatic regions, can indicate the participation of these elements in the diversification and evolution of these species through the molecular domestication by genomes of hosts, with these sequences being a co-option for new functions.

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Miniature inverted-repeat transposable elements drive rapid microRNA diversification in angiosperms

10.1101/2021.07.25.453727 ◽

2021 ◽

Author(s):

Zhonglong Guo ◽

Zheng Kuang ◽

Yihan Tao ◽

Haotian Wang ◽

Miaomiao Wan ◽

...

Keyword(s):

Transposable Elements ◽

Inverted Repeat ◽

Small Rnas ◽

De Novo ◽

Arms Race ◽

Plant Adaptation ◽

Molecular Domestication ◽

Transcription Process ◽

Sporadic Cases ◽

And Behavior

MicroRNAs (miRNAs) are rapidly evolving endogenous small RNAs programing organism function and behavior. Although models for miRNA origination have been proposed based on sporadic cases, the genomic mechanisms driving swift diversification of the miRNA repertoires in plants remain elusive. Here, by comprehensively analyzing 20 phylogenetically representative plant species, we identified miniature inverted-repeat transposable elements (MITEs) as the predominant genomic sources for de novo miRNAs in angiosperms. Our data illustrated a transposition-transcription process whereby properly sized MITEs transposed into active genic regions could be converted into new miRNAs, termed MITE-miRNAs, in as few as 20 generations. We showed that this molecular domestication mechanism leads to a possible evolutionary arms race between the MITEs and the host genomes that rapidly and continuously changes the miRNA repertoires. We found that the MITE-miRNAs are selected for targeting genes associated with plant adaptation and habitat expansion, thereby constituting a genomic innovation potentially underlying angiosperm megadiversity.

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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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