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Promiscuous DNA: horizontal transfer of transposable elements and why it matters for eukaryotic evolution.

ABSTRACT: Horizontal transfer is the passage of genetic material between genomes by means other than parent-to-offspring inheritance. Although the transfer of genes is thought to be crucial in prokaryotic evolution, few instances of horizontal gene transfer have been reported in multicellular eukaryotes; instead, most cases involve transposable elements. With over 200 cases now documented, it is possible to assess the importance of horizontal transfer for the evolution of transposable elements and their host genomes. We review criteria for detecting horizontal transfers and examine recent examples of the phenomenon, shedding light on its mechanistic underpinnings, including the role of host-parasite interactions. We argue that the introduction of transposable elements by horizontal transfer in eukaryotic genomes has been a major force propelling genomic variation and biological innovation.

SUBMITTER: Schaack S

PROVIDER: S-EPMC2940939 | biostudies-literature | 2010 Sep

REPOSITORIES: biostudies-literature

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Promiscuous DNA: horizontal transfer of transposable elements and why it matters for eukaryotic evolution.

Schaack Sarah S Gilbert Clément C Feschotte Cédric C

Trends in ecology & evolution 20100628 9

Horizontal transfer is the passage of genetic material between genomes by means other than parent-to-offspring inheritance. Although the transfer of genes is thought to be crucial in prokaryotic evolution, few instances of horizontal gene transfer have been reported in multicellular eukaryotes; instead, most cases involve transposable elements. With over 200 cases now documented, it is possible to assess the importance of horizontal transfer for the evolution of transposable elements and their h ...[more]

PMID: 20591532

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Project description:BackgroundMutator-like elements (MULEs) are a significant superfamily of DNA transposons on account of their: (i) great transpositional activity and propensity for insertion in or near gene sequences, (ii) their consequent high mutagenic capacity, and, (iii) their tendency to acquire host gene fragments. Consequently, MULEs are important genetic tools and represent a key study system for research into host-transposon interactions. Yet, while several studies have focused on the impacts of MULEs on crop and fungus genomes, their evolution remains poorly explored.ResultsWe perform comprehensive bioinformatic and phylogenetic analyses to address currently available MULE diversity and reconstruct evolution for the group. For this, we mine MULEs from online databases, and combine search results with available transposase sequences retrieved from previously published studies. Our analyses uncover two entirely new MULE clades that contain elements almost entirely restricted to arthropod hosts, considerably expanding the set of MULEs known from this group, suggesting that many additional MULEs may await discovery from further arthropod genomes. In several cases, close relationships occur between MULEs recovered from distantly related host organisms, suggesting that horizontal transfer events may have played an important role in the evolution of the group. However, it is apparent that MULEs from plants remain separate from MULEs identified from other host groups. MULE structure varies considerably across phylogeny, and TIR length is shown to vary greatly both within and between MULE groups. Our phylogeny suggests that MULE diversity is clustered in well-supported groups, typically according to host taxonomy. With reference to this, we make suggestions on how MULE diversity can be partitioned to provide a robust taxonomic framework.ConclusionsOur study represents a considerable advance in the understanding of MULE diversity, host range and evolution, and provides a taxonomic framework for the classification of further MULE elements that await discovery. Our findings also raise a number of questions relating to MULE biology, suggesting that this group will provide a rich avenue for future study.

Project description:BackgroundA fraction of all genomes is composed of transposable elements (TEs) whose mobility needs to be carefully controlled. In gonads, TE activity is repressed by PIWI-interacting RNAs (piRNAs), a class of small RNAs synthesized by heterochromatic loci enriched in TE fragments, called piRNA clusters. Maintenance of active piRNA clusters across generations is secured by maternal piRNA inheritance providing the memory for TE repression. On rare occasions, genomes encounter horizontal transfer (HT) of new TEs with no piRNA targeting them, threatening the host genome integrity. Naïve genomes can eventually start to produce new piRNAs against these genomic invaders, but the timing of their emergence remains elusive.ResultsUsing a set of TE-derived transgenes inserted in different germline piRNA clusters and functional assays, we have modeled a TE HT in Drosophila melanogaster. We have found that the complete co-option of these transgenes by a germline piRNA cluster can occur within four generations associated with the production of new piRNAs all along the transgenes and the germline silencing of piRNA sensors. Synthesis of new transgenic TE piRNAs is linked to piRNA cluster transcription dependent on Moonshiner and heterochromatin mark deposition that propagates more efficiently on short sequences. Moreover, we found that sequences located within piRNA clusters can have different piRNA profiles and can influence transcript accumulation of nearby sequences.ConclusionsOur study reveals that genetic and epigenetic properties, such as transcription, piRNA profiles, heterochromatin, and conversion efficiency along piRNA clusters, could be heterogeneous depending on the sequences that compose them. These findings suggest that the capacity of transcriptional signal erasure induced by the chromatin complex specific of the piRNA cluster can be incomplete through the piRNA cluster loci. Finally, these results have revealed an unexpected level of complexity that highlights a new magnitude of piRNA cluster plasticity fundamental for the maintenance of genome integrity.

Dataset Information

Promiscuous DNA: horizontal transfer of transposable elements and why it matters for eukaryotic evolution.

Publications

Promiscuous DNA: horizontal transfer of transposable elements and why it matters for eukaryotic evolution.

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