Dataset Information

Massive horizontal transfer of transposable elements in insects.

ABSTRACT: Horizontal transfer (HT) of genetic material is central to the architecture and evolution of prokaryote genomes. Within eukaryotes, the majority of HTs reported so far are transfers of transposable elements (TEs). These reports essentially come from studies focusing on specific lineages or types of TEs. Because of the lack of large-scale survey, the amount and impact of HT of TEs (HTT) in eukaryote evolution, as well as the trends and factors shaping these transfers, are poorly known. Here, we report a comprehensive analysis of HTT in 195 insect genomes, representing 123 genera and 13 of the 28 insect orders. We found that these insects were involved in at least 2,248 HTT events that essentially occurred during the last 10 My. We show that DNA transposons transfer horizontally more often than retrotransposons, and unveil phylogenetic relatedness and geographical proximity as major factors facilitating HTT in insects. Even though our study is restricted to a small fraction of insect biodiversity and to a recent evolutionary timeframe, the TEs we found to be horizontally transferred generated up to 24% (2.08% on average) of all nucleotides of insect genomes. Together, our results establish HTT as a major force shaping insect genome evolution.

SUBMITTER: Peccoud J

PROVIDER: S-EPMC5422770 | biostudies-literature | 2017 May

REPOSITORIES: biostudies-literature

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Massive horizontal transfer of transposable elements in insects.

Peccoud Jean J Loiseau Vincent V Cordaux Richard R Gilbert Clément C

Proceedings of the National Academy of Sciences of the United States of America 20170417 18

Horizontal transfer (HT) of genetic material is central to the architecture and evolution of prokaryote genomes. Within eukaryotes, the majority of HTs reported so far are transfers of transposable elements (TEs). These reports essentially come from studies focusing on specific lineages or types of TEs. Because of the lack of large-scale survey, the amount and impact of HT of TEs (HTT) in eukaryote evolution, as well as the trends and factors shaping these transfers, are poorly known. Here, we r ...[more]

PMID: 28416702

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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

Massive horizontal transfer of transposable elements in insects.

Publications

Massive horizontal transfer of transposable elements in insects.

Similar Datasets

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