Dataset Information

Short and long-term evolutionary dynamics of subtelomeric piRNA clusters in Drosophila.

ABSTRACT: Two Telomeric Associated Sequences, TAS-R and TAS-L, form the principal subtelomeric repeat families identified in Drosophila melanogaster. They are PIWI-interacting RNA (piRNA) clusters involved in repression of Transposable Elements. In this study, we revisited TAS structural and functional dynamics in D. melanogaster and in related species. In silico analysis revealed that TAS-R family members are composed of previously uncharacterized domains. This analysis also showed that TAS-L repeats are composed of arrays of a region we have named "TAS-L like" (TLL) identified specifically in one TAS-R family member, X-TAS. TLL were also present in other species of the melanogaster subgroup. Therefore, it is possible that TLL represents an ancestral subtelomeric piRNA core-cluster. Furthermore, all D. melanogaster genomes tested possessed at least one TAS-R locus, whereas TAS-L can be absent. A screen of 110 D. melanogaster lines showed that X-TAS is always present in flies living in the wild, but often absent in long-term laboratory stocks and that natural populations frequently lost their X-TAS within 2 years upon lab conditioning. Therefore, the unexpected structural and temporal dynamics of subtelomeric piRNA clusters demonstrated here suggests that genome organization is subjected to distinct selective pressures in the wild and upon domestication in the laboratory.

SUBMITTER: Asif-Laidin A

PROVIDER: S-EPMC5737368 | biostudies-literature | 2017 Oct

REPOSITORIES: biostudies-literature

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Short and long-term evolutionary dynamics of subtelomeric piRNA clusters in Drosophila.

Asif-Laidin Amna A Delmarre Valérie V Laurentie Jeanne J Miller Wolfgang J WJ Ronsseray Stéphane S Teysset Laure L

DNA research : an international journal for rapid publication of reports on genes and genomes 20171001 5

Two Telomeric Associated Sequences, TAS-R and TAS-L, form the principal subtelomeric repeat families identified in Drosophila melanogaster. They are PIWI-interacting RNA (piRNA) clusters involved in repression of Transposable Elements. In this study, we revisited TAS structural and functional dynamics in D. melanogaster and in related species. In silico analysis revealed that TAS-R family members are composed of previously uncharacterized domains. This analysis also showed that TAS-L repeats are ...[more]

PMID: 28459978

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Project description:Animal genomes are parasitized by a horde of transposable elements (TEs) whose mutagenic activity can have catastrophic consequences. The piRNA pathway is a conserved mechanism to repress TE activity in the germline via a specialized class of small RNAs associated with effector Piwi proteins called piwi-associated RNAs (piRNAs). piRNAs are produced from discrete genomic regions called piRNA clusters (piCs). While piCs are generally enriched for TE sequences and the molecular processes by which they are transcribed and regulated are relatively well understood in Drosophila melanogaster , much less is known about the origin and evolution of piCs in this or any other species. To investigate piC evolution, we use a population genomics approach to compare piC activity and sequence composition across 8 geographically distant strains of D. melanogaster with high quality long-read genome assemblies. We perform extensive annotations of ovary piCs and TE content in each strain and test predictions of two proposed models of piC evolution. The 'de novo' model posits that individual TE insertions can spontaneously attain the status of a small piC to generate piRNAs silencing the entire TE family. The 'trap' model envisions large and evolutionary stable genomic clusters where TEs tend to accumulate and serves as a long-term "memory" of ancient TE invasions and produce a great variety of piRNAs protecting against related TEs entering the genome. It remains unclear which model best describes the evolution of piCs. Our analysis uncovers extensive variation in piC activity across strains and signatures of rapid birth and death of piCs in natural populations. Most TE families inferred to be recently or currently active show an enrichment of strain-specific insertions into large piCs, consistent with the trap model. By contrast, only a small subset of active LTR retrotransposon families is enriched for the formation of strain-specific piCs, suggesting that these families have an inherent proclivity to form de novo piCs. Thus, our findings support aspects of both 'de novo' and 'trap' models of piC evolution. We propose that these two models represent two extreme stages along an evolutionary continuum, which begins with the emergence of piCs de novo from a few specific LTR retrotransposon insertions that subsequently expand by accretion of other TE insertions during evolution to form larger 'trap' clusters. Our study shows that piCs are evolutionarily labile and that TEs themselves are the major force driving the formation and evolution of piCs.

Dataset Information

Short and long-term evolutionary dynamics of subtelomeric piRNA clusters in Drosophila.

Publications

Short and long-term evolutionary dynamics of subtelomeric piRNA clusters in Drosophila.

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