Revisiting horizontal transfer of transposable elements in Drosophila

Most of our understanding of Drosophila heterochromatin structure and evolution has come from the annotation of heterochromatin from the isogenic y; cn bw sp strain. However, almost nothing is known about the heterochromatin's structural dynamics and evolution. Here, we focus on a 180-kb heterochromatic locus producing Piwi-interacting RNAs (piRNA cluster), the flamenco (flam) locus, known to be responsible for the control of at least three transposable elements (TEs). We report its detailed structure in three different Drosophila lines chosen according to their capacity to repress or not to repress the expression of two retrotransposons named ZAM and Idefix, and we show that they display high structural diversity. Numerous rearrangements due to homologous and nonhomologous recombination, deletions and segmental duplications, and loss and gain of TEs are diverse sources of active genomic variation at this locus. Notably, we evidence a correlation between the presence of ZAM and Idefix in this piRNA cluster and their silencing. They are absent from flam in the strain where they are derepressed. We show that, unexpectedly, more than half of the flam locus results from recent TE insertions and that most of the elements concerned are prone to horizontal transfer between species of the melanogaster subgroup. We build a model showing how such high and constant dynamics of a piRNA master locus open the way to continual emergence of new patterns of piRNA biogenesis leading to changes in the level of transposition control.RNAi | gene silencing | epigenetics O ver the course of evolution, transposable elements (TEs) have accumulated in the genomes of eukaryotes, where they can account for up to 85% of the DNA (1). Most of these sequences have lost their ability to transpose. They are now stable components of the genomes. Their conservation throughout evolution suggests that they may confer advantageous effects to their hosts. However, transposition of the copies that remain functional could generate deleterious mutations if they were not severely repressed by their host. RNAi, which is a gene-silencing mechanism triggered by small RNAs (reviewed in ref.2), has been identified as being the main cellular machinery involved in the "taming" of TEs (reviewed in refs. 3-5). RNAi pathways involve small RNAs of diverse families. Among them, Piwiinteracting RNAs (piRNAs) have been shown to be involved in TE silencing in the Drosophila ovary. These piRNAs, 23-29 nt long, are bound by the Argonaute proteins Piwi, Argonaute 3, or Aubergine. They are produced by discrete genomic loci named piRNA clusters, which have been described as containing vestiges of TEs (6). One of these loci, the flamenco (flam) locus, extends over 180 kilobases (kb) on the Drosophila X chromosome. It is proximal to the DISCO interacting protein 1 gene (DIP1) and close to pericentromeric heterochromatin. Before the identification of piRNAs, this locus had been shown to regulate the Gypsy retrotransposon (7, 8 (6) showed the potential for the flam cluster to pr...

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“…High sequence similarity suggests horizontal transfer (reviewed in ref. 25). Sequence similarity was compared with the one found for R1.…”

Section: Structural Modifications Affecting Flam May Explain Differenmentioning

confidence: 99%

Distribution, evolution, and diversity of retrotransposons at the flamenco locus reflect the regulatory properties of piRNA clusters

Zanni

Eymery

Coiffet

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

120

159

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“…The best documented instances of HT between the nuclear genomes of multicellular eukaryotes involve mobile genetic elements, and in particular class 2 or DNA mediated transposons (7,8). Thus far, conspicuous cases of HT of DNA transposons have been detected among insects (8)(9)(10)(11)(12), fish (13) and, in one example, between plants (14). Germline invasions by retroviruses have been documented for several mammals (15)(16)(17)(18), and there is mounting evidence supporting the horizontal introduction of a snake retroposon in ruminants (19,20).…”

mentioning

confidence: 99%

Repeated horizontal transfer of a DNA transposon in mammals and other tetrapods

Pace

Gilbert

Clark

et al. 2008

Proc. Natl. Acad. Sci. U.S.A.

196

214

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Horizontal transfer (HT) is central to the evolution of prokaryotic species. Selfish and mobile genetic elements, such as phages, plasmids, and transposons, are the primary vehicles for HT among prokaryotes. In multicellular eukaryotes, the prevalence and evolutionary significance of HT remain unclear. Here, we identified a set of DNA transposon families dubbed SPACE INVADERS (or SPIN) whose consensus sequences are Ϸ96% identical over their entire length (2.9 kb) in the genomes of murine rodents (rat/mouse), bushbaby (prosimian primate), little brown bat (laurasiatherian), tenrec (afrotherian), opossum (marsupial), and two non-mammalian tetrapods (anole lizard and African clawed frog). In contrast, SPIN elements were undetectable in other species represented in the sequence databases, including 19 other mammals with draft whole-genome assemblies. This patchy distribution, coupled with the extreme level of SPIN identity in widely divergent tetrapods and the overall lack of selective constraint acting on these elements, is incompatible with vertical inheritance, but strongly indicative of multiple horizontal introductions. We show that these germline infiltrations likely occurred around the same evolutionary time (15-46 mya) and spawned some of the largest bursts of DNA transposon activity ever recorded in any species lineage (nearly 100,000 SPIN copies per haploid genome in tenrec). The process also led to the emergence of a new gene in the murine lineage derived from a SPIN transposase. In summary, HT of DNA transposons has contributed significantly to shaping and diversifying the genomes of multiple mammalian and tetrapod species. genome evolution ͉ lateral gene transfer ͉ transposable elements ͉ transposase L ateral or horizontal transfer (HT), the transfer of genetic material between reproductively isolated species, is a frequent occurrence in prokaryotes with selfish and mobile genetic elements such as phages, plasmids, and transposons, serving as the primary vehicles for HT of prokaryotic genes (1). In contrast, reports of HT are scarce in eukaryotes and most cases of nuclear acquisition implicate transfers from prokaryotes or endosymbionts (2-6). The best documented instances of HT between the nuclear genomes of multicellular eukaryotes involve mobile genetic elements, and in particular class 2 or DNA mediated transposons (7,8). Thus far, conspicuous cases of HT of DNA transposons have been detected among insects (8-12), fish (13) and, in one example, between plants (14). Germline invasions by retroviruses have been documented for several mammals (15-18), and there is mounting evidence supporting the horizontal introduction of a snake retroposon in ruminants (19,20). However, to our knowledge, there has been no substantiated report of HT of DNA transposons in mammals. Here, we present unequivocal evidence for the repeated HT of a DNA transposon family named SPACE INVADERS in 7 tetrapod lineages, including 5 mammalian orders. ResultsDiscovery of SPIN Transposons. While surveying DNA transposons in the draft...

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“…Indeed, in organisms with random mating and weak linkage disequilibrium (e.g., Drosophila), a host variant suppressing a single TE family will enjoy only weak adaptive advantage (Charlesworth and Langley 1986). If the suppression of TE transposition involves specific associations between host alleles and TE variants, this is unlikely to drive the fast evolution of host genes involved in TE suppression.In rare cases, TEs are observed to have been horizontally transferred between host species (reviewed by Silva et al 2004;Loreto et al 2008;Schaack et al 2010). In these cases, the evolutionary impacts of TEs on the host may be more analogous to those of nongenomic pathogens.…”

mentioning

confidence: 99%

“…In rare cases, TEs are observed to have been horizontally transferred between host species (reviewed by Silva et al 2004;Loreto et al 2008;Schaack et al 2010). In these cases, the evolutionary impacts of TEs on the host may be more analogous to those of nongenomic pathogens.…”

mentioning

confidence: 99%

Long-Term and Short-Term Evolutionary Impacts of Transposable Elements onDrosophila

Lee

Langley

2012

Genetics

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Transposable elements (TEs) are considered to be genomic parasites and their interactions with their hosts have been likened to the coevolution between host and other nongenomic, horizontally transferred pathogens. TE families, however, are vertically inherited as integral segments of the nuclear genome. This transmission strategy has been suggested to weaken the selective benefits of host alleles repressing the transposition of specific TE variants. On the other hand, the elevated rates of TE transposition and high incidences of deleterious mutations observed during the rare cases of horizontal transfers of TE families between species could create at least a transient process analogous to the influence of horizontally transmitted pathogens. Here, we formally address this analogy, using empirical and theoretical analysis to specify the mechanism of how host-TE interactions may drive the evolution of host genes. We found that host TE-interacting genes actually have more pervasive evidence of adaptive evolution than immunity genes that interact with nongenomic pathogens in Drosophila. Yet, both our theoretical modeling and empirical observations comparing Drosophila melanogaster populations before and after the horizontal transfer of P elements, which invaded D. melanogaster early last century, demonstrated that horizontally transferred TEs have only a limited influence on host TE-interacting genes. We propose that the more prevalent and constant interaction with multiple vertically transmitted TE families may instead be the main force driving the fast evolution of TE-interacting genes, which is fundamentally different from the gene-for-gene interaction of host-pathogen coevolution. HOST-PATHOGEN interactions affect the population dynamics and the evolutionary trajectories of both species. In particular, coevolutionary dynamics will affect the pattern of polymorphism and divergence of genes underlying hostparasite interactions either through an arms race (Van Valen 1973;Dawkins and Krebs 1979) or through balancing selection (Haldane 1949;Hughes et al. 1990; Takahata et al. 1992;Hughes and Yeager 1998;Rose et al. 2004). In either case, accelerated rates of protein evolution and/or recurrent adaptive substitutions are expected in genes engaged in these interactions, which has been observed in both immunity genes (Schlenke and Begun 2003;Jiggins and Kim 2007;Sackton et al. 2007;Obbard et al. 2009b) and antivirus siRNA genes (Obbard et al. 2006(Obbard et al. , 2009a(Obbard et al. ,b, 2011 in Drosophila.Transposable elements (TEs) are ubiquitous genomic constituents that increase their copy number (the number of TEs in a host genome) by replicative transposition (copying to new genomic locations). Like Drosophila, most host genomes are occupied by multiple TE families, which are defined by sequence similarity (homology) and by replication and transposition mechanisms. Even though incidences of potentially adaptive individual TE insertions with high population frequencies have been reported (Daborn et al. 20...

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Revisiting horizontal transfer of transposable elements in Drosophila

Cited by 165 publications

References 96 publications

Distribution, evolution, and diversity of retrotransposons at the flamenco locus reflect the regulatory properties of piRNA clusters

Distribution, evolution, and diversity of retrotransposons at the flamenco locus reflect the regulatory properties of piRNA clusters

Repeated horizontal transfer of a DNA transposon in mammals and other tetrapods

Long-Term and Short-Term Evolutionary Impacts of Transposable Elements onDrosophila

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