Comparative analysis of transposable elements in the melanogaster subgroup sequenced genomes

Lerat, Emmanuelle; Burlet, Nelly; Biémont, Christian; Vieira, Cristina

doi:10.1016/j.gene.2010.11.009

Cited by 59 publications

(91 citation statements)

References 55 publications

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“…Therefore, tirant appears to be a newly identified active endogenous retrovirus of D. simulans, a species in which no other active endogenous retrovirus has been reported thus far. (12). These findings indicate that each strain of D. simulans studied possesses at least one potentially complete functional tirant env gene in its genome.…”

Section: Discussionmentioning

confidence: 74%

tirant , a Newly Discovered Active Endogenous Retrovirus in Drosophila simulans

Akkouche

Rebollo

Burlet

et al. 2012

J Virol

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cEndogenous retroviruses have the ability to become permanently integrated into the genomes of their host, and they are generally transmitted vertically from parent to progeny. With the exception of gypsy, few endogenous retroviruses have been identified in insects. In this study, we describe the tirant endogenous retrovirus in a subset of Drosophila simulans natural populations. By focusing on the envelope gene, we show that the entire retroviral cycle (transcription, translation, and retrotransposition) can be completed for tirant within one population of this species. Endogenous retroviruses are genomic sequences that are widely dispersed throughout the host genome. These sequences constitute 8% of the human genome and represent the remnants of ancient infections by retroviruses (1). Some of these retroviruses were domesticated and generated cellular neogenes, such as the syncytin gene (9, 14). The structure of a canonical endogenous retrovirus consists of three open reading frames (ORFs), which are bordered by long terminal repeats (LTRs). The third ORF encodes the envelope protein (Env), which possesses fusogenic properties and is responsible for the infectious behavior of exogenous retroviruses. In insects, several endogenous retroviruses have been described, and most of them possess a complete retroviral structure. Representative insect endogenous retroviruses (IERVs) or insect ErantiViruses (24) include the following: gypsy, ZAM, Idefix, tirant, 17.6, 297, and nomad in Drosophila melanogaster; tom in Drosophila ananassae; Tv1 in Drosophila virilis; TED in Trichoplusia ni; Osvaldo in Drosophila buzzatii; and Yoyo in Ceratitis capitata (see reference 19 for a review). With the exception of nomad and Tv1, each of these displays a complete env ORF. Thus far, only the well-known gypsy element of D. melanogaster has been shown to possess infectious properties (10), as Moloney murine leukemia virus pseudotypes with the gypsy Env protein were shown to infect insect cells (25).The tirant LTR retrotransposon of D. melanogaster was previously described to share sequence similarity with the fusion proteins of certain baculoviruses (13,16,20) (see Fig. 1 for the tirant structure). In a phylogenetic study of numerous elements from insects, Terzian et al. (24) proposed that the tirant element from D. melanogaster (GenBank accession number X93507) belongs to the IERVs. Thus, the tirant element was placed into this clade of retroviruses, which uses a tRNA-Ser binding site to prime reverse transcription (RT). In the study described in this report, we examined this ERV family in Drosophila simulans using a collection of strains with variable numbers of genomic insertions (7), and we demonstrated that this family was able to produce Env proteins in the ovaries of the host. We found that tirant was capable of performing the first step required for infection, i.e., the production of a functional Env protein, which suggests that it could be classified as an active endogenous retrovirus of D. simulans. Furthermore, we demonstr...

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Section: Discussionmentioning

confidence: 74%

tirant , a Newly Discovered Active Endogenous Retrovirus in Drosophila simulans

Akkouche

Rebollo

Burlet

et al. 2012

J Virol

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“…D. melanogaster and D. simulans are sibling species that can be intercrossed but contain substantial divergence. Alignable synonymous nucleotide sites are 12-13% diverged (Begun et al 2007), and the species are strikingly different in repetitive DNA content and heterochromatin, with D. simulans having substantially fewer transposable elements and less satellite DNA (Lohe and Roberts 1988;Bosco et al 2007;Lerat et al 2011). They also have experienced adaptive evolution in genes that are essential for chromosome segregation Anderson et al 2009).…”

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confidence: 99%

Normal Segregation of a Foreign-Species Chromosome During Drosophila Female Meiosis Despite Extensive Heterochromatin Divergence

et al. 2014

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The abundance and composition of heterochromatin changes rapidly between species and contributes to hybrid incompatibility and reproductive isolation. Heterochromatin differences may also destabilize chromosome segregation and cause meiotic drive, the non-Mendelian segregation of homologous chromosomes. Here we use a range of genetic and cytological assays to examine the meiotic properties of a Drosophila simulans chromosome 4 (sim-IV) introgressed into D. melanogaster. These two species differ by 12-13% at synonymous sites and several genes essential for chromosome segregation have experienced recurrent adaptive evolution since their divergence. Furthermore, their chromosome 4s are visibly different due to heterochromatin divergence, including in the AATAT pericentromeric satellite DNA. We find a visible imbalance in the positioning of the two chromosome 4s in sim-IV/mel-IV heterozygote and also replicate this finding with a D. melanogaster 4 containing a heterochromatic deletion. These results demonstrate that heterochromatin abundance can have a visible effect on chromosome positioning during meiosis. Despite this effect, however, we find that sim-IV segregates normally in both diplo and triplo 4 D. melanogaster females and does not experience elevated nondisjunction. We conclude that segregation abnormalities and a high level of meiotic drive are not inevitable byproducts of extensive heterochromatin divergence. Animal chromosomes typically contain large amounts of noncoding repetitive DNA that nevertheless varies widely between species. This variation may potentially induce non-Mendelian transmission of chromosomes. We have examined the meiotic properties and transmission of a highly diverged chromosome 4 from a foreign species within the fruitfly Drosophila melanogaster. This chromosome has substantially less of a simple sequence repeat than does D. melanogaster 4, and we find that this difference results in altered positioning when chromosomes align during meiosis. Yet this foreign chromosome segregates at normal frequencies, demonstrating that chromosome segregation can be robust to major differences in repetitive DNA abundance.H ETEROCHROMATIC repeats at and near telomeres and centromeres turn over rapidly at short evolutionary time scales (Charlesworth et al. 1994). A subset of genes involved in meiosis, chromosome and chromatin function, and transposable element defense also show high rates of divergence between sibling species, often with accompanying signatures of adaptive evolution Begun et al. 2007;Larracuente et al. 2008;Anderson et al. 2009;Obbard et al. 2009;Raffa et al. 2011;Langley et al. 2012). These patterns suggest that organisms need to mount a continual adaptive response to suppress deleterious consequences caused by heterochromatic repetitive DNAs. Satellite DNAs and transposable elements, the major components of heterochromatin, can increase their copy numbers by unequal crossing over and transposition. These expansions can reduce fitness by increasing genome size and rates of...

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“…As mentioned above, the D. melanogaster genome contains three times as many TEs as that of D. simulans, essentially because the copies of TEs found in the former species are mainly full-length. With respect to the number of TE fragments present, D. simulans displays a greater number than D. melanogaster, largely because most of the copies in the former species are degraded and consist of small fragments (Lerat et al, 2011). The Cyp flanking regions and the non-Cyp neighbors harbor a higher diversity of TEs, retrotransposons and DNA transposons in D. melanogaster than in D. simulans, which contains few insertions other than Gypsy and DNAREP1-like (Fig.…”

Section: Discussionmentioning

confidence: 99%

“…These two species also exhibit different responses to insecticides (Windelspecht et al, 1995) and display different proportions of TEs within their genomic sequence, with three times as many TEs being found in D. melanogaster than in D. simulans (Dowsett and Young, 1982;Drosophila 12 genomes consortium, 2007;Hoskins et al, 2002;Kaminker et al, 2002;Vieira et al, 1999). However, the number of TE insertions in D. simulans is greater than in D. melanogaster because most of the copies in the former are degraded into small fragments (Lerat et al, 2011).…”

Section: Introductionmentioning

confidence: 99%

Genomic regions harboring insecticide resistance-associated Cyp genes are enriched by transposable element fragments carrying putative transcription factor binding sites in two sibling Drosophila species

Carareto

Hernandez

Vieira

2014

Gene

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a b s t r a c tIn the present study, an in silico analysis was performed to identify transposable element (TE) fragments inserted in Cyps with functions associated with resistance to insecticides and developmental regulation as well as in neighboring genes in two sibling species , Drosophila melanogaster and Drosophila simulans . The Cyps associated with insecticide resistance and their neighboring non-Cyp genes have accumulated a greater number of TE fragments than the other Cyps or a random sample of genes, predominantly in the 5′-flanking regions. Most of the insertions were due to DNA transposons, with DNAREP1 fragments being the most common. These fragments carry putative binding sites for transcription factors, which reinforces the hypothesis that DNAREP1 may influence gene regulation and play a role in the adaptation of the Drosophila species.

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Comparative analysis of transposable elements in the melanogaster subgroup sequenced genomes

Cited by 59 publications

References 55 publications

tirant , a Newly Discovered Active Endogenous Retrovirus in Drosophila simulans

tirant , a Newly Discovered Active Endogenous Retrovirus in Drosophila simulans

Normal Segregation of a Foreign-Species Chromosome During Drosophila Female Meiosis Despite Extensive Heterochromatin Divergence

Genomic regions harboring insecticide resistance-associated Cyp genes are enriched by transposable element fragments carrying putative transcription factor binding sites in two sibling Drosophila species

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