P elements and MITE relatives in the whole genome sequence of Anopheles gambiae

BACKGROUND: Miniature Inverted-repeat Terminal Elements (MITEs), which are particular class-II transposable elements (TEs), play an important role in genome evolution, because they have very high copy numbers and display recurrent bursts of transposition. The 5' and 3' subterminal regions of a given MITE family often show a high sequence similarity with the corresponding regions of an autonomous Class-II TE family. However, the sustained presence over a prolonged evolutionary time of MITEs and TE master copies able to promote their mobility has been rarely reported within the same genome, and this raises fascinating evolutionary questions. RESULTS: We report here the presence of P transposable elements with related MITE families in the Anopheles gambiae genome. Using a TE annotation pipeline we have identified and analyzed all the P sequences in the sequenced A. gambiae PEST strain genome. More than 0.49% of the genome consists of P elements and derivates. P elements can be divided into 9 different subfamilies, separated by more than 30% of nucleotide divergence. Seven of them present full length copies. Ten MITE families are associated with 6 out of the 9 Psubfamilies. Comparing their intra-element nucleotide diversities and their structures allows us to propose the putative dynamics of their emergence. In particular, one MITE family which has a hybrid structure, with ends each of which is related to a different P-subfamily, suggests a new mechanism for their emergence and their mobility. CONCLUSION: This work contributes to a greater understanding of the relationship between full-length class-II TEs and MITEs, in this case P elements and their derivatives in the genome of A. gambiae. Moreover, it provides the most comprehensive catalogue to date of P-like transposons in this genome and provides convincing yet indirect evidence that some of the subfamilies have been recently active

Domesticated P elements in the Drosophila montium species subgroup have a new function related to a DNA binding property.

Molecular domestication of a transposable element is defined as its functional recruitment by the host genome. To date, two independent events of molecular domestication of the P transposable element have been described: in the Drosophila obscura species group and in the Drosophila montium species subgroup. These P neogenes consist to stationary, non repeated sequences, potentially encoding 66 kDa repressor-like proteins (RLs). Here we investigate the function of the montium P neogenes. We provide evidence for the presence of RLs proteins in two montium species (D. tsacasi and D. bocqueti) specifically expressed in adult and larval brain and gonads. We tested the hypothesis that the montium P neogenes function is related to the repression of the transposition of distant related mobile P elements which coexist in the genome. Our results strongly suggest that the montium P neogenes are not recruited to down regulate the P element transposition. Given that all the proteins encoded by mobile or stationary P homologous sequences show a strong conservation of the DNA Binding Domain, we tested the capacity of the RLs proteins to bind DNA in vivo. Immunstaining of polytene chromosomes in D. melanogaster transgenic lines strongly suggest that montium P neogenes encode proteins that bind DNA in vivo. RLs proteins show multiple binding to the chromosomes. We suggest that the property recruited in the case of the montium P neoproteins is their DNA binding property. The possible functions of these neogenes are discussed

Recurrent insertion and duplication generate networks of transposable element sequences in the Drosophila melanogaster genome.

BACKGROUND: The recent availability of genome sequences has provided unparalleled insights into the broad-scale patterns of transposable element (TE) sequences in eukaryotic genomes. Nevertheless, the difficulties that TEs pose for genome assembly and annotation have prevented detailed, quantitative inferences about the contribution of TEs to genomes sequences. RESULTS: Using a high-resolution annotation of TEs in Release 4 genome sequence, we revise estimates of TE abundance in Drosophila melanogaster. We show that TEs are non-randomly distributed within regions of high and low TE abundance, and that pericentromeric regions with high TE abundance are mosaics of distinct regions of extreme and normal TE density. Comparative analysis revealed that this punctate pattern evolves jointly by transposition and duplication, but not by inversion of TE-rich regions from unsequenced heterochromatin. Analysis of genome-wide patterns of TE nesting revealed a 'nesting network' that includes virtually all of the known TE families in the genome. Numerous directed cycles exist among TE families in the nesting network, implying concurrent or overlapping periods of transpositional activity. CONCLUSION: Rapid restructuring of the genomic landscape by transposition and duplication has recently added hundreds of kilobases of TE sequence to pericentromeric regions in D. melanogaster. These events create ragged transitions between unique and repetitive sequences in the zone between euchromatic and beta-heterochromatic regions. Complex relationships of TE nesting in beta-heterochromatic regions raise the possibility of a co-suppression network that may act as a global surveillance system against the majority of TE families in D. melanogaster.RIGHTS : This article is licensed under the BioMed Central licence at http://www.biomedcentral.com/about/license which is similar to the 'Creative Commons Attribution Licence'. In brief you may : copy, distribute, and display the work; make derivative works; or make commercial use of the work - under the following conditions: the original author must be given credit; for any reuse or distribution, it must be made clear to others what the license terms of this work are

Telomeric Trans-Silencing: An Epigenetic Repression Combining RNA Silencing and Heterochromatin Formation

The study of P-element repression in Drosophila melanogaster led to the discovery of the telomeric Trans-Silencing Effect (TSE), a repression mechanism by which a transposon or a transgene inserted in subtelomeric heterochromatin (Telomeric Associated Sequence or TAS) has the capacity to repress in trans in the female germline, a homologous transposon, or transgene located in euchromatin. TSE shows variegation among egg chambers in ovaries when silencing is incomplete. Here, we report that TSE displays an epigenetic transmission through meiosis, which involves an extrachromosomal maternally transmitted factor. We show that this silencing is highly sensitive to mutations affecting both heterochromatin formation (Su(var)205 encoding Heterochromatin Protein 1 and Su(var)3–7) and the repeat-associated small interfering RNA (or rasiRNA) silencing pathway (aubergine, homeless, armitage, and piwi). In contrast, TSE is not sensitive to mutations affecting r2d2, which is involved in the small interfering RNA (or siRNA) silencing pathway, nor is it sensitive to a mutation in loquacious, which is involved in the micro RNA (or miRNA) silencing pathway. These results, taken together with the recent discovery of TAS homologous small RNAs associated to PIWI proteins, support the proposition that TSE involves a repeat-associated small interfering RNA pathway linked to heterochromatin formation, which was co-opted by the P element to establish repression of its own transposition after its recent invasion of the D. melanogaster genome. Therefore, the study of TSE provides insight into the genetic properties of a germline-specific small RNA silencing pathway

Traces of transposable elements in genome dark matter co-opted by flowering gene regulation networks

International audienc

Traces of transposable elements in genome dark matter co-opted by flowering gene regulation networks

International audienc

Telomeric Trans-Silencing in Drosophila melanogaster: Tissue Specificity, Development and Functional Interactions between Non-Homologous Telomeres

BACKGROUND: The study of P element repression in Drosophila melanogaster led to the discovery of the telomeric Trans-Silencing Effect (TSE), a homology-dependent repression mechanism by which a P-transgene inserted in subtelomeric heterochromatin (Telomeric Associated Sequences, "TAS") has the capacity to repress in trans, in the female germline, a homologous P-lacZ transgene located in euchromatin. TSE can show variegation in ovaries, displays a maternal effect as well as an epigenetic transmission through meiosis and involves heterochromatin and RNA silencing pathways. PRINCIPAL FINDINGS: Here, we analyze phenotypic and genetic properties of TSE. We report that TSE does not occur in the soma at the adult stage, but appears restricted to the female germline. It is detectable during development at the third instar larvae where it presents the same tissue specificity and maternal effect as in adults. Transgenes located in TAS at the telomeres of the main chromosomes can be silencers which in each case show the maternal effect. Silencers located at non-homologous telomeres functionally interact since they stimulate each other via the maternally-transmitted component. All germinally-expressed euchromatic transgenes tested, located on all major chromosomes, were found to be repressed by a telomeric silencer: thus we detected no TSE escaper. The presence of the euchromatic target transgene is not necessary to establish the maternal inheritance of TSE, responsible for its epigenetic behavior. A single telomeric silencer locus can simultaneously repress two P-lacZ targets located on different chromosomal arms. CONCLUSIONS AND SIGNIFICANCE: Therefore TSE appears to be a widespread phenomenon which can involve different telomeres and work across the genome. It can explain the P cytotype establishment by telomeric P elements in natural Drosophila populations

Genetic algorithm-based model of evolutionary dynamics of class II transposable elements

International audienceWe propose a new conceptual framework to study the dynamics of transposable elements. Based on a genetic algorithm, our model is designed as a self-organizing system. Our results show that transposable elements could emerge from a single endonuclease gene. The DNA repair mechanisms appear to condition the emergence success of class II TEs. Antagonist selective forces acting on transposable elements and their hosts induce by their opposition differences in the sequence evolution of the functional domains and of the copies

Recurrent exon shuffling between distant P-element families

International audienceTwo independent stationary P-related neogenes had been previously described in the Drosophila obscura species group and in the Drosophila montium species subgroup. In Drosophila melanogaster, P-transposable elements can encode an 87 kDa transposase and a 66 kDa repressor, but the P-neogenes have only conserved the capacity to encode a 66 kDa repressor-like protein specified by the first three exons. We have previously analyzed the genomic modifications associated with the transition of a P-element into the montium P-neogene, the coding capacity of which has been conserved for around 20 Myr ( Nouaud, D., and D. Anxolabéhère. 1997. Mol. Biol. Evol. 14:1132-1144). Here we show that the P-neogene of some species of the montium subgroup presents a new structure involving the capture of an additional exon from a very distant P-element subfamily. This additional exon is inserted either upstream or downstream of the first exon of the P-neogene. As a result of alternative splicing, these modified neogenes can produce, in addition to the repressor-like protein, a new protein which differs only by the NH2-terminal region. We hypothesize that this protein diversity within an organism results in a functional diversification due to the selective advantage associated with the domestication of the P-neogene in these species. Moreover, the autonomous P-element which provides the additional exons is still present in the genome. Its nucleotide sequence is more than 45% distant from the previously defined P-type element (M-type, O-type, T-type) and defines a new P-type element subfamily referred to as the K-type

Detection of new transposable element families in Drosophila melanogaster and Anopheles gambiae genomes

International audienceThe techniques that are usually used to detect transposable elements (TEs) in nucleic acid sequences rely on sequence similarity with previously characterized elements. However, these methods are likely to miss many elements in various organisms. We tested two strategies for the detection of unknown elements. The first, which we call "TBLASTX strategy," searches for TE sequences by comparing the six-frame translations of the nucleic acid sequences of known TEs with the genomic sequence of interest. The second, "repeat-based strategy," searches genomic sequences for long repeats and clusters them in groups of similar sequences. TE copies from a given family are expected to cluster together. We tested the Drosophila melanogaster genomic sequence and the recently sequenced Anopheles gambiae genome in which most TEs remain unknown. We showed that the "TBLASTX strategy" is very efficient as it detected at least 332 new TE families in D. melanogaster and 400 in A. gambiae. This was unexpected in Drosophila as TEs of this organism have been extensively studied. The "repeat-based strategy" appeared to be very inefficient because of two problems: (i) TE copies are heavily deleted and few copies share homologous regions, and (ii) segmental duplications are frequent and it is not easy to distinguish them from TE copies