What makes transposable elements move in the Drosophila genome?

Transposable elements (TEs), by their capacity of moving and inducing mutations in the genome, are considered important drivers of species evolution. The successful invasions of TEs in genomes, despite their mutational properties, are an apparent paradox. TEs' transposition is usually strongly regulated to low value, but in some cases these elements can also show high transposition rates, which has been associated sometimes to changes in environmental conditions. It is evident that factors susceptible to induce transpositions in natural populations contribute to TE perpetuation. Different factors were proposed as causative agents of TE mobilization in a wide range of organisms: biotic and abiotic stresses, inter- and intraspecific crosses and populational factors. However, there is no clear evidence of the factors capable of inducing TE mobilization in Drosophila, and data on laboratory stocks show contradictory results. The aim of this review is to have an update critical revision about mechanisms promoting transposition of TEs in Drosophila, and to provide to the readers a global vision of the dynamics of these genomic elements in the Drosophila genome.

Molecular characterization and genomic distribution of Isis: a new retrotransposon of Drosophila buzzatii.

A new transposable element, Isis, is identified as a LTR retrotransposon in Drosophila buzzatii. DNA sequence analysis shows that Isis contains three long ORFs similar to gag, pol and env genes of retroviruses. The ORF1 exhibits sequence homology to matrix, capsid and nucleocapsid gag proteins and ORF2 encodes a putative protease (PR), a reverse transcriptase (RT), an Rnase H (RH) and an integrase (IN) region. The analysis of a putative env product, encoded by the env ORF3, shows a degenerated protein containing several stop codons. The molecular study of the putative proteins coded by this new element shows striking similarities to both Ulysses and Osvaldo elements, two LTR retrotransposons, present in D. virilis and D. buzzatii, respectively. Comparisons of the predicted Isis RT to several known retrotransposons show strong phylogenetic relationships to gypsy-like elements, particulary to Ulysses retrotransposon. Studies of Isis chromosomal distribution show a strong hybridization signal in centromeric and pericentromeric regions, and a scattered distribution along all chromosomal arms. The existence of insertional polymorphisms between different strains and high molecular weight bands by Southern blot suggests the existence of full-sized copies that have been active recently. The presence of euchromatic insertion sites coincident between Isis and Osvaldo could indicate preferential insertion sites of Osvaldo element into Isis sequence or vice versa. Moreover, the presence of Isis in different species of the buzzatii complex indicates the ancient origin of this element.

Behaviour of the transposable elements copia and mdg1 in hybrids between the sibling species Drosophila melanogaster and D. simulans.

The behaviour of the retrotransposons copia and mdg1 was analysed in hybrids between Drosophila melanogaster and D. simulans. Females of a highly inbred line of D. melanogaster were crossed with D. simulans males from three natural populations. The insertion site profiles for the two elements were determined in F1 hybrid larvae by in situ hybridization to polytene chromosomes, and were compared with that of their parents. No somatic transposition events were detected after this genomic stress of interspecific hybridization for the two transposable elements concerned.

Changes in the chromosomal insertion pattern of the copia element during the process of making chromosomes homozygous in Drosophila melanogaster.

In situ hybridization on polytene chromosomes of Drosophila melanogaster was used to compare the insertion patterns of copia and mdg1 transposable elements on chromosome 2 in male gametes sampled by two different methods: (i) by crossing the males tested with females from a highly inbred line with known copia and mdg1 insertion profiles; (ii) by crossing the same males with females from a marked strain, and analysing the resulting homozygous chromosomes. Crossing of the males with the inbred line led to homogeneous insertion profiles for both the copia and mdg1 elements in larvae, thus giving an accurate estimation of the patterns in the two gamete classes of each male. Crossing with the marked strain led, however, to heterogeneity in insertion patterns of the copia transposable element, while no significant polymorphism was observed for mdg1. The use of balancer chromosomes is thus not an adequate way of inferring transposable element insertion patterns of Drosophila males, at least for the copia element. This technique could, however, be powerful for investigating the control of movements of this element.

Population dynamics of the copia, mdg1, mdg3, gypsy, and P transposable elements in a natural population of Drosophila melanogaster.

The insertion site polymorphism of the copia, mdg1, mdg3, gypsy, and P transposable elements was analysed by in situ hybridization to the polytene chromosomes in genomes of males from a natural population of Drosophila melanogaster. Parameters of various theoretical models of the population biology of transposable elements were estimated from our data, and different hypotheses explaining TE copy number containment were tested. The copia, mdg1 and gypsy elements show evidence for a deficiency of insertions on the X chromosomes, a result consistent with selection against the mutational effects of insertions. On the contrary, mdg3 and P copy numbers fit a neutral model with a balance between regulated transposition and excisions. There is no strong evidence of a systematic accumulation of elements in the distal and proximal regions of the chromosomes where crossing over and ectopic exchanges are reduced. For all chromosome arms but 3L, however, the TE site density increases from the proximal to the distal parts of the chromosomes (the centromeric regions were excluded in this analysis) with sometimes a sharp decrease in density at the extreme tip, following in part the exchange coefficient. The way the copy number of TEs is contained in genomes depends thus on the element considered, and on various forces acting simultaneously, indicating that models of TE dynamics should include details of each element.

Transposable element insertion patterns as test of contamination of a Drosophila melanogaster inbred line.

A highly inbred line of Drosophila melanogaster, stable for the insertion pattern of the transposable elements copia and mdg1, was experimentally contaminated by flies from another line. We show that the alien genome income is clearly detectable by the changes induced in the insertion profiles of transposable elements, even twenty generations later.