The evolutionary dynamics of the Helena retrotransposon revealed by sequenced Drosophila genomes

Abstract

Background: Several studies have shown that genomes contain a mixture of transposable elements, some of which are still active and others ancient relics that have degenerated. This is true for the non-LTR retrotransposon Helena, of which only degenerate sequences have been shown to be present in some species (Drosophila melanogaster), whereas putatively active sequences are present in others (D. simulans). Combining experimental and population analyses with the sequence analysis of the 12 Drosophila genomes, we have investigated the evolution of Helena, and propose a possible scenario for the evolution of this element.

Results: We show that six species of Drosophila have the Helena transposable element at different stages of its evolution. The copy number is highly variable among these species, but most of them are truncated at the 5' ends and also harbor several internal deletions and insertions suggesting that they are inactive in all species, except in D. mojavensis in which quantitative RT-PCR experiments have identified a putative active copy.

Conclusion: Our data suggest that Helena was present in the common ancestor of the Drosophila genus, which has been vertically transmitted to the derived lineages, but that it has been lost in some of them. The wide variation in copy number and sequence degeneration in the different species suggest that the evolutionary dynamics of Helena depends on the genomic environment of the host species.

Figure 1

Phylogenetic tree of the Drosophila genus. Phylogenetic relationships between the Drosophila species of which the genomes have been sequenced (modified from http://rana.lbl.gov/drosophila). Presence (+) and absence (-) of Helena.

Figure 2

Helena structure in Drosophila species. Structure of the reference copies of Helena-like elements. DNA sequences: AAA, poly-A tail. Protein sequences: gag, nucleocapsid-like domain; RTase, reverse transcriptase; *: position of start codons; #: position of stop codons. D. simulans and D. melanogaster structures are from Rebollo et al. [18]. The sequences are in Additional file 1.

Figure 3

Helena copies in different genomes. Distribution of the lengths (intervals: 350 bp) and percentage identity of the Helena copies in D. simulans, D. melanogaster, D. sechellia, D. yakuba, D. erecta, D. ananassae, D. mojavensis and D. virilis.

Figure 4

Phylogenetic tree of RT proteins. The reconstruction was performed by the maximum likelihood method with the LG model, using the Helena reference copies obtained in this study and other LINE elements based on their partial reverse transcriptase domains. The sequences used were obtained from GenBank, and are identified by the TE name and the host names (* Sequences obtained from GenBank; ¹Sequences obtained in this study; ²Helena sequences obtained by Rebollo et al. [18)]. The numbers indicate the branch support calculated by bootstrap analysis consisting of 100 replicates. Only bootstrap values greater than 50% are indicated.

Figure 5

Southern blot analysis of Helena in D. simulans and D. mojavensis populations. Lanes 1 to 8 are D. simulans populations (1: North America (Tucson stock center: 14021-0251.195), 2: Junco do Serido (PB, Brazil), 3: Itaúnas (ES, Brazil), 4: Lençóis (BA, Brazil), 5: Onda Verde (SP, Brazil), 6: Ratones (SC, Brazil), 7: Seychelles (Seychelles), 8: New Caledonia (Tucson stock center: 14021-0251.216). Lanes 9–11 are D. mojavensis populations (9: Catalina Island (California, U.S.A, Tucson stock center 15081-1352.02), 10: Grand Canyon (Arizona, U.S.A), 11: Sonora (Mexico, Tucson stock center: 15081-1352.24)).

Figure 6

Analysis of Helena activity in natural populations. Helena transcripts (ratio Helena/rp49) of ovaries and carcasses of D. simulans and D. mojavensis (see Methods for additional information). D. simulans strains from the Drosophila species stock center: 1 (14021-0251.195 – North America, U.S.A), 2 (14021-0251.194 – Winters, California, U.S.A), 3 (14021-0251.198 – Noumea, New Caledonia), and from natural populations 4 (Amieu, France), 5 (Valence, France). D. mojavensis strains from natural populations: 1 (Grand Canyon, Arizona, U.S.A), and from the Drosophila species stock center 2 (15081-1352.02 – Catalina Island, California, U.S.A), 3 (15081-1352.09 – Santa Rosa Mountains, Arizona, U.S.A), 4 (15081-1352.24 – Sonora, Mexico), 5 (15081-1352.22 – Catalina Island, California, U.S.A). Black = ovaries. Gray = Carcasses. Standard deviation is indicated with bars.