Penelope , a new family of transposable elements and its possible role in hybrid dysgenesis in Drosophila virilis

Abstract

A hybrid dysgenesis syndrome occurs in Drosophila virilis when males from an established laboratory strain are crossed to females obtained from the wild, causing the simultaneous mobilization of several different transposable elements. The insertion sequence responsible for the mutant phenotype of a dysgenic yellow allele has been characterized and named Penelope. In situ hybridization and Southern analyses reveal the presence of more than 30 copies of this element in the P-like parental strain, whereas Penelope is absent in all M-like strains tested. Penelope contains one 2.5-kb-long ORF that could encode products with homology to integrase and reverse transcriptase. Northern analysis and whole-mount in situ hybridization show strong induction of a 2.6-kb RNA in the ovaries of dysgenic females that is expressed at very low levels in the parental strains or in the progeny from the reciprocal cross. Injection of Penelope-containing plasmids into preblastoderm embryos of an M-like strain results in mutant progeny caused by insertion of Ulysses and perhaps other transposons, suggesting that Penelope expression might be responsible for the observed dysgenesis syndrome and the simultaneous mobilization of other transposable elements.Hybrid dysgenesis in Drosophila melanogaster results in high sterility and mutation rates, male recombination, segregation distortion, and chromosome nondisjunction (1-3). The transposase-encoding P element is responsible for the P-M hybrid dysgenesis syndrome in this species (4, 5). A second hybrid dysgenesis system, designated I-R, also leads to similar abnormalities. Although the dysgenic traits that arise in P-M and I-R crosses are similar, the nature of the transposable elements involved is very different. The I transposable element differs from the P element in that it encodes a protein with sequence similarities to reverse transcriptase (RT) (6). Some dysgenic traits have also been observed in systems involving the hobo family of transposable elements, which can promote high rates of chromosomal rearrangements and other dysgenic traits (7).A similar dysgenic syndrome takes place in Drosophila virilis in unidirectional crosses between males of a strain named 160 and females of strain 9 (8). These two strains are respectively designated P-like and M-like based on the parallels in their behavior with P and M strains in D. melanogaster. The above cross results in characteristic traits in the progeny such as a high level of gonadal sterility in F 1 males and females, chromosomal nondisjunction and rearrangements, male recombination, and the occurrence of multiple visible mutations, although it was shown that neither P nor I elements are present in this species (8). A white mutation (w d9 ) isolated from the progeny of a dysgenic cross has been characterized, and the insertion sequence responsible for the mutant phenotype has been isolated (9, 10). This sequence is a 10.6-kb long terminal repeat-containing retrotransposon named Ulysses. The transcription pattern of Ulysses is the...

Mobile elements and chromosomal evolution in the virilis group of Drosophila

“…These families include Ulysses, Helena, Paris, Telemac, and Penelope (13-15). The Penelope family of elements has been identified as playing a critical role in D. virilis hybrid dysgenesis (15,16). This family is also exceptional in being absent from a number of D. virilis strains but is present and active in others.…”

Reverse transcriptase and endonuclease activities encoded by Penelope -like retroelements

“…The cleavage specificity of the Penelope EN observed in plasmids containing the 34-bp tail provides a plausible explanation for the previously noticed tendency of Penelope to form partial-tandem structures, resulting in an LTR-like arrangement (4,12). Such specificity may serve as a mechanism that ensures preservation of the complete element by enabling the 5Ј LTR formed in this way to provide the site of transcription initiation for the ORF located downstream, in a manner analogous to the tandemly arranged HeT-A elements of Drosophila (40).…”

“…The demonstration of RT and EN activities associated with the Penelope polyprotein is of evolutionary significance, taking into account the recently documented wide distribution of PLEs (refs. 5-8 and this study) and the key role of Penelope in D. virilis hybrid dysgenesis (4). Along with the discovery of a retroelement from Caenorhabditis elegans that encodes a cysteine protease instead of a typical aspartate protease (41), these observations suggest that nonorthologous domain displacement (42) might have occurred during evolution of retroelements.…”

“…This phenomenon is observed when females from strains lacking Penelope are crossed with males carrying multiple active Penelope copies. Elements from several different families, both transposons and retrotransposons, transpose in the progeny of such a cross, with Penelope apparently playing a key role in mobilizing the others (4). PLEs have been reported in genomes of crustaceans, echinoderms, fish, amphibians, f latworms, roundworms, and rotifers (5)(6)(7)(8).…”

“…The Penelope-like elements (PLEs) are highly unusual elements discovered in Drosophila and other organisms. Penelope was isolated from Drosophila virilis after the discovery of hybrid dysgenesis in this species (3,4). This phenomenon is observed when females from strains lacking Penelope are crossed with males carrying multiple active Penelope copies.…”