*Departamento de Genética, Facultad de Ciencias Biológicas, Universitat de València, Burjassot, Spain; and
Departamento de Genética, Universidad de La Laguna, La Laguna, Tenerife, Spain
Abstract
The Ty3/gypsy family of retroelements is closely related to retroviruses, and some of their members have an open reading frame resembling the retroviral gene env. Sequences homologous to the gypsy element from Drosophila melanogaster are widely distributed among Drosophila species. In this work, we report a phylogenetic study based mainly on the analysis of the 5' region of the env gene from several species of the obscura group, and also from sequences already reported of D. melanogaster, Drosophila virilis, and Drosophila hydei. Our results indicate that the gypsy elements from species of the obscura group constitute a monophyletic group which has strongly diverged from the prototypic D. melanogaster gypsy element. Phylogenetic relationships between gypsy sequences from the obscura group are consistent with those of their hosts, indicating vertical transmission. However, D. hydei and D. virilis gypsy sequences are closely related to those of the affinis subgroup, which could be indicative of horizontal transmission.
Introduction
The Ty3/gypsy family of retroelements is widely distributed among eukaryotes. In addition to the yeast Ty3 and Drosophila melanogaster gypsy elements, a large number of families have been described in a wide range of organisms. Most of these elements have been found in Drosophila and plant species, but they are also present in protozoa, fungi, nematodes, vertebrates, and insects other than Drosophila. Retrotransposons constitute a variable fraction of their host genomes; they seem to account for a significant fraction of plant genomes, up to 50% in the case of Zea mays (SanMiguel et al. 1996
). In D. melanogaster, a large number of different retrotransposon families have been found. In spite of this variety, the total amount of retrotransposons seems to be small, only 1.8% of the 2.9-Mb-long Adh region from D. melanogaster corresponded to identified transposable elements (Ashburner et al. 1999
).
The Ty3/gypsy family is closely related to retroviruses. In the phylogenetic trees, based on the analyses of conserved domains from reverse transcriptase, integrase, and RNasa H, Ty3/gypsy elements cluster with retroviruses (Xiong and Eickbush 1988, 1990
; Springer and Britten 1993
; Malik and Eickbush 1999
). Several features from the Ty3/gypsy elements are similar to those of retroviruses, for example, in both groups, reverse transcriptase always precedes integrase. This fact has been used as a systematic tool, and in this way, eukaryotic retrotransposon have been divided into Metaviridae (Ty3/gypsy elements) and Pseudoviridae (Ty1/copia elements) (Boeke et al. 1998a, 1998b
). This resemblance is more remarkable in the Ty3/gypsy element skipper, where pro appears as a separate gene, as it does in retroviruses (Leng et al. 1998
). Inside the Metaviridae family, a group of elements present a third open reading frame (ORF) resembling the retroviral gene env, which would place them even closer to retroviruses. Based on the absence or presence of env-like genes in the retroelements, the Metaviridae family has been divided into two genera, Metavirus and Errantivirus, respectively (Boeke et al. 1998a
).
Kim et al. (1994)
provided the first evidence of horizontal transfer from a strain containing actively transposing gypsy elements to an "empty" strain, suggesting that the gypsy element from D. melanogaster is an infectious retrovirus. It was subsequently reported that the 2.1-kb mRNA produced by differential splicing generates a predicted protein with the characteristics of functional retroviral envelope protein. The gypsy Env protein is glycosylated and processed as in retroviruses and is found associated with viruslike particles (VLPs) from flies carrying the flam permissive mutation, which allows the mobilization of gypsy elements (Pélisson et al. 1994, 1997
; Song et al. 1994, 1997
; Bucheton 1995
; Prud'homme et al. 1995
; Chalvet et al. 1998, 1999
). These facts suggest that viral infectivity of the D. melanogaster gypsy element is dependent on Env. It was recently established that viral particles formed by the MoMLV-based retroviral vector packaged with the gypsy Env protein are able to infect Drosophila cells, which strongly supports the role of Env as the infectious property of gypsy (Teysset et al. 1998
).
The Errantivirus elements are present in fungui, plants, nematodes, and insects, and all of them possess env-like genes, which, in the case of 297, 17.6, TED, Tom, ZAM, Idefix, and Athila, display potentially functional structures such as those shown for gypsy (Song et al. 1994
; Leblanc et al. 1997
; Wright and Voytas 1998
; Desset et al. 1999
). However, ZAM and Idefix from D. melanogaster and TED from the lepidopteron Trichoplusia ni seem to be infective. The presence of env genes is not restricted to Errantivirus, and thus the copia/Ty1 SIRE-1 element encodes an envelope-like protein as well (Laten, Majumdar, and Gaucher 1998
).
Sequences homologous to gypsy from D. melanogaster are distributed throughout Drosophila species. Southern hybridization signals have been detected in most of the analyzed species belonging to Sophophora and Drosophila subgenera (Stacey et al. 1986
; de Frutos, Peterson, and Kidwell 1992
; Loreto et al. 1998
). The widespread presence of gypsy-like sequences suggests the existence of ancestral elements in the genomes of Drosophila species before early radiations. Full gypsy-like sequences in Drosophila subobscura and Drosophila virilis have already been analyzed (Mizrokhi and Mazo 1991
; Alberola and de Frutos 1996
), showing a structure similar to that of the gypsy element from D. melanogaster, which indicates that they are transcriptionally and transpositionally active. The three species posses well-conserved Env proteins, although the D. subobscura and D. virilis ones lack some essential domains needed to produce functional proteins (Alberola and de Frutos 1996
). In this paper, we report a phylogenetic study based mainly on the analysis of the 5' region of the env genes from different species of the obscura group, including previously reported sequences from D. melanogaster, D. virilis, and Drosophila hydei. Our work shows that gypsy elements from the analyzed species of the obscura group appear as a monophyletic group, which is highly diverged from the D. melanogaster prototypic gypsy element. Phylogenetic relationships between gypsy sequences from the obscura group are consistent with those of their hosts, supporting vertical transmission.
Materials and Methods
Drosophila Stocks
Ten species from the obscura group were analyzed. Drosophila obscura, Drosophila ambigua, Drosophila bifasciata, Drosophila pseudoobscura, Drosophila miranda, Drosophila persimilis, Drosophila azteca, and Drosophila affinis were obtained from The National Drosophila Species Resources Centre, Bowling Green State University. Drosophila madeirensis and Drosophila guanche, are laboratory strains from Tenerife (Canary Island).
PCR DNA Amplification
Genomic DNA from each species was prepared as in Junakovic, Caneva, and Ballard (1984)
, with some modifications. Degenerate primers were designed from alignments of gypsy elements from D. melanogaster, D. subobscura, D. virilis, and D. hydei. These primers amplify a fragment of approximately 450 bp corresponding to positions 53545801 of the D. subobscura gypsy element (fig. 1
). Because the amplification was not successful in D. guanche and D. azteca, two new primers were used (positions 52295972). The sequences of these primers and their positions are as follows: DIR5354, 5'-CTG T(CT)C T(CT)C TTA AGG GGA GGG-3' REV5801, 5'-(AG)CC (AC)GC (AC)AC AAG CTT (CT)AA GGC-3' DIR5229, 5'-(CT)(GC)C (AT)AC CCG GCA AAA CCG CG-3' REV5972, 5'-(AT)GG AGT GTC GAC CAA (AG)TC GCC-3'.
|
Cloning and Sequence Analysis
Electroeluted fragments were cloned into pCRscript Amp (+) (Stratagene) at the EcoRV site. Vector restriction and ligation was carried out at the same time on the ligase buffer, at room temperature (2025°C). Four to six clones from each species were sequenced in an automatic ABI-Prism sequencer. Multiple alignments were performed with the CLUSTAL X program (Thompson et al. 1997
). Phylogenetic trees were inferred by the neighbor-joining method (Saitou and Nei 1987
), based on the p-distance MEGA program, version 1.02 (Kumar, Tamura, and Nei 1993
), and by the parsimony method with PAUP program, version 3.1.1.1 (Swofford 1993
), using the heuristic option with random stepwise addition of sequences (10 replicates) and tree bisection-reconnection (TBR) branch swapping. Bootstrapping was performed using both neighbor-joining and parsimony methods (200 replicates).
Results
Phylogenetic Analyses of gypsy Sequences
DNA amplification was obtained from all of the analyzed species with the exception of D. guanche, indicating that they are widely distributed among the obscura group. The presence of deleted gypsy elements in D. guanche, which would explain the absence of amplification in this species, had already been described by de Frutos, Peterson, and Kidwell (1992)
. The genomic DNA of all analyzed species was probed against the amplified PCR fragment from D. subobscura obtained in our study. Hybridization was observed in all the species except D. guanche (data not shown), indicating that in this species the deletion of gypsy elements completely includes the analyzed region.
Figure 2
shows the phylogenetic relationships between gypsy elements from Drosophila species. The tree is based on the comparison of the 450-bp PCR sequences obtained in our study and the gypsy sequences of D. melanogaster (Z31368, the proptotypic element, and AC006215), D. virilis (M38438), and D. hydei (X74538, X74539, and X74543). The amplified fragment includes the 3' end of the pol gene, the 5' region of the env gene, and the intergenic region between them (fig. 1
). We selected the intergenic region because of scarce variability described for the coding regions of Drosophila gypsy elements (Alberola and de Frutos 1996
). In order to determine the potential functionality of Env, we also included the N-terminal env region. The phylogenetic tree was constructed by the neighbor-joining method (Saitou and Nei 1987
) using the yoyo element as the outgroup (Zhou and Haymer 1998
). An identical topology was obtained with the parsimony method. The branching of the tree was supported by high bootstrap values. The most remarkable facts that could be inferred from the analysis of the phylogenetic tree are as follows:
|
Env Region
In addition to the pol 3' end and the intergenic region, the 450-bp analyzed fragment encompasses the 5' region of the env gene. The last region extends over the signal peptide (SP) and a stretch of approximately 100 amino acids of the Env protein surface domain (SU), including the gypsy splicing sites. As in retroviruses, the gypsy Env protein from D. melanogaster is generated from a subgenomic RNA produced by splicing. Remarkably, this splicing event generates a new start codon (Pélisson et al. 1994
) with an AT pair provided by the 5' site and a G from the 3' site. We performed multiple alignments of the putative 3' splice sites from all of the analyzed sequences and the prototypic gypsy sequence of D. melanogaster (Z31368). All of them display a conserved motif, with the exception of the six D. azteca clones and D. hydei (X74543), where some deletions are present. This 3' splice motif includes the above-mentioned G in all sequences except D. hydei (X74539) and D. virilis (M38438). This chimerical structure for the ATG start codon of the Env protein is frequently found in retroviruses. Taking this ATG triplet as a start codon, the predicted polypeptides obtained are highly similar to those found in the functional Env product of D. melanogaster (fig. 3A
). The N-terminal region of the retroviral Env protein invariably contains a short hydrophobic signal peptide (Swanstrom and Wills 1997
); we checked for the presence of this signal in all of the analyzed sequences with the PSORT program and found the N-terminal signal peptide extending through the first 15 amino acids, while in D. melanogaster (Z31368) the length was 13 residues, which is in agreement with the data from Pélisson et al. (1994)
. In D. melanogaster (AC006215) and D. hydei (X74538) sequences, a stop codon is present, originating truncated proteins. In the obscura species, the first 100 amino acids of the Env could produce functional proteins, as in D. melanogaster, although point mutations or single indels downstream of the analyzed region could originate frameshift or truncated proteins. A full gypsy element from D. subosbcura (X72390) had already been analyzed by Alberola and de Frutos (1996)
. Several Env regions from different D. subobscura strains were analyzed later by Alberola, Bori, and de Frutos (1997)
. In these works, an ATG codon located downstream of a putative one generated by splicing was considered as a functional start codon, and all of the analyzed sequences presented frameshift mutations induced by single indels, originating truncated proteins. We reanalyzed these sequences, taking the ATG generated by splicing as the start codon, but in all the cases the results where the same as before, with single indels causing truncated proteins (fig. 3B
).
|
The close phylogenetic relationships between Ty3/gypsy family of retrotransposons and retroviruses have been firmly established (Xiong and Eickbush 1988, 1990
; Springer and Britten 1993
; Wright and Voytas 1998
; Malik and Eickbush 1999
; Lerat and Capy 1999
). However, the phylogenetic relationships between members of this family are not conclusive. This family constitutes a heterogenous group which is broadly extended among eukaryotes, from fungi to vertebrates. In this work, we analyzed the evolutionary relationships among gypsy elements belonging to Drosophila species. In the gypsy group of retroelements, gypsy presents characteristics of endogenous retroviruses (Kim et al. 1994
; Pélisson et al. 1994
; Song et al. 1994
; Chalvet et al. 1998, 1999
; Teysset et al. 1998
). Under some circumstances, they can be rendered infective, but if they persist in the genome of a given species, their dynamic of expansion does not generate deleterious effects in their hosts. Endogenous retroviruses can be subject to constraints in order to acquire a lifestyle that is compatible with their host (Boeke and Stoye 1997
). Transposition and/or infectious properties of gypsy seem to be controlled by the flamenco (flam) host gene (Bucheton 1995
; Prud'homme et al 1995
; Pélisson et al. 1997
; Song et al. 1997
). gypsy is stable in most Drosophila strains, but it transposes at high frequency in the unstable (MG) strains (Kim, Belyaeva, and Aslanian 1990
; Lyubomirskaya et al. 1990, 1993
, Prud'homme et al. 1995
), where the number of copies is higher than in stable strains. On the other hand, gypsy is widely extended among species from Sophophora and Drosophila subgenera (Stacey et al. 1986
; de Frutos, Peterson, and Kidwell 1992
; Loreto et al. 1998
; Biémont and Cizeron 1999
). This widespread distribution indicates the existence of ancient gypsy elements in Drosophila. If the specific characteristics of the gypsy retrotransposon of D. melanogaster were already present in the ancestral elements, transpositionally burst and/or infective events could have occurred in their evolutiary history. In species other than D. melanogaster, gypsy-like retrotransposons seem to be mainly located at the chromocentric region, with a small number of copies on the chromosome arms (Junakovic et al. 1998
; Biémont and Cizeron 1999
; Vieira et al. 1999
). No vestiges of uncontrolled expansions can be inferred from these data; on the contrary, a strict control seems to limit the number of gypsy elements in the genomes of Drosophila species.
The gypsy elements analyzed in this work belong to the obscura species group of Drosophila. Since the pioneering works of Sturtevant (1942)
and Buzzati-Traverso and Scossiroli (1955)
, the phylogenetic relationships among species of this group have been extensively analyzed (Powell [1997]
for a review). Although phylogenetic relationships within species of the obscura group are not completely resolved, a division of the group into Palearctic and Nearctic species has been classically proposed. The Nearctic group presents the pseudoobscura and affinis subgroups, and Palearctic species are divided into subosbcura and obscura subgroups. A fifth subgroup, microlabis, which encompasses African species, has been described (Cariou et al. 1988
). The phylogenetic analysis carried out here extends over species of the Nearctic and Palearctic subgroups, as no microlabis species were available. gypsy elements from species of the obscura group seem to constitute a highly homogeneous monophyletic group in which elements from Nearctic and Palaearctic species are sharply differentiated. The high bootstrap values support the monophyly of the pseudoobscura clade and the divergence between obscura and subosbcura subgroups. In summary, phylogenetic relationships among gypsy elements of the obscura group nearly coincide with those of its hosts, and we can conclude that no evidence of horizontal transmission has been found. We find that the location of D. bifasciata in this phylogenetic tree is quite remarkable. As we discussed previously, D. bifasciata ambiguously clustered with different species of the obscura group in the various phylogenetic analyses carried out before (Powell 1997
). In addition, P and bilbo transposable elements from D. bifasciata are fairly diverged with respect to those of the obscura group (Clark, Maddison, and Kidwell 1994
; Hagemann, Miller, and Pinsker 1994
; Hagemann, Haring, and Pinsker 1996
; García-Planells et al. 1998
; Blesa, Gandía, and Martínez-Sebastián, unpublished data).
In contrast to the evolutionary pattern of gypsy elements among the obscura group species, elements from D. hydei and D. virilis are closely related to obscura-like elements; they turn out to be nearly identical to gypsy elements from Neartic species. It had already been established that gypsy elements of D. subosbcura were much closer to the ones from D. virilis than to those of D. melanogaster (Alberola and de Frutos 1993, 1996
). Horizontal transfer between D. virilis and D. subobscura was proposed to explain this striking similarity. Our present data agree with this hypothesis. Horizontal transfer has been invoked to explain the evolutionary patterns of several families of transposable elements. In addition to evolution of the P element, for which horizontal transfer events are strongly documented (Daniels et al. 1990
; Houck et al. 1991
; Kidwell 1993
; Clark and Kidwell 1997
), apparent cases of horizontal transfer have been reported in mariner from Drosophila (Maruyama and Hartl 1991
; Robertson 1993
), SURL elements from echinoids (Springer et al. 1995
; Gonzalez and Lessios 1999
), magellan from Zea species (Purugganan and Wessler 1994
), gypsy/Ty3-like elements from the tomato (Su and Brown 1997
), and diverse vertebrate species (Miller et al. 1999
), among others. Recently, direct evidence for a recent horizontal transfer of the copia between D. melanogaster and D. willistoni has also been reported (Jordan, Matyunina, and McDonald 1999
). However, horizontal transfer as a mechanism to explain these phylogenetic discrepancies must be proposed with caution. Although transference of gypsy obscura-like elements from affinis species to the virilis group could have occurred, the scenario seems to be more complex. Both D. hydei (X74538) and (X74539) gypsy elements are truncated and rather degraded copies, lack LTRs, and are located on the heterochromatic Y chromosome (Hochstenbach et al. 1994, 1996
). To decisively establish the existence of horizontal transfer will necessitate additional data about the presence of functional env genes in both species, as well as the evolution rates of active and defective elements. In fact, chromosome stochastic losses, existence of ancestral polymorphism, and variable evolution rates have been considered as alternative hypotheses (Capy, Anxolabéhère, and Langin 1994
; Capy et al. 1997
), and we cannot disregard them with our data.
Among the Ty3/gypsy family, gypsy is considered a retrovirus because it has the env gene, which is necessary for infection. All gypsy elements analyzed in this work have an env domain. Most of the obscura-like elements maintain the structural characteristics of an enveloped protein (obviously, these characteristics refer to approximately 100 amino acids of the N-terminal region). It will be interesting to analyze the full env region of the obscura-like gypsy elements in order to ascertain if gypsy retroviral lineages other than the prototypic element of D. melanogaster exist.
Acknowledgements
This work was supported by grant PB960803 DGYCIT.
Footnotes
1 Present address: Unidad de Genética y Diagnóstico Prenatal, Hospital Universitario La Fe, Avda, Campanar, Valencia, Spain.
2 Keywords: Drosophila,
gypsy,
retrotransposons
endogenous retroviruses
evolution of transposable elements
3 Address for correspondence and reprints: Rosa de Frutos, Departamento de Genética, Facultad de Ciencias Biológicas, Dr. Moliner 50, 46100 Burjasot, Valencia, Spain. E-mail: rosa.frutos{at}uv.es
literature cited
Acosta, T., F. Pinto, M. Hernández, A. M. González, V. M. Cabrera, and J. M. Larruga. 1995. Phylogeny of the Drosophila obscura group as inferred from one- and two-dimensional protein electrophoresis. J. Zool. Syst. Evol. Res. 33:101108.[ISI]
Alberola, T. M., L. Bori, and R. de Frutos. 1997. Structural analysis of D. subosbcura gypsy elements (gypsyDs). Genetica 100:3948.
Alberola, T. M., and R. de Frutos. 1993. gypsy homologous sequences in D. subobscura (gypsyDs). J. Mol. Evol. 36:127135.
. 1996. Molecular structure of a gypsy element of D. subobscura (gypsyDs) constituting a degenerate form of insect retroviruses. Nucleic Acids Res. 24:914923.
Ashburner, M., S. Misra, J. Roote et al. (27 co-authors). 1999. An exploration of the sequence of a 2.9-Mb region of the genome of D. melanogaster: the Adh region. Genetics 153:179219.
Barrio, E., and F. J. Ayala. 1997. Evolution of the Drosophila obscura species group inferred from the Gpdh and Sod genes. Mol. Phylogenet. Evol. 7:7993.[ISI][Medline]
Barrio, E., A. Latorre, and A. Moya. 1994. Phylogeny of the Drosophila obscura species group deduced from mitochondrial DNA sequences. J. Mol. Evol. 39:478488.[ISI][Medline]
Barrio, E., A. Latorre, A. Moya, and F. J. Ayala. 1992. Phylogenetic reconstruction of the Drosophila obscura group, on the basis of mitochondrial DNA. Mol. Biol. Evol. 9:621635.[Abstract]
Beckenbach, A. T., Y. W. Wei, and H. Liu. 1993. Relationships in the Drosophila obscura species group, inferred from mitochondrial cytochrome oxidase II sequences. Mol. Biol. Evol. 10:619634.[Abstract]
Beverley, S. M., and A. C. Wilson. 1984. Molecular evolution in Drosophila and the higher Diptera. II. A time scale for fly evolution. J. Mol. Evol. 21:113.[ISI][Medline]
Biémont, C., and G. Cizeron. 1999. Distribution of transposable elements in Drosophila species. Genetica 105:4362.
Boeke, J. D., and J. P. Stoye. 1997. Retrotransposons, endogenous retroviruses, and the evolution of retroelements. Pp. 343435 In J. M. Coffin, S. H. Hughes, and H. E. Varmus, eds. Retroviruses. Cold Spring Harbor Laboratory Press, New York.
Boeke, J. D., T. Eickbush, S. B. Sandmeyer, and D. F. Voytas. 1998a. Metaviridae. In F. A. Murphy, ed. Virus taxonomy: ICTV VIIth report. Springer-Verlag, New York.
. 1998b. Pseudoviridae. In F. A. Murphy, ed. Virus taxonomy: ICTV VII report. Springer-Verlag, New York.
Bucheton, A. 1995. The relationship between the flamenco gene and gypsy in Drosophila: how to tame a retrovirus. Trends Genet. 11:349353.[ISI][Medline]
Buzzati-Traverso, A. A., and R. E. Scossiroli. 1955. The obscura group of the genus Drosophila. Adv. Genet. 7:4792.
Capy, P., D. Anxolabéhère, and T. Langin. 1994. The strange phylogenies of transposable elements: are horizontal transfer the only explanation?. Trends Genet. 10:712.[ISI][Medline]
Capy, P., C. Bazin, D. Higuet, and T. Langin. 1997. Dynamics and evolution of transposable elements. Landes Company, Austin, Tex.
Cariou, M. L., D. Lachaise, L. Tsacas, J. Sourdis, C. B. Krimbas, and M. Ashburner. 1988. New African species in the Drosophila obscura species group: genetic variation, differentiation and evolution. Heredity 61:7384.
Chalvet, F., C. Di Franco, A. Terrinoni, A. Pélisson, N. Junakovic, and A. Bucheton. 1998. Potentially active copies of the gypsy retroelement are confined to the Y chromosome of some strains of D. melanogaster possibly as the result of the female-specific effect of the flamenco gene. J. Mol. Evol. 46:437441.
Chalvet, F., L. Teysset, C. Terzian, N. Prud'homme, P. Santamaria, A. Bucheton, and A. Pélisson. 1999. Proviral amplification of the gypsy endogenous retrovirus of D. melanogaster involves env-independent invasion of the female germline. EMBO J. 18:26592669.
Clark, J. B., and M. G. Kidwell. 1997. A phylogenetic perspective on P transposable element evolution in Drosophila. Proc. Natl. Acad. Sci. USA 94:1142811433.
Clark, J. B., W. P. Maddison, and M. G. Kidwell. 1994. Phylogenetic analysis supports horizontal transfer of P transposable elements. Mol. Biol. Evol. 11:4050.[Abstract]
Daniels, S. B., K. R. Peterson, L. D. Strausbaugh, M. G. Kidwell, and A. C. Chovnick. 1990. Evidence for horizontal transmission of the P transposable element between Drosophila species. Genetics 124:339355.
de Frutos, R., K. R. Peterson, and M. G. Kidwell. 1992. Distribution of D. melanogaster transposable element sequences in species of the obscura group. Chromosoma 101:293300.
Desset, S., C. Conte, P. Dimitri, V. Calco, B. Dastugue, and C. Vaury. 1999. Mobilization of two retroelements, ZAM and Idefix, in a novel unstable line of D. melanogaster. Mol. Biol. Evol. 16:5466.[Abstract]
GarcÍa-Planells, J., N. Paricio, J. B. Clark, R. de Frutos, and M. G. Kidwell. 1998. Molecular evolution of P transposable elements in the genus Drosophila. II. The obscura species group. J. Mol. Evol. 47:282291.
Gleason, J. M., A. Caccone, E. N. Moriyama, A. White, and J. R. Powell. 1997. Mitochondrial DNA phylogenies for the Drosophila obscura group. Evolution 51:433440.
González, A. M., M. Hernández, A. Volz, J. Pestano, J. M. Larruga, D. Sperlich, and V. M. Cabrera. 1990. Mitochondrial DNA evolution in the obscura species subgroup of Drosophila. J. Mol. Evol. 31:122131.[ISI][Medline]
Gonzalez, P., and H. A. Lessios. 1999. Evolution of sea urchin retroviral-like (SURL) elements: evidence from 40 echinoid species. Mol. Biol. Evol. 16:938952.[Abstract]
Hagemann, S., E. Haring, and W. Pinsker. 1996. Repeated horizontal transfer of P transposons between S. pallida and D. bifasciata. Genetica 98:4351.
Hagemann, S., W. J. Miller, and W. Pinsker. 1994. Two distinct P element subfamilies in the genome of D. bifasciata. Mol. Gen. Genet. 244:168175.
Hochstenbach, R., H. Harhangi, K. Schouren, P. Bindels, R. Suijkerbuijk, and W. Hennig. 1996. Transcription of gypsy elements in a Y-chromosome male fertility gene of D. hydei. Genetics 142:437446.
Hochstenbach, R., H. Harhangi, K. Schouren, and W. Hennig. 1994. Degenerating gypsy retrotransposon in a male fertility gene on the Y chromosome of D. hydei. J. Mol. Evol. 39:452465.
Houck, M. A., J. B. Clark, K. R. Peterson, and M. G. Kidwell. 1991. Possible horizontal transfer of Drosophila genes by the mite P. regalis. Science 253:11251129.
Jordan, I. K., L. V. Matyunina, and J. F. McDonald. 1999. Evidence for the recent horizontal transfer of long terminal repeat retrotransposon. Proc. Natl. Acad. Sci. USA 26:1262112625.
Junakovic, N., R. Caneva, and P. Ballario. 1984. Genomic distribution of copia-like elements in laboratory stocks of D. melanogaster. Chromosoma 90:378382.
Junakovic, N., A. Terrinoni, C. Di Franco, C. Vieira, and C. Loevenbruck. 1998. Accumulation of transposable elements in the heterochromatin and on the Y chromosome of D. simulans and D. melanogaster. J. Mol. Evol. 46:661668.
Kidwell, M. G. 1993. Lateral transfer in natural populations of eukaryotes. Annu. Rev. Genet. 27:235256.[ISI][Medline]
Kim, A. I., E. S. Belyaeva, and M. M. Aslanian. 1990. Autonomous transposition of gypsy mobile elements and genetic instability in D. melanogaster. Mol. Gen. Genet. 224:303308.
Kim, A., C. Terzian, P. Santamaria, A. Pélisson, N. Prud'homme, and A. Bucheton. 1994. Retroviruses in invertebrates: the gypsy retrotransposon is apparently an infectious retrovirus of D. melanogaster. Proc. Natl. Acad. Sci. USA 91:12851289.
Kumar, S., K. Tamura, and M. Nei. 1993. MEGA: molecular evolutionary genetic analysis. Version 1.02. The Pennsylvania State University, University Park.
Lambertsson, A., S. Andersson, and T. Johansson. 1989. Cloning and characterization of variable-sized gypsy mobile elements in D. melanogaster. Plasmid 22:2231.
Laten, H. M., A. Majumdar, and E. A. Gaucher. 1998. SIRE-1, a copia/Ty1-like retroelement from soybean, encodes a retroviral envelope-like protein. Proc. Natl. Acad. Sci. USA 95:68976902.
Leblanc, P., S. Desset, B. Dastugue, and C. Vaury. 1997. Invertebrate retroviruses: ZAM a new candidate in D. melanogaster. EMBO J. 16:75217531.
Leng, P., D. H. Klatte, G. Schumann, J. D. Boeke, and T. L. Steck. 1998. Skipper, an LTR retrotransposon of Dictyostelium. Nucleic Acids Res. 26:20082015.
Lerat, E., and P. Capy. 1999. Retrotransposons and retroviruses: analysis of the envelope gene. Mol. Biol. Evol. 16:11981207.[Abstract]
Loreto, E. L., L. Basso Da Silva, A. Zaha, and V. L. Da S. Valente. 1998. Distribution of transposable elements in neotropical species of Drosophila. Genetica 101:153165.
Loukas, M., C. B. Krimbas, and Y. Vergini. 1984. Evolution of the obscura group Drosophila species. II. Phylogeny of ten species based on electrophoretic data. Heredity 53:483493.
Lyubomirskaya, N. V., I. R. Arkhipova, Y. V. Ilyin, and A. I. Kim. 1990. Molecular analysis of the gypsy (mdg4) retrotransposon in two D. melanogaster strains differing by genetic instability. Mol. Gen. Genet. 223:305309.
Lyubomirskaya, N. V., S. N. Avedisov, S. A. Surkov, and V. Ilyin. 1993. Two Drosophila retrotransposon gypsy subfamilies differ in ability to produce new DNA copies via reverse transcription in Drosophila cultured cells. Nucleic Acids Res. 21:32653268.[Abstract]
Malik, H. S., and T. H. Eickbush. 1999. Modular evolution of the integrase domain in the Ty3/gypsy class of LTR retrotransposons. J. Virol. 73:51865190.
Maruyama, K., and D. L. Hartl. 1991. Evidence for interspecific transfer of the transposable element mariner between Drosophila and Zaprionus. J. Mol. Evol. 33:514524.[ISI][Medline]
Miller, K., C. Lynch, J. Martin, E. Herniou, and M. Tristem. 1999. Identification of multiple gypsy LTR-retrotransposon lineages in vertebrate genomes. J. Mol. Evol. 49:358366.[ISI][Medline]
Mizrokhi, L. V., and A. M. Mazo. 1991. Cloning and analysis of the mobile element gypsy from D. virilis. Nucleic Acids Res. 19:913916.
Pélisson, A., S. U. Song, N. Prud'homme, P. A. Smith, A. Bucheton, and V. G. Corces. 1994. gypsy transposition correlates with the production of a retroviral envelope-like protein under the tissue-specific control of the Drosophila flamenco gene. EMBO J. 13:44014411.[Abstract]
Pélisson, A., L. Teysset, F. Chalvet, A. Kim, N. Prud'homme, C. Terzian, and A. Bucheton. 1997. About the origin of retroviruses and the co-evolution of the gypsy retrovirus with the Drosophila flamenco host gene. Genetica 100:2937.
Powell, J. R. 1997. Progress and prospects in evolutionary biology. The Drosophila model. Oxford University Press. New York.
Powell, J. R., and R. DeSalle. 1995. Drosophila molecular phylogenies and their uses. Evol. Biol. 28:87138.[ISI]
Prud'homme, N., M. Gans, M. Masson, C. Terzian, and A. Bucheton. 1995. Flamenco, a gene controlling the gypsy retrovirus of D. melanogaster. Genetics 139:697711.
Purugganan, M. D., and S. R. Wessler. 1994. Molecular evolution of magellan, a maize Ty3/gypsy-like retrotransposon. Proc. Natl. Acad. Sci. USA 91:1167411678.
Robertson, H. M. 1993. The mariner transposable element is widespread in insects. Nature 362:241245.
Saitou, N., and M. Nei. 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4:406425.[Abstract]
SanMiguel, P., A. Tikhonov, Y. K. Jin et al. (11 co-authors). 1996. Nested retrotransposons in the intergenic regions of the maize genome. Science 274:765768.
Song, S. U., T. Gerasimova, M. Kurkulos, J. D. Boeke, and V. G. Corces. 1994. An Env-like protein encoded by a Drosophila retroelement: evidence that gypsy is an infectious retrovirus. Genes Dev. 8:20462057.[Abstract]
Song, S. U., M. Kurkulos, J. D. Boeke, and V. G. Corces. 1997. Infection of germ line by retroviral particles produced in the follicle cells: a possible mechanism for the mobilization of the gypsy retroelement of Drosophila. Development 124:27892798.
Springer, M. S., and R. J. Britten. 1993. Phylogenetic relationships of reverse transcriptase and RNase H sequences and aspects of genome structure in the gypsy group of retrotransposons. Mol. Biol. Evol. 10:13701379.[Abstract]
Springer, M. S., N. A. Tusneem, E. S. Davidson, and R. J. Britten. 1995. Phylogeny, rates of evolution, and patterns of codon usage among sea urchin retroviral-like elements, with implications for the recognition of horizontal transfer. Mol. Biol. Evol. 12:219230.[Abstract]
Stacey, S. N., R. A. Lansman, H. W. Brock, and T. A. Grigliatti. 1986. Distribution and conservation of mobile elements in the genus Drosophila. Mol. Biol. Evol. 3:522534.[Abstract]
Sturtevant, A. H. 1942. The classification of the genus Drosophila with the description of nine new species. Univ. Tex. Publ. 4213:551.
Su, P. Y., and T. A. Brown. 1997. Ty3/gypsy like retrotransposon sequences in tomato. Plasmid 38:148157.
Swanstrom, R., and J. W. Wills. 1997. Synthesis, assembly, and processing of viral proteins. Pp. 263334 in J. M. Coffin, S. H. Hughes, and H. E. Varmus, eds. Retroviruses. Cold Spring Harbor Laboratory Press, New York.
Swofford, D. L. 1993. Phylogenetic analysis using parsimony. Version 3.1.1. Smithsonian Institution, Washington, D.C.
Teysset, L., J. C. Burns, H. Shike, B. L. Sullivan, A. Bucheton, and C. Terzian. 1998. A Moloney murine leukemia virus-based retroviral vector pseudotyped by the insect retroviral gypsy envelope can infect Drosophila cells. J. Virol. 72:853856.
Thompson, J. D, F. P. Gibson, F. Jeanmongin, and D. G. Higgins. 1997. The CLUSTALX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tool. Nucleic Acids Res. 24:48764882.
Throckmorton, L. H. 1975. The phylogeny, ecology and geography of Drosophila. Pp. 421469 in R. C. King, ed. Handbook of genetics. Plenum Press, New York.
Vieira, C., D. Lepetit, S. Dumont, and C. Biémont. 1999. Wake up of transposable elements following D. simulans worldwide colonization. Mol. Biol. Evol. 16:12511255.
Wright, D. A., and D. F. Voytas. 1998. Potential retroviruses in plants: Tat1 is related to a group of A. thaliana Ty3/gypsy retrotransposons that encode envelope-like proteins. Genetics 149:703715.
Xiong, Y., and T. H. Eickbush. 1988. Similarity of reverse transcriptase-like sequences of viruses, transposable elements, and mitochondrial introns. Mol. Biol. Evol. 5:675690.[Abstract]
. 1990. Origin and evolution of retroelements based upon their reverse transcriptase sequences. EMBO J. 9:33533362.[Abstract]
Zhou, Q., and D. S. Haymer. 1998. Molecular structure of yoyo, a gypsy-like retrotransposon from the Mediterranean fruit fly, C. capitata. Genetica 101:167178.