Instituto Cavanilles de Biodiversidad y Biología Evolutiva and Departamento de Genética, Universidad de Valencia, Spain
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Abstract |
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Introduction |
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Structural and functional data converged when it was shown that the Gypsy element of D. melanogaster was able in some circumstances to function as a retrovirus (Song et al. 1994
; Kim et al. 1994
). This result established the convenience of classifying LTR retrotransposons as viruses. In the most recent virus taxonomy, LTR-containing retroelements are classified into two main families, Pseudoviridae (corresponding to the Ty1/Copia subgroup) and Metaviridae (Ty3/Gypsy elements). The Metaviridae are further split according to the presence of the env gene (genus Errantivirus) or its absence (genus Metavirus) (reviewed in Pringle 1998, 1999
; Hull 1999
).
Various studies have analyzed in depth the evolution of Ty3/Gypsy elements using either the slowly evolving RT domain sequences or several pol domains at the same time, progressively including more sequences as they became available (Xiong and Eickbush 1990
; Springer and Britten 1993
; Eickbush 1994
; Wright and Voytas 1998
; Malik and Eickbush 1999
; Pantazidis, Labrador, and Fontdevila 1999
). In a recent study, Malik and Eickbush (1999)
used phylogenetic analyses of the RT, RH, and IN domains to operatively define eight clades of Ty3/Gypsy elements. It is unclear whether all eight of those clades correspond to ancient classes of Ty3/Gypsy retrotransposons or some of them are relatively recent, because the inner branches that relate the clades in the phylogenetic tree essentially form a polytomy.
With respect to the most common approach, using just the slowly evolving RT domain sequences, the analysis of multiple domains has the obvious advantage of increasing the amount of information. However, it also has the drawback that many elements for which only partial (often RT domain) sequences are available cannot be included. This has two effects: (1) complete clades of Ty3/Gypsy retrotransposons may be missed, and (2) the phylogenetic range of a particular clade may be underestimated. Moreover, if elements of recombinant origin were present, they would be difficult to detect due to lack of resolution of the trees obtained independently with the sequences of each domain (especially those obtained from RH and IN sequences, which evolve rapidly). Thus, the comparison of trees obtained combining several domains but having a limited number of elements versus those obtained using only RT domain sequences but having many more elements is advisable. In this study, we analyzed all of the Ty3/Gypsy RT domain sequences currently available, with an emphasis on detecting and comparing the many new sequences generated by the genome sequencing projects. Particularly interesting are the results obtained for plant elements, results that allow us to describe the evolution of Ty3/Gypsy retrotransposons in plant species for the last 200 Myr. General conclusions about the success of this group of elements in different organisms were also obtained. Finally, we argue for additional taxonomic criteria to classify the Metaviridae.
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Materials and Methods |
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Methods to obtain the multiple alignments, phylogenetic trees (based on the neighbor-joining algorithm; Saitou and Nei 1987
), and bootstrapping values for the branches were those described previously (Marín et al. 1998
), except that in this work the program ClustalX (Thompson et al. 1997
) was used instead of CLUSTAL W (Thompson, Higgins, and Gibson 1994
). The program GeneDoc (Nicholas and Nicholas 1997
) was used to edit the sequences for manual refinement of the multiple alignments. The multiple alignments on which the phylogenetic trees shown in figures 1 and 3 are based are available at the EMBL European Bioinformatics Institute web pages (ftp://ftp.ebi.ac.uk/pub/databases/embl/align), with accession numbers DS41404 and DS41405, respectively. In order to establish the structure of the Arabidopsis thaliana elements that we describe for the first time in this study, we used (1) the local alignment program LALIGN (designed by W. R. Pearson, based on Huang and Miller [1991
]; online at the Genestream Network Server, http://xylian.igh.cnrs.fr/) to determine the lengths and sizes of the LTRs; (2) TBLASTN to establish the relationships among the different copies of a same element; (3) the ORF Finder tool, also implemented at NCBI, to determine whether the ORFs of the elements were truncated or intact; and (4) BLASTP and TBLASTN to determine, by comparison with previously described elements, the positions of the different protein domains presented in figure 2
. Phylogenetic trees were obtained using TreeView (Page 1996
).
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Results |
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We now summarize the results of the analyses for the nine A. thaliana lineages. In particular, for the new lineages defined in figure 1 , the copies structurally most similar to active elements are described.
Tit-for-Tat1 and Tit-for-Tat2 (Tft1 and Tft2) are represented by four and six sequences, respectively. The name is inspired by the fact that they are close relatives of Tat. They form two well-supported monophyletic groups according to their RT domain sequences (fig. 1 ), but it is unclear at present whether active Tft1 or Tft2 elements exist in A. thaliana. None of the Tft1 copies available seem to be functional. The structurally best conserved element is the one found in the sequence with accession number AC006194.2. The element contained in this sequence is 8,449 bp long (nucleotides 2065512207) and has 96% identical, 1,327-bp-long LTRs. These LTRs are totally unrelated to those in Tat. The putative ORFs of this copy contain several frameshifts and many stop codons (fig. 2 ).
None of the six Tft2 sequences are intact enough to precisely describe the structure of the element, particularly their LTRs. It is thus possible that Tft2 is actually a particular Tft1-like lineage, inactivated long ago. The Tft2 elements would be at least 6,600 bp long. We used the RT of the element present in sequence AC006067 as the canonical copy for the analyses presented in figure 3 (see below).
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Gimli and Gloin (named after Tolkien 1954
) are the smallest Ty3/Gypsy elements found so far in Arabidopsis. They are closely related and represented by four and three sequences, respectively (fig. 1
). The Gimli element found in sequence AL049655.2 may be active. It is 5,221 bp long (nucleotides 7711082330 in AL049655.2) with 341-bp-long LTRs that are 98% identical. These LTRs are unrelated to those of other elements, including Gloin. Two contiguous ORFs of 868 and 593 amino acids are apparent in this sequence. However, both ORFs are in the same frame, and thus it is possible that they both actually form a single continuous ORF about 1,500 amino acids long. However, such a single ORF would contain a stop codon between the RT and RH domains (fig. 2
). At the end of the integrase, a chromodomain is observed (detailed in fig. 4
). Isolated Gimli LTRs have not been found.
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The name Tma defines a clearly monophyletic group of similar sequences, including the canonical copies Tma1-1 and Tma3-1 (Wright and Voytas 1998
). Wright and Voytas (1998)
showed that Tma elements are about 7.8 kb long and have LTRs that are 1.15 kb long. We found that these elements also have a chromodomain-containing integrase (fig. 4
).
Legolas (name also from Tolkien 1954
) is a relative of Tma (fig. 1
). The copy found in AC006570.4 has the typical structure of an active Ty3/Gypsy retrotransposon (fig. 2
). The element is 7,740 bp long (nucleotides 4599438255 in AC006570.4), with 1,347-bp-long LTRs that are 99% identical. It has two ORFs of 498 and 1,215 amino acids, respectively. At the end of the first ORF, homology to the gag proteins is found, including three C2HC zinc fingers. The second ORF contains the pol domains. Its integrase also has a chromodomain (fig. 4
). The structure of Legolas is very similar to that of the Tma elements described above.
Little Athila (new element) is represented by four RT domain sequences, as shown in figure 1 . The name refers to the fact that this element is closely related to Athila but shorter, lacking an ORF3. It is unclear whether active Little Athila elements exist. For the canonical copy, we took the one present in AF147260.1. This copy is 8,658 bp long (nucleotides 4608954746 in AF147260.1) with asymmetrical LTRs (1,133 and 1,148 bp long, respectively; 92% identical). This is an inactive copy. A frameshift in the IN domain and stop codons in the RT and RH domains were observed (fig. 2 ). Moreover, its RH domain is C-terminally truncated. Isolated LTRs almost identical to the ones present in this copy are found in the databases (not shown). They are totally unrelated to Athila LTRs.
We have reserved the name Athila (Pelissier et al. 1995
; Wright and Voytas 1998
) for the very large group of elements, many of them with env-containing ORF3, that are included in an apparently monophyletic branch (fig. 1
). However, whether one or several closely related Athila-like elements are present deserves further study, because these sequences are substantially heterogeneous. Together with the previously characterized copy Athila1-1 (Wright and Voytas 1998
), we included in our analyses (see fig. 3
) a copy that is central in the tree, located in sequence AC007209.4 (nucleotides 857122061), which we called Athila4.
Plant Ty3/GypsyElements Can Be Grouped into Two Classes, but at Least Four Lineages of These Elements Predate the Monocot/Dicot Split
Figure 3
shows the phylogenetic tree obtained using all of the sequences detected in our exhaustive database screenings. Only the canonical representatives of the A. thaliana lineages described in the previous section were included. We will now summarize the main results deduced from this tree for plant elements. In the next section, we describe some new findings for other species.
The tree presented in figure 3
is very similar to those found, with a more limited set of elements, by Wright and Voytas (1998)
and Malik and Eickbush (1999)
. As first described by Wright and Voytas (1998)
, all plant elements fall into two branches, forming what we call classes A and B. Class B corresponds to elements with chromodomain-containing integrases (Malik and Eickbush 1999
; see also fig. 4
). Class B elements are part of the only group in the whole tree that has a phylogenetic range spanning fungi, animals, and plants and at the same time is well-supported by bootstrap data. The precise relationship of class A plant elements with animal or fungal elements is unclear. The group formed by the animal Mag and SURL elements is the closest one to class A elements, but the bootstrap values supporting this association are low (277 out of 1,000 replicates).
A major result for plant elements is that there are several branches of the tree shown in figure 3 that comprise elements in both monocot and dicot species. As can be seen in figure 3 , class A is divided into two groups. One of the groups (ancestral lineage I) is itself divided into two subgroups, containing, respectively, elements of monocot species (Grande from Zea diploperennis, Cinful from Zea mays, and Retrosor1 from Sorghum bicolor) and of the dicot A. thaliana (Tat, Tft1, and Tft2). Elements of a second group, formed by the retrotransposons Diaspora (Glycine max), Cyclops1 (Pisum sativum), and Cyclops-Vicia (Vicia faba) and the A. thaliana elements Athila and Little Athila have been found so far only in dicot species. Assuming no horizontal transmission, these results suggest that at least one class A lineage was already present before the monocot-dicot split.
Class B elements have a more complex history. Data suggest that at least three different lineages were present before the monocot-dicot split (fig. 3
). One of these lineages (ancestral lineage II) comprises 11 elements, some from monocot species (Lilium henryi element Del1; S. bicolor elements Retrosor2 and Retrosor3; Oryza sativa elements Retrosat2 and RIRE3 and Retrosor-2-like sequence found in AP000364.1; Ananas comosus Dea1) and some from dicots (A. thaliana elements Legolas and Tma; P. sativum element Peabody). In addition to such large group, there are two other class B ancestral lineages (III and IV in fig. 3
), with two and four elements, respectively, that seem to correspond to other types of Ty3/Gypsy elements existent before the monocot-dicot split. One branch contains the new element Galadriel from the dicot Lycopersicon esculentum (also named after Tolkien [1954
] by J. Jones [John Innes Centre, Norwich, England] and the authors) and Monkey from the monocot Musa acuminata. The second comprises element Reina (from the monocot Z. mays), the A. thaliana (dicot) elements Gimli and Gloin and, most interestingly, the only element so far found in conifers, the Ifg7 element from Pinus radiata. The close relationship of Ifg7 and the A. thaliana retrotransposons Gimli and Gloin suggests that elements of this branch existed before the Coniferophyta/Magnoliophyta separation.
Therefore, assuming no horizontal transmission, our data support the hypothesis that at least four lineages of Ty3/Gypsy elements coexisted in the last common ancestor of monocots and dicots, roughly 200 MYA. In fact, considering the topology we have obtained and that information is still fragmentary, especially for monocot species, the number of lineages in this ancestor may well have been much larger than four.
Other Interesting New Elements and Comparisons with Previous Evolutionary Studies
Apart from the A. thaliana elements described above, several of the sequences presented in figure 3
are analyzed from a phylogenetic point of view for the first time in this study. The most interesting additions are concentrated in a particular branch of the tree that corresponds to what Malik and Eickbush (1999)
called the Osvaldo clade. So far, only three insect elements (Drosophila buzzatii Osvaldo, Drosophila virilis Ulysses, and Tribolium castaneum Woot) were included in this clade. However, the D. melanogaster genome project has unearthed sequences that are closely related to both Osvaldo and Ulysses, two elements discovered in species of the Drosophila genus but never before detected in D. melanogaster. Moreover, our data suggest that there may be representatives of the Osvaldo clade in many other species, perhaps even including chordates (the fish Gadus morhua contains an RT sequence closely related to that of Osvaldo; see fig. 3
). The rest of the D. melanogaster sequences are close relatives of previously known elements that belong to the Gypsy and Mdg3 clades defined by Malik and Eickbush (1999)
(fig. 3
).
An important conclusion that derives from our data is that the number of different Ty3/Gypsy lineages is much larger for some species than for others. In D. melanogaster this number is very high, around 20. We reported in this study that A. thaliana contains at least nine Ty3/Gypsy lineages. We also characterized four in C. elegans (see fig. 3
), and, in a study published after our analyses were finished, Bowen and McDonald (1999)
detected sequences that may correspond to two other lineages, closely related to the Mag-like and Z46828 sequences, respectively. Finally, S. cerevisiae has only one lineage, namely, Ty3.
Two differences of our tree from those of previous studies concern the positions of the elements Ty3 and, particularly, Skipper. Ty3 is included by Malik and Eickbush (1999)
together with the chromodomain-containing elements to define the Ty3 clade. Our results, as well as those by Wright and Voytas (1998), situate Ty3 outside of the group formed by the chromodomain-containing elements. More pronounced is the difference that concerns the Dictyostelium discoideum element Skipper (Leng et al. 1998
). This is an element with chromodomain-containing integrase and, in Malik and Eickbush's (1999)
study using sequences of the RT, RH, and IN domains together, appears closely related to the other chromodomain-containing elements. However, RT domain sequences alone situate Skipper outside of the tree formed by the other Ty3/Gypsy elements.
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Discussion |
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The A. thaliana results parallel those found for the D. melanogaster genome, in which also many different, perhaps 20, types of Ty3/Gypsy retrotransposons coexist (fig. 3
). However, in other genomes, there are limited numbers of successful Ty3/Gypsy lineages. In particular, in the completely sequenced genome of S. cerevisiae, only one lineage (Ty3) has been found. Ty3/Gypsy elements seem to also be rare in vertebrates. Figure 3
shows two independent lineages in fishes (Sushi from the pufferfish Fugu rubripes, and the Osvaldo-like sequence in G. morhua). Sushi-related sequences are also present in amphibians and reptiles, and a third lineage might exist also in fishes (Miller et al. 1999
). However, in spite of abundant available data, none has been found so far in mammalian genomes. Considering the relatively small sizes of the genomes of A. thaliana and D. melanogaster with respect to vertebrates, we can rule out the explanation that the success of Ty3/Gypsy elements is correlated with large genome sizes. It is more likely that genome-specific factors determine the success or failure of these retrotransposons (see Labrador and Corces 1997
).
The presence of a third ORF putatively encoding an ENV protein in distantly related elements (so far, Gypsy and some of its close relatives, Cer1, Athila, and Osvaldo) that belong to four different clades of the Ty3/Gypsy group (Malik and Eickbush 1999
) can be explained by losses of the env gene in many different lineages or by recent independent acquisitions of an ORF3 by certain elements. In favor of this latter hypothesis, an important result is the finding of an ORF3 in a member of the Ty1/Copia group (Laten, Majumdar, and Gaucher 1998
) that moreover encodes a protein lacking certain common motifs present in the ENV protein or retroviruses or Gypsy and its relatives (Lerat and Capy 1999
). Bowen and McDonald (1999)
also detected a third ORF in a C. elegans LTR retrotransposon (Cer7) that belongs to a group of elements phylogenetically situated between the Ty1/Copia and Ty3/Gypsy groups. If multiple independent acquisitions of an ORF3 have occurred, the classification of the Metaviridae, based on the Errantivirus (with env)Metavirus (without env) dichotomy, should be reconsidered. On the other hand, chromodomain-containing elements form the only group of Ty3/Gypsy elements that is well supported by two independent lines of evidence (RT-based phylogeny: see fig. 3
; presence of chromodomain in their integrases: see fig. 4
) and whose origin seems to predate the plant/fungal/animal split. Although horizontal transmission has been proposed to explain the wide phylogenetic range of these elements (Poulter and Butler 1998
; Miller et al. 1999
), the negative evidence invoked (i.e., absence of these elements in invertebrates) is hardly compelling. The simplest hypothesis is that the acquisition of a chromodomain was a very old, unique event and that elements with this characteristic have been vertically transmitted, being eventually lost in some lineages. Therefore, we propose giving genus status to the monophyletic group formed by chromodomain-containing elements and their closest relatives (that lack this domain as a result of a secondary loss). We propose the name Chromovirus for this genus.
Whether it is convenient to classify the elements Ty3 and Skipper as chromoviruses is unclear. Malik and Eickbushs (1999)
analyses placed Ty3 and Skipper together with the chromodomain-containing elements. However, Ty3 lacks a chromodomain, and RT sequences alone (Wright and Voytas 1998
and this study) do not support this association. On the other hand, Skipper has a chromodomain, but our RT-based analysis places it outside of the tree formed by the rest of Ty3/Gypsy elements (fig. 3
). The contradictory results for Skipper when the RT domain alone are considered versus those when several pol protein domains are considered can be explained in three ways: (1) Skipper has a recombinant origin: The RT sequences would derive from certain highly divergent elements, while the IN domain would come from a typical chromodomain-containing element (see Jordan and McDonald 1999
a for an example of such a of process in retrotransposons); (2) Skipper RT sequences are evolving at an abnormally fast rate; and (3) Skipper integrase has acquired a chromodomain independently of the other elements. Thus, Ty3 and Skipper may provisionally be considered chromoviruses, following Malik and Eickbush's (1999)
results, but this classification should be reconsidered when more data are obtained.
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Acknowledgements |
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Footnotes |
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1 Keywords: Gypsy,
genome sequencing
Arabidopsis,
Drosophila,
evolution
2 Address for correspondence and reprints: Ignacio Marín, Departamento de Genética, Universidad de Valencia, Calle Doctor Moliner, 50, Burjassot 46100, Valencia, Spain. E-mail: ignacio.marin{at}uv.es
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