Botanical Institute, University of Copenhagen, Copenhagen, Denmark
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Abstract |
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Introduction |
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One such group of elements is miniature inverted-repeat transposable elements (MITEs) (Wessler, Bureau, and White 1995
). MITEs are short (
60700 bp) with no coding capacity, they have conserved, usually short, terminal inverted repeats (TIR), they usually have the potential to form a hairpin-like secondary structure, and they show target site preference (Pozueta-Romero et al. 1995
; Wessler, Bureau, and White 1995
; Wessler 1998
; present study). The target site is frequently only 23 bp long, often TA(A) (Wessler, Bureau, and White 1995
), but recently, target sites up to 9 bp have been reported (Song et al. 1998
; Charrier et al. 1999
). The target site is duplicated at insertion so that the MITE is flanked by a direct repeat. The conserved TIRs are 1030 bp long (Pozueta-Romero et al. 1995
; Wessler, Bureau, and White 1995
). The sequence between the TIRs is A+T-rich, but many elements have only limited sequence similarity. MITEs are often inserted near nuclear genes in introns or near the 5' or 3' ends of genes. In a few cases, they have been suggested to supply cis-acting domains involved in gene expression (Bureau and Wessler 1994a
; Bureau, Ronald, and Wessler 1996
; Pozueta-Romero, Houlné, and Schantz 1996
). The difference, if any, between MITEs and another group of unclassified transposable elements, Foldback elements (Rebatchouk and Narita 1997
; Adé and Belzile 1999
), is unclear, and most likely the two types are fundamentally similar.
Some evidence indicates that MITEs are related to DNA transposons and hence are class II elements (Izsvák et al. 1999
). The TIR sequences sometimes resemble those of DNA transposons (Morgan 1995
; Ünsal and Morgan 1995
; Yeadon and Catcheside 1995
), suggesting that the mechanisms of transposition may be related. However, unlike autonomous DNA transposons, MITEs do not encode their own transposase, and Flavell, Pearce, and Kumar (1994)
suggested that they might be defective, internally deleted versions. The calculated copy numbers of 1,00010,000 elements belonging to just one family of MITEs (Wessler, Bureau, and White 1995
; Tu 1997
) suggest that they are able to use a basic cellular mechanism for amplification and transposition (Izsvák et al. 1999
). A model for duplication, detachment, and reinsertion dependent on the inverted-repeat structure of the entire element has been proposed by Izsvák et al. (1999)
. If this model is correct, excision of MITEs does not occur or is rare, as previously suggested by Wessler et al. (Wessler, Bureau, and White 1995
; Wessler 1998
).
MITEs are classified into families according to target site and TIR sequence. First discovered in plants (Bureau and Wessler 1992
), MITEs have also been found in fungi (Yeadon and Catcheside 1995
), frogs (Ünsal and Morgan 1995
), mosquitoes (Tu 1997
), fish (Izsvák et al. 1999
), and humans (Morgan 1995
). In plants, elements of the Stowaway family have been identified in numerous dicots and monocots, whereas elements of other families have only been identified in narrow taxonomic groups (Bureau and Wessler 1994a
). Hence, Tourist elements are known only from grasses (Bureau and Wessler 1992, 1994b
), the Emigrant family only from Arabidopsis (Casacuberta et al. 1998
), and Bigfoot only from Medicago (Charrier et al. 1999
); Ditto, Wanderer, Explorer, Snap, Crackle, and Pop are restricted to Oryza, whereas Castaway was described from Oryza and Zea and Gaijin was described from Oryza and Saccharum (Bureau, Ronald, and Wessler 1996
; Song et al. 1998
). Alien has been described from species of the Solanaceae but may occur in other dicots and in monocots (Pozueta-Romero et al. 1995
; Pozueta-Romero, Houlné, and Schantz 1996
).
The Stowaway elements were first described by Bureau and Wessler (1994a)
, who discovered the first element as an insert into a Tourist element in Sorghum bicolor. At that time, a GenBank survey revealed the presence of 22 Stowaway elements in 6 species of grasses and 26 elements in 12 dicot species (Bureau and Wessler 1994a
), but many more can be found now. Stowaway elements recognize a 2-bp target site (TA) and have a more-or-less conserved TIR sequence of 11 bp (CTCCCTCCGTT), and the entire element is capable of forming a more-or-less perfect hairpin-like secondary structure (Bureau and Wessler 1994a
). In contrast to some other MITE families, Stowaway elements vary considerably in length, from 59 bp (this study) to 323 bp (Bureau and Wessler 1994a
). Both extremes are found among the grasses, whereas the Stowaway elements of dicots are more homogeneous in size, i.e., (167)220290 bp (Bureau and Wessler 1994a
).
To understand the evolution of Stowaway or other transposable elements, studies need to be performed in a monophyletic group of species. As discussed by VanderWiel, Voytas, and Wendel (1993)
, most studies of transposable-element evolution are flawed by an inadequate sampling of taxa or elements. For studies of retrotransposons, VanderWiel, Voytas, and Wendel (1993)
suggested as a possible strategy an in-depth sampling of elements from a few closely related species with a well-known phylogeny. However, this is not feasible for studying the evolution of Stowaway. Thorough sampling of elements from any taxon is not easy. Due to the high sequence diversity, screening by hybridization techniques is not feasible, and the conserved TIRs are too short to act as primer sites for PCR. Even if a sufficient number of elements were detected, severe alignment problems remain, due to considerable differences in length (see above) and a high A+T content of the core region. A further difficulty arises as the secondary structure of Stowaway makes it problematic to determine the orientation of an element prior to alignment.
An alternative strategy for studying the evolution of transposable elements such as Stowaway is to concentrate on putative homologous (Patterson 1988
) elements, i.e., elements found at exactly the same position in the genome in a monophyletic group of organisms. This is best done with elements located in introns flanked by conserved exon sequences suitable for designing PCR primers. This strategy will also circumvent the nontrivial problem of the placement of the root in a purely element-based "phylogeny," as the position of the root is decided by the organismal phylogeny. Hence, this framework provides an opportunity to study patterns of sequence evolution and possible insertion and excision events of transposable elements. Among the relevant questions that could be answered: Are elements excised? Is there a relationship between secondary structure and insertion/excision? Are substitutions in one part of the hairpin compensated by substitutions in the other?
The discovery of new members of the Stowaway family in an intron of the DMC1 gene (disrupted meiotic cDNA1) in species of the Triticeae, coupled with the possibility of constructing a gene phylogeny for the group, gave us an excellent opportunity to investigate some of the above aspects of the evolution of Stowaway.
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Materials and Methods |
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DNA Amplification and Sequencing
For species of the Triticeae primers TDMC1e10 (5'-TGCCAATTGCTGAGAGATTTG-3') and TDMC1e15R (5'-AGCCACCTGTTGTAATCTGG-3') were used for PCR amplification of the region spanning exon 10 to exon 15, numbered according to the Arabidopsis DMC1 gene structure (Klimyuk and Jones 1997
). For amplification of the same sequence in Bromus, the primer BDMC1e15R (5'-CCTGTTGTAATCTGGAAAACGTG-3') was used instead of TDMC1e15R. For sequencing additional primers, TDMC1e13 (5'-CTGGCACAAATGCTGTCCCG-3'), TDMC1e13R (5'-TGGTTGGTGATGTACACTGCA-3'), and TDMC1i14 (5'-TTGTTTACTGCTTGTGC-3') were used. PCR amplification was performed under standard conditions, and the products were purified using the QIAquick PCR purification kit (QIAGEN) according to the manufacturer's instructions. Cycle sequencing was performed using the ABI PRISM Dye Terminator Cycle Sequencing Ready Reaction kit with AmpliTaq DNA Polymerase, FS (PE Biosystems), and the products purified as above. DNA fragments were separated on an ABI 377 (PE Biosystems) automated sequencer, and sequence manipulation/editing was done using Sequencher 3.0. The sequences reported in this paper are deposited in GenBank under accession numbers AF277234AF277264.
Sequence Analyses
Sequence alignment was mainly straightforward and was done manually. Only a small region of intron 12 caused problems, and 11 positions of the alignment were excluded in the subsequent phylogenetic analysis. A region (positions 20101 of intron 14
) including a Stowaway element was also excluded. Gaps introduced into the alignment were coded according to the following criteria: gaps of uniform length aligned to similar positions were coded as absence/presence characters irrespective of the length of the gaps; the gapped regions in the alignment were subsequently excluded from analysis unless some positions also included nucleotide variation; such positions were kept in the analysis, and the gaps were treated as missing entries (?). The aligned matrix is available on request.
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Minimum-energy folding of elements was performed using MFOLD (M. Zuker, Washington University School of Medicine) and free energies as described by SantaLucia (1998)
.
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Results and Discussion |
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Stowaway Elements in DMC1 Sequences
Six Stowaway elements were found in five species of Triticeae; all were located in intron 14 of the DMC1 gene. Taeniatherum caput-medusae, Australopyrum retrofractum, Australopyrum pectinatum, and Australopyrum velutinum share the presence of an element of length 76, 59, 59, and 75 bp, respectively, inserted some 20 bases downstream of the 5' end of intron 14 (fig. 2
). In the following discussion, these elements will be referred to as "short." The remaining Triticeae species do not have this element, although footprints (remains of an element left after excision) seem to be present in 12 species (fig. 2
).
Two other Stowaway elements were discovered in Heteranthelium piliferum 100 bases downstream of the insertion site in Australopyrum and Taeniatherum. One 123-bp element seems to be inserted into a 160-bp element (fig. 3 ). A 4-bp footprint sequence corresponding to the Heteranthelium element is present in Dasypyrum. Stowaway elements inserted into one another have not previously been described, but in GenBank two more occurrences of double Stowaway elements may be found. In a hypothetical intron of a rice BAC clone (GenBank accession number AF119222), two Stowaway elements are seen: a 320-bp element inserted into a 243-bp element. The other possible event involves a 253-bp element located in a pseudogene in Triticum (GenBank accession number AF085168). This element is capable of forming a double hairpin-like structure like the Heteranthelium insertion and has a length comparable to two shorter elements. However, whereas the conserved TIRs characteristic of Stowaway elements are present surrounding the inner element in Heteranthelium, such sequences are not recognizable in the AF085168 element.
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Insertion and Excision of Stowaway Elements
Under the assumption that the DMC1 gene tree represents the true evolutionary history of the gene, insertion and excision events of Stowaway elements can be traced. As the four short elements are present in a well-defined monophyletic group consisting of Taeniatherum plus the three species of Australopyrum, it is straightforward to assume just one insertion. The unique occurrence of a double element in Heteranthelium can likewise be regarded as one or possibly two insertions, depending on whether the outer element was inserted in Heteranthelium before or after it acquired the inner element.
However, the presence of footprints in some species lacking the short Stowaway elements complicates the scenario. Five species (Henrardia persica, Agropyron cristatum, Eremopyrum distans, Sitopsis speltoides, and Amblyopyrum muticum) have 46 nt located immediately downstream of the TA recognition site, of which two to four are identical to the nucleotides of the TIRs of a Stowaway and the latter two are the repeated TA sequence (fig. 2 ). This lends very strong support to the hypothesis that they are footprints left after excision of a Stowaway element. An alternative hypothesis, suggesting that these nucleotides stem from normal insertion events, is possible but highly unlikely considering the sequence similarity to a Stowaway element. The five species, which belong to three different clades, all share a C immediately upstream of the TA recognition site (fig. 2 ; position 21); hence, it is likely that the C is inserted as a result of excision. Seven more species (Peridictyon sanctum, Thinopyrum bessarabicum, Crithodium monococcum, Lophopyrum elongatum, Crithopsis delileana, Comopyrum comosum, and Patropyrum tauschii) share the presence of a C preceding the TA recognition site (CA in P. sanctum; fig. 2 ) but lack the TA repeat at the 3' end. With the exception of Peridictyon, the distribution of these species makes it most probable that the CTA (and possibly the CCA) sequence should also be interpreted as remnants of excision (fig. 1 ).
Thus, embedded in the gene tree is a clade of 11 species, all of which, except Eremopyrum triticeum, possess footprints. The sister taxon of the remaining Triticeae, Henrardia, also possesses indisputable footprints, and Peridictyon, the sister taxon of Heteranthelium (which lacks a footprint), most likely has footprints as well.
In order to trace the number of insertion and excision events of Stowaway elements, it is necessary to develop a simple, asymmetric model accounting for their insertion and excision. Whereas insertion is straightforward, excision may be more complicated. Hence, excision is most likely a two-step procedure in which the element is excised, leaving recognizable footprints that may subsequently be removed. It seems highly improbable to possess footprints without having had an element at an earlier stage.
Under these assumptions, the most parsimonious explanation of the occurrence of the short elements and footprints requires eight evolutionary events: four independent insertions (in Henrardia, in the progenitor of the Taeniatherum-Australopyrum clade, in Peridictyon, and in the progenitor of the "11-species" clade), three excisions (from all but the Taeniatherum-Australopyrum clade) leaving footprints, and one complete removal of footprints (from E. triticeum).
A less parsimonious scenario, requiring nine evolutionary events, that minimizes the number of insertion and excision events may, however, be constructed. This necessitates that a Stowaway element was inserted in the progenitor of the Triticeae but was excised, leaving footprints, prior to speciation (two events). No matter what the resolution of the trichotomy marked with an asterisk in figure 1 , the footprints were subsequently deleted in the progenitor of the Pseudoroegneria-Taeniatherum-Australopyrum clade and from Heteranthelium, and a new element was later inserted at exactly the same position in the ancestor of the Taeniatherum-Australopyrum clade (three events). If the resolution that makes Hordeum and Psathyrostachys monophyletic is chosen among the possible resolutions of the trichotomy marked with two asterisks in figure 1 , the footprints were also deleted from the progenitor of the Hordeum-Psathyrostachys clade, from Festucopsis, from the progenitor of the Secale-Dasypyrum clade, and from E. triticeum (four events). All other resolutions of this trichotomy require one extra evolutionary event. The scenario reduces the number of insertions to only two and the number of excisions to just one, implying that all footprints can be traced back to the same excision event.
To explain the presence of the double Stowaway element in Heteranthelium and the putative footprints in Dasypyrum most parsimoniously, two independent insertion events and one excision are needed. If the footprints are supposed to originate from a single insertion, two excisions and at least three subsequent deletions of footprints must be inferred.
The first scenario explaining the distribution of the short elements and footprints is, of course, the most parsimonious. However, as many of the basal nodes in the trees have jackknife support values below 67%, this explanation may possibly be further simplified. If only nodes with support higher than 67% are taken into account, it is possible to draw a scenario in which only one insertion event, one excision event, and one deletion of footprints are needed to account for the occurrence of the Taeniatherum-Australopyrum elements and the footprints. Likewise, the footprints in Dasypyrum may be remnants from excision of the double Heteranthelium element. Hence, even a very conservative and cautious estimate of the resolution of the gene tree necessitates two insertions and two excisions of Stowaway elements in intron 14 of the DMC1 gene. A different gene tree may invalidate our hypotheses of the number of insertion/excision events necessary to explain the occurrence of Stowaway in the Triticeae, but only nonmonophyly of the Triticeae will invalidate our hypothesis of excision and our interpretation of footprints. However, the monophyly of the Triticeae is well-established (Kellogg 1992
; Davis and Soreng 1993
; Hilu, Alice, and Liang 1999
; Mathews, Tsai, and Kellogg 2000
).
This questions the validity of the proposed model for MITE transposition (Izsvák et al. 1999
). According to the model, as well as to previous suggestions (Wessler, Bureau, and White 1995
; Wessler 1998
), elements do not, or only rarely, excise. However, previous investigations of Stowaway and other MITEs have not been designed to detect possible excisions, basically all lacking a phylogenetic framework. Tenzen et al. (1994)
reported three possible Stowaway excisions in species of Oryza, but in no case has the postulated excision left a footprint, nor did Tenzen et al. base their suggestions on phylogenetic evidence. Firmer evidence for excision of a Stowaway element can be found by comparing three elements located in Secale thaumatin-like genes (TLP13; GenBank accession numbers AF096927, AF099670, and AF099671) with the sequence for an additional thaumatin-like gene, TLP4 (GenBank accession number AF100142), lacking the element but containing a GTA footprint, aligning with the 3' end of the element, with the TA being the duplicated target site. Evidence for excision of other MITE families also exists. Excision of a Tourist element in Zea was reported by Bureau and Wessler (1992)
, who showed the presence of a duplicated recognition sequence flanking a 4-bp sequence, possibly a remnant of an excised element. A similar case was reported in species of Oryza, where a Ditto element was excised, leaving a duplicated recognition sequence (TTA) flanking a single nucleotide similar to the first nucleotide of the TIR (Bureau, Ronald, and Wessler 1996
). In Solanum, Pozueta-Romero et al. (1995) provided evidence for the excision of an Alien element. Despite these rather obvious examples, Wessler (1998)
maintains that "no MITE has been shown to excise." Given the present data, it seems unavoidable to conclude that MITEs do excise and leave footprints in the process. This supports the notion that MITEs are DNA transposons and hence should be classified as class II elements.
Evolution of Stowaway Elements and Footprints in the Triticeae
The present gene tree offers the possibility of examining both the sequence evolution of a Stowaway element and the evolution of footprints. As observed with Ac/Ds transposon excision, the present excision events leave not only the direct repeat unit, but also part of the TIRs (Scott, LaFoe, and Weil 1996
; Rinehart, Dean, and Weil 1997
). The footprints left immediately after excision may be useful in predicting the actual mechanism of excision, whereas shorter footprints must be considered due to subsequent deletions.
If the optimization of occurrence of the short elements and footprints postulating four insertions and three excisions is correct, three different "initial" footprints can be described: 5'-CTACT ... GTA-3', 5'-CCA ... -3', and 5'-C[Y]AC ... GGAGTA-3'. If, however, only one excision has occurred, the "initial" footprint must have been 5'-CTACT ... GGAGTA-3'. Strictly speaking, the 5'-end CTA sequence may not be included as a footprint, as the TA is the recognition sequence, which may be present in taxa never having had an element, and the C is located upstream of the insertion site. However, as argued previously, the presence of the upstream C is best explained as a result of excision. Excision of the double element located farther downstream in intron 14 has left a 5'-TAC ... GTA-3' footprint. Evidence from the above-cited Secale thaumatin-like sequences suggests a 5'-TA ... GTA-3' footprint (the TA recognition site is included for comparison only).
A consensus sequence, 5'-[C]TA[CT] ... [GGA]GTA-3', can be constructed from the above footprints, but apart from their presence, the information content is limited. None of the "initial" footprints are similar. Hence, either the excision process produces different footprints or they have been modified subsequently. Observations of many more footprints are needed to clarify the issue.
The gene tree also gives indications of sequence evolution of the inserted element. The four short Stowaway elements differ from each other by five substitutions and two indels (fig. 2 ). The distribution of two of the substitutions (positions 32 and 80 in fig. 2 ) allows determination of the direction of change. Both changes lead to mismatch in the hairpin-like structure. Two of the five substitutions are located in the TIRs; hence, once the element is inserted, the TIRs seem as prone to change as the core. The polarity of the single indel at position 61 cannot be inferred, but the change occurs in the very short loop region. The 1617-bp length difference at positions 5975 is a deletion producing the shortest Stowaway element (59 bp) recorded. This deletion also involves the loop region but is strongly asymmetric. Hence, there is no evidence that inserted elements maintain a perfect inverted repeat structure. Rather, there seems to be a gradual increase of mismatch.
MITEs and Phylogeny
Both in morphology and in molecular biology, similarity is the first indicator of homology (orthology): "In the absence of a phylogenetic analysis, one can only propose homologies based on character similarity; one cannot test hypotheses of homology" (Lauder 1994
, p. 188).
Hence, if a number of taxa have a MITE inserted at exactly the same position on the chromosome, i.e., between the same two bases (viz., at the same recognition site) with the same flanking sequences, this is the first indication of homology. The ultimate test of homology is, however, congruence with other characters (Patterson 1982, 1988
; Moritz and Hillis 1996
). Consequently, MITEs with a known position in the genome may provide a phylogenetic signal as long as they are homologous (see, e.g., Iwamoto et al. 1999
). Their identity may be totally obscured by substitutions and indels, or they may be excised, leaving footprints, which may be deleted subsequently. What may cause problems is if an element of the same family of MITEs is inserted at a location where a similar MITE has been excised. Hence, the elements are not homologous. However, none of these problems are fatal to phylogenetic analysis, and all have parallels in morphology.
The Evolution of MITEs
Studies of the evolution of individual Stowaway elements or other MITEs are straightforward as long as they can be considered homologous. In a phylogenetic framework, insertion and the relative sequence excision events and of substitutions and indels may be established. On such a background, a number of interesting questions (e.g., What constraints apply to the elements themselves and to the sequence at or near the insertion site for successful insertion? What is the fate of the elements once inserted?) may be clarified.
Without a phylogenetic framework, and given the fact that the genome may contain as many as 1,00010,000 elements of just a single family of MITEs (Wessler, Bureau, and White 1995
; Tu 1997
), it is extremely difficult to resolve their evolutionary history. That they may be grouped according to structural characteristics (e.g., recognition sites, TIRs, sequence similarity) makes no difference. The immense problem of homology assignment aside, it is difficult to believe that a few hundred base pairs retain enough information about their own history to resolve it. Evidently, the only way one can understand the evolution of MITEs is within a phylogenetic framework.
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Acknowledgements |
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Footnotes |
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1 Abbreviations: MITE, miniature inverted-repeat transposable element; TIR, terminal inverted repeat.
2 Keywords: DMC1
molecular evolution
class II element
MITE
footprint
3 Address for correspondence and reprints: Gitte Petersen, Botanical Institute, University of Copenhagen, Gothersgade 140, DK-1123 Copenhagen K, Denmark. E-mail: gittep{at}bot.ku.dk
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