Molecular Biology and Evolution 18:954-961 (2001)
© 2001 Society for Molecular Biology and Evolution
ARTICLE |
Loss of Transposase-DNA Interaction May Underlie the Divergence of mariner Family Transposable Elements and the Ability of More than One mariner to Occupy the Same Genome
Department of Biological Sciences, Duquesne University
Department of Entomology, University of Illinois
 |
Abstract |
|---|
 TOP Abstract IntroductionMaterials and MethodsResultsDiscussionAcknowledgementsliterature cited |
|---|
Mariners are a large family of eukaryotic DNA-mediated transposable elements that move via a cut-and-paste mechanism. Several features of the evolutionary history of mariners are unusual. First, they appear to undergo horizontal transfer commonly between species on an evolutionary timescale. They can do this because they are able to transpose using only their own self-encoded transposase and not host-specific factors. One consequence of this phenomenon is that more than one kind of mariner can be present in the same genome. We hypothesized that two mariners occupying the same genome would not interact. We tested the limits of mariner interactions using an in vitro transposition system, purified mariner transposases, and DNAse I footprinting. Only mariner elements that were very closely related to each other (ca. 84% identity) cross-mobilized, and then inefficiently. Because of the dramatic suppression of transposition between closely related elements, we propose that to isolate elements functionally, only minor changes might be necessary between elements, in both inverted terminal repeat and amino acid sequence. We further propose a mechanism to explain mariner diversification based on this phenomenon.
|
Introduction |
|---|
|
TOPAbstractIntroductionMaterials and MethodsResultsDiscussionAcknowledgementsliterature cited |
|---|
Mariner elements are short inverted terminal repeat (ITR)–type transposons that compose a large family of related transposons that are widely distributed among metazoans. To date, more than 13 subfamilies of these elements have been described, typically sharing ca. 25% amino acid identity between subfamilies and from 25% to nearly 100% amino acid identity within a subfamily (Robertson 1993
; Robertson and MacLeod 1993
).
The phylogenetic history of mariner family elements is dominated by extensive horizontal transfer between species, some separated by great phylogenetic distances (e.g., Garcia-Fernandez et al. 1995
; Lohe et al. 1995
; Robertson and Lampe 1995
). When species are examined for the presence of mariners, multiple different kinds are commonly found occupying the same genome (fig. 1
). For example, the human genome contains two distinct mariner family elements. Hsmar1 (Homo sapiens mariner 1) belongs to the cecropia subfamily, while Hsmar2 belongs to the irritans subfamily (Robertson and Martos 1997
; Robertson and Zumpano 1997
) (fig. 1
). These two elements share about 37% amino acid identity, and each is present in many hundreds of copies. They presumably result from two independent invasions of the human genome lineage. Some species harbor even more kinds of mariners. The nematode Caenorhabditis elegans, for example, contains nine distinct kinds of mariner elements from three different subfamilies.
|
The presence of distinct mariner family elements in the same genome, each with multiple copies, suggests that they do not interact. If interactions occurred, then elements would be subject to each other's regulatory systems, and it is difficult to imagine how a new element could invade a genome already occupied by another mariner. Regardless of the mechanism that leads to the presence of distinct mariners, some interesting mechanistic questions are raised. Can divergent elements interact through sequence-specific DNA binding? If so, can divergent elements cleave DNA at the ITRs? Finally, how much divergence is necessary before elements fail to interact? The latter question is particularly interesting, as it may underlie the diversification of mariners over evolutionary time.
To investigate whether mariner family elements were capable of interacting, we analyzed the ability of purified Himar1 and Mos1 mariner transposases (the only known active mariners) to mobilize Kanr-marked elements representing different mariner subfamilies in an in vitro reaction. These reactions were followed by DNAse I footprinting and DNA cleavage reactions to determine the nature of the interactions, or lack thereof. We conclude that a relatively small amount of divergence in ITR sequence is necessary to substantially reduce the interactions between elements, and we propose two scenarios in which this divergence may drive mariner evolution.
|
Materials and Methods |
|---|
|
TOPAbstractIntroductionMaterials and MethodsResultsDiscussionAcknowledgementsliterature cited |
|---|
Recombinant DNA
Mini-mariner elements representing irritans, mellifera, cecropia, and mauritiana subfamilies (see fig. 1 ) were constructed by selecting genomic clones that contained ITR sequences closest in DNA sequence to the subfamily consensus. The Himar1 mini-mariner was previously constructed (Lampe, Grant, and Robertson 1998
). Mantispa pulchella4.1 (a genomic clone containing a mariner insertion isolated from the neuropteroid insect Mantispa pulchella) was used to create the most closely related mini-mariner to Himar1 (Robertson and Lampe 1995
). A third representative of the irritans subfamily was constructed from the Hsmar2 group using human cDNA clone 199288 and human cDNA clone 27609 for the 5' and 3' ITR ends, respectively, because they represent the consensus sequence (Robertson and Martos 1997
). Genomic libraries were constructed and screened for the honeybee Apis mellifera and for a beetle, Carpelimus sp. (Staphylinidae), essentially as described (Robertson and Lampe 1995
), using specific probes obtained by PCR (Robertson 1993
; Robertson and MacLeod 1993
). For the mellifera subfamily, genomic clones A.mellifera.2 and A.mellifera.19 were used for the 5' and 3' ends. Genomic clones Staphylinid.18.3 and Staphylinid.18.1 served as the starting material for the cecropia subfamily 5' and 3' ITRs (Csmar1). Mos1 (a gift of D. Hartl) was used as the template for a mauritiana subfamily representative.
Genomic copies of mariners from the four subfamilies were amplified by PCR using primers designed to the ITR regions of each genomic clone. The PCR primers contained an ATA at the 5' end to facilitate TA cloning into a t-tailed pcDNAII vector and to provide a duplicated target site context in which all mariners were found. The appropriate single ITR from each clone was then amplified during PCR using Pfu DNA polymerase (Stratagene) with a pcDNAII vector primer and a custom internal mariner primer. The custom internal mariner primers, designed to the 5' end of the ITR, contained a SmaI site at their 5' ends. PCR products corresponding to the 5'- and 3'-end ITRs of each subfamily of mini-mariner were kinased and ligated together. They were then used in a PCR using Pfu polymerase with vector primers to amplify the ligated ITR ends. The products were digested with XhoI and HindIII and cloned into an XhoI/HindIII cut pcDNAII vector. Individual clones were manually sequenced with pcDNAII vector primers to verify the sequence. The mini-mariner constructs were next digested with SmaI, and a 1.5-kb fragment of pK19 (Schafer et al. 1994
) digested with BspHI and BglII containing a kanamycin-resistance (KanR) gene was cloned into the SmaI site, separating the two ITRs. Finally, a portion of the AmpR gene was removed as described previously, making the clones KanR only (Lampe, Grant, and Robertson 1998
). These are the donor plasmids shown in figure 2
.
|
For footprint and cleavage analysis, single ITR's were amplified by PCR using Pfu polymerase and the subfamily mini-mariner constructs as templates. The vector primer T7 and a custom internal mariner primer, designed with a SalI site at its 5' end, generated products that contained the first 61 bp of each 5'-end ITR. These products were digested with XbaI and SalI and then cloned into similarly cut pKAN19. Individual clones were sequenced for verification.
Transposase Purification
Himar1 transposase was purified as described previously (Lampe, Churchill, and Robertson 1996
). Mos1 mariner transposases were a gift of D. Finnegan and S. Beverley.
In Vitro Transposition Assays
In vitro transposition assays were carried out according to Lampe, Churchill, and Robertson (1996)
with the following modifications (fig. 2
). Donor plasmids from the four different subfamilies were combined in equimolar amounts with the pBSKS+ target plasmid and Himar1 transposase and allowed to react for 2 h at 28°C. The target plasmid was a tetramer of a pUC plasmid, and so all transposition products formed by insertion into it, even those into the AmpR gene or origin of replication, could be recovered. Two concentrations of Himar1 transposase (0.5 nM and 2.5 nM) were tested with each mariner subfamily donor. After reaction cleanup and electroporation into competent cells, 200 µl of the cell culture was plated on LB-kanamycin-ampicillin plates, and 100 µl of a 10-3 dilution was plated on LB-amp plates. Several colonies containing transposition products were miniprepped and analyzed by restriction digestion with BamHI. Mpmar1 (Mantispa pulchella mariner 1) transposition products were further verified by digesting with BamHI and NsiI to discriminate potentially contaminating Himar1 products that contained NsiI. Genuine Mpmar1 transposition products were sequenced manually with Oncor's Fidelity sequencing kit and 35S dATP to determine insertion site sequences. Mos1 in vitro transposition assays were carried out as described by Tosi and Beverley (2000) using 125 nM purified Mos1 transposase (a gift of S. Beverley).
Footprinting and Cleavage Assays
Footprint fragments containing one ITR sequence were radiolabeled on the top strand by first cutting 
3 µg of plasmid DNA with 15 U of SalI in Promega restriction enzyme buffer D in a total volume of 20 µl for 1 h at 37°C and 20 min at 65°C. The buffer was exchanged to water by spinning the sample through a Sephadex G-50 column for 2 min. To the elute we added 5 µl BRL React 2 buffer, 1 µl 1.5 mM dGTP, 1 µl 1.5 mM dTTP, 4 µl 3,000 mCi/mmol 32P dATP, 4 µl 3,000 mCi/mmol 32P dCTP, 5 U Klenow, and water to bring the volume to 50 µl. The reactions were left at room temperature for 25 min and were then chased with 1 µl of 10 mM dNTPs for 5 min. The reactions were heated to 65°C for 20 min to destroy the polymerase. The DNA was again digested with 15 U of XbaI for 1 h at 37°C and 20 min at 65°C. The radiolabeled footprint fragments were isolated as described previously (Lampe, Churchill, and Robertson 1996
). The DNA was resuspended in 50 µl of TE (10 mM Tris-Cl, pH 8.0, 1 mM EDTA), and 1 µl was counted in a scintillation counter. Each sample was diluted to 25,000 cpm/µl.
DNase I footprinting reactions were carried out as described previously using purified Himar1 transposase and purified Mos1 transposase. The reactions were incubated at room temperature for 30 min, after which 0.75 U of DNase I was added to each tube. After precisely 2 min, the reactions were stopped with 70 µl of stop buffer (64.5 µl 100% ethanol, 0.5 µl tRNA [1 mg/ml], 5 µl saturated ammonium acetate) and chilled in a dry ice/ethanol bath for 15 min. The DNA was centrifuged for 30 min, and the pellets were washed once with 70% ethanol. The pellets were resuspended in 10–15 µl of sequencing stop buffer (US Biochemicals). Size standards and footprint reactions were resolved as in Lampe, Churchill, and Robertson (1996)
.
Cleavage assays were set up in the same way as the footprint reactions and incubated at 30°C for 2.5 h, omitting the DNase I step. The reactions were terminated and processed as per the footprint reactions.
|
Results |
|---|
|
TOPAbstractIntroductionMaterials and MethodsResultsDiscussionAcknowledgementsliterature cited |
|---|
Choice of mariner Elements
We chose to examine the interactions of two purified mariner family transposases with the ITRs from six different mariner family elements. The elements examined in this study are listed in table 1 , along with the sequences of the ITRs for each and the percentage of identity of the ITRs to those of Himar1 and Mos1 mariner, elements whose transposases were used in this study. The tree shown in figure 1 graphically represents the relationships of the elements to each other. We examined a mixture of elements from the same subfamily and from different subfamilies. Himar1, Mpmar1, and Hsmar2 are all members of the irritans subfamily (fig. 1 ). Mpmar1 was the element that was most closely related (82% amino acid identity) to Himar1, which showed any significant divergence in its ITRs, while Hsmar2, although in the subfamily, was very divergent (39% identity with Himar1). Each of the others, Csmar1 (cecropia subfamily), Ammar1 (mellifera subfamily), and Mos1 (mauritiana subfamily), was an element from another subfamily. We reasoned that a mixture of members within a subfamily and from other divergent subfamilies would allow us to probe the limits of site-specific DNA binding within the mariner family of transposons. Finally, it was important for us to limit ourselves to naturally occurring elements because these are presumably selected for activity in nature.
|
In Vitro Transposition
In vitro transposition was performed using combinations of both purified transposases at various concentrations and all six elements as donors (fig. 2 ). As table 2 shows, Himar1 transposase was able to mobilize its cognate element and, to a much lesser degree, the Mpmar1 element, whose ITR is 83% identical to that of Himar1. The degree to which Himar1 transposase was able to interact with Mpmar1 ITRs was strongly dependent on the transposase concentration. At 2.5 nM Himar1 transposase, Mpmar1 was mobilized about 26-fold less frequently than was Himar1. At 0.5 nM purified Himar1 transposase, this value plummeted such that Mpmar1 was mobilized 419-fold less frequently than was Himar1. These results indicate a much lower affinity of Himar1 transposase for Mpmar1 ITR DNA than for the cognate Himar1 ITR sequence. Insertions of Mpmar1 were sequenced to determine the site of insertion and were similar to those of Himar1 (data not shown).
|
Hsmar2, which is also an irritans subfamily element, was not mobilized at all by Himar1 transposase. No member of any other subfamily was mobilized by Himar1 transposase. Mos1 transposase was able to mobilize only its cognate element, with no evidence of mobilization of any other element. We note, however, that the level of activity shown by Mos1 transposase to its own ITRs was lower than that of Himar1; thus, the limit of detection for interactions was reduced in the Mos1 comparisons.
Interaction of Purified Transposases with ITR DNAs from Various mariner Family Elements
We next asked what is responsible for the failure of the purified transposases to mobilize other elements. In principle, failure to transpose could be caused by either lack of binding to ITR DNA or a failure to cleave the DNA after binding. Figure 3
shows the results of DNAse I footprinting and cleavage analysis using purified Himar1 and Mos1 transposases with radiolabeled ITR DNA from each of the elements used in this study. In each case in which a transposase was able to mobilize an element in the in vitro transposition assay, the transposase was able to bind and cleave the ITR DNA of the element. The footprint of Himar1 on Mpmar1 ITR DNA above required approximately five times the amount of transposase necessary to bind the cognate Himar1 ITR DNA, and still the footprinting and cleavage was not as intense as that produced on the cognate ITR. The amount of transposase used here was the maximum amount that could be practically accommodated in the assay. These results indicate a decreased affinity of Himar1 transposase for Mpmar1 DNA, which correlates with the decreased ability to mobilize the Mpmar1 element.
|
In every case in which the transposase was unable to mobilize the element in the in vitro assay, there was no indication of an interaction of the transposase with the ITR of the element. We therefore conclude that the failure of mariner family elements to interact with each other lies at the level of site-specific DNA binding of the transposase to the ITR.
Are All Nucleotide Positions in the Inverted Repeats Important?
We were surprised at the degree to which transposition was suppressed between Himar1 and Mpmar1, given that their ITRs are 83% identical. Such a degree of difference is often seen between the two ITRs in the same transposon in other systems. For example, the bacterial insertion sequence IS50 has inverted terminal repeats (the "outer end" and "inner end") that differ at 7 out of 19 bp (i.e., 63% identical) (Sasakawa, Carle, and Berg 1983
). Indeed, even Mos1 mariner has mismatches between its ITRs which make each end ca. 90% identical to the other (Maruyama, Schoor, and Hartl 1991
). One way to analyze homologous sequences to determine important conserved positions is through sequence logo analysis (Schneider and Stephens 1990
). We generated a sequence logo of the ITRs used in this study and two other mariners from two other subfamilies (C.elegans.mar1 and B.mori.mar1; see fig. 1 ), which are representative of mariner element diversity as a whole (fig. 4
). The sequence logo strongly suggests that certain positions in mariner ITRs are more conserved than others. Two regions of the ITRs, positions 3–8 and positions 14–18, appear to be most conserved. Conservation of these positions suggests that the transposase might be making base-specific contacts within these regions of the ITR. Indeed, the most conserved positions in each region (positions 5 and 15) are one helical turn away from each other, suggesting that transposase might be making contact with the DNA on one face of the ITR in two locations of the major groove. Conservation at a subset of ITR positions also suggests that not all of the five differences between Mpmar1 and Himar1 ITRs may be equally important. Positions 7, 10, and 11 in the sequence logo are not strongly conserved between mariners, while positions 6 and 17 are moderately conserved. Thus, only positions 6 and 17 might be contributing most of the functional divergence between the two elements. This implies that relatively few changes in the inverted terminal repeat may have dramatic effects on the ability of transposase to interact with the ITR, which may strongly affect how these elements diverge from one another.
|
|
Discussion |
|---|
|
TOPAbstractIntroductionMaterials and MethodsResultsDiscussionAcknowledgementsliterature cited |
|---|
Lack of Site-Specific DNA Binding Underlies the Ability of More than One mariner to Occupy a Single Genome
Phylogenetic analysis of mariner family transposable elements reveals several striking features about their evolutionary history. First, a phylogeny based on mariner sequences usually shows large discrepancies with the phylogenies of the host species in which they are found (Robertson 1993
; Robertson and MacLeod 1993
; Robertson and Lampe 1995
). Although long-branch attraction is sometimes invoked to explain incogruencies in phylogenetic trees, the most likely explanation for this phenomenon is horizontal transfer between host species (Maruyama and Hartl 1991
; Lohe et al. 1995
; Robertson and Lampe 1995
). We do not understand how this happens, but we do know that transposition is possible using only the mariner-encoded transposase protein which infers a lack of host-specific factors in transposition and which would greatly facilitate the process of horizontal transfer (Lampe, Churchill, and Robertson 1996
; Tosi and Beverley 2000
).
Two other features of mariner element phylogenies are the sheer diversity of the elements and the fact that any given host genome may harbor more than one kind of mariner element. In some cases, at least nine distinct kinds of mariners have been detected in the same genome (see fig. 1
). Our analysis here demonstrated that divergent mariner elements do not interact and, indeed, the elements need not be very diverged to lose a substantial degree of interaction. This has important evolutionary and practical implications. Any given mariner element is likely to see a new genome as virgin territory upon a horizontal transfer, even if that genome is already occupied by other mariner elements and their regulatory systems, assuming the invading element is sufficiently divergent. This phenomenon probably underlies the fact that many genomes contain more than one kind of mariner element. Similar conclusions have been reached using genetic crosses combining different elements in flies, although this study did not compare elements on as fine a scale as the work herein (De Aguiar and Hartl 1999
).
Practical Implications
Noninteraction of divergent elements has practical implications as well. First, mariner elements have been advanced as genetic tools for germ line transformation of a variety of organisms, some intended for eventual release into the wild (Lampe, Churchill, and Robertson 1996
; Lohe and Hartl 1996b
; Hoy et al. 1997
). The stability of mariner-based transgenes in these organisms has been questioned given the apparent ubiquity of mariners. We feel that there is very little likelihood of any transgene instability given the fact that most mariners we know about are sufficiently divergent so as to not interact with either Mos1 or Himar1, the elements most likely to deliver transgenes. This is in contrast to the situation found between the related hAT family elements, Hermes and hobo, which do cross-react (Sundararajan, Atkinson, and O'Brochta 1999
).
Second, Himar1 and Mos1 have been successfully used as genetic tools in a variety of organisms (Lidholm, Lohe, and Hartl 1993
; Lohe and Hartl 1996b
; Gueiros-Filho and Beverley 1997
; Fadool, Hartl, and Dowling 1998
; Sherman et al. 1998
; Rubin et al. 1999
). It is now clear that these elements could be used together in the same genome to create organisms containing more than one transgene without fear of cross-mobilization.
Speculation: Does Divergence of Transposase-DNA Interactions Drive mariner Family Diversity?
Despite the great diversity of mariner elements, we do not yet understand how this diversity is generated. A model for the life cycle of mariners based on that of Hartl et al. (1997)
and others (Robertson 1993
; Robertson and MacLeod 1993
; Robertson and Lampe 1995
; Hartl et al. 1997
) is shown in figure 5
. A key feature of this model is horizontal transfer, and hereinafter we will refer to this model as the horizontal transfer model. The portion of the model outlined in solid arrows indicates the probable fate of the vast majority of mariners in nature, namely, vertical inactivation and stochastic loss from the species (Lohe et al. 1995
; Robertson and Lampe 1995
) and the possible further horizontal transfer of the identical element. Nevertheless, our data suggest that other fates are available to certain diverged mariner copies.
|
In all cases, elements diverge from the original invading copy by the accumulation of point mutations (Lohe et al. 1995
; Robertson and Lampe 1995
). Many of these mutations inactivate particular copies and lead to the eventual vertical inactivation of the element in the species as proposed by the horizontal-transfer model. Like any mutation, however, some will be neutral and some will change the function of a cis sequence or the transposase-coding sequence. This change in function could be either a loss or a gain of function. Elements carrying neutral or functionally different (yet still active) mutations can proceed down two other paths besides the most common one emphasized by the horizontal-transfer model. The first path is horizontal transfer of a divergent copy to another species. Phylogenetic evidence indicates that this almost certainly involves the invasion of a single active copy of a mariner into a new genome. Horizontal transfer and establishment of the element in a new lineage implies that the transferred element must be functional (Silva and Kidwell 2000). There is no guarantee, however, that the mutated copy will have the same degree of activity as the parental element. Mutations isolated in mariner in D. melanogaster and in Himar1 in an Escherichia coli screen show that both inactivating and hyperactive mutations can be isolated (Lohe, De Aguiar, and Hartl 1997
; Lampe et al. 1999
). After horizontal transfer, the number of copies an element can make is probably directly dependent on its intrinsic activity. Thus, any mutation that can increase an element's activity will be of benefit to the element, provided that increased activity does not grossly affect the fitness of the host. If, for example, an amino acid mutation is present in a transferred copy that lowered, but did not eliminate, its activity, one class of mutations that might increase the activity of this enfeebled element would be a cis-acting suppressor mutation in the ITR. A side effect of such a suppressor mutation may be reduced interaction with the parental element. If this process were to be repeated sequentially, the descendants of the original element could be expected to diverge to the extent that they could no longer interact with the parent if the two were ever to reestablish contact. This is essentially diversification by repeated founder effects, with selection at the time of horizontal transfer for some degree of activity. The second alternative path emphasizes divergence primarily within a single species. This path consists of a new (i.e., noninteracting) element arising within the same host species as the parental element. If this model were true, slight coevolutionary changes in ITR and transposase sequences would be sufficient to allow the new element to preferentially mobilize itself, which is not normally the case. A transposase gene transcribed and translated from one particular copy of an element normally has no guarantee that it will mobilize the same copy from which it was transcribed.
We realize that coevolutionary changes occurring in the same element would be rare. Nevertheless, at least three factors mitigate this rarity. First, elements have many chances to undergo this phenomenon, since they can occupy many genomes essentially simultaneously (Robertson and Lampe 1995
). Second, recent evidence on Tc1 transposition in C. elegans indicates that gap repair mechanisms that repair donor sites after transposition sometimes produce chimeric elements due to template switching (S. Fisher, E. Wienholds, and R. Plasterk, personal communication). Thus, the host can perform gene shuffling of the transposable elements, which may mean that the actual diversity of changes in elements is much greater than that derived from simple point mutations. This would dramatically increase the chances of coevolutionary changes occurring in the same element. Future studies on the interaction of mariner transposases and their cognate ITRs will shed much light on the degree to which slight changes in the ITRs can disrupt transposase binding and whether, or if, these changes can be compensated for by slight mutations in the transposase.
Finally, there may be a selective advantage to any particular copy of an element that can undergo the process of within-species divergence. The ultimate fate of mariners in a species is inactivation through point mutation, emergent regulatory processes, or stochastic loss (Hartl, Lohe, and Lozovskaya 1997
). Any element that can escape the regulatory systems of the parental element can found its own lineage and start down the mariner life cycle anew (Lohe and Hartl 1996a
).
To date, sequences collected from a variety of species by PCR and data mining from genome projects overwhelmingly support the diversification of mariners by the first path. Nevertheless, the data presented herein demonstrate that a relatively slight degree of divergence between ITRs and transposase sequences is sufficient to dramatically decrease the amount of interaction between two elements, so in a minority of cases, path 2 conceivably might be utilized. Evidence gathered primarily from elements in protist genomes suggests that diversification can occur within a genome and not depend solely on a benefit to the host (Witherspoon et al. 1997
; Witherspoon 1999
). Divergence by path 2 could be tested in two ways. First, a careful analysis of element lineages within a single species should show closely related elements coexisting and certain fixed amino acid sequences correlating with certain fixed ITR changes. Second, this process could be tested with Himar1 in the laboratory by introducing mutations into the ITR that lower transposition frequency and then screening for transposase mutants that suppress these changes in an E. coli–based screen (Lampe et al. 1999
).
|
Acknowledgements |
|---|
|
TOPAbstractIntroductionMaterials and MethodsResultsDiscussionAcknowledgementsliterature cited |
|---|
We thank D. Hartl for the gift of Mos1 DNA; D. Finnegan and S. Beverly for providing purified Mos1 transposase; A. Dawson for help in interpreting the Mos1 cleavage data; W. Engels, G. Herrick, and D. Witherspoon for helpful discussions; S. Fisher, E. Wienholds, and R. Plasterk for permission to cite unpublished data; and two anonymous reviewers for their comments. This work was supported by PHS grant 2RO1AI33586-04 to H.M.R. and D.J.L. D.J.L. and K.K.O.W. contributed equally to this work.
|
Footnotes |
|---|
Thomas H. Eickbush, Reviewing Editor
1 Abbreviation: ITR, inverted terminal repeat. 
2 Keywords: mariner,
transposon
transposase
3 Address for correspondence and reprints: David J. Lampe, Department of Biological Sciences, Duquesne University, Pittsburgh, Pennsylvania 15282. lampe{at}duq.edu
|
literature cited |
|---|
|
TOPAbstractIntroductionMaterials and MethodsResultsDiscussionAcknowledgementsliterature cited |
|---|
De Aguiar, D., D. L. Hartl. 1999. Regulatory potential of nonautonomous mariner elements and subfamily crosstalk. Genetica. 107:79–85[ISI][Medline]
Fadool, J. M., D. L. Hartl, J. E. Dowling. 1998. Transposition of the mariner element from Drosophila mauritiana in zebrafish. Proc. Natl. Acad. Sci. USA. 95:5182–5186
Garcia-Fernandez, J., J. R. Bayascas-Ramirez, G. Marfany, A. M. Munoz-Marmol, A. Casali, J. Baguna, E. Salo. 1995. High copy number of highly similar mariner-like transposons in planarian (Platyhelminthe): evidence for a trans-phyla horizontal transfer. Mol. Biol. Evol. 12:421–31[Abstract]
Gomulski, L. M., C. Torti, A. R. Malacrida, G. Gasperi. 1997. Ccmar1, a full-length mariner element from the Mediterranean fruit fly, Ceratitis capitata. Insect Mol. Biol. 6:241–253[ISI][Medline]
Grenier, E., M. Abadon, F. Brunet, P. Capy, P. Abad. 1999. A mariner-like transposable element in the insect parasite nematode Heterorhabditis bacteriophora. J. Mol. Evol. 48:328–336[ISI][Medline]
Gueiros-Filho, F. J., S. M. Beverley. 1997. Trans-kingdom transposition of the Drosophila element mariner within the protozoan Leishmania. Science. 276:1716–1719[published erratum appears in Science 277:753]
Hartl, D. L., A. R. Lohe, E. R. Lozovskaya. 1997. Regulation of the transposable element mariner. Genetica. 100:177–184[ISI][Medline]
Hartl, D. L., E. R. Lozovskaya, D. I. Nurminsky, A. R. Lohe. 1997. What restricts the activity of mariner-like transposable elements. Trends Genet. 13:197–201[ISI][Medline]
Hoy, M. E., R. D. Gaskalla, J. L. Capinera, C. N. Keierleber. 1997. Laboratory containment of transgenic arthropods. Am. Entomol. Winter:206–209
Jeanmougin, F., J. D. Thompson, M. Gouy, D. G. Higgins, T. J. Gibson. 1998. Multiple sequence alignment with Clustal X. Trends Biochem. Sci. 23:403–405[ISI][Medline]
Lampe, D. J., B. J. Akerley, E. J. Rubin, J. J. Mekalanos, H. M. Robertson. 1999. Hyperactive transposase mutants of the Himar1 mariner transposon. Proc. Natl. Acad. Sci. USA. 96:11428–11433
Lampe, D. J., M. E. Churchill, H. M. Robertson. 1996. A purified mariner transposase is sufficient to mediate transposition in vitro. EMBO J15:5470–5479 [published erratum appears in EMBO J. 16:4153]
Lampe, D. J., T. E. Grant, H. M. Robertson. 1998. Factors affecting transposition of the Himar1 mariner transposon in vitro. Genetics. 149:179–187
Lidholm, D. A., A. R. Lohe, D. L. Hartl. 1993. The transposable element mariner mediates germline transformation in Drosophila melanogaster. Genetics. 134:859–868[Abstract]
Lohe, A. R., D. De Aguiar, D. L. Hartl. 1997. Mutations in the mariner transposase: the D,D(35)E consensus sequence is nonfunctional. Proc. Natl. Acad. Sci. USA. 94:1293–1297
Lohe, A. R., D. L. Hartl. 1996a.. Autoregulation of mariner transposase activity by overproduction and dominant-negative complementation. Mol. Biol. Evol. 13:549–555
———.1996b.. Germline transformation of Drosophila virilis with the transposable element mariner. Genetics. 143:365–374
Lohe, A. R., E. N. Moriyama, D. A. Lidholm, D. L. Hartl. 1995. Horizontal transmission, vertical inactivation, and stochastic loss of mariner-like transposable elements. Mol. Biol. Evol. 12:62–72[Abstract]
Maruyama, K., D. L. Hartl. 1991. Evidence for interspecific transfer of the transposable element mariner between Drosophila and Zaprionus. J. Mol. Evol. 33:514–524[ISI][Medline]
Maruyama, K., K. D. Schoor, D. L. Hartl. 1991. Identification of nucleotide substitutions necessary for trans-activation of mariner transposable elements in Drosophila: analysis of naturally occurring elements. Genetics. 128:777–784[Abstract]
Robertson, H. M.. 1993. The mariner transposable element is widespread in insects. Nature. 362:241–245[Medline]
Robertson, H. M., M. L. Asplund. 1996. Bmmar1: a basal lineage of the mariner family of transposable elements in the silkworm moth, Bombyx mori. Insect Biochem. Mol. Biol. 26:945–954[ISI][Medline]
Robertson, H. M., D. J. Lampe. 1995. Recent horizontal transfer of a mariner transposable element among and between Diptera and Neuroptera. Mol. Biol. Evol. 12:850–862[Abstract]
Robertson, H. M., E. G. MacLeod. 1993. Five major subfamilies of mariner transposable elements in insects, including the Mediterranean fruit fly, and related arthropods. Insect Mol. Biol. 2:125–139[Medline]
Robertson, H. M., R. Martos. 1997. Molecular evolution of the second ancient human mariner transposon, Hsmar2, illustrates patterns of neutral evolution in the human genome lineage. Gene. 205:219–228[ISI][Medline]
Robertson, H. M., K. L. Zumpano. 1997. Molecular evolution of an ancient mariner transposon, Hsmar1, in the human genome. Gene. 205:203–217[ISI][Medline]
Rubin, E. J., B. J. Akerley, V. N. Novik, D. J. Lampe, R. N. Husson, J. J. Mekalanos. 1999. In vivo transposition of mariner-based elements in enteric bacteria and mycobacteria. Proc. Natl. Acad. Sci. USA. 96:1645–1650
Sasakawa, C., G. F. Carle, D. E. Berg. 1983. Sequences essential for transposition at the termini of IS50. Proc. Natl. Acad. Sci. USA. 80:7293–7297
Schafer, A., A. Tauch, W. Jager, J. Kalinowski, G. Thierbach, A. Puhler. 1994. Small mobilizable multi-purpose cloning vectors derived from the Escherichia coli plasmids pK18 and pK19: selection of defined deletions in the chromosome of Corynebacterium glutamicum. Gene. 145:69–73[ISI][Medline]
Schneider, T. D., R. M. Stephens. 1990. Sequence logos: a new way to display consensus sequences. Nucleic Acids Res. 18:6097–7100
Sherman, A., A. Dawson, C. Mather, H. Gilhooley, Y. Li, R. Mitchell, D. Finnegan, H. Sang. 1998. Transposition of the Drosophila element mariner into the chicken germ line. Nat. Biotechnol. 16:1050–1053[ISI][Medline]
Silva, J. C., M. G. Kidwell. 2000. Horizontal transfer and selection in the evolution of P elements. Mol. Biol. Evol. 17:1542–1557
Sundararajan, P., P. W. Atkinson, D. A. O'Brochta. 1999. Transposable element interactions in insects: crossmobilization of hobo and Hermes. Insect Mol. Biol. 8:359–368[ISI][Medline]
Swofford, D. L.. 2000. PAUP*Phylogenetic analysis using parsimony (*and other methods). Sinauer, Sunderland, Mass
Tosi, L. R., S. M. Beverley. 2000. cis and trans factors affecting Mos1 mariner evolution and transposition in vitro, and its potential for functional genomics. Nucleic Acids Res. 28:784–790
Witherspoon, D. J.. 1999. Selective constraints on P-element evolution. Mol. Biol. Evol. 16:472–478[Abstract]
Witherspoon, D. J., T. G. Doak, K. R. Williams, A. Seegmiller, J. Seger, G. Herrick. 1997. Selection on the protein-coding genes of the TBE1 family of transposable elements in the ciliates Oxytricha fallax and O. trifallax. Mol. Biol. Evol. 14:696–706
CiteULike 
Connotea 
Del.icio.us What's this?
This article has been cited by other articles:
|
|
 |
|
  C. Miskey, B. Papp, L. Mates, L. Sinzelle, H. Keller, Z. Izsvak, and Z. Ivics The Ancient mariner Sails Again: Transposition of the Human Hsmar1 Element by a Reconstructed Transposase and Activities of the SETMAR Protein on Transposon Ends Mol. Cell. Biol., June 15, 2007; 27(12): 4589 - 4600. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 I. R. Arkhipova and M. Meselson Diverse DNA transposons in rotifers of the class Bdelloidea PNAS, August 16, 2005; 102(33): 11781 - 11786. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 C. Feschotte, M. T. Osterlund, R. Peeler, and S. R. Wessler DNA-binding specificity of rice mariner-like transposases and interactions with Stowaway MITEs Nucleic Acids Res., April 14, 2005; 33(7): 2153 - 2165. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 Z. Xu and H. K. Dooner Mx-rMx, a Family of Interacting Transposons in the Growing hAT Superfamily of Maize PLANT CELL, February 1, 2005; 17(2): 375 - 388. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 C. Feschotte Merlin, a New Superfamily of DNA Transposons Identified in Diverse Animal Genomes and Related to Bacterial IS1016 Insertion Sequences Mol. Biol. Evol., September 1, 2004; 21(9): 1769 - 1780. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 E. G. Barry, D. J. Witherspoon, and D. J. Lampe A Bacterial Genetic Screen Identifies Functional Coding Sequences of the Insect mariner Transposable Element Famar1 Amplified From the Genome of the Earwig, Forficula auricularia Genetics, February 1, 2004; 166(2): 823 - 833. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
X. Zhang, N. Jiang, C. Feschotte, and S. R. Wessler PIF- and Pong-Like Transposable Elements: Distribution, Evolution and Relationship With Tourist-Like Miniature Inverted-Repeat Transposable Elements Genetics, February 1, 2004; 166(2): 971 - 986. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. E. J. Fischer, E. Wienholds, and R. H. A. Plasterk Continuous Exchange of Sequence Information Between Dispersed Tc1 Transposons in the Caenorhabditis elegans Genome Genetics, May 1, 2003; 164(1): 127 - 134. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
D. J. Lampe, D. J. Witherspoon, F. N. Soto-Adames, and H. M. Robertson Recent Horizontal Transfer of Mellifera Subfamily Mariner Transposons into Insect Lineages Representing Four Different Orders Shows that Selection Acts Only During Horizontal Transfer Mol. Biol. Evol., April 1, 2003; 20(4): 554 - 562. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
C. Feschotte, L. Swamy, and S. R. Wessler Genome-Wide Analysis of mariner-Like Transposable Elements in Rice Reveals Complex Relationships With Stowaway Miniature Inverted Repeat Transposable Elements (MITEs) Genetics, February 1, 2003; 163(2): 747 - 758. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 I. Holmes Transcendent Elements: Whole-Genome Transposon Screens and Open Evolutionary Questions Genome Res., August 1, 2002; 12(8): 1152 - 1155. [Full Text] [PDF]
|
|
|
|
|
|
H. Shao and Z. Tu Expanding the Diversity of the IS630-Tc1-mariner Superfamily: Discovery of a Unique DD37E Transposon and Reclassification of the DD37D and DD39D Transposons Genetics, November 1, 2001; 159(3): 1103 - 1115. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||