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Plant Physiol, December 2002, Vol. 130, pp. 1697-1705
Dasheng and RIRE2. A Nonautonomous Long
Terminal Repeat Element and Its Putative Autonomous Partner in
the Rice Genome1
Ning
Jiang,
I. King
Jordan, and
Susan R.
Wessler*
Department of Plant Biology, University of Georgia, Athens, Georgia
30602 (N.J., S.R.W.); and National Center for Biotechnology
Information, National Institutes of Health, Bethesda, Maryland 20894 (I.K.J.)
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ABSTRACT |
Dasheng is one of the highest copy number
long terminal repeat elements and one of the most recent elements to
amplify in the rice (Oryza sativa) genome.
However, the absence of any significant coding capacity for retroviral
proteins, including gag and pol, suggests
that Dasheng is a nonautonomous element. Here, we have exploited the availability of 360 Mb of rice genomic sequence to
identify a candidate autonomous element. RIRE2 is a
previously described gypsy-like long terminal repeat
retrotransposon with significant sequence similarity to
Dasheng in the regions where putative cis factors for
retrotransposition are thought to be located. Dasheng
and RIRE2 elements have similar chromosomal distribution patterns and similar target site sequences, suggesting that they use
the same transposition machinery. In addition, the presence of several
RIRE2-Dasheng element chimeras in the
genome is consistent with the copackaging of element mRNAs in the same
virus-like particle. Finally, both families have recently amplified
members, suggesting that they could have been co-expressed, a necessary
prerequisite for RIRE2 to serve as the source of
transposition machinery for Dasheng. Consistent with
this hypothesis, transcripts from both elements were found in the same
expressed sequence tag library.
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INTRODUCTION |
Transposable elements fall into two
classes based on their transposition mechanisms. DNA or class II
elements are characterized by short terminal inverted repeats and
transposition via a DNA intermediate (Kunze et al.,
1997 ). Because of their conservative mechanism of
transposition, the copy number of DNA element families is usually less
than 100 per haploid genome. In contrast, RNA or class I elements are
capable of attaining very high copy numbers in a relatively short
period of time because the element-encoded mRNA, and not the element
itself, forms the transposition intermediate. Based on their structural
features, class I elements are further divided into two subclasses.
Non-long terminal repeat (LTR) elements, including long interspersed
nuclear elements and short interspersed nuclear elements, are the most
abundant class I elements in mammalian genomes (Smit,
1996; Lander et al., 2001). LTR
retrotransposons, on the other hand, are the most abundant elements in
plants and compose a significant fraction of the genome (Kumar
and Bennetzen, 1999). In the grass clade, the differential
amplification of LTR retrotransposon has been shown to be largely
responsible for the significant difference in genome size among members
(Chen et al., 1997; Dubcovsky et al.,
2001).
LTR retrotransposons are either copia like or
gypsy like, depending on the order of retroviral domains
encoded by the gag and pol genes (Xiong
and Eickbush, 1990). The products of gag comprise
the major structural proteins of the virus-like particle (VLP), which
is involved in maturation and packaging of element RNA and other
proteins. As is typical for many retroelements, translation of
element-encoded RNA generates a long poly-protein precursor, which is
specifically cleaved by a pol-encoded protease, releasing
mature proteins. In addition to the protease, the pol gene
also encodes reverse transcriptase (RT), RNase H, and integrase, proteins involved in the synthesis and integration of the element DNA
into the host genome. In addition to these coding regions, cis
sequences within the element are also necessary for transposition. The
LTR usually contains initiation and termination sites for transcription. Immediately internal to the LTR is the primer binding site (PBS) and the polypurine tract (PPT; Fig.
1), which are necessary for the
initiation of the synthesis of element DNA from the RNA intermediate
(Boeke and Corces, 1989).
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Figure 1.
Comparison of Dasheng and
RIRE2. LTRs are shown as yellow or orange boxes. Open
reading frames (ORFs) in RIRE2 are shown as green and blue
boxes. Regions of sequence similarity (between Dasheng and
RIRE2) upstream of the PPT are shown as purple boxes. pro,
Protease; rt, RT; rh, RNase H; int, integrase. A, Typical
Dasheng element. Red arrows represent the 89- to 90-bp
tandem repeat. B, Typical RIRE2 element. C, Sequence
comparison of the related regions of Dasheng and
RIRE2. The 3' LTR and the internal sequence that is not
related are not shown. The positions of the PBS, PPT, and the start
codon of gag in RIRE2 are indicated. Comparisons
are based on consensus sequences (see "Materials and
Methods").
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Although the vast majority of previously reported LTR retrotransposons
are copia or gypsy like, an increasing number of
elements lacking any significant retroviral domains cannot be
classified in this way. These elements are considered to be
nonautonomous because they require the products from another element in
trans to amplify in the genome. One such element is MaLR, an
ancient element family with the highest copy (approximately 240,000 copies) among LTR elements in the human genome (Smit,
1993; Lander et al., 2001). Bs1, a
maize (Zea mays) LTR element with one to five copies,
was first detected as a new insertion into adh1
(Johns et al., 1985; Jin and Bennetzen,
1989). Zeon-1 is another maize nonautonomous LTR
element, with a copy number of up to 32,000 (Hu et al.,
1995; Meyers et al., 2001). Despite these and
several other examples, virtually nothing is known about how
nonautonomous LTR retroelements originate or the trans-encoded products
necessary for their transposition.
As mentioned above, LTR retrotransposons make up a significant fraction
of most plant genomes, and account for at least 15% of the relatively
small rice (Oryza sativa) genome (Tarchini et al.,
2000; Turcotte et al., 2001). The availability
of a substantial amount of rice genomic sequence provides a unique
opportunity to identify both nonautonomous LTR retrotransposons and
their autonomous partners. A previous study reported the discovery of Dasheng, a high-copy number nonautonomous LTR element that
amplified very recently in the rice genome (Jiang et al.,
2002). In this study, 360 Mb of publicly available rice cv
Nipponbare genomic sequence has been searched for candidate autonomous
LTR retrotransposons that may have provided the proteins necessary for
Dasheng to spread throughout the rice genome. To our
knowledge, this study provides, for the first time, several lines of
evidence implicating a distinct but related LTR retrotransposon family
(RIRE2) as the source of the transposition machinery for a
nonautonomous LTR element (Dasheng).
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RESULTS AND DISCUSSION |
Sequence Similarity between RIRE2 and
Dasheng
Candidate autonomous elements were selected by searching public
databases of rice genomic sequence for LTR retrotransposon families
that displayed significant sequence similarity to Dasheng. This search led to the identification of a single candidate,
RIRE2, a previously described rice LTR retrotransposon
(Ohtsubo et al., 1999; Fig. 1B). RIRE2 is a
gypsy-type element that, unlike Dasheng, encodes
all of the protein products necessary for retrotransposition. The two
elements have similar LTRs, PBS and PPT (Fig. 1C). In addition,
sequences downstream of the PBS and upstream of the PPT displayed
substantial sequence similarity.
The extent of similarity is striking given that LTRs, as noncoding DNA,
usually evolve much more rapidly than other regions of a
retrotransposon. Even within a single element family, LTRs can diverge
by almost 50%, whereas families of closely related elements (as
determined by RT sequence comparisons) often have LTRs with no
detectable sequence similarity (Arkhipova et al., 1995;
Jordan and McDonald, 1998). One explanation for the
conservation of LTR sequences is that RIRE2 and
Dasheng must be co-expressed if Dasheng is to
gain access to the RIRE2-encoded retrotransposition machinery. Because the transcriptional regulatory sequences reside in
the LTR, it follows that selection would favor the conservation of LTR
sequences in autonomous and nonautonomous partners. Sequences adjacent
to both the 5' and 3' LTRs also show significant similarity, and this
too may reflect the conservation of cis sequences required for
retrotransposition. This is certainly true for the PPT and the PBS. In
addition, cis-packaging signals, which are essential for VLP mRNA
recognition, should also be conserved. Although not well studied in LTR
retrotransposons, cis-packaging signals have been investigated in
several retroviruses, including human immunodeficiency virus type 1 and
murine leukemia virus. In both cases, these signals are located
upstream or near the start codon of gag and interact directly with the Gag proteins (Adam and Miller, 1988;
Clever et al., 1995). In addition, a 17-bp sequence
upstream of the PPT was shown to be involved in murine leukemia virus
packaging (Yu et al., 2000). Analogous regions appear to
be conserved in Dasheng and RIRE2 (Fig. 1),
perhaps because they enable the mRNA of the two elements to be packaged
by RIRE2-encoded proteins (see below).
Distribution of RIRE2 and Dasheng on
Rice Chromosomes
During retrotransposition, element cDNA, generated by reverse
transcription, is integrated into host chromosomes through interactions with the element-encoded integrase. Given this mechanism, it should follow that if RIRE2 integrase is recognizing
Dasheng cDNA and directing its integration, the two elements
should have similar targeting preference as reflected in chromosomal
distribution patterns.
As noted previously, Dasheng has a striking distribution,
with more than one-half the elements in the family clustered in pericentromeric heterochromatin (Jiang et al., 2002).
Since the Dasheng study, there has been a tremendous
increase in the amount of rice genomic DNA in public databases. For
this reason, the distribution of both Dasheng and
RIRE2 in rice cv Nipponbare was carried out. The
distribution of these elements in complete or nearly complete
chromosomes (1, 2, 4, 6, 8, and 10) at the time of this analysis is
shown in Figure 2. It is clear from these data that the distribution of both families is remarkably consistent in
terms of clustering in pericentromeric regions.
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Figure 2.
Chromosomal distribution of Dasheng and
RIRE2 elements. Only the finished or nearly finished
chromosomes are shown. Dasheng and RIRE2
insertions are in red and green, respectively. Each insertion is
represented by a horizontal line. The position of each insertion was
based on the position of the relevant bacterial artificial
chromosome (BAC) or Pi-derived artifical chromosome (PAC) on
the genetic map (see "Materials and Methods"), as shown by
the black bars and numbers (cM) to the left of each chromosome. The
position of all centromeres (in purple) is from Harushima et al.
(1998), except the centromere of chromosome 10 (Cheng et
al., 2001).
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Similarity of Dasheng and RIRE2 Insertion
Sites
Although Dasheng and RIRE2 have similar
distribution patterns, clustering in pericentromeric regions is a
feature of other LTR retrotransposons. For example, another rice LTR
retrotransposon, RIRE8, is clustered in pericentromeric
regions (Nonomura and Kurata, 2001), as are most of the
retrotransposons in Arabidopsis (Arabidopsis Genome Initiative,
2000). To test whether the distribution of Dasheng and RIRE2 results from similarities in
their targeting mechanisms or only reflects a general feature of rice
LTR elements, the target sequences of the two elements were determined
and compared.
Analysis of 240 Dasheng and 194 RIRE2
insertion sites clearly demonstrates that neither element
inserts randomly into the chromosome and, more importantly, their
consensus insertion sites are almost identical (Tables
I and
II). Both Dasheng and
RIRE2 show an overall bias for AT-rich insertion sites (56%
and 58% AT content, respectively), which is attributable to the strong bias for A or T in a few positions (see below). More
significantly, of the 15 nucleotides including and surrounding the 5-bp
target site that is duplicated upon insertion (designated T1-T5 in
Tables I-III), 10 of 15 for
Dasheng and 11 of 15 for RIRE2 were not random (tested by
 2 test). For example, both Dasheng
and RIRE2 show a strong bias for A or T at positions  3 and
+3, whereas a strong bias against T and a strong bias against A were
observed at T1 and T5, respectively. For all positions examined, the
two elements show a similar bias except for positions 5, T1, and T2.
At these positions, RIRE2 shows a slightly stronger bias for
A or T, which could be explained by the fact that RIRE2
insertions are generally older than Dasheng (see below). In
this case, RIRE2 elements with GC-rich TSDs are more likely
to be excluded from the survey because of the frequent C to T
transition, which leads to unmatched TSD (see "Materials and
Methods").
As mentioned above, RIRE8 is a previously described rice LTR
retrotransposon (gypsy type) that localizes to
pericentromeric and centromeric regions. However, unlike
RIRE2, it is not a candidate autonomous element because
it shares no significant sequence similarity with Dasheng.
As such, although its chromosomal distribution is similar to
RIRE2 and Dasheng, it should display a different
target site consensus (Table III). In contrast to Dasheng
and RIRE2, the target sequences for RIRE8 appear
more random. No significant preference for AT- or GC-rich regions was
found (49% versus 51%). Furthermore, significant bias was observed in
only five of the 15 positions, and these sites differ from the
Dasheng/RIRE2 consensus.
Chimeric Dasheng/RIRE2 Elements
The data thus far are consistent with a scenario whereby
RIRE2 and Dasheng mRNAs are reverse transcribed
in the same VLP. The simultaneous presence of distinct but related
mRNAs in VLPs has been shown to result in the formation of chimeric
elements during reverse transcription, through a process called
template switching (Boeke et al., 1986; Jordan
and McDonald, 1999). Evidence for the simultaneous
presence of Dasheng and RIRE2 mRNAs in the same
VLP might be preserved in the genome as chimeric elements (Fig.
3).
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Figure 3.
RIRE2-Dasheng chimeric elements. The
TSD of each element is shown along with the accession number of the BAC
or PAC that contains each element. To simplify the comparison, an
insertion of an 11-kb LTR element in the Dasheng fragment in
B is shown as a vertical arrow (in green). The hatched box in D
indicates a fragment with unknown sequence identity; such a fragment is
frequently located in the 5' region of Dasheng (Jiang
et al., 2002).
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Analysis of 318 RIRE2 elements revealed four apparent
chimeras where a fragment of Dasheng is contiguous with
RIRE2 sequence (Fig. 3). It is unlikely that these chimeras
are the result of genome rearrangements because, in each case, the
RIRE2 element appears to be normal except for the presence
of Dasheng sequence. The TSDs that flank these elements
indicated that they resulted from insertion instead of recombination
(Fig. 3). Similarly, it is unlikely that these structures resulted from
the insertion of Dasheng into RIRE2 for several
reasons. First, in all cases, only a fragment of Dasheng is
present in the RIRE2 element. There are other cases in the
rice genome where a full-length Dasheng element has
apparently inserted into RIRE2. For example, a
Dasheng element, flanked by a perfect TSD, was found in
RIRE2 at 121,909 bp in BAC clone OSJNBa0016D02 (accession
no. AP004731). Furthermore, these are the only examples where a
fragment of Dasheng is found within another transposable
element. That is, the association between RIRE2 and
Dasheng sequences appears to be unique, again suggesting a
specific interaction between these two LTR element families.
Phylogenetic Relationship and Dating of Dasheng and
RIRE2 Insertions
Four Monophyletic Groups of Related Elements
Based on intraelement LTR identity of family members, it was
previously reported that Dasheng is one of the most recent
elements to amplify in the rice genome (Jiang et al.,
2002). If RIRE2 has provided the machinery necessary
for Dasheng retrotransposition, it follows that they had to
be co-expressed. For this to happen, at least some RIRE2
elements must be as young as Dasheng elements. To estimate
the age of the two element families, sequences homologous to
Dasheng and RIRE2 LTRs were retrieved and
aligned, and the alignments used to reconstruct their evolutionary
histories (see "Materials and Methods").
The resulting phylogeny has four distinct monophyletic groups (Fig.
4). One consists entirely of closely
related Dasheng sequences, whereas another consists solely
of RIRE2 sequences. Both of these groups include solo LTR
sequences as well as the LTRs of full-length elements. Between these
two groups, and basal to the Dasheng group, is an
intermediate group that has both an element with Dasheng internal sequence and an element with RIRE2 internal
sequence. Finally, there is a fourth monophyletic group of relatively
distantly related solo LTRs with similarity to both Dasheng
and RIRE2 elements. Because this group consists only of solo
LTR sequences (i.e. no family-specific internal sequences), it was not
possible to definitively classify them as either Dasheng or
RIRE2. However, this group is clearly the most divergent of
the four, and its distance from the other groups indicates that it
represents a related but unique family of elements that has become
extinct since diverging from the Dasheng-RIRE2
common ancestor.
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Figure 4.
Phylogenetic tree based on the LTR sequence of
Dasheng and RIRE2. LTR nucleotide sequences
homologous to Dasheng and RIRE2 were aligned
using the ClustalX program. Phylogenetic reconstruction used the
neighbor-joining method with Kimura-2 parameter distances implemented
in the MEGA program (see "Materials and Methods").
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Young RIRE2 Elements
Because the 5' and 3' LTRs of individual full-length
retrotransposons are identical at the time of insertion, their
divergence has been used to estimate when insertion occurred
(SanMiguel et al., 1998; Bowen and McDonald,
2001). Based on an analysis of 4 times as many elements as the
previous study, the Dasheng family still appears to be very
young. Fifty-nine of 238 full-length Dasheng elements (25%)
have identical LTRs and are estimated to have inserted within the last
150,000 years (see "Materials and Methods"). Although most
RIRE2 insertions are more ancient than full-length
Dasheng elements (data not shown), 39 of 182 full-length RIRE2 elements (21%) have identical LTRs. In addition, all
39 appear to have perfect ORFs encoding proteins for
retrotransposition. Furthermore, several putative transcripts from
Dasheng and RIRE2 (LTRs and internal regions)
were found in the expressed sequence tag database
(http://www.ncbi.nih.gov/dbEST/index.html; the
search was performed on September 27, 2002) in a variety of rice
cDNA clones, suggesting that both elements are still transcribed. More importantly, the fact that both Dasheng and RIRE2
hits were found in the same cDNA library (accession nos. AU078092 and
AU078094) suggests that they were co-expressed.
Dating the Four Monophyletic Groups
The relative time of insertion of monophyletic groups of LTR
sequences can also be determined from the level of sequence divergence. This approach relies on the estimation of a consensus sequence, which
approximates the common ancestor of the group, and comparison of extant
sequences in the group with this putative ancestral sequence. The
average divergence between the group ancestor and all of its sequences
is calibrated with the substitution rate to estimate the time elapsed
since the elements of the group last shared a common ancestor (i.e. the
age of the group). The Dasheng group, at 7.1 million years
old, is by far the youngest group (Fig.
5). This value is consistent with the
dating based on LTR comparisons of full-length elements and on the high
level of Dasheng insertion site polymorphism between rice
ssp. indica and ssp. japonica (up to 80%;
Jiang et al., 2002). In addition, the fact that
Dasheng is widespread in the Oryza genus suggests
that this family originated earlier than or around the time of
speciation, approximately 5 to 10 million years ago (Kellogg,
2001; Jiang et al., 2002). The next oldest
groups are RIRE2 and the intermediate group, respectively.
The intermediate group appears to be slightly older, but the difference
from RIRE2 is not significant (Student's t
test). Both groups are more than twice as old as the Dasheng group, indicating that they evolved before Dasheng. The
fourth group is by far the most ancient, consistent with the hypothesis that it represents a unique but extinct family of elements.
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Figure 5.
Dating the four monophyletic groups. Each groups
is shown as a triangle, where the horizontal distance is proportional
to the age and the vertical distance is proportional to the number of
sequences in the group. Support for the internal branches of the
phylogeny was assessed using 100 bootstrap replicates and the interior
branch test (see "Materials and Methods").
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A Scenario for the Origin and Spread of the Dasheng Family
The topological relationships and ages of the four
phylogenetically distinct groups of elements (Figs. 4 and 5) suggest
that there was a bifurcation early in RIRE2 evolution. One
of the resulting groups became the modern RIRE2 family,
whereas the other gave rise to the intermediate group where we
hypothesize the nonautonomous Dasheng elements originated.
This first Dasheng element may have been formed by template
switching during an aberrant retrotransposition event when heterologous
RNA templates (RIRE2 and something else) were accidentally
packaged in a single VLP. Alternatively, Dasheng may have
originated at the chromosomal level because of ectopic recombination.
Based on their low copy numbers, these ancestral Dasheng
elements appear to have been largely quiescent or otherwise unsuccessful in the genome. The RIRE2 elements of this
intermediate group also may have been doomed to extinction. At about
the same time, the ancestors of the modern RIRE2 group were
successfully amplifying in the genome. However, sometime after the
initial formation of the Dasheng retrotransposons in the
intermediate group (approximately 10-13 million years), a subset of
these nonautonomous elements became active and spread. This young and
prolific Dasheng group appears to still be active, or has
been recently active. As discussed above, it is most likely that these
active but nonautonomous Dasheng elements utilized the
enzymatic machinery of RIRE2. In support of this is the fact
that although the RIRE2 group is older than the
Dasheng group, there are still many recently transposed RIRE2 elements, suggesting it is temporally compatible for
RIRE2 products to act in trans on Dasheng transcripts.
Concluding Remarks
Several lines of evidence presented in this study indicate that
the previously described RIRE2 family of LTR
retrotransposons is the only candidate autonomous partner of the
nonautonomous Dasheng family currently in the rice genome.
By this, we mean that RIRE2 is the probable source of
enzymes for Dasheng retrotransposition, and may have been
the source of Dasheng itself. In the absence of demonstrated
activity for either family, our evidence remains circumstantial. The
identification of strains harboring active elements or establishment of
systems where the elements can be activated will ultimately facilitate
our understanding about whether and how RIRE2 serves as the
autonomous element for Dasheng.
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MATERIALS AND METHODS |
DNA Sequence Analysis
Rice (Oryza sativa) sequences used in this study
are publicly available (Nipponbare sequence) at
http://rgp.dna.affrc.go.jp. Sequence analysis (pair-wise comparisons,
multiple sequence alignments, sequence assembling, and formatting) was
performed with programs in the University of Wisconsin Genetics
Computer Group program suite (version 10.1) accessed through Research
Computing Resources (University of Georgia, Athens). The ORFs
were defined using the ORF finder at
http://www.ncbi.nlm.nih.gov/gorf/gorf.html.
Chromosomal Distribution of Dasheng and
RIRE2
Sequences used to determine chromosomal locations of
Dasheng and RIRE2 were downloaded as
described above on August 8, 2002 (360 Mb including overlaps). Based on
the frequency of detecting duplicates (same element appearing multiple
times in overlapping regions) for Dasheng and
RIRE2 elements, the redundancy of the sequence at the
time of analysis was about 25%, corresponding to about 270 Mb of
nonredundant sequence. The consensus sequence of Dasheng
and RIRE2 used for retrieving elements (with
WU-BLASTN2.0, http://blast.wustl.edu) in this study was built based on
the elements from 100 Mb of rice sequence (Jiang et al.,
2002; also see below), and the cutoff E value is e-25. For
full-length and truncated elements, Dasheng and
RIRE2 were distinguished by their internal sequence. For
solo LTRs (approximately 10%), only those falling into
Dasheng or RIRE2 groups (Fig. 4) were
considered. The positions of insertions were determined by the
chromosomal position of BACs and PACs containing the elements
(http://rgp.dna.affrc.go.jp, http://www.usricegenome.org,
http://www.gramene.org, and
http://www.genome.arizona.edu/fpc/rice/WebChrom).
Target Site Sequence of Dasheng, RIRE2, and
RIRE8
LTR hits and 20 bp of flanking sequence were
retrieved from the database. Resulting sequence files were then masked
with Dasheng and RIRE2 LTR sequence, and
the TSD and flanking sequences were recorded. The same approach is not
suitable for RIRE8 because of its long LTR
(approximately 3 kb) and high level of sequence divergence among family
members. For RIRE8, elements were randomly chosen from
RepeatMasker (Smit and Green, XXXX;
http://ftp.genome.washington.edu/RM/webrepeatmaskerhelp.html) output of rice genomic sequences, and target sequences were recorded. Only Dasheng, RIRE2, and
RIRE8 elements (solo LTRs) with identical TSDs were
considered for the determination of target sites.
Screening for Chimeric Elements
The sequence context for each element was obtained by retrieving
the element plus 10 kb of flanking sequence per end and masked with a
comprehensive database of rice repeats (Jiang and Wessler, 2001, Jiang et al., 2002). An element fragment
present in another element and not flanked by a TSD was considered a
chimeric element (see text).
Phylogenetic Analysis
LTR nucleotide sequences homologous to Dasheng
and RIRE2 were aligned using the ClustalX program
(Thompson et al., 1997) with default options. The
phylogeny of these sequences was reconstructed using the
neighbor-joining method (Saitou and Nei, 1987) with Kimura-2 parameter distances (Kimura, 1980) implemented
in the MEGA program (Kumar et al., 2001). Support for
the internal branches on the phylogeny was assessed using 100 bootstrap
replicates (Felsenstein, 1985) and the interior branch
test (Nei and Kumar, 2000).
Dating Element Insertions
Full-length elements were aged (as in SanMiguel et al.,
1998) by comparing their 5' and 3' LTRs. Kimura-2 parameter
distances (K) between 5' and 3' LTRs of individual elements were
calculated using MEGA. An average substitution rate (r) of 6.5 × 10 9 substitutions per synonymous site per year for
grasses (Gaut et al., 1996) was used for calculations.
The time (T) since element insertion was estimated using the formula:
T = K/2r. Phylogenetic groups (families) of elements were dated
(as in Kapitonov and Jurka, 1996; Costas and
Naveira, 2000) by calculating the average Kimura
2-parameter distance (K) from sequences in a group to the consensus
sequence of that group and calibrating with the average synonymous
substitution rate (r) for grasses. Fifty percent consensus sequences were determined from group-specific alignments using the EMBL
consensus sequence server
(http://www.bork.embl-heidelberg.de/Alignment/consensus.html). The age
of each group (T), or time since divergence from the group's common
ancestor, was estimated using the formula: T = K/r.
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ACKNOWLEDGMENT |
We thank Zhirong Bao (Washington University, St. Louis) for help
with DNA sequence analysis.
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FOOTNOTES |
Received September 30, 2002; returned for revision October 4, 2002; accepted October 8, 2002.
1
This study was supported by the U.S. Department
of Energy (grant to S.R.W.) and by the National Science Foundation
(grant to S.R.W.).
*
Corresponding author; e-mail sue{at}dogwood.botany.uga.edu;
fax 706-542-1805.
Article, publication date, and citation information can be found at
www.plantphysiol.org/cgi/doi/10.1104/pp.015412.
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