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Plant Physiol. Dec 2002; 130(4): 1697–1705.
PMCID: PMC166684

Dasheng and RIRE2. A Nonautonomous Long Terminal Repeat Element and Its Putative Autonomous Partner in the Rice Genome1

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.

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. Fig.1),1), which are necessary for the initiation of the synthesis of element DNA from the RNA intermediate (Boeke and Corces, 1989).

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. ...

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).

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. Fig.1B).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. (Fig.1C).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. (Fig.1),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 Figure2.2. It is clear from these data that the distribution of both families is remarkably consistent in terms of clustering in pericentromeric regions.

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 ...

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 (TablesII and andII).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 TablesIIIII), 10 of 15 for Dasheng and 11 of 15 for RIRE2 were not random (tested by χ2 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”).

Table I
The target sequences of 240 Dasheng elementsa
Table II
The target sequences of 194 RIRE2 elementsa
Table III
The target sequences of 120 RIRE8 elementsa

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. (Fig.3).3).

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 ...

Analysis of 318 RIRE2 elements revealed four apparent chimeras where a fragment of Dasheng is contiguous with RIRE2 sequence (Fig. (Fig.3).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. (Fig.3).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. (Fig.4).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.

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 ...

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. (Fig.5).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.

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 ...

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. (Figs.44 and and5)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.

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. (Fig.4)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.

ACKNOWLEDGMENT

We thank Zhirong Bao (Washington University, St. Louis) for help with DNA sequence analysis.

Footnotes

1This 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.).

Article, publication date, and citation information can be found at www.plantphysiol.org/cgi/doi/10.1104/pp.015412.

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