Rapid and Differential Proliferation of the Ty3-Gypsy LTR Retrotransposon Atlantys in the Genus Oryza
© Springer Science + Business Media, LLC 2008
Received: 16 January 2008
Accepted: 20 May 2008
Published: 15 August 2008
Here, we present the results of a comprehensive study of the distribution, evolution, heterogeneity, and phylogenetic relationships of the Ty3-Gypsy Atlantys long terminal repeat retrotransposable element family in Oryza. Atlantys element-related sequences make up a significant fraction of the genomes of species from the Officinalis complex as well as the Oryza ridleyi and O. granulata genomes. The proliferation of Atlantys elements, in many cases, took place after respective speciation events occurred. Most of the retrotranspositional events occurred within the last three million years. Atlantys is an ancient and ubiquitous component of the genus Oryza and has made significant contributions to genome size variation across the genus. Its structure is unusual when compared to other Ty3-Gypsy elements and its proliferation in the different Oryza species has been rapid and differential.
KeywordsTy3-gypsy LTR retrotransposon Oryza Officinalis complex Genome size
Repetitive sequences play significant roles in the evolution of genome architecture, gene expression, and speciation. The largest fraction of repetitive sequences in most plant genomes is composed of transposable elements  that are classified into two main major categories: class 1 RNA elements and class 2 or DNA elements, based on the kind of molecules used as intermediates in the replicative mechanism of transposition . Long terminal repeat (LTR) retrotransposons, (LTR-RTs), a particular group of class 1 elements, are ubiquitous in plants [12, 18, 45, 53]. The biology of retrotransposition, whereby identical LTRs are found at the ends of retrotransposons after transposition, makes long terminal repeat sequences ideal molecular signatures for understanding the timing of LTR-RT insertion, for understanding the mechanisms of LTR-RT elimination, and for the determining the phylogenetic relationships of LTR-RT families.
Several studies have shown that LTR-RTs are the principal components responsible for genome size expansion in the grasses, accounting for as much as 50–90% of the barley, maize, and wheat genomes [29, 35, 42, 46, 47]. The spectacular effects of retrotranspositional bursts of single LTR-RT families on the genome size variation have been recently described in Gossypium ssp., Oryza var., and Vicia pannonica [3, 17, 36, 39]. For example, both the Oryza australiensis [EE] and O. granulata [GG] diploid genomes increased by 100% and 50%, respectively, by bursts of a few LTR-RTs families in a relatively short periods of time, subsequent to speciation.
LTR-RTs can also act as potential controlling elements. Through insertion, they can inactivate or modify genes [27, 49] and can also have genome wide effects contributing to transcriptional interference by producing sense or antisense transcripts of adjacent genes . Retrotransposon activity has been reported in plants for some LTR-RTs such as Tnt1 in tobacco , BARE-1 in barley [46, 47], Tos10, Tos17, and Tos19 elements in rice  and OGRE in V. pannonica .
The genus Oryza is composed of 24 species comprising [26, 50] 10 distinct genome types (six diploid; four tetraploid) and having a 3.6-fold genome size variation. Two species are cultivated with O. sativa being the most important food crop in the world. The relevance of rice as staple food resource, its compact genome, and role as a “model” species for the genomic studies of cereals  have spawned massive research efforts that have led to the production of an extensive set of structural and functional genomics information, including two draft genomic sequences of the O. sativa subspecies indica and japonica [15, 56] as well as a high quality finished sequence of the japonica genome . We are using a whole genus approach to study the genus Oryza and have established an experimental research platform composed of 12 bacterial artificial chromosome (BAC) fingerprint/end sequence physical maps of the 10 genome types aligned to the rice reference genome sequence (www.omap.org) , as well as an unbiased set of genomic sequences derived from random sheared shotgun libraries , to address fundamental questions in plant evolution and biology. Using this platform, we previously described the discovery and analysis of several retrotranspositional bursts that have led to large increases in the genome sizes of both the EE (O. australiensis) and GG (O. granulata) genome species [3, 39]. Here, we present the results of a comprehensive study of the Ty3-Gypsy Atlantys  element in the genus Oryza. We explored the distribution, evolution, heterogeneity, and phylogenetic relationships of the Atlantys element both within and between the Oryza species using three different sets of data. First, 27 BACs representative of 11 Oryza species were used to isolate complete Atlantys elements and LTRs. Secondly, more than 72,000 random sheared sequences representative of 12 Oryza species were used in abundance estimates and phylogenetic analyses. Finally, the complete genomic sequences of both the indica and japonica subspecies of O. sativa were used to complement and validate the results on a whole genome scale.
Atlantys is ubiquitous in the genus Oryza
General Features of Oryza Atlantys Elements
O. sativa japonica
O. sativa indica
O. alta (solo-LTR)
O. australiensis (solo-LTR)
O. glaberrima (joined-LTR)
O. nivara (joined-LTR)
O. rufipogon (joined-LTR)
O. minuta (solo-LTR)
O. ridleyi (solo-LTR)
Oryza Random Sheared Library Statistics
Genome size (in MBp)
Nr. of sequences
Reads mean length
% genome sequenced
Dramatic abundance variation of Atlantys elements in the Oryza
We estimated the abundance of Atlantys elements in the Oryza in three ways. First, we determined the number of Atlantys elements (complete, truncated, and solo LTRs) in the genome sequences of both japonica and indica rice using LTRs as the query sequence in similarity searches. Only hits longer than 90% of the query length were taken into account. In the case of O. sativa ssp. indica, a total of 501 Atlantys LTRs were identified, of which 70 belonged to 35 complete elements (a complete element is constituted by the two LTRs plus the internal coding domains), 164 were part of truncated elements (because one LTR was missing and the remaining had close to its ends PBS or PPT or the integrase Ty3-Gypsy conserved domain), 182 were solo-LTR originated by intra-element recombination (all showed the canonical 5 bp long target site duplication (TSD)), and 85 LTRs were not classified because no significant signals such as PBS or PPT or TSD were found in their proximity. The latter ones could be solo-LTRs originating from inter-element unequal recombination or they could be part of highly rearranged and incomplete elements. In japonica rice, 529 complete LTRs were identified, 102 from 51 complete retroelements, 166 from truncated elements, 162 are solo-LTRs, and 99 unclassified. Considering only complete elements and solo-LTRs showing TSD, the ratio of complete elements versus solo-LTRs in indica and japonica rice was roughly 1:5 and 1:3, respectively. It should, however, be noted that the reliability of the ratio calculated in indica is questionable since the sequence used to estimate this is yet to be completed. Since the settings used in the search were extremely stringent (all the instances shorter than 90% of the query length were discarded), these figures are an underestimate of the actual amount of LTR Atlantys related sequences in O. sativa. A BlastN search collecting all the hits having significant similarity (e-value lower than 1e–10) with the Atlantys LTRs gave much higher figures—1,892 hits in O. sativa ssp. japonica and 1,945 in O. sativa ssp. indica.
Abundance of Atlantys Elements in the Oryza
Estimated LTRs copy #
We estimated the copy number of Atlantys LTR-related sequences in each of the 12 Oryza genomes using the results of BlastN searches and the method proposed by Hawkins et al. . Surprisingly, the estimated number of Atlantys LTR-related sequences in several genomes was well above 10,000 copies: O. officinalis—16,293; O. coarctata—11,500; O. granulate—18,578; O. minuta—28,055; O. australiensis—22,583, O. alta—26,466; and O. ridleyi—20,929 (Table 3). The reliability of this approach was confirmed by analyzing 10 sets of 3,000 O. sativa in silico random sheared sequences each. The 22 significant hits obtained on average, translated into 1,426 predicted instances for O. sativa japonica which is in good agreement with the 1,892 hits obtained when the complete Oryza genome, was scanned using BlastN (Table 3).
Finally, to approximate the total genomic contribution of Atlantys related sequences to the Oryza genus, we assumed that the ratio of complete elements to solo LTRs was 1:3, as previously calculated for O. sativa var. japonica (we did not use the ratio calculated for O. sativa var. indica sequence because we consider the map-based O. sativa var. japonica sequence more reliable) and that the Atlantys element and LTR sizes were 13,000 and 1,500 bp, respectively. When these assumptions are applied to the rice RefSeq, we obtained a figure of 4.99 Mb which is about 6% lower than number of bases actually masked using RepeatMasker (5.32 Mbp). Under these assumptions, we calculated that over 8.31%, 7.90%, 7.93%, 5.93%, and 7.41% of the O. alta, O. minuta, O. officinalis, O. punctata, and O. australiensis genomes are composed of Atlantys-related sequences, respectively. Furthermore, Atlantys-related elements also appeared to make up a considerable portion of the O. ridleyi and O. granulata genomes, approximately 66.3 Mbp and 58.8 Mbp, respectively (Table 3).
Combined, these results suggest that the Atlantys transposable element family is significantly responsible for genome size increase in many of the Oryza genomes studied in this work and especially in those belonging to the Officinalis complex.
Phylogenetic relationships and variability of Atlantys in the Oryza
Atlantys Reverse Transcriptase Genetic Variability in the Oryza
Solo-LTRs, timing of Atlantys retrotransposition, and removal through unequal homologous recombination
Furthermore, it should be noted that many of the BACs used to identify Atlantys elements from the wild relatives of rice also contained solo LTRs (e.g., O. alta, O. minuta, O. australiensis, and O. ridleyi). Although the sample is limited, the presence of solo LTRs provides additional evidence that removal of complete Atlantys elements by unequal homologous recombination was active in other Oryza species.
Distribution of the Insertion Time of Atlantys Elements in Both Japonica and Indica Rice
The analysis of 12 random sheared genomic libraries representative of 12 Oryza species and 10 distinct genome types enabled us to gain important insights into the distribution and the evolutionary history of what appears to be one of the most significant genomic components of many Oryza genomes—the Ty3-Gypsy element Atlantys. This element was found to be ubiquitous in the Oryza which is not surprising since the ubiquity of LTR retrotransposons in the entire plant kingdom has been well established and the presence of the same family could easily cross the genus divide. For example, Atlantys-like elements have also been found in A. thaliana and Lotus corniculatus . More interesting, however, is that Atlantys accumulated differentially across the Oryza. Although differential accumulation of LTR-RTs families has already been demonstrated in the Oryza, for Wallabi  and Gran3  in O. australiensis and in O. granulata, respectively, Atlantys has attained extremely elevated copy number levels in several species but especially in the “Officinalis complex”  where it represents a significant fraction of these genomes: 8.31%, 7.90%, 7.93%, 5.93%, and 7.41% of the O. alta [CCDD], O. minuta [BBCC], O. officinalis [CC], O. punctata [BB], and O. australiensis [EE] genomes, respectively.
We demonstrated through phylogenetic and comparative approaches that the Atlantys element has proliferated rapidly in various Oryza genomes. In many cases, its copy number increase postdates speciation events (e.g., O. alta, O. australiensis, O. granulata, O. ridleyi, O. coarctata). Interesting insights into Atlantys proliferation dynamics were provided by the analysis of the polyploids O. minuta [BBCC] and O. alta [CCDD] and their diploid counterparts (O. punctata [BB] and O. officinalis [CC]). In O. alta, Atlantys proliferation events postdated its speciation thereby constituting an example of retrotransposition activation that could have been induced by “genomic shock”  during polyploidization. Some studies have indicated that O. australiensis [EE] is the closest living relative of the CCDD genome species; in particular, the E genome has been proposed as being related to the DD subgenome suggesting that an E genome ancestor may have played a role in the formation of CCDD tetraploids [4, 13, 54]. The Atlantys phylogenetic analysis does not support such a view but it is consistent with a different one which rules out the E genome as direct donor of O. alta . However, it should be noted that our study focused on the phylogenetic history of the retrotransposon Atlantys and not on that of its hosts. Indeed, the lack of clustering of Atlantys copies of O. australiensis and O. alta could simply reflect the effects of the recent (postspeciation) retrotranspositional burst that occurred in the polyploid O. alta without any implication in host species phylogenetic relationships. In the polyploid, O. minuta, the complement of Atlantys retroelements seems to have been inherited from the two diploid counterparts (O. punctata and O. officinalis) or, at least, there is no evidence of any postspeciation burst. The rapidity of these events is also supported by insertion date estimates performed on complete Atlantys elements isolated from various Oryza hosts where we found that the vast majority of the events detected took place in a time frame of less than 3 million years. However, we should not discount the effects of a bias toward younger elements due to our strategy of mainly relying on similarity searches used to isolate the Atlantys-like sequences and the uncertainty that is inherent with the mutation rate we used.
The mechanisms underlying the differential accumulation of Atlantys elements throughout the genus Oryza remain to be determined but are likely to have been affected by numerous factors including the effects from different genomic environments as well as different ecological conditions. Since the Atlantys element is ancient but its retrotranspositional history is recent in the Oryza, it is possible to speculate as to whether differential accumulation of Atlantys was the result of differential rates of transposition rather than different effectiveness of element removal or the combined results of the two forces. One of the possible removal mechanisms, i.e., unequal homologous recombination  was shown to have been active for Atlantys in almost all the species considered here, and at least in the case of O. sativa, it was contemporary to the retrotranspositional events. In both O. sativa subspecies, a large number of truncated incomplete elements were found suggesting the parallel action of illegitimate recombination  along with unequal homologous recombination in removing Atlantys elements.
Even if the Atlantys-like element structure is retained throughout the Oryza, not surprisingly their LTR sequences are quite divergent. Such evidence, coupled with the high copy number of this element, makes Atlantys LTRs promising candidates for the design of species-specific (or at least genome type-specific) probes. Indeed, some of the most repeated species-specific probes already isolated in Oryza genomes are, as a matter of fact, tracts of the Atlantys LTRs. This is the case for the HindIII repetitive element pOD3 isolated in O. latifolia [CCDD]  that shares significant similarity with Atlantys LTRs isolated in our analysis from O. alta [CCDD] (more than 77% over 1,790 bp). Interestingly, no traces of this sequence could be found in the CC genomes of O. officinalis [CC] or O. minuta [BBCC] suggesting that the pOD3 repeat is DD subgenome specific or that it proliferated only in the CCDD polyploid genomes, as our phylogenetic analysis and nucleotide diversity estimates suggest. Another genome specific example is that of probe pBO03  which is part of the Atlantys-like element LTR from O. officinalis [CC]. In this case, the authors estimated a copy number for this sequence to be around 30,000 copies assuming (wrongly) that the O. officinalis genome size was about 900 Mbp. If the correct size (651 Mbp) is used, the estimated copy number should be ∼21,700 which is in good agreement with the 16,293 figure we obtained in silico. In both cases, the authors were not able to identify these sequences as part of an LTR retroelement.
A third ORF is retained in all Atlantys elements isolated from the Oryza species. The third ORF follows the gag_pol gene but is situated on the opposite strand. This configuration eliminates the possibility that it is an envelope-like gene (in this case, it should have found in the same strand of gag_pol gene). A similar opposite strand ORF feature was found in the recently described LTR retroelement REM-1 . The third ORF conservation in the Atlantys-like elements isolated in very different hosts strongly suggests that it has been selectively maintained. Although few clues are available about the function of this third ORF (it is similar to a putative AA-transferase), it is tempting to speculate about its possible role in making Atlantys one of the most important players in Oryza genomes size variation by contributing to its retrotranspositional success.
According to the model proposed by Charlesworth , genetic divergence of RTs should be correlated with an element’s abundance in a genome. This was not the case for the Atlantys RTs as in the case of O. alta were the copy number is elevated but the nucleotide variability is not. This discrepancy could be explained in the light of phylogenetic evidence that suggest a recent burst of Atlantys retrotransposition in this species subsequent to speciation. If the O. alta case is excluded, a clear relationship exists between nucleotide diversity values and polyploidy. Nucleotide diversity exhibited its highest values in polyploids which could be expected considering the contribution of at least two distinct subpopulations of Atlantys-like elements to these genomes. Finally, the interspecies diversity is higher than any of the intraspecies values once again pointing towards a recent time frame of retrotranspositional events.
Sequence variation was studied in depth in Atlantys element LTRs in both the indica and japonica subspecies of O. sativa. We observed a significant amount of nucleotide variation across the LTRs suggesting that there are different levels of selective pressures on these sequences, which is similar to what has been demonstrated for the LTRs of BARE-1  in barley. In particular, we found a sharp decrease of nucleotide diversity in close proximity to most of the putative TATA boxes identified in silico. One sequence was highly conserved in all the Atlantys-like elements throughout the genus Oryza and is therefore considered a strong candidate for a TATA box.
Materials and methods
Random sheared libraries
Random sheared libraries were constructed as previously described .
O. sativa whole genome sequences
In our analyses, we used the version 3 of the IRGSP O. sativa var. japonica sequence (accession numbers AP008207 to AP008218) and the Beijing Institute of Genomics O. sativa var. indica sequence (accession numbers CM000126.1 to CM000137.1)
Putative Atlantys LTRs reconstruction
For those species in which it was not possible to identify any complete Atlantys LTRs in the BAC sequences, the corresponding random sheared sequences were searched using BlastN and the complete Atlantys LTR of the closest species as query. The significant similar tracts identified were then aligned and joined to construct the putative Atlantys LTR.
Similarity searches using Atlantys LTRs as queries were carried out using the BlastN algorithm  run under relaxed settings (−q −2 −r 3) in order to accommodate for divergence between species. Only hits having an e value equal or lower to 1e–10 were used. The equation proposed by Hawkins et al.  was used to estimate the number of significantly similar hits present in the entire genome of each of the 12 Oryza species: , where “Xobs” is the observed number of copies, N is the total number of sequence reads, n is number of targets in the genome, L is length of target sequence, m is estimated minimum length required to identify a sequence in a BLAST search (the extremely conservative value of 100 bp was used), e is number of bp sequenced from each insert and G is genome size. Cluster analysis was performed using “blastclust” (ftp://ftp.ncbi.nih.gov/blast/documents/blastclust.html) with the following settings, L 0.98 S 97, meaning that all the LTR 300 bp tracts sharing at least 97% similarity over at least 98% of their length were included in the same cluster. BlastN search results were complemented and confirmed using RepeatMasker (www.repeatmasker.org) run under default settings.
Isolation of first 5′ 300 nucleotides of LTR sequences
The first 300 bp of the 5′ Atlantys LTRs isolated in BACs were used to search the random sheared sequences. All the positive hits spanning at least 90% of the query length (270 out of 300 bp) were extracted and used in phylogenetic analyses.
All alignments were carried out using the program “MUSCLE”  run under default settings. Neighbor-joining trees were produced and edited using the program MEGA (version 3) . Nucleotide distances were calculated using the program DNAsp  and the program “Distmat” included in EMBOSS package . All sequence editing was performed using the appropriate programs from the EMBOSS package.
Search for putative TATA boxes
- O. rufipogon :
four BACs were sequenced from the individual with the accession ID #IRGC 105491 for a total of 545,208 bp
- O. glaberrima :
two BACs from accession ID #IRGC 96717; total bp of 268,621
- O. nivara :
two BACs from accession ID #IRGC 100897; total bp of 382,790
- O. punctata :
two BACs from accession ID #IRGC 105690; total bp of 295,593
- O. officinalis :
two BACs from accession ID #IRGC 100896; total bp of 273,319
- O. minuta :
two BACs from accession ID #IRGC 101141; total bp of 257,921
- O. alta :
two BACs from accession ID #IRGC 105143; total bp of 362,466
- O. australiensis :
three BACs from accession ID #IRGC 100882; total bp of 423,968
- O. ridley :
two BACs from accession ID #IRGC 100821; total bp of 352,702
- O. coarctata :
two BACs from accession ID #IRGC 104502; total bp of 360,876
- O. granulata :
four BACs from accession ID #IRGC 102118; total bp of 619,459
Random Sheared libraries: EI028463–EI035999 (O. alta), EI36000–EI043358 (O. australiensis), EI043359–EI046735 (O. brachyantha), EI46736–EI56259 (O. coarctata), EI056260–EI59753 (O. glaberrima), EI059754–EI066441 (O. granulata), EI066442–EI075900 (O. minuta), EI-075901–EI079003 (O. nivara), EI079004–EI083851 (O. officinalis), EI083852–EI86995 (O. punctata), EI086996–EI098086 (O. ridleyi), EI098087–EI100641 (O. rufipogon).
O. alta complete “Atlantys” element: EU257654
O. granulata compete “Atlantys” element: EU257655
O. officinalis truncated “Atlantys” element: EU257656
O. punctata complete “Atlantys” element: EU257657
O. minuta solo “Atlantys” LTR: EU257658
O. glaberrima joined “Atlantys” LTR: EU257659
O. nivara joined “Atlantys” LTR: EU257660
O. rufipogon joined “Atlantys” LTR: EU257661
O. alta solo “Atlantys” LTR: EU257662
O. australiensis solo “Atlantys” LTR: EU257663
O. ridleyi solo “Atlantys” LTR: EU257664
O. sativa var. Japonica complete “Atlantys” element: AP008212.1 from 17105002 to 17118729
O. sativa var. indica complete “Atlantys” element: CM000136 from 18570076 to 18583547
This work was funded by the NSF Plant Genome Program award #DBI-0321678 and the Bud Antle Endowed Chair to RAW. We also thank the AGI technical staff that supported this project, especially members of the BAC/EST Resource, Sequencing, and Bioinformatics Centers.
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