© 2006 Society of Systematic Biologists
Short Interspersed Elements (SINEs) in Plants: Origin, Classification, and Use as Phylogenetic Markers
Edited by Andrew Shedlock: Associate Editor
1 CNRS UMR6547, GDR2157 Biomove, Université Blaise Pascal 24 Avenue des Landais, 63177, Aubière, France E-mail: j-marc.deragon{at}univ-bpclermont.fr
2 Department of Molecular, Cell, and Developmental Biology, University of California Los Angeles, California, 90095-1606, USA
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Short interspersed elements (SINEs) are a class of dispersed mobile sequences that use RNA as an intermediate in an amplification process called retroposition. The presence-absence of a SINE at a given locus has been used as a meaningful classification criterion to evaluate phylogenetic relations among species. We review here recent developments in the characterisation of plant SINEs and their use as molecular makers to retrace phylogenetic relations among wild and cultivated Oryza and Brassica species. In Brassicaceae, further use of SINE markers is limited by our partial knowledge of endogenous SINE families (their origin and evolution histories) and by the absence of a clear classification. To solve this problem, phylogenetic relations among all known Brassicaceae SINEs were analyzed and a new classification, grouping SINEs in 15 different families, is proposed. The relative age and size of each Brassicaceae SINE family was evaluated and new phylogenetically supported subfamilies were described. We also present evidence suggesting that new potentially active SINEs recently emerged in Brassica oleracea from the shuffling of preexisting SINE portions. Finally, the comparative evolution history of SINE families present in Arabidopsis thaliana and Brassica oleracea revealed that SINEs were in general more active in the Brassica lineage. The importance of these new data for the use of Brassicaceae SINEs as molecular markers in future applications is discussed.
Keywords: Arabidopsis; Brassica; molecular markers; retroposon; retrotransposon; rice; SINE; transposable element; transposon
Received January 18, 2006; Revised March 28, 2006; Accepted April 16, 2006
Transposable elements (TEs) are defined as DNA sequences able to move from one genomic position to another in a replicative or nonreplicative process (Capy et al., 1998). In denaturation-reassociation experiments, they represent a large part of the middle repetitive fraction of most eukaryotic genomes. SINEs are nonautonomous retroelements that use the enzymatic machinery of autonomous LINEs (long interspersed elements) to retropose (Boeke, 1997; Dewannieux et al., 2003; Kajikawa and Okada, 2002). SINEs are 80 to 500 base pairs long and their genomic copy number usually ranges from a few hundreds to more than a million copies for the human Alu family (Jurka, 1995; Okada and Ohshima, 1995). In Primates, the dominant SINEs are ancestrally related to 7SL RNA, whereas, for other eukaryotes, SINEs derived from tRNAs (or more exceptionally from 5S RNAs) are dominant (Jurka, 1995; Kapitonov and Jurka, 2003). SINEs derived from tRNAs usually have a composite structure made of a 5' tRNA-related portion followed by a tRNA-unrelated portion (Okada and Ohshima, 1995). In all cases, an internal promoter (composed of A and B boxes and recognized by the RNA polymerase III machinery (Arnaud et al., 2001) is present in the SINE tRNA-related portion. New SINE insertions occur without the loss of the donor element and because these insertions are essentially irreversible, the presence or absence of a SINE at a given locus is an information that can be used to design polymorphic molecular markers (reviewed in (Cook and Tristem, 1997; Shedlock and Okada, 2000). A major advantage of this type of marker is that the probability of independent insertions at the same exact chromosomal site or exact deletions are virtually nil so that all organisms carrying a particular SINE insertion are derived from a unique event that happened in their common ancestor. Also, SINE markers are well suited to detect unambiguously gene flow between closely related species.
A relatively small number of plant SINE families have been described to date because, until recently, plant genomic data sequence were scarce, and due to their low level of natural retroposition and their small size making SINE insertion less deleterious compared to larger element, they were rarely trapped inactivating a key cellular gene. SINEs are also very short, and have no conserved coding sequence, making their research by molecular hybridizations very difficult. Despite these difficulties, SINEs have been identified in many plant families including Gramineae, Commelinaceae, Rosaceae, Solanaceae, Fabaceae, and Brassicaceae (Borodulina and Kramerov, 1999; Deragon et al., 1994; Umeda et al., 1991; Yasui, 2001; Yoshioka et al., 1993). All plant SINEs share key characteristics, including a tRNA origin, an internal polymerase III promoter (made of A and B boxes) in their 5' tRNA-related region, a tRNA-unrelated region of variable length, a short strech of T or A at their 3'-end, and the presence of flanking direct repeats. Plant SINEs are mainly dispersed randomly in genomes although they are rarely present in heterochromatic, pericentromeric regions, and have a preference for gene-rich regions. Many SINE families have been amplified recently leading to insertional polymorphism between closely related taxa a desirable trait for a molecular genetic marker.
The first SINE described in plants, p-SINE1, was found in the Oryza sativa (rice) Waxy gene (Umeda et al., 1991). All species in the Oryza genus can be classified into six diploid genome type (AA, BB, CC, EE, FF, and GG) and four tetraploid genome types (BBCC, CCDD, HHJJ, and HHKK). P-SINE1, and closely related p-SINE2 elements, are present in all species of the Oryza genus, whereas the distribution of the "youngest" p-SINE3 family is limited to the subgroup of Oryza diploid species composed of the AA genome (Xu et al., 2005b). Consensus sequences of the three p-SINE elements from rice are between 122 and 127 base pair (bp) long and the copy number of p-SINE1 in rice is estimated to be 6500 per haploid genome (Motohashi, 1997). Almost all members of the three SINE families are flanked by 9 to 20-bp direct repeats and end with a short poly(T) repeats (Xu et al., 2005b). Several other rice sequences, annotated as SINEs, have been recently deposited in REPBASE (Jurka et al., 2005) and it is therefore likely that many other rice SINE families remain to be characterized.
The TS SINE family have been found in the genome of several Solanaceae species = Nicotiana tabacum (tobacco) (Yoshioka et al., 1993), Capsicum annuum (bell pepper), Lycopersicon esculentum (tomato), and Solanum tuberosum (potato) (Pozueta-Romero et al., 1998) and in one Convolvulaceae species, Pharbitis nil (morning glory) (Yoshioka et al., 1993). The copy number of TS element in tobacco is estimated to be 5 x 104 per haploid genome. Most TS elements are around 200 bp, end with a TTG repeat of variable length, and are flanked by short direct repeats. The TS family can be divided into two major subfamily (TSa and TSb) of different evolutionary ages, TSa being the youngest (Yoshioka et al., 1993).
The AU SINE family shows the broadest distribution in plants, with related elements being found in Gramineae (Aegilops umbellulata, Zea mays, Triticum aestivum), in Fabaceae (Medicago truncatula, Lotus japonicus, Glycine max), and in Solanaceae (N. tabacum, L. esculentum) species (Yasui, 2001). AU SINEs are between 170 and 200 bp long. The highest copy number is found in A. umbellulata and T. aestivum (around 1 x 104 copies) where the element underwent a recent explosive increase in its copy number (Yasui, 2001). Copy number is much lower in other plant species (around 100 copies), and the elements are more degenerated suggesting that AU SINEs did not amplify recently in these lineages.
The first Brassicaceae SINE family (called S1; Deragon et al., 1994) was identified in Brassica napus (oilseed rape), an amphidiploid species (AACC) that recently emerged from the fusion of two diploid species genomes, Brassica oleracea (CC) and Brassica rapa (AA) (Lenoir et al., 1997). S1 was latter found to be present in all species of the Brassiceae tribe. In a recent work, we characterized three new SINE families, called RathE1, RathE2, and RathE3, (RathE3 and RathE1 are also called Atsn1 and Atsn2, respectively; Myouga et al., 2001), two of which are shared between A. thaliana and B. oleracea (Lenoir et al., 2005). At about the same time, 15 new SINE populations from B. oleracea (called BoS) were discovered (Zhang and Wessler, 2005), but without a global phylogenetic analysis, the placement of these SINEs in a single family was arbitrary. A general description of Brassicaceae SINE families is presented below (see Table 1). The size of Brassicaceae consensus SINE sequences are highly variable (due the variation in length of the tRNA-unrelated portion) and in opposition to other plant SINEs, they end with a perfect poly(A) region.
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SINE families are also likely to be present in Funkia ovata (a moss) and Fagopyrum tataricum (buckwheat) because PCR products of expected sizes were obtained using corresponding genomic DNA and SINE-specific primers (Borodulina and Kramerov, 1999). The current distribution of known SINE families suggests that SINEs are ubiquitous in plants and that the number of characterized plant SINE families will increase with the number of sequenced plant genomes.
Despite the presence of SINE families in plant species of prime agricultural importance (rice, wheat, potato, tobacco, tomato, bean, oilseed rape, cabbages, etc.), plant SINEs are largely unexploited as a source of highly informative molecular markers. The rice p-SINE1 and the Brassicaceae S1 (now SB1, see the classification below) are the two single SINE families that have been used to derive molecular markers. In two complementary studies, the polyphyletic origin of cultivated rice was inferred from the interspersion pattern of p-SINE1 element (Cheng et al., 2003; Ohtsubo, 2004). Cultivated Oryza sativa has five wild relatives that belong to the Oryza genus with the AA genome. Of these, Oryza rufipogon is the species closest to the Asian cultivated O. sativa and is generally thought to be its progenitor. Based on the presence-absence of p-SINE1 copies in 101 cultivated and wild rice strains, these studies showed that two different groups of O. rufipogon are at the origin of the two strain of Asian cultivated rice (indica and japonica) and confirmed the polyphyletical origin of Asian cultivated rice from O. rufipogon. In another study, p-SINE1 elements were also used to propose that cultivated African rice (Oryza glaberrina) is most closely related to another wild rice species, Oryza barthii (Cheng, 2002). In the same study, a phylogenetic analysis based on the p-SINE1 insertion patterns showed that the five wild rice species with the AA genome form a distinct cluster and that one of them Oryza longistaminata (a wild African species) is most closely related to the hypothetical ancestor. These results suggest that the Oryza genus with AA genome have originated in Africa, rather than in Asia. Finally, p-SINE1 elements were also used to confirm that Oryzameridionalis is a distinct species from Oryza rufipogon (Xu et al., 2005a).
The insertion of Brassicaceae S1 (SB1) SINEs has also been used as a classification criteria to study relations among wild Brassicaceae species that belongs to the Brassica oleracea cytodeme (Tatout et al., 1999). In this study, the microsatellite-like variation of the SINE 3' poly(A) region was also used as a complementary classification criterion to obtain internal resolution in the different clades. This study allowed for the first time to retrace the origin of several wild species. For example, Brassica drepanensis was proposed as a species that recently emerged for a Brassica incana/Brassica villosa hybrid (with B. villosa as the maternal parent) following backcrosses to B. incana. The study also allowed the characterization of several introgressions, confirming that these highly related species are capable of genetic exchange in their natural habitat. Finally, S1 (SB1) elements were also used to propose a polyphetic origin for cultivated Brassica oleracea, with important contributions from several Mediterranean wild species (J.M. Deragon, unpublished results). In another study, S1 (SB1) SINE markers were generated to help in evaluating the risk of transgene flow from a cultivated species (Brassica napus) to natural populations of a closely related species (Raphanus raphanistrum) (Prieto et al., 2005). To assess the long-term stabilization of crop genes within the genome of weedy relatives, natural populations need to be screened for introgressed crop genes. However, this is barely feasible because of the difficulty in identifying unambiguously crop-specific markers. This is particularly the case when the crop and its weedy relatives share a close common ancestor and display high levels of intraspecific diversity like for B. napus and R. raphanistrum. Forty-seven SINE markers distributed on all of the C genome linkage groups and distinguishing unambiguously the two species were produced and should be utilized to trace the occurrence and frequency of introgressions of B. napus C genomic region within wild R. raphanistrum populations. SINEs specific for the A genome will be characterized to complete this new collection of markers.
Despite these examples, Brassicaceae SINEs are largely underexploited as markers. This is in part due to the incomplete description of SINEs in this plant family and to an arbitrary classification of described elements. In this work, phylogenetic relations among all Brassicaceae SINEs were evaluated and a new classification, grouping SINEs in 15 different families, including 3 new ones is proposed. We also present data on their origin and evolution history and discuss their use as phylogenetic markers.
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Database Searches
Computer-assisted searches to identify new SINE elements were performed using the Blast program against the TAIR A. thaliana and B. oleracea genome databases (http://www.arabidopsis.org/Blast) with default parameters. A small number of additional SINEs could also be found by searching B. oleracea trace data (http://www.ncbi.nlm.nih.gov/blast/mmtrace.shtml). The tRNA-related and tRNA-unrelated portions of known SINE consensus sequences were used separately for the initial Blast searches. Significant hits with one SINE portion, but not with the other, were analyzed further using a second Blast search and sequences corresponding to known SINE families were discarded. The definition of a new SINE element was based on several criteria, including the presence of internal A and B boxes, 3' A-rich region, flanking target site duplications (TSDs), and the repetitiveness of the sequence in the genome.
Phylogenetic Analysis
Sequences were aligned using the ClustalX software (available at ftp://ftp-igbmc.u-strasbg.fr/pub/ClustalX). All phylogenies were inferred using the Bayesian method provided in the MrBayes 3 software (Ronquist and Huelsenbeck, 2003). To evaluate genetic distances, we used the general time-reversible (GTR) model with gamma-distributed rate variation across sites and a proportion of invariable sites. Analyses were run for a variable number of generations until the standard deviation of split frequencies dropped below 0.05 (for the SB5 and SB6 analysis, the temperature parameter was decreased to 0.1 to facilitate chain convergence). The cladogram obtained is a consensus that includes the posterior probability for each node.
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Description of New SINE Families and Subfamilies in Brassicaceae
The complete sequencing of the Arabidopsis thaliana genome and the partial sequencing of the Brassica oleracea genome provided opportunities to identify new SINE families in Brassicaceae. A. thaliana and B. oleracea diverged from a common ancestor 16 to 19 million years ago, and because the age of the Brassicaceae family is evaluated to be at most 20 millions years (concomitant with the formation of the Mediterranean region; Muller, 1984; Oosterbroek, 1992), these two species diverged early during the evolution of this plant family. Therefore, a SINE family shared by A. thaliana and B. oleracea is likely to be present in most if not all Brassicaceae species. In view of the high diversity of SINE families and subfamilies in Brassicaceae, we needed to adopt a more systematic and meaningful classification. All SINE copies presenting significant sequence identities over their entire length were grouped in an independent family. Phylogenetic analyses were systematically performed for each family to identify subfamily organizations (Deragon et al., 1994; Lenoir et al., 2005) (Fig. 1 and data not shown). Well-supported clusters were used to define the different subfamilies. In each case, majority-rule consensus sequences were constructed (either a general consensus when no subfamily organization was detected, or several subfamily consensus if clear subfamilies were identified, see Appendix 1 at http://systematicbiology.org for the sequence of each consensus). Family or subfamily consensus are used to approximate the "founder" sequence: the SINE element, active in retroposition, that is responsible for a given burst of SINE amplification (Jurka, 1998). Therefore, the mean genetic distance from consensus is used to approximate the relative age of the amplification burst (Jurka, 1998), and assuming that the rate of evolution is approximately clock-like, the lower the genetic distance is, the "younger" is the burst. These consensus sequences are also very useful to search for new members of a given SINE family and to evaluate the total copy number in a given species. We suggest naming all SINE families from Brassicaceae, "SB," followed by a number. To indicate a particular species of origin, initials of the species can be added in front of the name (AtSB6 and BoSB6 being the SB6 family of Arabidopsisthaliana and Brassicaoleracea, respectively), whereas a subfamily is indicated by a terminal letter (BoSB6A being the subfamily "A" of BoSB6). In Table 1, the new and former names (when applicable) of families and subfamilies are indicated. The organization of the former BoS family has been largely modified, as many of the BoS previous "subfamilies" could be fused together to form new families (BoS a, ab, b, and ai into SB5; BoS c and f into SB9; BoS d and e into SB10; and BoS j and k into SB14), whereas others are really distinct families (BoS i1 is SB12 and BoS i2 is SB13).
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The copy number for each SINE family was determined for A. thaliana and estimated for B. oleracea (because only 20% of the sequence is available in the B. oleracea database, see Table 1). For A. thaliana, 308 SINE elements, distributed in six different families (AtSB2 to AtSB7), were detected, representing 0.05% of the genome. The largest family is AtSB2 with 144 members, whereas the smallest family is AtSB7 with only 3 members. For B. oleracea, the estimated copy number for SINE is 4290, representing 0.16% of the genome. All SINE families are present in B. oleracea, with the exception of SB4; the largest family is BoSB6 (735 members distributed in five different subfamilies) and the smallest BoSB15 (with 40 members). Based on the average distance to consensus (see Table 1), the youngest burst of SINE amplification in A. thaliana produced the AtSB5 family. This is surprising because this family has only seven members, but several of those are very close to each other (see Fig. 1A) and to the consensus, suggesting a recent, but very limited, burst of amplification for these SINEs in A. thaliana. The AtSB2, AtSB3, and AtSB6 families also possess several closely related SINE copies, suggesting that these families may still be active today in A. thaliana (Deragon et al., 1994; Lenoir et al., 2005) and Fig. 1B). In B. oleracea, the youngest burst of SINE amplification generated the BoSB1A subfamily (formerly S1Ea). The founder genomic copy involved in this burst of SINE amplification (called na7) have been characterized in detail and found to be expressed in vivo (Arnaud et al., 2001) and to generate a putative retroposition intermediate (Pelissier et al., 2004). Many B. oleracea SINE families and subfamilies have a low mean genetic distance to consensus (see BoSB1, BoSB5, BoSB7A, BoSB9, BoSB10A, BoSB13, BoSB14A; Table 1), suggesting that, in general, SINE amplification is more dynamic in B. oleracea compared to A. thaliana.
The size of the different consensus SINE sequences is quite variable, the smallest SINE being less than 100 base pairs long (BoSB8A: 95 base pairs), whereas the largest being more than 350 base pairs (BoSB7B: 353 base pairs). It is possible that SINE families with large elements (SB3, SB6, and SB7) are composed of "dimeric" elements that resulted from the fusion of two "monomeric" copies. Dimerization of tRNA-derived SINEs have been reported for different SINE families including for the flying lemur CYN elements (Schmitz and Zischler, 2003) and the Twin SINEs from Culex pipiens (Feschotte et al., 2001). For BoSB3 and AtSB3, this scenario is supported by the observation of slightly degenerated A and B boxes in "the right monomer" of the element (Lenoir et al., 2005). However, for SB6 and SB7, we were unable to observe relics of these motifs and whether these elements are long monomeric or dimeric SINEs remains unknown.
Origin of the Different SINE Families in A. thaliana and B. oleracea
All Brassicaceae SINE consensus sequences possess a potentially active internal promoter, composed of A and B boxes, responding to the RNA polymerase III machinery. Based on the structure of this promoter, the ancestral origin of Brassicaceae SINEs is likely to be one or several tRNA sequences. However, using the different SINE consensus sequences, we were not able to retrace unambiguously which tRNA(s) was at the origin of the different SINE families, suggesting that the original event, where one (or several) tRNA was turned into a SINE element, is likely to be an old one. Most tRNA-derived SINEs can be separated in tRNA-related and tRNA-unrelated portions. The tRNA-related portion is defined from position one of the element to 14 nucleotides after the end of the B box (the usual end of a tRNA molecule), whereas the tRNA-unrelated portion is the rest of the sequence. We observed that different SINE consensus sequences shared primary sequence homologies in their tRNA-related portions but not in their tRNA-unrelated portions, suggesting that tRNA-related portions can be "shuffled" and fused to "new" tRNA-unrelated portions to generate different SINEs. To test this possibility, we constructed a phylogenetic tree using only the tRNA-related portion of the different family and subfamily consensus sequences (Fig. 2). We observed three relatively well supported clusters (boxes in Fig. 2), suggesting that SINE tRNA-related portions can be grouped in three "superfamilies." In two of these three "super-families," recent shuffling events can be identified (arrows in Fig. 2). For example, although BoSB6 and BoSB7 families have similar tRNA-related portions, this region is almost identical between BoSB6D and BoSB7A, suggesting a recent transfer (see Fig. 2). This shuffling event maybe in relation with the recent burst of amplification of the BoSB7A subfamily, which is much younger than the BoSB7B subfamily (see Table 1). In this scenario, a fusion between the BoSB6D tRNA-related region and a BoSB7 tRNA-unrelated region generated a new founder element responsible for the BoSB7A subfamily. The fact that the BoSB6D subfamily is significantly older than the BoSB7A subfamily is compatible with the directionality of the exchange proposed in this scenario (BoSB6D giving its tRNA-related portion to BoSB7A and not the opposite). A similar scenario is possible for the "young" BoSB9A founder element, with the acquisition of a new tRNA-related portion from BoSB10A (Fig. 2). These data suggest that, inside "superfamilies," the shuffling of tRNA-related portions can result in new SINE amplifications. tRNA-unrelated portion from different SINE families are completely different and therefore cannot be aligned, with a single exception; the BoSB5D and BoSB13 tRNA-unrelated portions that share 97% sequence identities. In fact, the BoSB13 founder copy was apparently generated by the acquisition of the BoSB12 tRNA-related portion and the BosB5D tRNA-unrelated portion (Fig. 2). The mechanism responsible for these shuffling events is unknown but could well involve template switching during reverse transcription, a process already described for retroposons (Brosius, 1999).
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Comparative Evolution History of SINE Families Shared by A. thaliana and B. oleracea
We have shown recently that the amplification success of two SINE families present in A. thaliana and B. oleracea can be very different. We observed that BoSB3 was much more active compared to AtSB3 but that the opposite was true for the SB2 family (Lenoir et al., 2005). In this previous work, a subfamily organization could not be inferred from the phylogenies, suggesting that a single founder element was responsible, in each species, for the retroposition activity of SB2 and SB3. Here we compare the evolution history of SB5, SB6, and SB7, the three other SINE families shared between the two species (Fig. 1). The three phylogenies show a clear subfamilies organization for B. oleracea elements, with several well-supported clusters corresponding to the different bursts of SINE amplification depending on different founder copies. In contrast, for A. thaliana elements, a single cluster was obtained in all three cases, suggesting a single burst of amplification. It is clear from this analysis that SB5, SB6, and SB7 amplification is much more dynamic in B. oleracea, with at least one very young subfamily in all cases, compared to A. thaliana. However, AtSB5 and AtSB6 families may still be active today as several SINE copies very close to the consensus sequences were detected. For AtSB7, the three copies detected are probably relics of transposition events that happened in the common ancestor of the two species or soon after their divergence. Although these three families are shared between the two species, we have failed to detect orthologous elements (element present at the same genomic sites in both species). This is also the case for SB2 and SB3 (Lenoir et al., 2005). One possibility to explain this observation is that these families did not amplify to a significant extent in the common ancestor of both species and we may have failed to detect the "rare" orthologous sites because only one fifth of the B. oleracea genome is available. Another possibility is that older retroposition events were lost and that we can only observe the more recent (lineage-specific) SINE integrations. However, because the time to a common ancestor for these two species is relatively short (16 to 19 millions years), this latter hypothesis implies a fast rate of turn over for SINEs in one or both plant lineages. Evidence for a high rate of turn over for SB2, SB3, and SB4 have been described and include the presence of a significant amount of truncated SINE copies (Lenoir et al., 2005). The amount of truncated elements identified for the other SINE families is in general much lower (data not shown) but most of these families are also younger compared to SB2, SB3, and SB4.
Use of Brassicaceae SINEs as Molecular Markers
The apparent rapid turn over of Brassicaceae SINEs should limit their use as molecular markers to the classification of evolutionary events separated by short distances. As described above we already used SINE from the "young" SB1 family as molecular markers to study relations among wild species of the Brassica oleracea cytodeme (Tatout et al., 1999) and filiations to cultivated Brassica oleracea species (J. M. Deragon, unpublished results). Recently, we also produced a collection of SB1 markers to monitor gene flow between a cultivated species, Brassica napus (oilseed rape), and a wild relative species, Raphanus raphanistrum (Prieto et al., 2005). Agriculturally important Brassica crops (turnips, cabbages, kales, swedes, rapes, and mustards) are all closely related and elements from very young B. oleracea SINE families described in this work (BoSB1, 5, 6, 7, 9, and 13 to 15) should be extremely helpful tools to evaluate relations among wild and cultivated species. So, despite their possible inability to retrace long-term evolutionary events, Brassicaceae SINEs are still very efficient tools to establish phylogenetic relations and to monitor gene flow among closely related species.
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We are grateful to Thierry Pélissier and Cécile Bousquet-Antonelli for critical reading. This work was supported by the CNRS (UMR 6547 Biomove and GDR2157) and by Université Blaise Pascal.
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Arnaud P., Yukawa Y., Lavie L., Pelissier T., Sugiura M., Deragon J. M. Analysis of the SINE S1 pol III promoter from Brassica; impact of methylation and influence of external sequences. Plant J. (2001) 26:295–305.[CrossRef][Web of Science][Medline]
Boeke J. D. LINEs and Alus—The polyA connection. Nat. Genet. (1997) 16:6–7.[CrossRef][Web of Science][Medline]
Borodulina O. R., Kramerov D. A. Wide distribution of short interspersed elements among eukaryotic genomes. FEBS Lett. (1999) 457:409–13.[CrossRef][Web of Science][Medline]
Brosius J. Genomes were forged by massive bombardments with retroelements and retrosequences. Genetica (1999) 107:209–238.[CrossRef][Web of Science][Medline]
Capy P., Bazin C., Higuet D., Langin T. Dynamics and evolution of transposable elements (1998) Austin, Texas, USA: RG Landes Compagny, Springer.
Cheng C., Motohashi R., Tsuchimoto S., Fukuta Y., Ohtsubo H., Ohtsubo E. Polyphyletic origin of cultivated rice: Based on the interspersion pattern of SINEs. Mol. Biol. Evol. (2003) 20:67–75.
Cheng C., Tsuchimoto S., Ohtsubo H., Ohtsubo E. Evolutionary relationships among rice species with AA genome based on SINE insertion analysis. Genes. Genet. Syst. (2002) 77:323–334.[CrossRef][Web of Science][Medline]
Cook J., Tristem M. "SINEs of the times"—Transposable elements as clade markers for their hosts. Trends. Ecol. Evol. (1997) 12:295–297.[CrossRef]
Deragon J. M., Landry B. S., Pelissier T., Tutois S., Tourmente S., Picard G. An analysis of retroposition in plants based on a family of SINEs from Brassica napus. J. Mol. Evol. (1994) 39:378–386.[CrossRef][Web of Science][Medline]
Dewannieux M., Esnault C., Heidmann T. LINE-mediated retrotransposition of marked Alu sequences. Nat. Genet. (2003) 35:41–48.[CrossRef][Web of Science][Medline]
Feschotte C., Fourrier N., Desmons I., Mouches C. Birth of a retroposon: The Twin SINE family from the vector mosquito Culex pipiens may have originated from a dimeric tRNA precursor. Mol. Biol. Evol. (2001) 18:74–84.
Jurka J. Origin and evolution of Alu repetitive elements. In: The impact of short interspersed elements (SINEs) on the host genome—Maraia R., ed. (1995) Austin: RG Landes Compagny, Springer. 25–41.
Jurka J. Repeats in genomic DNA: Mining and meaning. Curr. Opin. Struct. Biol. (1998) 8:333–337.[CrossRef][Web of Science][Medline]
Jurka J., Kapitonov V. V., Pavlicek A., Klonowski P., Kohany O., Walichiewicz J. Repbase update, a database of eukaryotic repetitive elements. Cytogenet. Genome Res. (2005) 110:462–467.[CrossRef][Web of Science][Medline]
Kajikawa M., Okada N. LINEs mobilize SINEs in the eel through a shared 3' sequence. Cell (2002) 111:433–444.[CrossRef][Web of Science][Medline]
Kapitonov V. V., Jurka J. A novel class of SINE elements derived from 5S rRNA. Mol. Biol. Evol. (2003) 20:694–702.
Lenoir A., Cournoyer B., Warwick S., Picard G., Deragon J. M. Evolution of SINE S1 retroposons in Cruciferae plant species. Mol. Biol. Evol. (1997) 14:934–941.[Abstract]
Lenoir A., Pelissier T., Bousquet-Antonelli C., Deragon J. M. Comparative evolution history of SINEs in Arabidopsis thaliana Brassica oleracea: Evidence for a high rate of SINE loss. Cytogenet. Genome. Res. (2005) 110:441–447.[CrossRef][Web of Science][Medline]
Motohashi R., Mochizuki K., Ohtsubo H., Ohtsubo E. Structure and distribution of p-SINE1 members in rice genomes. Theor. Appl. Genet. (1997) 95:359–368.[CrossRef][Web of Science]
Muller J. Significance of fossil pollen for angiosperm history. Ann. Missouri Bot. Gard. (1984) 71:419–443.[CrossRef][Web of Science]
Myouga F., Tsuchimoto S., Noma K., Ohtsubo H., Ohtsubo E. Identification and structural analysis of SINE elements in the Arabidopsis thaliana genome. Genes Genet. Syst. (2001) 76:169–179.[CrossRef][Web of Science][Medline]
Ohtsubo H., Cheng C., Ohsawa I., Tsuchimoto S., Ohtsubo E. Rice retroposon p-SINE1 and origin of cultivated rice. Breed. Sci. (2004) 54:1–11.[CrossRef]
Okada N., Ohshima K. Evolution of tRNA-derived SINEs. In: The impact of short interspersed elements (SINEs) on the host genome—Maraia R., ed. (1995) Austin, Texas: RG Landes Company, Springer. 61–80.
Oosterbroek J. A. a. P. Area-cladograms of circum-Mediterranean taxa in relation to Mediterranean palaeogeography. J. Biogeogr. (1992) 19:3–20.[CrossRef]
Pelissier T., Bousquet-Antonelli C., Lavie L., Deragon J. M. Synthesis and processing of tRNA-related SINE transcripts in Arabidopsis thaliana. Nucleic Acids Res. (2004) 32:3957–3966.
Pozueta-Romero J., Houlne G., Schantz R. Identification of a short interspersed repetitive element in partially spliced transcripts of the bell pepper (Capsicum annuum) PAP gene: New evolutionary and regulatory aspects on plant tRNA-related SINEs. Gene (1998) 214:51–58.[CrossRef][Web of Science][Medline]
Prieto J. L., Pouilly N., Jenczewski E., Deragon J. M., Chevre A. M. Development of crop-specific transposable element (SINE) markers for studying gene flow from oilseed rape to wild radish. Theor. Appl. Genet. (2005) 111:446–455.[CrossRef][Web of Science][Medline]
Ronquist F., Huelsenbeck J. P. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics (2003) 19:1572–1574.
Schmitz J., Zischler H. A novel family of tRNA-derived SINEs in the colugo and two new retrotransposable markers separating dermopterans from primates. Mol. Phylogenet. Evol. (2003) 28:341–349.[CrossRef][Web of Science][Medline]
Shedlock A. M., Okada N. SINE insertions: Powerful tools for molecular systematics. Bioessays (2000) 22:148–160.[CrossRef][Web of Science][Medline]
Tatout C., Warwick S. I., Lenoir A., Deragon J. M. SINE insertion as clade markers for wild Cruciferae species. Mol. Biol. Evol. (1999) 16:1614–1621.[Web of Science]
Umeda M., Ohtsubo H., Ohtsubo E. Diversification of the rice Waxy gene by insertion of mobile DNA elements into introns. Jpn. J. Genet. (1991) 66:569–586.[CrossRef][Medline]
Xu J. H., Kurata N., Akimoto M., Ohtsubo H., Ohtsubo E. Identification and characterization of Australian wild rice strains of Oryza meridionalis Oryza rufipogon by SINE insertion polymorphism. Genes Genet. Syst. (2005a) 80:129–134.[CrossRef][Web of Science][Medline]
Xu J. H., Osawa I., Tsuchimoto S., Ohtsubo E., Ohtsubo H. Two new SINE elements, p-SINE2 and p-SINE3, from rice. Genes Genet. Syst. (2005b) 80:161–171.[CrossRef][Web of Science][Medline]
Yasui Y., Nasuda S., Matsuoka Y., Kawahara T. The Au family, a novel short interspersed element (SINE) from Aegilops umbellulata. Theor. Appl. Genet. (2001) 102:463–470.[CrossRef][Web of Science]
Yoshioka Y., Matsumoto S., Kojima S., Ohshima K., Okada N., Machida Y. Molecular characterization of a short interspersed repetitive element from tobacco that exhibits sequence homology to specific tRNAs. Proc. Natl. Acad. Sci. USA (1993) 90:6562–6566.
Zhang X., Wessler S. R. BoS: A large and diverse family of short interspersed elements (SINEs) in Brassica oleracea. J. Mol. Evol. (2005) 60:677–687.[CrossRef][Web of Science][Medline]
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