Two new SINE elements, p-sine2 and p-sine3, from rice
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1 Genes Genet. Syst. (2005) 80, p Two new SINE elements, p-sine2 and p-sine3, from rice Jian-Hong Xu, Isaku Osawa, Suguru Tsuchimoto, Eiichi Ohtsubo and Hisako Ohtsubo* Institute of Molecular and Cellular Biosciences, the University of Tokyo, Bunkyo-ku, Tokyo , Japan (Received 26 April 2005, accepted 10 June 2005) p-sine1 was the first plant SINE element identified in the Waxy gene in Oryza sativa, and since then a large number of p-sine1-family members have been identified from rice species with the AA or non-aa genome. In this paper, we report two new rice SINE elements, designated p-sine2 and p-sine3, which form distinct families from that of p-sine1. Each of the two new elements is significantly homologous to p-sine1 in their 5 -end regions with that of the polymerase III promoter (A box and B box), but not significantly homologous in the 3 -end regions, although they all have a T-rich tail at the 3 terminus. Despite the three elements sharing minimal homology in their 3 -end regions, the deduced RNA secondary structures of p-sine1, p-sine2 and p-sine3 were found to be similar to one another, such that a stem-loop structure seen in the 3 -end region of each element is well conserved, suggesting that the structure has an important role on the p-sine retroposition. These findings suggest that the three p-sine elements originated from a common ancestor. Similar to members of the p-sine1 family, the members of p-sine2 or p-sine3 are almost randomly dispersed in each of the 12 rice chromosomes, but appear to be preferentially inserted into gene-rich regions. The p-sine2 members were present at respective loci not only in the strains of the species with the AA genome in the O. sativa complex, but also in those of other species with the BB, CC, DD, or EE genome in the O. officinalis complex. The p-sine3 members were, however, only present in strains of species in the O. sativa complex. These findings suggest that p-sine2 originated in an ancestral species with the AA, BB, CC, DD and EE genomes, like p-sine1, whereas p-sine3 originated in an ancestral strain of the species with the AA genome. The nucleotide sequences of p-sine1 members are more divergent than those of p-sine2 or p-sine3, indicating that p-sine1 is likely to be older than p- SINE2 and p-sine3. This suggests that p-sine2 and p-sine3 have been derived from p-sine1. Key words: SINE, LINE, transposable element, retroposition, rice INTRODUCTION SINEs (Short INterspersed Elements) are bp repetitive DNA sequences that proliferate via transcription followed by reverse transcription. SINEs are found in a wide variety of eukaryotes, including animals, fungi and plants (Umeda et al., 1991; Okada, 1991; Yoshioka et al., 1993; Deragon et al., 1994; Kachroo et al., 1995). SINEs contain an internal RNA polymerase III promoter, which is involved in their transcription, but have no open reading frames. The 5 -regions of SINEs are related to trna (Lawrence et al., 1985; Daniels and Deininger, Edited by Yoshio Sano * Corresponding author. hohtsubo@ims.u-tokyo.ac.jp 1985; Endoh and Okada, 1986; Yoshioka et al., 1993) or to 7SL RNA, as shown for animal SINEs, such as the primate Alu and rodent B1 family elements (Weiner, 1980; Ullu and Tschudi, 1984), or to 5S rrna, such as SINE3 in the zebra fish genome (Kapitonov and Jurka, 2003). All these SINEs have a poly (A) tract or an A- or T- rich sequence in their 3 -end regions. The 3 -regions of some SINEs show similarity to the 3 -end regions of LINEs (=non-ltr retrotransposons). Specific families of SINEs are found only in closely related species and it has thus been postulated that each family of SINEs originated relatively recently on the evolutionary time scale (Kido et al., 1991). The rice genus, Oryza, comprises approximately 22 species with six diploid genome types AA, BB, CC, EE, FF,
2 162 J.-H. XU et al. GG and four tetraploid genome types BBCC, CCDD, HHJJ and HHKK, and these species are divided into several complexes (Khush, 1997; Ge et al., 1999; Vaughan et al., 2003). Of these complexes, the Oryza sativa complex contains seven AA-genome species, including two cultivated species, O. sativa and Oryza glaberrima. The Oryza officinalis complex, which is most closely related to the O. sativa complex, contains nine species including diploid (BB, CC, and EE) and tetraploid (BBCC and CCDD) species. The first plant SINE, which is named p-sine1 (plant Short INterspersed Element No. 1), was identified in the introns of the Waxy gene in O. sativa (Umeda et al., 1991), and since then a large number of p-sine1 members have been identified from rice species in the O. sativa and O. officinalis complexes (Mochizuki et al., 1993; Motohashi et al., 1997; Cheng et al., 2002, 2003; Xu, 2004). These include members of the RA (Recently Amplified) subfamily that consists of two groups, RAα and RAβ (see Ohtsubo et al., 2004), most of which show insertion polymorphisms within O. sativa and its ancestral wild species O. rufipogon with the AA genome. The presence or absence of these polymorphic members has been used for phylogenetic analysis of strains in these species (Cheng et al., 2003; also Xu, 2004). In this study, we identified and characterized two new families of SINEs from rice. Seventeen members of the p-sine2 family and 24 members of the p-sine3 family were screened among rice strains of species with different genome types. Consensus sequences derived from the alignments of the sequences of members of each p-sine family revealed that their 5 -end regions with the polymerase III promoter show significant homology with the 5 -end region of p-sine1, but not with the 3 -end region of p-sine1. The deduced RNA secondary structures of p-sine1, p-sine2 and p-sine3 were, however, similar to one another. Similar to the p-sine1 family members, the members of the p-sine2 or p-sine3 family were located at random on the 12 rice chromosomes. Sequence divergence observed among members of each p-sine family suggests that p-sine2 and p-sine3 were derived from p-sine1. MATERIALS AND METHODS Rice strains. Rice strains used are described in the Results and Discussion section. Total genomic DNA samples of rice strains were previously described (Cheng et al., 2002; Xu, 2004). Computer analyses. Nucleotide sequence searches in databases (DDBJ, EMBL, and Genbank) were performed with the BLAST program (Altschul et al., 1990). Primary nucleotide sequences were analyzed with the GENETYX- Fig. 1. Phylogenetic trees of p-sine members. A. A phylogenetic tree of p-sine1-family members. B. A phylogenetic tree of p- SINE2- and p-sine3-family members. Only two p-sine1 members are included. These trees were constructed based on their nucleotide sequences. The scale bar equals a distance of 0.1.
3 Two new SINE elements from rice 163 Mac 12 system program. Multiple sequences were aligned by use of the program GENETYX-Mac 12 and Clustal W version 1.7 (Thompson et al., 1994). A phylogenetic tree was constructed based on the nucleotide sequences of p-sine members by the computer program Clustal W version 1.7. The mean genetic distance was calculated according to Lenoir et al. (2001). Polymerase Chain Reaction. The PCR analysis was performed with Ex Taq DNA polymerase (Takara), as described previously (Motohashi et al., 1997). The presence or absence of each p-sine member was determined by identifying one unique PCR fragment with or without a p-sine member after electrophoresis in a 1.8% agarose gel. When the fragments differed in size or when two or Fig. 2. Alignments of nucleotide sequences of members of two new p-sine families. (A) p-sine2 family members. (B) p-sine3 family members. All members of p-sine2 and p-sine3 were identified from O. sativa japonica variety Nipponbare, except r3001, which was identified from O. sativa indica variety The consensus sequences of p-sine2 and p-sine3 are shown at the top. Bars denote identical nucleotides to those in the respective consensus sequences and slashes indicate gaps introduced to maximize homology. Sequences corresponding to the A- and B-boxes of the polymerase III promoter are shown by boldface letters. Almost all members of p-sine2 and p-sine3 families are flanked by direct repeats of a target site sequence, 9 20 bp in length, which are double-underlined, except one member (r2012) of p-sine2 and three members (r3007, r3016a and r3018) of p-sine3. Fig. 3. Comparison of consensus sequences of three p-sine elements from rice. Schematic structures of the three elements are shown at the top. RNA polymerase III promoter elements (A box and B box), the AT rich region and the T-rich tail are indicated by different geometrical patterns. Alignments of consensus sequences of p-sine1, p-sine2 and p-sine3 are shown at the bottom. Identical nucleotides and gaps are indicated by asterisks and bars, respectively. The nucleotides of the A- and B-boxes are shown in boldface letters.
4 164 J.-H. XU et al. more bands were generated, the presence or absence of the p-sine member in the fragments was confirmed by Southern hybridization or by direct sequencing of the PCR products, as described previously (Cheng et al., 2003). Accessions. Nucleotide sequence data with information for p-sine2 and its members (r2001. r2010 and r2012 r2018) and for p-sine3 and its members (r3001 r3024) appear in the DDBJ/EMBL/GenBank International Nucleotide Sequence Databases under the accession number AB AB206884, AB AB and AB AB206918, respectively. RESULTS AND DISCUSSION Identification and characterization of p-sine2 and p-sine3 families. We have previously identified and characterized many p-sine1 members in several O. sativa strains. All of them appear to be very closely related to one another, except for two members, r24 and r3011 (Fig. 1A). We searched for homologous sequences to each of the two members firstly in chromosome 3 and chromosome 10 of O. sativa var. Nipponbare in genomic DNA databases ( We identified some members showing strong homology with each member, suggesting that these two form new SINE families. The two new SINE families were, therefore, designated as p-sine2 and p-sine3 to distinguish them from p-sine1. Using a consensus sequence derived from each of the p-sine family members, we identified 17 members of p-sine2 and 24 members of p-sine3 in O. sativa in nucleotide sequence databases (Fig. 2). The members of p-sine2 or p-sine3 formed a branch different from each other and from p-sine1 (Fig. 1B), confirming that p-sine2 and p-sine3 are new families distinct from p-sine1. Almost all members of p-sine2 and p- SINE3 are flanked by direct repeats of a sequence, 8 20 bp in length, at a target site, except one member of p- SINE2 and three members of p-sine3 (Fig. 2). The consensus sequences derived from the nucleotide sequences of all the members of each family (Fig. 2) were compared Fig. 4. RNA secondary structures of three rice p-sine elements. Structures shown in A C are derived from consensus sequences of p-sine1, p-sine2 and p-sine3, respectively. The structure of p-sine1 shown in A has been determined previously (Osawa, 2003). The nucleotides substituted in p-sine2 and p-sine3 are indicated by letters in red in comparison with the p-sine1 sequence.
5 Two new SINE elements from rice 165 with the p-sine1 consensus sequence, and found to have significant homology (about 80%) in their 5 -end regions with the polymerase III promoter (A box and B box), but have poor homology in their 3 -end regions (less than 40%), although they all contained T-rich tails at their 3 ends (Fig. 3). The 5 -end regions had no significant homology to any other SINEs. This suggests that the three p-sine families originated from a common ancestor. The RNA secondary structure of p-sine1 has been previously determined (Fig. 4; Osawa, 2003). Based on this Fig. 5. Chromosomal locations of p-sine members. A. p-sine2 family members. B. p-sine3 family members. Positions of the members are located on marker-based physical maps derived from the International Rice Genome Sequencing Project homepage ( /rgp.dna.affrc.go.jp/irgsp/download.html). Horizontal bars on each of 12 rice chromosomes indicate members present in the Nipponbare genome, except a p-sine3 member r3001 on chromosome 11, which is not present in the Nipponbare genome but in the genome. A p-sine3 member r3005 on chromosome 1 is not present in the genome. Centromeric regions (solid boxes) are depicted according to the physical maps shown in the URL above.
6 166 J.-H. XU et al. Table 1. Locations of p-sine2 and p-sine3 family members Member a Accession b Position c Chrom. Orien d Location e Genes or cdna accessions f p-sine2 r24 AP C 5094bp downstream OSJNBa0041F13.48 r2001 AC C Exon AK r2002 AP D Intron P0009G03.1, AK r2003 AC D Intron AK r2004 AC C 486bp downstream OSJNBa0023I19.1 r2005 AL C Intron OSJNBb0065L13.3, CAE r2006 AC C 2215bp upstream OSJNBa0027P10.6 r2007 AC D Intron OSJNBa0014G15.8, AK r2009 AC C 24bp downstream OSJNBa0065C16.6 r2010 AC C 2232bp upstream OSJNBa0093I09.4 r2012 AC D ND r2013 AL C ND r2014 AP C Intron P0596H10.5, AK r2015 AP D Intron OJ1134_B10.16, AK r2016 AP C 2550bp upstream P0705E11.4 r2017 AP D 75bp upstream OJ1540_G08.29 r2018 BX D ND p-sine3 r3001 AC Exon AK102193, AK r3002 AC D ND r3003 AC C Intron OSJNBa0030I14.5, AK r3004 AL D ND r3005 AP C Intron P0416D03.42 r3006 AP C 1965bp upstream P0012B02.21 r3007 AP D 558bp downstream P0428D r3008 AP D Exon and intron B1142B04.19 r3009 AP D Intron P0686H11.28 r3010 AB C Intron P0681F10.39, AK r3011 AC C Intron OJ1127_B08.12, AK r3012 AC C 4042bp downstream OJ1537_B05.9 r3013 AC C 527bp downstream OJ1489_G03.15 r3014 AC C 1294bp upstream OJ1654_B10.13 r3015 AC C ND r3016a AC D 1527bp downstream P0668F02.1 r3016b AC D 1382bp downstream P0668F02.1 r3017 AC C Exon AK (28bp in ORF) r3018 AL C ND r3019 AP D 5220bp upstream P0515G01.28 r3020 AP D Exon AK067454, AF r3021 AP D Intron P0529H11.35 r3022 AP C Exon and intron P0005H10.14 r3023 AP C 420bp upstream P0673E01.19 r3024 BX C ND a p-sine2 and p-sine3 members, which were identified by database searches performed in March A p-sine3 member r3001 is present in indica strain 93 11, but not in japonica strain Nipponbare. b Accession numbers of BAC or PAC clones from the Nipponbare genome. c Positions of the p-sine members in BAC or PAC clones (updated in March 2005). d Chromosomal orientation. Letters D and C indicate direct or reverse orientations of p-sine members. e Locations of p-sine members relative to hypothetical genes. ND, not determined. f Names or accession numbers of hypothetical genes or cdna sequences are shown.
7 Two new SINE elements from rice 167 structure, the RNA secondary structures of p-sine2 and p-sine3 were deduced (Fig. 4). They were found to be similar to one another, although they contained many nucleotide substitutions at their 3 -end regions. It is particularly interesting that a stem-loop structure seen in the 3 -end region in the RNA secondary structure is highly conserved, despite the large number of substituted nucleotides (Fig. 4). The conservation of the stem-loop structure suggests that the structure has an important role in p-sine retroposition. Chromosomal locations of p-sine2 and p-sine3 members. In a similar manner to the p-sine1 members, the p-sine2 and p-sine3 members appear to be dispersed randomly along each of the 12 chromosomes (Fig. 5; Ohtsubo et al., 2004), but unlike other retrotransposons and autonomous transposable elements that form a cluster in the heterochromatin of pericentromeric regions (Sasaki et al., 2002; Feng et al., 2002; The Rice Chromosome 10 Sequencing Consortium 2003). Of 17 p- SINE2 members, 10 were present in the putative or hypothetical exons or introns, or within a 0.5 kb region of genes or the putative coding regions (Table 1). Of 24 p-sine3 members, 12 were present in the putative or hypothetical exons or introns, or within a 0.5 kb region of genes or the putative coding regions (Table 1). This suggests that p-sine2 and p-sine3 tend to be inserted within or near genes, like p-sine1 (Ohtsubo et al., 2004) and other SINEs from Arabidopsis and Alu elements from human (Lenoir et al., 2001; Grover et al., 2004). Although SINEs may have an impact on gene expression (Oldridge et al., 1999; Deininger and Batzer, 1999), the presence of p-sine elements in gene-rich regions may be explained by their short size, which may be better tolerated in such regions than those with longer size, and by their non-autonomous characteristics, which may lead to their survival in gene-rich regions. Distribution of p-sine2 and p-sine3 members in rice strains of species with various genome types. We examined the presence or absence of the p-sine2 members at respective loci in 19 strains of species with various genome types (Table 2), by PCR using a pair of primers that hybridize to the flanking regions of each p- Table 2. The presence or absence of p-sine2 family members at respective loci in the rice strains of various species p-sine2 a Species Strains Genome r2001 r2002 r2003 r2004 r2005 r2007 r24 r2009 r2013 r2014 r2015 r2016 O. sativa Nipponbare AA O. rufipogon W593 AA O. glaberrima W0025 AA O. barthii W1581 AA O. glumaepatula W1192 AA O. longistaminata W1444 AA O. meridionalis W1625 AA O. punctata W1514 BB / + + O. punctata W1023 BBCC O. minuta W1323 BBCC O. eichingeri W1519 CC O. officinalis W0002 CC O. latifolia W1166 CCDD +/ / + +/+ + +/ + + O. alta W0017 CCDD +/ +/ / + +/+ + +/ + + O. grandiglumis W0613 CCDD +/ +/+ +/+ + +/ + +/+ + +/ + + O. australiensis W0008 EE / / / O. brachyantha W1401 FF / / / / / / / / O. granulata W0067 GG / / / / / / O. ridleyi W0001 HHJJ / / / / / / / / a p-sine2 family members examined for their presence (+) or absence ( ) at respective loci by PCR. +/ indicates that PCR fragments with and without a p-sine2 member were amplified. Slashes indicate that no PCR fragment was amplified. + indicates that the p-sine2 member r2002 has a tandem duplication of a 40-bp sequence in its flanking region; + indicates that the p-sine2 member r2003 has a tandem duplication of a 63-bp sequence; and + indicates that p-sine2 member r24 has a 239- bp insertion of a Tc1/Mariner-like element in its flanking region (Xu, 2004). Five other p-sine2 members (r2006, r2010, r2012, r2017 and r2018) were not examined here.
8 168 J.-H. XU et al. Table 3. The presence or absence of p-sine3 family members at respective loci in various rice strains p-sine3 b Strain a r3001 r3002 r3003 r3004 r3005 r3006 r3007 r3008 r3009 r3010 r3011 r3012 r3013 r3014 r3015 r3016 r3017 r3018 r3019 r3020 r3021 r3023 r3024 O. sativa Nipponbare Koshihikari C / Nanjing O. rufipogon W1681 / / + + W W / + + / + + W1943 / W1945 / W / W / + W596 / / + W2007 / / / + O. glaberrima W / / + + W440 / / / + + C7599 / / / + + C8527 / / / + + C8538 / / / + + O. barthii W / / + + W0698 / / / + / W1410 / / / + + W1588 / / / + / W1605 / / / + / O. glumaepatula W1191 / / / W1192 / / / W1186 / / / / / W1196 / / / / W1183 / / / / O. longistaminata W1444 / + + / + / / / + / W1004 / + + / + / / + + / + / / / W1052 / + + / + / / / / W1508 / / +/ + / + / / / / / W1540 / / +/ + / + / / / / O. meridionalis W1625 / + / + / / / + +* / / W1635 / / + / + / / / + +* / / / W2069 / + / + / / / + +* / / W2077 / + / + / / / + +* / / W2079 / + / + / / / + +* / / O. punctata W1582 / / / / / / / / / / / / / / O. officinalis W0006 / / / / / / / / / / / / a Strains of seven AA genome species, one BB-genome species O. punctata and one CC-genome species O. officinalis were used. b p-sine3 family members examined for their presence (+) or absence ( ) at respective loci by PCR. +/ indicates that fragments with or without a p-sine3 member were amplified by PCR. Slashes indicate that no PCR fragment was amplified. +* shows a p-sine3 member r3016 with an 834-bp insertion. Another p-sine3 member r3022 was not examined here.
9 Two new SINE elements from rice 169 SINE2 member. All p-sine2 members were present in the strains of all or some species with the AA, BB, BBCC, CC, CCDD or EE genome, but appeared to be absent in the strains of species with the FF, GG or HHJJ genome (Table 2). This shows that they are distributed in the species of the O. sativa and O. officinalis complexes, which suggests that the p-sine2 family originated in an ancestor of a species with the AA, BB, CC, DD or EE genome. Almost all the p-sine2 members characterized do not show any insertion polymorphism in the O. sativa complex (Table 2). This suggests that the p-sine2 family members may have retroposed in the past and stably maintained in recent times. We examined the presence or absence of p-sine3 members in some of the strains analyzed above and obtained results suggesting that p-sine3 members are present in the strains of the AA-genome species, but not in those of the non-aa genome species, such as O. punctata and O. officinalis. Therefore, we examined 39 strains of seven AA genome species (Table 3), for the presence or absence of the p-sine3 members, as described above. Some p- SINE3 members (such as r3007, r3010, and r3015) were present in the strains of all species with the AA genome (Table 3). This suggests that p-sine3 originated in a common ancestral strain of the species with the AA genome. Other p-sine3 members (such as r3001, r3005, r3009 and r3018) showed intra-species insertion polymorphisms. This suggests that p-sine3 was amplified recently on an evolutionary time scale. Sequence divergence among members of p-sine1, p-sine2 and p-sine3. The consensus sequence derived from nucleotide sequences of members of an element family approximates the sequence of the founder element (Jurka, 1998), and the genetic distance of the members from its consensus sequence is related to the age of the family. To estimate the age of each of the three p-sine families, we aligned the nucleotide sequences of 52 members of p-sine1, 17 of p-sine2 or 24 of p-sine3, with the consensus sequence of each element and calculated the genetic distance of the members of each family. The mean distance from the consensus sequence was determined to be for the p-sine3 family members, which was much smaller than those (0.151 and 0.114) for the p-sine1 and p-sine2 family members, respectively. This finding indicates that the p-sine3 family is younger than the p-sine1 and p-sine2 families. This is consistent with the fact that the p-sine3 family members are only present in the strains of the species with the AA genome, whereas members of the p-sine1 and p-sine2 families are not only present in strains of the AA-genome species, but also in those of the non-aa genome species, as described in the previous section. The above finding also indicates that p-sine1 is older than p-sine2. As described earlier, the three p-sine families are thought to have originated from a common ancestor. The largest mean distance of p-sine1 suggests that p-sine2 and p- SINE3 were derived from p-sine1. Partner elements for the two new SINE families. SINEs are non-autonomous elements that must use the enzymatic machinery from an autonomous retroelement in trans for their retroposition. Since some SINEs and LINEs share a 3 -tail sequence, the most probable candidates for providing the retroposition machinery to SINEs are retrotranspositionally active LINE elements (Ohshima et al., 1996; Smit, 1996; Gilbert and Labuda, 1999; see Okada et al., 1997 for a review), which suggests that the LINE-encoded RTase mobilizes the passive SINE by recognizing the 3 tail of the SINE RNA as the template for reverse transcription (Luan et al., 1993; Luan and Eichbush, 1995; Ohshima et al., 1996). A HeLa-cell retrotransposition assay was used to demonstrate that the proteins encoded by an eel LINE element could function in trans to mobilize an eel SINE (Kajikawa and Okada, 2002). Recently, it has been reported that a tagged reporter gene driven by transcription of a young Alu sequence could be trans-mobilized by human LINE L1 (Dewannieux et al., 2003). This indicates that the mobilization of SINE elements is mediated by their partner LINE elements. 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