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Tnr8, a Foldback Transposable Element from Rice Genes Genet. Syst. (2000) 75, p. 327–333 Tnr8, a foldback transposable element from rice Chaoyang Cheng, Suguru Tsuchimoto, Hisako Ohtsubo, and Eiichi Ohtsubo* Institute of Molecular and Cellular Biosciences, The University of Tokyo, Bunkyo-ku, Tokyo 113-0032, Japan (Received 19 December 2000, accepted 4 Junuary 2001) An insertion sequence 418 bp in length was found in one member of rice retroposon p-SINE1 in Oryza glaberrima. This sequence had long terminal inverted repeats (TIRs) and is flanked by direct repeats of a 9-bp sequence at the target site, indicative that the insertion sequence is a rice transposable element, which we named Tnr8. Interestingly, each TIR sequence consisted of a unique 9-bp terminal sequence and six tandem repeats of a sequence about 30 bp in length, like the foldback transposable element first identified in Drosophila. A homology search of databases and analysis by PCR revealed that a large number of Tnr8 members with sequence variations were present in the rice genome. Some of these members were not present at given loci in several rice species with the AA ge- nome. These findings suggest that the Tnr8 family members transposed long ago, but some appear to have mobilized after rice strains with the AA genome diverged. The Tnr8 members are thought to be involved in rearrangements of the rice genome. in sea urchin (Hoffman-Liebermann et al., 1985), TFB1 in INTRODUCTION Chiromomus thummi (Hankeln and Schmidt, 1990), and Numerous kinds of transposable elements have been SoFT in Solanaceae plants (Rebatchouk and Narita, described in plants, animals and other organisms (for 1997). review, see Berg and Howe, 1989). Based on their trans- In this report, we show that a member of the rice position mechanisms, they are divided into two classes. retroposon p-SINE1 family (Umeda et al., 1991) in O. One is the DNA-type transposable element which moves glaberrima contains an FB-like element, named Tnr8, via a DNA form using a cut-and-paste mechanism and is which has TIRs that contain tandem repeats of a sequence characterized by the presence of terminal inverted repeats about 30 bp in length. This element is distinct from other (TIRs). The other is the retroelement, which moves via rice transposable elements. No sequence similarity was an RNA intermediate using a mechanism involving re- found between Tnr8 and the foldback transposable ele- verse transcription of the intermediate and integration of ments identified in other organisms. Tnr8 appears to cDNA into another location in the genome. All of these constitute a large family in the rice genome, whose mem- elements, however, generate a duplication of the target bers have a variation(s) in their sequences. We discuss site sequence of several bp long upon their transposition. the possibility that the Tnr8 members are involved in re- The Drosophila FB (foldback) element is a transposable arrangements of the rice genome. element with long TIRs, which contain tandem repeats of a conserved sequence (Potter et al., 1980). These TIRs MATERIALS AND METHODS vary in the length from several hundred bp to several kb due to a variation in the number of the tandem repeats Plant materials. Rice strains with the AA genome, (Levis et al., 1982; Potter, 1982a; 1982b; Trutt et al., 1981). Oryza sativa (Nipponbare and IR36), O. glaberrima About 10% of the FB element members carry a well-con- (GMS1), O. longistaminata (W1451), O. meridionalis served 4-kb internal sequence between TIRs, whereas the (W1625), and O. glumaepatula (W1192) were obtained other members have no or a very short internal sequence from the Genetic Strains Research Center of National (Brierley and Potter, 1985). The FB element is supposed Institute of Genetics, Japan. Total genomic DNAs were to be a DNA-type transposable element (Potter, 1982a). isolated from these strains as described previously FB-like transposable elements with TIRs consisting of tan- (Ohtsubo et al., 1991). dem repeats have been identified in other organisms: TU Computer analysis. Primary nucleotide sequences Edited by Takashi Endo were analyzed with the program HarrPlot 1.2.2 and the * Corresponding author. E-mail: [email protected] GENETYX-Mac 10.1 system. The computer-assisted 328 C. CHENG et al. Table 1. Primers used for PCR Primera Sequence (5' to 3') dTnr8-P ＧＡＧＴＡＡＡＴＴＴＣＡＣＡＡＡＣＴＡＣＡ G23-46-3F ＡＴＴＧＧＣＣＴＧＡＡＴＧＡＴＴＧＧＧＴ Try1 ＧＡＧＡＡＣＣＡＡＴＧＡＡＡＡＧＡＧＴＧ AQ365837-2F ＧＡＣＧＡＡＣＧＧＧＡＴＣＡＧＣＧＴＧＴ AQ365837-2R ＡＴＣＴＴＴＴＴＡＣＣＴＴＧＧＡＣＣＡＡＴＴＡＡＣ AP000391-F ＡＴＧＴＧＴＡＧＧＧＴＧＡＣＴＧＧＡＴＧ AP000391-R ＣＡＡＣＴＣＧＧＴＧＧＧＣＣＡＣＧＴＴＧ AC051633-F ＣＴＧＣＡＧＡＴＣＧＴＣＡＡＴＡＡＣＧＧ AC051633-R ＡＴＧＴＧＣＴＡＡＧＣＣＡＡＴＴＴＣＧＧ AC027133-F ＣＣＡＣＡＴＧＣＡＴＧＧＣＧＣＡＧＴＡＧ AC027133-R ＴＡＴＧＴＧＣＡＣＡＣＧＣＴＴＡＧＣＡＴ a Primer dTnr8-P was used to isolate the fragment with Tnr8-21, and others were used to amplify the fragments with each of Tnr8-1 - Tnr8-5. nucleotide sequence searches for Tnr8 homologs in the DDBJ/Genbank/EMBL databases were done using the programs BLAST (Altschul et al., 1990) and Smith- Waterman search (Smith and Waterman, 1981). Mul- tiple sequences were aligned using the program CLUSTAL W (version 1.7) with some manual modifications. Polymerase chain reaction (PCR), cloning, and DNA sequencing. The primers used are listed in Table 1. The PCR was carried out in a reaction mixture (20 µl) con- taining 100 to 200 ng total rice DNA and Ex Taq DNA polymerase (Takara). Thirty repeats of thermal cycling, consisting of denaturation at 94°C for 30 sec, annealing at 60–65°C for 30 sec and extension at 72°C for 1 min, were Fig. 1. (A) The structure of Tnr8. Tnr8 has TIRs, each consist- done. The PCR products were analyzed by electrophore- ing of a terminal 9-bp sequence (TSL or TSR; solid short arrows) sis in a 1.8 % agarose gel, and directly sequenced by using and tandem repeats (1L -6L or 1R - 6R; open arrows), in which tandem repeat units in the left and right TIR are numbered with a BigDye Terminator kit (PE Biosystem) and an ABI377 L and R in the order from each end of Tnr8, respectively. The sequencing apparatus. Some PCR products were cloned two TIRs flank a 40-bp internal sequence (a thin line). The un- into pGEM-T Easy Vector (Promega) and sequenced as derlined 9-bp sequences in the regions flanking Tnr8 represent described above. the target site sequence duplicated upon insertion. (B) The nucleotide sequence of Tnr8. The terminal 9-bp sequence and the tandem repeats are indicated. The 40-bp internal region is Accessions. Nucleotide sequence data appear in the shown in boldface. DDBJ/EMBL/GenBank International Nucleotide Se- quence Databases under the accession numbers AB052632 - AB052634. indicates that the insertion sequence in p-SINE1-r32 is a transposable element, and we therefore named it Tnr8 (Transposable element of rice No. 8). Tnr8 had long ter- RESULTS ―― ― ― minal inverted repeats (TIRs), 189 bp in length, which An insertion sequence (named Tnr8) in p-SINE1- flank an internal 40-bp sequence. Each TIR consisted of r32. A PCR-amplified fragment containing a p-SINE1 a 9-bp unique terminal sequence and six tandem repeats member (p-SINE1-r32) at a locus in the O. glaberrima ge- of a sequence about 30 bp in length (Fig. 1). These struc- nome was found to be larger than that from O. sativa. tural features in Tnr8 are distinct from those in other rice Nucleotide sequencing revealed that the fragment con- transposable elements, but are reminiscent of foldback tained an insertion of a 418-bp sequence which was not transposable elements such as FB of Drosophila, TU of sea present in p-SINE1-r32 at the same locus in the O. sativa urchin, and SoFT of Solanaceae plants, all of which have genome (Fig. 1). This insertion sequence was flanked by TIRs with tandem repeats. Tnr8, however, did not show direct repeats of a 9-bp sequence in p-SINE1-r32, which any sequence homology with the foldback transposable has been duplicated by the insertion event (Fig. 1). This elements. A foldback transposable element from rice 329 Tnr8-homologous members in the rice genome. than rice. Fig. 2 shows schematic structures of 35 mem- A homology search in databases using Tnr8 as the query bers that we characterized, in which the Tnr8-1 is the first sequence revealed that many Tnr8 homologous members one found in p-SINE1-r32 of O. glaberrima. Although the were present in the O. sativa genome. No Tnr8 homolo- Tnr8 members showed high variations both in size and in gous members were, however, found in plant species other sequence, these members were essentially similar in struc- Fig. 2. Structures of Tnr8-homolog members. Tnr8-1 is the first element found in O. glaberrima. Tnr8-21 is a member isolated as a PCR-amplified fragment from O. sativa using a primer hybridizing to two terminal regions of the TIRs in Tnr8. The other Tnr8 mem- bers were identified by a homology search of databases. The terminal 9-bp sequences (solid arrowheads), tandem repeats (open ar- rows), and conserved internal region (short thick lines) are shown. Broken lines indicate the absence of Tnr8 sequences. Deleted regions of length more than 4 bp are shown by blank spaces. Non-Tnr8 chromosomal sequences are shown by thin solid lines. Sizes of Tnr8 members are shown in bp. Note that structures of 14 members (Tnr8-22 - Tnr8-35) are not fully drawn, because sequence data are not available. Sizes of the duplicated target site sequences are shown in bp. Some Tnr8 members appear to be truncated in either of the two end regions, and thus the duplicated target site sequences in these members could not be assigned. Homology with the consen- sus sequence of Tnr8 is shown in percentage. The accession numbers to the sequences containing Tnr8 members are given.
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