Interstitial telomere-like repeats in the Arabidopsis thaliana genome
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1 Genes Genet. Syst. (2002) 77, p Interstitial telomere-like repeats in the Arabidopsis thaliana genome Wakana Uchida 1, Sachihiro Matsunaga 1 *, Ryuji Sugiyama 2, and Shigeyuki Kawano 1,2 1 Department of Integrated Biosciences, Graduate School of Frontier Sciences, University of Tokyo, Kashiwanoha 5-1-5, Kashiwa, Chiba , Japan 2 Department of Biological Sciences, Graduate School of Science, University of Tokyo, Hongo 7-3-1, Bunkyo, Tokyo , Japan (Received 3 December 2001, accepted 5 January 2002) Eukaryotic chromosomal ends are protected by telomeres, which are thought to play an important role in ensuring the complete replication of chromosomes. On the other hand, non-functional telomere-like repeats in the interchromosomal regions (interstitial telomeric repeats; ITRs) have been reported in several eukaryotes. In this study, we identified eight ITRs in the Arabidopsis thaliana genome, each consisting of complete and degenerate 300- to 1200-bp sequences. The ITRs were grouped into three classes (class IA-B, class II, and class IIIA-E) based on the degeneracy of the telomeric repeats in ITRs. The telomeric repeats of the two ITRs in class I were conserved for the most part, whereas the single ITR in class II, and the five ITRs in class III were relatively degenerated. In addition, degenerate ITRs were surrounded by common sequences that shared % homology to each other; these are named ITR-adjacent sequences (IAS). Although the genomic regions around ITRs in class I lacked IAS, those around ITRs in class II contained IAS (IASa), and those around five ITRs in class III had nine types of IAS (IASb, c, d, e, f, g, h, i, and j). Ten IAS types in classes II and III showed no significant homology to each other. The chromosomal locations of ITRs and IAS were not category-related, but most of them were adjacent to, or part of, a centromere. These results show that the A. thaliana genome has undergone chromosomal rearrangements, such as end-fusions and segmental duplications. Telomeres consist of multiple tandem repeats of a simple nucleotide sequence, and they perform critical functions in the protection and replication of chromosome ends (Shore, 2001). In addition to the telomeres located at the ends of chromosomes, various types of telomere-like repeats have been found at interstitial chromosomal regions (ITR) in diverse species. Several hundred kilobases of telomere-like repeats have been located at heterochromatic or pericentric regions of chromosomes in vertebrates and plants using the fluorescent in situ hybridization (FISH) method (Meyne et al., 1990; Biessmann et al., 1994; Fuchs et al., 1995). ITRs are thought to originate from ancestral chromosomal rearrangements. ITRs identified in the human chromosome 2 resulted from ancestral chromosomal end-fusion (Ijdo et al., 1991). Small (approximately 1 kb in size) ITRs were also identified near the centromeres of some tomato chromosomes (Presting et al., 1996). Other types of ITRs have been reported, such Edited by Akio Toh-e * Corresponding author. sachi@k.u-tokyo.ac.jp as telomere-associated sequences (TAS) with several telomeric repeat units, which form a major component of plant subtelomeres, e.g., NP3R and NP4R in Nicotiana (Chen et al., 1997) and PSRs in wheat (Mao et al., 1997). ITRs that were derived from de novo synthesis of telomeric repeats with telomerase have been identified at double-strand break-repair sites in human germline chromosomes (Azzalin et al., 2001), and at the healed brokenends of deletion chromosomes in wheat (Tsujimoto et al., 1999). In order to locate ancestral chromosomal rearrangement sites in the Arabidopsis thaliana genome, we used BLASTN to identify Arabidopsis-like telomeric (5'- TTTAGGG-3') 15 motifs (Richards et al., 1988) in the entire genome sequence (The Arabidopsis Genome Initiative, 2000). Since the 5'-AAACCCTAA-3' sequence, which corresponds to 1.3 units of the plant telomeric repeat 5'-AAACCCT-3', is over-represented in the A. thaliana genome (Regad et al., 1994), we selected telomeric arrays that were composed of at least three units [i.e., perfect triple telomeric repeats: (AAACCCT) 3, (AACCCTA) 3,
2 64 W. UCHIDA et al. (ACCCTAA) 3, (CCCTAAA) 3, (CCTAAAC) 3, (CTAAACC) 3 or (TAAACCC) 3 ] in order to exclude random hits. Surprisingly, only eight interstitial genomic regions that contained telomeric repeat units were identified (Table 1). In addition to these perfect telomeric repeats, short (less than 3 units long) and degenerate telomeric repeats were found in the flanking regions (Fig. 1). We defined these regions as ITRs in A. thaliana. Eight ITRs were grouped into three classes (classes I, II and III) based on two parameters (A and B) of ITR degeneracy (Table. 1). Parameter A represented the percentage homology between the ITR (sequences shown by the capital letters in Fig. 1) and same-sized perfect telomeric repeats. Parameter B represented the percentage of telomeric repeats in each ITR (underlined in Fig. 1). The value of A was greater than 90% for IA and IB of the ITRs in class I, 86% for II-ITR in class II, and 66 76% for five ITRs in class III. Furthermore, the values for B were 84% and 98% in IA and IB of the ITRs, respectively, 61% in II-ITR, and 30 39% in class III. ITRs in class I had highly conserved telomere sequences that corresponded to sequences in classes II and III. Table 1. ITRs Characterization of Interstitial telomeric repeats (ITRs) in Arabidopsis thaliana ITR degeneracy *2 Clone name ITR length *1 A (%) B (%) / Accession no. I A 300 (1) T25F15/AC I B 816 (1) patt51/ac II 919 (9) F9D18/AC IIIA 807 (3) F1I21/AC IIIB 589 (2) F1I21/AC IIIC 1200 (1) T12J2/AC IIID 966 (2) MED5/AB IIIE 690 (2) T32N15/AC *1: Each ITR consists of some islands of telomere sequences, and ITR length shows their total size (bp) and numbers of islands represent in a parenthesis. *2: A represented the percentage homology between the ITR (sequences shown by the capital letters in Fig. 1) and samesized perfect telomeric repeats. B represented the percentage of telomeric repeats in each ITR (underlined in Fig. 1) Interestingly, the ITRs in classes II and III were surrounded by highly conserved common sequences that shared % homology to each other (Fig. 2), while the IA and IB ITRs were not surrounded by sequences of this type. These common sequences were named IAS (ITR- adjacent sequences). II-ITR consisted of nine islands of telomeric repeats. Island lengths varied from 131 to 204 bp, and the islands were surrounded by nine IASa elements (21 to 317 bp) that were 71 91% identical to each other (Fig. 3A). IASa elements appeared to interrupt II-ITR. Two II-ITR islands, those with IASa4 and IASa5 (316 bp and 21 bp, respectively), were completely inverted (Fig. 2). On the other hand, nine types of IAS elements (IASb, c, d, e, f, g, h, i, and j) were identified around five ITRs in class III. IASe elements with 93-97% homology to each other were located just before the ITRs and around all five ITRs in class III (Fig. 3B). IASf elements were located just after four ITRs in class III, and were 70 97% identical to each other. IASb elements around IIIA, IIIB and IIIC of the ITRs shared 74 94% homology. IASh elements around IIIC, IIID and IIIE of ITRs were 92 98% identical to each other. IASc, IASd, and IASg elements around IIIA and IIIB of the ITRs shared homologies of 100%, 95 96%, and 99%, respectively. IASi elements around IIID and IIIE of the ITRs shared 76% homology, and IASj elements inserted into IIID and IIIE of the ITRs showed 86% homology (Fig. 2). The IASb, IASe, IASh and IASf elements around the IIIC-ITR appeared to be general components, i.e., they were present around more than three ITRs in class III. The eight ITRs had different chromosomal locations (Fig. 4). IA-ITR was near the centromere of chromosome 3, while IB-ITR was near the telomere of chromosome 2. ITR-II and ITR-IIIC formed parts of the centromeres of chromosome 1 and 2, respectively (The Arabidopsis genome initiative, 2000). IIIA and IIIB of the ITRs were localized near the centromere of chromosome 1, and had two tandemly repeated sequences, possibly as a result of duplication. IIID and IIIE of the ITRs were located in the long and short arms of chromosome 3, respectively. Interstitial telomere-like repeats probably originated Fig. 1. Nucleotide sequences of A. thaliana interstitial telomeric repeats. IA, II and IIIA of the ITRs are shown as representative nucleotide sequences of the ITR in classes I, II and III, respectively. Perfect telomeric sequences are underlined, telomere-homologous sequences are shown by the capital letters, and non-homologous sequences are indicated by small letters.
3 ITRs in the Arabidopsis thaliana genome 65 Fig. 2. The classification of ITRs in A. thaliana. A red arrowhead represents an approximately 200-bp ITR, and shows the direction of the telomeric sequences (5'-TTTAGGG-3') n. The flanking regions of ITR-IA and ITR-IB are not homologous regions to any other ITRsurrounding regions. The II-ITR in class II is interrupted by repetitive sequences (IASa, blue boxes). III-ITRs in class III are surrounded by sequences that are highly homologous to each other (IASb, light-blue boxes; IASc, light-green boxes; IASd, purple boxes; IASe, green boxes; IASf; yellow boxes; IASg, orange boxes; IASh, light-gray boxes; IASi, pink boxes; and IASj, light-orange boxes). The gray and open boxes represent transposable elements and unknown genes, respectively. The class IIIA and IIIB ITRs are tandemly duplicated with respect to their IAS elements. Asterisks show representative ITRs in each class (described in the legend to Fig. 1). Centromere and telomere positions are indicated by CEN and TELO, respectively. The class II and IIIC ITRs are located at the centromere. from telomere-mediated chromosomal rearrangements in the A. thaliana genome. Eight ITRs in A. thaliana could be classified according to ITR degeneracy, and the IAS elements of class II and class III shared no homology. These results suggest that the insertions of telomere-like repeats that led to the generation of IA, IB, II and one of the ITRs in class III, occurred at different times. The order of these events should be reflected in the pattern of ITR degeneracy; more recently rearranged ITRs should have telomeric repeats that are highly homologous to each other. Moreover, the ITRs in class I should have undergone rearrangements later in evolution, and thereby conserved telomeric repeats that lack ITR-adjacent homologous sequences. In contrast, the ITRs in classes II and III may have been rearranged earlier than ITRs in class I. In particular, the IIIC-ITR was found to be the most degenerated, and shared many IAS elements with other ITRs in class III. Therefore, ITRs in class III appear to have descended from the IIIC-ITR. In addition, the IIIC-ITR with IAS elements probably underwent duplication and divergence in the A. thaliana genome to form other class III ITRs. ITRs were identified in the human genome and classified into five groups according to flanking-region polymorphisms, such as repetitive elements and transposons (Azzalin et al., 2001). Similarly, transposable elements were identified in the A. thaliana genome in the ITRflanking regions, e.g., near IA and II of ITRs. However, the ITR-adjacent sequences (IAS) identified in A. thaliana have not been found in the human genome or the genomes of other animals. They display no significant homology to other nucleotide sequences, and are unique to ITR-adjacent genomic regions in A. thaliana. With the exception of transposable elements, these IAS appear to have been arranged around ITRs as a result of evolutionary pressure. Cytological studies suggest that ITRs are fragile sites that are involved in chromosomal aberrations (Bouffler,
4 66 W. UCHIDA et al. Fig. 3. Multiple arrangements of IASa1-7 in class II (A) and IASe1-5 in class III (B). Shaded nucleotides share more than 80% sequence homology. The nucleotide sequences of IASa1-7 and IASe1-5 are 71 90% and 93 97% identical to each other, respectively. Bars are used to indicate deletions in the sequence.
5 ITRs in the Arabidopsis thaliana genome 67 REFERENCES Fig. 4. Chromosomal localization of ITRs in the A. thaliana genome. Numbers on the top of bold lines indicate chromosome numbers. Bold lines show the chromosomes of A. thaliana. Ellipses represent the positions of centromeres. II-ITR and IIIC-ITR are parts of centromeres on chromosome 1 and 2, respectively. IIIA-ITR, IIIB-ITR and IA-ITR are near the centromeres and IB-ITR is near the telomere. 1998). The presence of ITRs has been correlated with general genomic instability, including the creation of recombination hotspots, chromosomal breakage, and subsequent telomere-mediated healing (Hastie et al., 1989; Biessmann et al., 1994). The insertion of telomeric repeats into the centromere, such as II and IIIC of the ITRs, might have had a detrimental effect on centromere functions. Therefore, the addition of specific sequences close to the ITRs might serve to interrupt and stabilize these fragile sites in the centromeres of the A. thaliana genome. Alternatively, the different types of IAS elements surrounding ITRs may simply reflect segmental chromosomal duplications. This work was supported by Grants-in-aid for Scientific Research to S. K. (No ) and S. M. (No ) from the Japanese Ministry of Education, Science and Culture, and by Research for the Future from the Japan Society for the Promotion of Science. Azzalin, C. M., Nergadze, S. G. and Giulotto, E. (2001) Human interchromosomal telomeric-like repeats: sequence organization and mechanisms of origin. Chromosoma 110, Biessmann, H. and Mason, J. M. (1994) Telomeric repeat sequences. Chromosoma 103, Bouffler, S.D., (1998) Involvement of telomeric sequences in chromosomal aberrations. Mutat. Res. 404, Chen, C. M., Wang, C. T., Wang, C. J., Ho, C. H., Kao, Y. Y. and Chen, C. C. (1997) Two tandemly repeated telomere-associated sequences in Nicotiana plumbaginifolia. Mol. Gen. Genet. 5, Fuchs, J., Brades, A. and Schubert, I. (1995) Telomere sequence localization and karyotype evolution in higher plants. Pl. Syst. Evol. 196, Hastie, N. D. and Allshire, R. C. (1989) Human telomeres: fusion and interstitial sites. Trends Genet. 5, Ijdo, J. W., Baldini, A. B., Reeders, S. T. and Wells, R. A. (1991) Origin of human chromosome 2: an ancestral telomere-telomere fusion. Proc. Natl. Acad. Sci. USA 88, Mao, L., Devos, K. M., Zhu, L. and Gale, M. D. (1997) Cloning and genetic mapping of wheat telomere-associated sequences. Mol. Gen. Genet. 254, Meyne, J., Baker, R. J., Hobart, H. H., Hsu, T. C., Ryder, O. A., Ward, O. G., Wiley, J. E., Wurster-Hill, D. H., Yate, T. L. And Moyzis, R. K. (1990) Distribution of non-telomeric sites of the (TTAGGG)n telomeric sequences in vertebrate chromosomes. Chromosoma 99, Presting, G. G., Frary, A., Pillen, K. and Tanksley, S. D. (1996) Telomere-homologous sequences occur near the centromeres of many tomato chromosomes. Mol. Gen. Genet. 252, Regad, F., Lebas, M. and Lescure, B. (1994) Interstitial telomeric repeats within the Arabidopsis thaliana genome. J. Mol. Biol. 239, Richards, E. J. and Ausubel, F. M. (1988) Isolation of a higher eukaryotic telomere from Arabidopsis thaliana. Cell 53, Shore, D. (2001) Telomeric chromatin: replicating and wrapping up chromosome ends. Curr. Opin. Genet. Dev. 11, The Arabidopsis Genome Initiative (2000) Analysis of the genome sequences of the flowering plant Arabidopsis thaliana. Nature 408, Tsujimoto, H., Usami, N., Hasegawa, K., Yamada, T., Nagaki, K. and Sasakuma, T. (1999) De novo synthesis of telomere sequences at the healed breakpoints of wheat deletion chromosomes. Mol. Gen. Genet. 262,
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