MBE Advance Access originally published online on October 16, 2007
Molecular Biology and Evolution 2008 25(1):62-68; doi:10.1093/molbev/msm227
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Research Articles |
Chromosome-Specific Distribution of Nucleotide Substitutions in Telomeric Repeats of Rice (Oryza sativa L.)
* National Institute of Agrobiological Sciences, 1-2, Kannondai 2-chome, Tsukuba, Ibaraki 305-8602, Japan
Institute of the Society for Techno-innovation of Agriculture, Forestry and Fisheries, 446-1, Ippaizuka, Kamiyokoba, Tsukuba, Ibaraki 305-0854, Japan
E-mail: mat{at}nias.affrc.go.jp.
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Abstract |
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Examination of the genomic sequence of the telomere region makes it possible to understand the evolution of the structure of chromosomal ends. We compared the genomic sequences of 14 chromosomal ends of rice, Oryza sativa, L., on the basis of the variation in TTTAGGG repeats. In the proximal telomere repeats, nucleotide substitution occurred more frequently than in the more distal repeats. The most significant diversity was observed at the 1st, 2nd, or 3rd position of TTTAGGG, suggesting that T has been a target of mutation preferentially. Copies of ATTAGGG, CTTAGGG, GTTAGGG, TTCAGGG, TTGAGGG, or TATAGGG were arrayed in tandem, or the same subtypes were located close to each other. The substituted variants were accumulated in chromosomes 2L, 3L, 7L, and 10S but not in the ends of the other chromosomes. In contrast, deletion variants, almost all of which were TTTAGGG to TTAGGG, were dispersed over approximately 4.9% of the sequenced telomere repeats. In summary, the rice proximal telomeric arrays were composed of blocks of at least 6 types of substituted variants and the canonical sequence in a chromosome-specific manner. These results suggest that the variants might arise from the rapid expansion of a single mutation rather than from the gradual accumulation of random mutations.
Key Words: plant telomere • tandem repeats • mutation
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Introduction |
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TOPAbstractIntroductionMaterials and MethodsResultsDiscussionSupplementary MaterialAcknowledgementsReferences |
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Telomere protein–DNA complexes form the ends of linear eukaryotic chromosomes and serve as protective caps that prevent fusion and degradation of the chromosomal ends (McEachern et al. 2000
; Cech 2004; McKnight and Shippen 2004; Blackburn 2005). The DNA component of the telomere complex consists of an array of repetitive sequences. The first plant telomere DNA was isolated from Arabidopsis thaliana and was shown to have tandemly repeated blocks of the sequence TTTAGGG (Richards and Ausubel 1988). The Arabidopsis-type telomere is widely distributed among plant species, including rice (Wu and Tanksley 1993), maize (Burr et al. 1992), and barley (Kilian et al. 1995). To maintain the chromosomal ends, telomerase extends the telomeric repeats using its own RNA as a template. As telomerase reconstructs only the distal end of the repeat, the proximal repeats might not have been reconstructed for a long time on an evolutionary time scale. Therefore, the rate of accumulation of mutations might differ between the proximal and distal ends of the telomere. Do the most proximal arrays accumulate random nucleotide changes?
The rice species Oryza sativa L. is considered to be a model monocot plant because of its small genome size and synteny with other cereal crops (Devos 2005). The International Rice Genome Sequencing Project (IRGSP) has completed a high-quality map-based sequencing of the genome of the japonica cultivar Nipponbare, and the whole-genomic sequence and its annotation are available in a public database (IRGSP 2005; Rice Annotation Project 2007). However, the highly repetitive regions, including the telomeres and centromeres, have not yet been fully characterized (Mizuno et al. 2006a, 2006b).
Here, we describe a comprehensive analysis of nucleotide substitutions in the telomeric arrays on the chromosome ends of rice. We obtained new genomic sequences for the ends of 6 chromosomes and compared them with 8 published genomic sequences. We elucidated the chromosome-specific distributions of substituted, deleted, or inserted telomere repeats; such distributions might be keys to investigations of the evolution of the structure of chromosomal ends. We address the comparative analysis of telomere variants among organisms. Finally, we discuss the mechanism for the generation of telomere variants and the functional effects in telomere homeostasis.
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Materials and Methods |
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TOPAbstractIntroductionMaterials and MethodsResultsDiscussionSupplementary MaterialAcknowledgementsReferences |
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Screening, Mapping, and Sequencing of Fosmid Clones
The fosmid library of genomic DNA derived from the rice cultivar Nipponbare (O. sativa L. ssp. japonica, JP229579 in Genebank of National Institute of Agrobiological Sciences) was screened with overgo probes, as described previously (Chen et al. 2002
). In brief, we designed overgo probes from the telomere repeats or unique sequences of the distal regions of chromosomes using the rice genome sequence (IRGSP 2005; Supplementary Material). High-density filters of fosmid clones provided by the Arizona Genomics Institute (Tucson, AZ) were hybridized by using pooled probes (Mizuno et al. 2006b). The screened fosmid clones were mapped onto the rice genome in silico on the basis of the end sequences, and the location of each screened fosmid was confirmed by polymerase chain reaction with chromosome-specific primers designed from the distal end sequence by using SEQUENCHER software (Gene Codes, Ann Arbor, MI). We selected those fosmid clones that could extend the previously mapped contigs of the chromosome ends (Wu et al. 2003) the most efficiently. Shotgun sequencing of fosmid clones was carried out according to the IRGSP sequencing guideline (http://demeter.bio.bnl.gov/Guidelines.html). |
Results |
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TOPAbstractIntroductionMaterials and MethodsResultsDiscussionSupplementary MaterialAcknowledgementsReferences |
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Mapping and Sequencing of Rice Telomere Repeats
We obtained the telomere sequences at the ends of several rice chromosomes. Fosmid clones that contained telomere tandem repeats were screened and mapped to the ends of chromosomes 3S, 3L, 4S, 4L, 5S, and 10S. They contained copies of TTTAGGG, its variants, and the adjacent chromosome-specific sequences (table 1). Eight other fosmid clones that also contained telomere tandem repeats were drawn from public databases (table 1); they had previously been mapped to the ends of chromosomes 1S, 2S, 2L, 6L, 7S, 7L, 8S, and 9S (Fujisawa et al. 2006
; Mizuno et al. 2006b). Consequently, 14 sequences out of 24 chromosomal ends of the rice genome were available for study (table 1).
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Accumulation of Substituted Variants in Proximal Telomere Repeats
We compared the numbers of TTTAGGG variants at the distal parts (distal to the centromere) and proximal parts (proximal to the centromere) of the first 50 telomere repeats. Fifty copies of telomere repeats adjacent to the chromosome-specific region on chromosomes 2S, 2L, 3L, 4S, 4L, 5S, 7L, 8S, 9S, and 10S were compared (fig. 1). As chromosomes 1S, 3S, 6L, and 7S contained fewer than 50 copies of sequenced telomere repeats (table 1), they were not examined. The sum of total variants in the 10 ends studied was higher in about the first 30 units from the beginning of the telomere array than in the remaining units (fig. 1A). The sum of substitution variants was higher among the first 30 units than among the remainder (fig. 1B) but that of deletion or insertion variants was spread about evenly among units (fig. 1C). Therefore, nucleotide substitution occurred at a high rate over a span of approximately 30 units from the beginning of the telomere array.
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Nucleotide Substitutions or Deletions in TTTAGGG Repeats
We characterized the rates of nucleotide change in the telomere repeats of 14 chromosomal ends. By comparing the 30-telomere units adjacent to the chromosome-specific region, we identified various kinds of nucleotide substitutions, deletions, and insertions in the TTTAGGG sequence (fig. 2). There were many nucleotide substitutions in chromosomes 2L, 3L, 7L, and 10S, and these chromosomes showed different patterns of substitution (fig. 2). Most substituted units contained 1-nt substitution, and there were no more than 2 substitutions in 1 unit (data not shown). Thus, we classified the patterns on the basis of the positions of the nucleotide substitutions (fig. 3):
- (i) 1st position in TTTAGGG. All types of substitutions (T–A, T–C, T–G) occurred, changing the sequence to ATTAGGG, CTTAGGG, or GTTAGGG. These TTTAGGG variants were found on chromosomes 2L, 3L, and 10S (fig. 3).
- (ii) 2nd position of TTTAGGG. Only one type of substitution (T–A) occurred, changing the sequence to TATAGGG (fig. 3). This type of substitution was previously reported from chromosomes 7L (Mizuno et al. 2006b
), but we found TATAGGG arrays on both chromosomes 7L and 3L (fig. 3).
- (iii) 3rd position of TTTAGGG. T–C or T–G substitutions changed the sequence to TTCAGGG or TTGAGGG (fig. 3). These TTTAGGG variants were specific to the end of chromosome 3L alone (fig. 3).
- (iv) 4th, 5th, 6th, or 7th position of TTTAGGG. There was no obvious clustering of TTTAGGG variants that had nucleotide substitutions at the 4th, 5th, 6th, or 7th positions of TTTAGGG.
- (ii) 2nd position of TTTAGGG. Only one type of substitution (T–A) occurred, changing the sequence to TATAGGG (fig. 3). This type of substitution was previously reported from chromosomes 7L (Mizuno et al. 2006b
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In total, the rice telomeres contained at least 6 types of TTTAGGG variant: ATTAGGG, CTTAGGG, GTTAGGG, TATAGGG, TTCAGGG, and TTGAGGG.
Most deletions occurred at one of the Ts in TTT, changing the sequence from TTTAGGG to TTAGGG. Few deletions of a G in GGG were observed (fig. 4A). The T nucleotide in the 7-nt unit was deleted in 4.9% (44/897) of sequenced repeats. Consequently, changes in sequence from T to N occurred preferentially because the nucleotide substitution or deletion occurred most commonly at the 1st, 2nd, or 3rd position of TTTAGGG.
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Distribution of TTTAGGG Variants
By comparing the TTTAGGG sequence or its variants, we found marked differences in distribution patterns depending on the subtype of variants. Nucleotide-substituted TTTAGGG variants were often arrayed in tandem, or the same subtypes were often close to each other (fig. 3). Among the 14 chromosomal ends, these variants were found only on the ends of chromosomes 2L, 3L, 7L, and 10S (fig. 3). The other ends had hardly any substituted repeats (data not shown). In contrast, TTTAGGG deletion or insertion variants were dispersed throughout the sequenced regions of almost all ends (typical examples: fig. 4B). Inversion of part of the array was observed in chromosomes 4L, 7S, and 9S (fig. 4C). These inversions were located adjacent to the chromosome-specific region and were followed by a 6-to 28-bp junction (fig. 4C). These results indicate that substitutions or inversions were accumulated in tandem and distributed in a chromosome-specific manner. On the other hand, TTTAGGG nucleotide deletion or insertion variants were dispersed over the ends of almost all chromosomes.
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Discussion |
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TOPAbstractIntroductionMaterials and MethodsResultsDiscussionSupplementary MaterialAcknowledgementsReferences |
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Evolution of Proximal Telomere Arrays
We compared the genomic sequences of 14 chromosomal ends in rice. The rate of accumulation of telomere variants was higher in the proximal region than in the distal region (fig. 1), suggesting that the proximal region had been rarely reconstructed by telomerase on an evolutionary time scale. On the basis of the following evidence, we consider that this change was not due to the accumulation of random mutations. The telomere array was composed of blocks of canonical sequences or 6 types of TTTAGGG variants (fig. 3). A change from T occurred preferentially (fig. 2). The most commonly substituted sequence contained 1-nt substitution, and there were no more than 2 substitutions in 1 unit (fig. 3); thus, these characteristic telomeric sequences ended abruptly at the junction between the telomere and the chromosome-specific region. These results suggest that the variants might arise from the rapid expansion of a single mutation rather than from the gradual accumulation of random mutations.
This expansion of telomere variants has made it possible to characterize the rice chromosomal end. Copies of ATTAGGG, CTTAGGG, GTTAGGG, TATAGGG, TTCAGGG, or TTGAGGG were arrayed in tandem, or the same subtypes were close to each other at the ends of 4 of the chromosomes (fig. 3). Inversion of telomere repeats was observed adjacent to the beginning of the telomere array on the ends of 3 chromosomes (fig. 4C). Therefore, the proximal telomeric sequences are composed of blocks of at least 6 types of TTTAGGG variants and the canonical sequence in a chromosome-specific manner.
Propensity for Nucleotide Substitutions, Deletions, and Insertions among Organisms
We found 6 types of TTTAGGG variants in rice (fig. 3). In A. thaliana, arrays of TTCAGGG and TTAAGGG are reported as telomere-associated sequences (Richards et al. 1992). Therefore, the TTCAGGG pattern is common between rice and A. thaliana (fig. 5A). But they could result from different origins. In humans, the telomeric array contains TGAGGG, TCAGGG, and TTGGGG on the Xp/Yp chromosome and on a few autosomes (Allshire et al. 1989; Baird et al. 1995; Coleman et al. 1999; Baird et al. 2000). Despite the fact that the length of a unit varies between rice and humans (Moyzis et al. 1988), T–C or T–G substitution next to A might occur preferentially in both organisms (fig. 5A). However, other frequently observed variants—TTAAGGG in A. thaliana and TTGGGG in humans—have hardly ever been observed in this study of rice, although single TTAAGGG variants were observed on chromosomes 2S, 8S, and 10S in rice (fig. 2). In summary, T–C substitution next to A is common among these organisms.
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We also addressed the propensity for nucleotide deletion or insertion among plants. The telomere of rice contained a nucleotide deletion or insertion at T in TTTAGGG (fig. 4A). It is interesting that the telomere sequences of Chlamydomonas and Asparagales are similar to that of rice but not identical: the insertion type in rice, TTTTAGGG, is present in Chlamydomonas (Petracek et al. 1990
), and the deletion type in rice, TTAGGG, is present in Asparagales (Sykorova et al. 2003) (fig. 5B). The partial or full replacement of the telomeric sequences by these variants is considered to be due to evolutionary changes in the genomic sequence that codes the RNA template or in the structural change of the catalytic subunit (Sykorova et al. 2003, 2006). As rice had a 4.9% content of deleted variants, which were dispersed throughout the whole of the sequenced region (fig. 4B), part of the genomic DNA coding the RNA template itself might have nucleotide deletions and therefore those deletions might explain the deletions in the telomere of rice.
Mechanism of Expansion of Substituted Variants among Chromosomal Ends
As the same substituted variants were close to each other on specific chromosomes (fig. 3), expansion of variants might have arisen from intrachromosomal processes such as sister-chromatid exchange or slip during DNA synthesis. The high frequency of DNA recombination in the subtelomeric region of rice (Wu et al. 2003; Gaut et al. 2007) might affect telomere–telomere DNA recombination. In addition to the expansion in single chromosomes, some ends had common substituted sequences (fig. 3). This common distribution may have resulted from interchromosomal telomere–telomere recombination, although there is a possibility that it has originated from independent mutations. As duplication of sequences was found on only 3 of the 14 ends, interchromosomal exchange might play only a minor role in the expansion of variants.
Do telomere variations inherit from generation to generation? We compared the genomic sequences between 2 individuals (fig. 3). The distribution of the 5 types of substituted variants in 3L, 7L, and 10S was almost identical, suggesting that it was stable and not temporal. However, the distribution in relatively distal parts of the sequenced repeats was not identical in 3L and 10S. It is possible that the region might have been deleted by telomere rapid deletion (Li and Lustig 1996; Watson and Shippen 2007) and subsequently reconstructed by telomerase.
Effect of Dispersed Deletion Variants on Telomere Homeostasis
Telomere arrays associate with telomere proteins to form specialized chromatin structures. The deletion process from TTTAGGG to TTAGGG occurred in approximately 4.9% of sequenced repeats and was spread all over the sequenced region (fig. 4B). Do many deletion variants work as alternatives to TTTAGGG? The effect of nucleotide substitution was previously examined on the basis of their binding affinity to RTBP1, a DNA-binding protein that recognizes the telomeric sequence in rice (Yu et al. 2000). Although the internal 6-bp GGGTTT sequence in the 2-telomere repeat is critical for binding of RTBP1, it has been shown that RTBP1 can bind to deletion variants with less affinity (Yu et al. 2000). Therefore, an abundance of dispersed TTAGGG sequences may not have much effect in the binding of RTBP1to telomere repeats.
Researchers have been viewing the chromosomal end as highly polymorphic and evolutionarily dynamic in various organisms (Mefford and Trask 2002; Eichler and Sankoff 2003; Kuo et al. 2006). We elucidated the variations in the sequence and distribution of the first 30–50 telomere repeats among chromosomal ends of rice. As rice telomeres have arrays of 730–1500 copies of TTTAGGG repeats (Mizuno et al. 2006b), genomic sequencing of all the arrays is not yet complete. It is possible that the mosaics of blocks of noncanonical telomere sequences in the remaining rice telomeres could have resulted from slips during DNA synthesis, high frequency of DNA recombination, and/or rapid deletion in the telomere region. Further analysis of the chromosome-specific distribution of variants would help to precisely determine the evolutionary history of rice chromosomal ends.
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Supplementary Material |
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TOPAbstractIntroductionMaterials and MethodsResultsDiscussionSupplementary MaterialAcknowledgementsReferences |
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Detailed maps and finished sequences of the whole rice genome are available at our Web site (http://rgp.dna.affrc.go.jp/).
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Acknowledgements |
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TOPAbstractIntroductionMaterials and MethodsResultsDiscussionSupplementary MaterialAcknowledgementsReferences |
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We thank Dr Rod A. Wing of the Arizona Genomics Institute for providing the Nipponbare fosmid library; F. Aota and K. Ohtsu for technical assistance; and Dr B. A. Antonio for critical reading of the manuscript. This study was supported by grant no. GD-2007 from the Ministry of Agriculture, Forestry, and Fisheries of Japan.
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Footnotes |
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Charles Delwiche, Associate Editor
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