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DNA Research Advance Access originally published online on November 16, 2006
DNA Research 2006 13(5):197-204; doi:10.1093/dnares/dsl012
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© The Author 2006. Kazusa DNA Research Institute.
The online version of this article has been published under an open access model. Users are entitled to use, reproduce, disseminate, or display the open access version of this article for non-commercial purposes provided that: the original authorship is properly and fully attributed; the Journal and Oxford University Press are attributed as the original place of publication with the correct citation details given; if an article is subsequently reproduced or disseminated not in its entirety but only in part or as a derivative work this must be clearly indicated. For commercial re-use, please contact journals.permissions@oxfordjournals.org

Pattern and Rate of Indel Evolution Inferred from Whole Chloroplast Intergenic Regions in Sugarcane, Maize and Rice

Kyoko Yamane1,2,*, Kentaro Yano3,4 and Taihachi Kawahara1

1 Laboratory of Crop evolution, Graduate School of Agriculture, Kyoto University Nakajoh, Mozume, Mukoh 617-0001, Japan
2 Plant resource Laboratory, Graduate School and School of Life and Environmental, Osaka Prefectural University 1-1 Gakuen-cho, Nakaku, Sakai, Osaka 599-8531, Japan
3 Plant Breeding Laboratory, Graduate School of Agriculture, Kyoto University Nakajoh, Oiwake-cho, Kitashirakawa, Sakyo-ku, Kyoto 606-8502, Japan
4 Kazusa DNA Research Institute 2-6-7 Kazusa-kamatari, Kisarazu, Chiba 292-0818, Japan

Received 3 August 2006; revised 19 October 2006


   Abstract
Top
 Abstract
1. Introduction
 2. Data and methods
 3. Results and discussion
 Acknowledgements
 REFERENCES
 
Microstructural changes such as insertions and deletions (=indels) are a major driving force in the evolution of non-coding DNA sequences. To better understand the mechanisms by which indel mutations arise, as well as the molecular evolution of non-coding regions, the number and pattern of indels and nucleotide substitutions were compared in the whole chloroplast genomes. Comparisons were made for a total of over 38 kb non-coding DNA sequences from 126 intergenic regions in two data sets representing species with different divergence times: sugarcane and maize and Oryza sativa var. indica and japonica. The main findings of this study are: (i) Approximately half of all indels are single nucleotide indels. This observation agrees with previous studies in various organisms. (ii) The distribution and number of indels was different between two data sets, and different patterns were observed for tandem repeat and non-repeat indels. (iii) Distribution pattern of tandem repeat indels showed statistically significant bias towards A/T-rich. (iv) The rate of indel mutation was estimated to be {approx}0.8 ± 0.04 x 10–9 per site per year, which was similar to previous estimates in other organisms. (v) The frequencies of nucleotide substitutions and indels were significantly lower in inverted repeat (IR).

Key words: chloroplast genome; evolutionary rate; indels; non-coding DNA sequence; intergenic region


   1. Introduction
Top
 Abstract
 1. Introduction
2. Data and methods
 3. Results and discussion
 Acknowledgements
 REFERENCES
 
Chloroplast non-coding regions evolve through accumulated nucleotide substitutions and microstructural mutations such as insertions and deletions (=indels, represented by gaps) and inversions. Indels and inversions are thought to be a major driving force in sequence evolution,1Go and Kelchner,2Go who recently reviewed the evolution of chloroplast non-coding sequences, suggested that microstructural mutations would not be randomly distributed throughout chloroplast genomes, because the frequency at which such mutations arise often depends strongly on sequence context. Kelchner2Go claimed, therefore, that it is essential to understand the evolutionary features of microstructural mutations in order to use them in phylogenetic or other evolutionary studies.

Ingvarsson et al.3Go studied indel evolution in three chloroplast intergenic regions (trnL-trnF, trnH-psbA and trnG-trnS) of two Silene species to assess the phylogenetic utility of indels. Hamilton et al.4Go also investigated the frequency and the distribution of indels in six chloroplast intergenic regions (psbB–psbH, atpB–rbcL, trnL–trnH, rpl20–5'rps12, trnS–trnG and trnH–psbA) from Lecythidaceae. These data suggest that chloroplast indels behave as neutral variants that arise randomly. However, it is still unsettled whether indels have a uniformly random distribution throughout chloroplast genome or whether indel frequencies are influenced by base composition or other DNA sequence-dependent influences. Thus, a comprehensive study is needed of sequence context-dependent variation in the frequency of microstructural mutations in whole chloroplast genomes.

More than 30 chloroplast genomes have been completely sequenced from eukaryotic algae and land plants including the three economically important Poaceae crop plants rice5Go, maize6Go and wheat7Go. Using these three chloroplast genome sequences, Matsuoka et al.8Go first conducted a comparative study of the nucleotide sequences of 106 chloroplast genes. In this study of coding regions, sequence alignments were unambiguous; however, the alignment of non-coding chloroplast sequences can be much more difficult and ambiguous, resulting in multiple alternative alignments and different patterns of indels. For this reason, there has been no large scale comparative study of entire non-coding regions. Thus, it is desirable to study closely related pairs of non-coding sequences, for which an unambiguous alignment can be made. Recently, the whole chloroplast genome sequence of a fourth grass plant, sugarcane, was determined.9Go Both sugarcane and maize belong to the subtribe Saccharinae of the tribe Andropogoneae, Poaceae, and are phylogenetically very close.10Go,11Go For example, Asano et al.9Go confirmed that the number and order of functional chloroplast genes are identical throughout the chloroplast genomes of sugarcane and maize. More recently, Tang et al.12Go determined the complete chloroplast genome sequence of cultivated rice var. indica and japonica. These data provided a good opportunity to conduct a comparative analysis of non-coding sequences in chloroplast genomes.

This study presents comparative analyses of number of indels and the distribution in two sequence data sets: data set (a) was the intergenic regions of the chloroplast genomes of sugarcane (Saccharum offcinarum) and maize (Zea mays); data set (b) includes Oryza sativa var. indica and var. japonica. These two data sets were chosen in part because the divergence time of DNA sequences in each data group is markedly different. Mutation frequencies were analyzed in >38 kb non-coding DNA sequences from 126 intergenic regions in the chloroplast genomes of these species. The number of indels was counted in each intergenic region independently, and their frequencies and distribution patterns in chloroplast genomes were calculated en masse, based on the idea that a single linear linkage profile is associated with uniparental inheritance of chloroplast DNA.13Go Furthermore, the evolutionary rate of indels in the chloroplast intergenic region was estimated. Based on these findings and previous reports, the evolutionary implications of indels are discussed.


   2. Data and methods
Top
 Abstract
 1. Introduction
 2. Data and methods
3. Results and discussion
 Acknowledgements
 REFERENCES
 
The entire chloroplast genome sequence from sugarcane (Saccharum offcinarum, DDBJ/EMBL/GenBank accession no. AP006714 [GenBank] ), maize (Zea mays, X86563 [GenBank] ) and rice (Oryza sativa var. japonica; AY522331 [GenBank] and var. indica; AY522329 [GenBank] )12Go were obtained from DDBJ. In this study, data for O. sativa var. japonica (GenBank accession no. X15901 [GenBank] )5Go was not analyzed, because Tang et al.12Go noticed that this accession is somewhat anomalous and may be a variant of the Nipponbare chloroplast.

Multiple sequences were aligned by Clustal W14Go using default settings which were adjusted manually. Indels were not classified as insertions or deletions, because an outgroup was not included in the data sets. The chloroplast genome is comprised of two large inverted repeat (IR) regions as well as large single copy (LSC) and small single copy (SSC) regions.15Go All mutations in IR, LSC and SSC were analyzed separately. Pseudogenes and their adjacent regions were excluded from all analyses, because the borders of pseudogenes tend to be ambiguous. Indel sequences were only analyzed when homologous genes were identified on both sides of the specific intergenic region. In vascular plants, introns are difficult to identify because most chloroplast genes are expressed as polycistronic transcription units (reviewed by Sugita and Sugiura16Go). In this study, therefore, intronic regions were not analyzed. The sequence alignments of multiple chloroplast genomes used in this study are available upon request.

DnaSP version 3.0017Go was used to estimate the number of net nucleotide substitutions between two populations (DXY)18Go in aligned sequence. Indels were classified into tandem repeat or non-repeat indels, according to Ingvarsson et al.3Go (see Supplementary Material online Table 1-1 and 1-2). Tandem repeat indels include both perfect and imperfect repeats of a sequence motif ≥2 bp in length.


   3. Results and discussion
Top
 Abstract
 1. Introduction
 2. Data and methods
 3. Results and discussion
Acknowledgements
 REFERENCES
 
Accurate DNA sequence alignments are essential when analyzing the evolution of DNA coding or non-coding sequences. In the present study, ambiguous sequence alignment of chloroplast non-coding regions and incorrect indel assignments were avoided by selecting input DNA sequences from plants belonging to closely related taxa. For the selected plant species and DNA regions, intergenic chloroplast DNA sequences were aligned without difficulty, and it was not necessary to exclude any DNA sequence regions due to ambiguity in the sequence alignment. This study analyzes indels and nucleotide substitutions in two data sets: data set (a) consisted of chloroplast DNA from sugarcane and maize; and data set (b) consisted of chloroplast DNA from O. sativa var. indica and japonica. The number and positions of all mutations in each data set were determined and are listed in Supplementary Tables 1-1 and 1-2, respectively. Table 1 summarizes the number of nucleotide substitutions, tandem repeat indels, non-repeat indels and the mean and median indel length for each data set.


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  		Table 1. Number of substitutions and indels in whole chloroplast intergenic regions in sugarcane and maize [data set (a)] or Oryza sativa var. japonica and var. indica [data set (b)].

 
3.1. Dominance of single nucleotide indels in non-coding regions
The distribution of indels of different length was determined in LSC and SSC regions for data set (a) and the results are presented graphically in Fig. 1A. The number of indels decreases rapidly as indel length increases, such that short indels, especially 1 bp indels, are highly enriched in this data set (Fig. 1A and B). A similar pattern was reported previously by Hamilton et al.4Go, who compared six chloroplast intergenic regions in species of Lecythidaceae. A strong linear relationship (R2 = 0.889, P < 0.001) was detected in a plot of ln (indel number) versus ln (indel length). These results agree with a previous study in which indel size distribution was analyzed in human and chimpanzee processed pseudogenes.19Go Furthermore, in the present study, single nucleotide indels represented 41% of total indels in LSC + SSC regions. Similar estimates have been reported previously in the following studies: 50% single nucleotide indels in human and rodent pseudogenes,19Go 45% in the {delta}-globin region and 43% in the {delta}-globin spacer region,20Go 50% in rodent processed pseudogenes21Go and 41% in plant non-coding DNA.22Go Thus, we noticed that single nucleotide indels are the predominant type of indel occurring between recently diverged DNA sequences from various organisms.


Figure 1
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  		Figure 1. Number of indels and length was counted in SC (LSC + SSC) regions in data set (a). [Note that there were too few indels for analysis in data set (b) or the IR (a + b) region.] (A) The distribution of indel length (= size) in the chloroplast intergenic regions. Number of indels (nk) is plotted versus indel length (k). The percent of single nucleotide indels is shown at top. The number of long indels was low, so the x-axis is truncated at 26 bp. (B) Relationship between indel length (bp) and number in SC (LSC + SSC) regions. Values are shown as a log–log plot.19Go The dashed line shows the best-fit to the data truncated at 95% of total indel events.

 
3.2. Number and distribution pattern of indels in chloroplast intergenic regions
The low level of variation between O. sativa var. indica and japonica was previously reported by Tang et al.12Go In this study, a large number of mutations were identified in data set (a) (201 indels and 373 base substitutions), while ~10-fold fewer mutations were identified in data set (b) (16 indels and 22 base substitutions), even though the total length of the intergenic sequences in the two data sets were very similar. In addition, in data set (a), the length distribution of indels was 1–264 bp, whereas which was 1–32 bp in data set (b). These different patterns of indel events between data sets (a) and (b) could be simply associated with the different level of divergence time. Interestingly, Golengerg et al.22Go has reported in a study of chloroplast non-coding DNA sequences in monocot crops that the relative proportion of indels in the mutation spectrum is lower in more highly diverged species than in closely related species. In data set (a), the number of indels was approximately half (50.3%) the number of nucleotide substitutions, while in data set (b), the number of indels was 72.7% the number of nucleotide substitutions. Regarding this tendency, Golengerg et al.22Go further suggested that ‘superimposed changes’ affects indel number depend on the divergence time increasing. Namely, ‘recurrent’ indel events could increase the size of an indel length with decreasing of indel number. Our results do not contradict the assumptions of Golengerg et al.22Go but the preset data is too deficient to test them. More sequence data from complete chloroplast genomes are needed.

Ingvarsson et al.3Go investigated indel frequencies among closely related taxa and they concluded that repeat indels evolve at a higher rate than non-repeat indels. In this study, as shown in Table 1, most indels in data set (b) were tandem repeat indels, whereas, the number and distribution of tandem repeat and non-repeat indels was similar in data set (a). This difference between data sets (a) and (b) is also attributable to the different divergence times for the two data sets. Why do the frequencies of tandem repeat and non-repeat indels differ as a function of divergence time? To explain this difference, the mechanism by which indels arise must be considered. It is not well established that tandem repeat indels, which involve adding or subtracting short repeat sequences, result from polymerase slippage (i.e. slipped strand mispairing) during DNA replication.23Go Although there have also been few evolutionary studies on non-repeat indels, Levinson and Gutman23Go proposed that non-repeat indels arise in DNA sequences whose flanking sequences include repeat sequences. This proposal implies that the mechanism by which tandem repeat sequences arise depends on the structure of an existing repeat at the site of the tandem repeat, whereas the mechanism by which arise depends on the presence of repeat sequences at a distant site in flanking DNA. Interestingly, if their mechanism is conceivable, their mechanism by which non-repeat indels arise increase a probability of ‘superimposed changes’. Briefly, it is likely that the rate of superimposed changes is accelerated by repeat sequences, which act as a mutational ‘trigger,’ explaining the fact that the rate of tandem repeat indels decrease as divergence time increases, as observed in data set (a).

3.3. Relationship between indel number and base composition
Here, the relationship between indel number and base composition in chloroplast DNA is considered. It is well known that the chloroplast genome in monocot plants is very AT-rich ({approx}61% A/T24Go). Morton25Go noted a positive correlation between the number of transversions and AT-richness in rice and maize chloroplast genomes, and he proposed that the AT-richness of chloroplast DNA might have an impact on patterns of nucleotide substitution. However, the relationships between base composition and ‘microstructural changes’ in plant whole genomes has not been systematically studied. Most of tandem repeat sequences in chloroplast DNA are composed of either poly A/T or poly G/C-containing repeats.2Go In data set (a), we observed that 20 of 104 tandem repeat indels include multiple Gs or Cs (Supplementary Table 1-1), indicating strong and statistically significant bias towards A/T-rich tandem repeat indels (Fisher's exact test, P < 0.001). This result also suggests that AT-richness influences the distribution of indels in the chloroplast genome. Zhou et al.26Go investigated the distribution of poly A/T and poly G/C repeats in 27 eukaryotes with various GC contents from 20 to 60%. Interestingly, their results also indicated that overall GC contents affect the number of poly A/T or poly G/C. These findings support the implication that the AT-richness of chloroplast DNA influences both the dynamics of nucleotide substitution and the number of tandem repeat indels.

3.4. Evolutionary rate of indels in chloroplast intergenic regions
Figure 2 shows the number of nucleotide substitutions and indels in each intergenic region examined in this study. Although the length of indels was not considered in this analysis, the number of indels correlated significantly with the length of the intergenic region. Linear regression analysis suggested a strong linear relationship between the two variables (P < 0.001), and a quadratic relationship did not provide a better fit for the data (quadratic fit for all indels: R2 adjusted = 0.6339; data not shown). These data indicate that the number of indels is proportionate to the length of the region and its divergence time. In addition, it can be concluded that the slope of each line is a reasonable estimate of the mutation number per base pair.


Figure 2
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  		Figure 2. Number of nucleotide substitutions and indels in data set (a) excluding IR (a + b). Total indels, tandem repeat indels and non-repeat indels are plotted versus length (bp) of each intergenic region. The x-axis is truncated at 90% of total indel events. The best-fit linear regression lines are shown.

 
The following calculations were made to estimate the rate of indel mutations in this study. The divergence time, T, for two species is given by T = DXY/2l,18Go where l is the rate of nucleotide substitution per site per year. Since there is no direct estimate of the divergence time between sugarcane and maize, we estimated the divergence time from analyzing variation in their rbcL sequences (GenBank accession nos AP006714 [GenBank] and ZMA86563, respectively). As a result, the number of nucleotide substitutions (DXY) between sugarcane and maize was 0.00699 for the rbcL gene and the synonymous and non-synonymous substitution rates for rbcL, I, were obtained from a previous estimate for the grass family.27Go This calculation indicates a putative divergence time for sugarcane and maize of {approx}7.6 million years (Mya). Takahashi et al.28Go also roughly estimated a divergence time of 5–6 Mya between Saccharum species and maize using 18 chloroplast regions. Therefore, we decided to use our estimated divergence time for the further analysis.

In this study, the rate of indel mutations was estimated using a novel method, as follows. The slope of the line in Fig. 2 is the mutation rate per base pair. Using the fact that the region length and indel number have a positive linear relationship (R2 = 0.62, P < 0.001), it can be calculated that the intergenic regions of chloroplast genomes accumulate indel mutations at an average rate of 0.006 ± 0.00037 per site (= slope of a line). As a result, the rate of indel mutation is estimated to be {approx}0.8 ± 0.04 x 10–9 mutations per site per year. Saitou and Ueda20Go calculated the rates of indels in non-coding sequences in primates as {approx}2 x 10–9 for mitochondrial DNA and {approx}0.2 x 10–9 for nuclear DNA, respectively. Thus, this study suggests that the indel mutation rate in chloroplast DNA is intermediate between the previous estimate for mitochondrial and nuclear DNA. However, Saitou and Ueda20Go also showed that the rate of nucleotide substitutions was ~10 times higher than the rate of indels for nuclear and mitochondrial non-coding DNA. In this study, the average nucleotide substitution rate was 0.0116 ± 0.00052 per site (= slope of a line, see Fig. 2), which is approximately half the average indel mutation rate (see Fig. 3). In order to validate the method used here, the same method was used to calculate that the nucleotide substitution rate in chloroplast DNA is {approx}1.52 ± 0.06 x 10–9 substitutions per site per year. This value is quite similar to the previously estimated substitution rate for rbcL in the grass family of {approx}1.3 x 10–9 substitutions per synonymous site per year.27Go These data suggest that the stated estimate for indel mutation rate in chloroplast intergenic DNA, 0.8 ± 0.04 x 10–9 mutations per site per year, is a reasonable estimate, and that the novel method used here to arrive at this estimate is valid.


Figure 3
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  		Figure 3. Relationship between number of substitutions (x-axis) and that of indels (y-axis) in each intergenic region from data set (a) excluding IR (a + b). The best-fit line from linear regression analysis is shown.

 
The validity of the estimated indel mutation rate was also tested by examining data set (b). Ma and Bennetzen29Go used variation in nuclear DNA to estimate that the indica and japonica genomes share a common ancestor {approx}0.44 Mya. Using nuclear genes, Zhu and Ge30Go also estimated the divergence time between var. japonica and indica ({approx}0.4 Mya). Based on this divergence time, the expected number of indels between indica and japonica is 8.92 ± 0.446 in a total of 12 657 bp excluding the IR region (Supplementary Table 1-2). This estimate is about half of the observed number of indels (16) in data set (b) (Table 1). If we assume that indel mutations have a Poisson distribution, the probability that 16 indels arose in the chloroplast intergenic regions in 0.44 million years is not rejected (P > 0.05). This means that the rate of indel mutations estimated here is at least possible in sugarcane, maize and rice, despite the fact that there are evolutionary heterogeneities for tandem repeat and non-repeat indels. This information will facilitate studies of genetic variation or differentiation in plant species and may be useful for management of germplasm, genotyping or phylogenetic analyses.

3.5. Conserved nature of IR region
In most of the chloroplast genomes, there are two large IR regions ({approx}30 kb each). The evolutionarily conserved nature of these large IR regions in chloroplast DNA has been reported by several authors.(31Go–33Go) Palmer32Go proposed that this highly conserved property may be attributed to the fact that approximately one-third of the IR region is occupied by rRNA genes. Recently, Matsuoka et al.8Go confirmed that rRNA genes are highly conserved compared with non-rRNA genes. Table 1 shows that the number of nucleotide substitutions in SC (LSC + SSC) was ~20 times higher than in the IR (a + b) region in data set (a). Furthermore, no substitutions or indels occurred in the IR (a + b) region in data set (b). These results clearly show that nucleotide substitutions and indels occur at a much lower rate in the IR (a + b) region than in SC (LSC + SSC) regions. Thus, the conserved nature of the IR (a + b) regions with respect to microstructural changes is confirmed in this study. Since functional constraints do not apply to non-coding regions and synonymous sites are implausible, another explanation for this phenomenon is needed. Wolfe et al.33Go already pointed out based on their sequence analyses that the highly conserved nature of IR sequences does depend on other dimension(s) for a reduced mutation rate in the IR region or a bias against mutations during DNA repair in IR DNA rather than on a functional constraint. Birky and Walsh34Go insisted from a theoretical study that a difference in the synonymous substitution rate for the IR and SC (LSC + SSC) regions was resulted from the fact that IR sequences are duplicated in the chloroplast genome. Perry and Wolfe35Go compared the synonymous substitution rate in chloroplast genes in duplicated IR (most plants are this type) and single-copy IR (only one single-copy IR in the chloroplast genome) in legume species. The result showed that the synonymous substitution rate in IR genes was 2.3-fold lower in duplicated IR than in single-copy IR. Based on these findings, consequently, it can be concluded that the highly conserved nature of duplicated IR is a function of DNA structure and not a function of primary DNA sequence.


   Acknowledgements
Top
 Abstract
 1. Introduction
 2. Data and methods
 3. Results and discussion
 Acknowledgements
REFERENCES
 
We are indebted Dr K. Tanno, Research Institute for Humanity and Nature, for his helpful and valuable comments. The authors are also indebted to Prof. O. Ohnishi and Dr Y. Yasui, Kyoto University, Dr T. Ohsako, Kyoto Prefectural University and Dr Y. Matsuoka, Fukui Prefectural University, for their useful advices. We are also grateful to assistant Prof. Y. Yamazaki, National institute of Genetics, for her helpful suggestions. This is contribution No. 129 from the Plant Germplasm Institute, Graduate School of Agriculture, Kyoto University. This research was partly supported by a grant from the ministry of culture, education and technology, the National BioResource Project KOMUGI.

Supplementary Data: Supplementary data are available online at http://dnaresearch.oxfordjournals.org.


   Footnotes
 
*To whom correspondence should be addressed. Tel. +81-75-921-0652, Fax. +81-75-932-8063, E-mail: m52297{at}mbox.kudpc.kyoto-u.ac.jp

Communicated by Masahiro Yano


   REFERENCES
Top
 Abstract
 1. Introduction
 2. Data and methods
 3. Results and discussion
 Acknowledgements
 REFERENCES
 

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