MBE Advance Access originally published online on July 11, 2006
Molecular Biology and Evolution 2006 23(10):1912-1921; doi:10.1093/molbev/msl054
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Research Article |
The Evolution of Chloroplast RNA Editing
* Cell Biology, Philipps–University of Marburg, Marburg, Germany; Indiji Software, Marburg, Germany; and Department of Biological Sciences, Barnard College, Columbia University
E-mail: maier{at}staff.uni-marburg.de.
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Abstract |
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RNA editing alters the nucleotide sequence of an RNA molecule so that it deviates from the sequence of its DNA template. Different RNA-editing systems are found in the major eukaryotic lineages, and these systems are thought to have evolved independently. In this study, we provide a detailed analysis of data on C-to-U editing sites in land plant chloroplasts and propose a model for the evolution of RNA editing in land plants. First, our data suggest that the limited RNA-editing system of seed plants and the much more extensive systems found in hornworts and ferns are of monophyletic origin. Further, although some eukaryotic editing systems appear to have evolved to regulate gene expression, or at least are now involved in gene regulation, there is no evidence that RNA editing plays a role in gene regulation in land plant chloroplasts. Instead, our results suggest that land plant chloroplast C-to-U RNA editing originated as a mechanism to generate variation at the RNA level, which could complement variation at the DNA level. Under this model, many of the original sites, particularly in seed plants, have been subsequently lost due to mutation at the DNA level, and the function of extant sites is merely to conserve certain codons. This is the first comprehensive model for the evolution of the chloroplast RNA-editing system of land plants and may also be applicable to the evolution of RNA editing in plant mitochondria.
Key Words: RNA editing • point mutation • chloroplast • plastid
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Introduction |
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RNA editing has been observed in the chloroplasts of all land plants analyzed to date with the exception of the marchantiid subclass of liverworts (Freyer et al. 1997
). In the mRNAs of seed plant chloroplasts, cytidine is converted into uridine (C-to-U RNA editing) at about 30 different positions (Maier et al. 1995; Wakasugi et al. 1996; Hirose et al. 1999; Schmitz-Linneweber et al. 2002; Tillich et al. 2005). These editing events are nonsynonymous with respect to the encoded polypeptide sequences and often affect amino acids that play a role in proper protein function (Bock et al. 1994; Zito et al. 1997; Sasaki et al. 2001). The editing sites themselves are recognized by relatively short sequence stretches in their immediate upstream region ("cis-elements," about 15 nt in length) (Bock et al. 1996; Chaudhuri and Maliga 1996; Bock et al. 1997; Hirose and Sugiura 2001; Reed, Peeters, et al. 2001; Miyamoto et al. 2002). Little is known about the factors responsible for this recognition, but various indirect data indicate that each editing site, or in some cases a small set of sites, must be recognized by specific proteinaceous factors encoded in the plant nuclear genome (Chaudhuri et al. 1995; Bock et al. 1996, 1997; Reed and Hanson 1997; Hirose and Sugiura 2001; Reed, Lyi, et al. 2001; Reed, Peeters, et al. 2001; Miyamoto et al. 2002, 2004). To date, though, only 2 nuclear encoded proteins have been shown to influence chloroplast RNA editing, and a direct participation in the editing process has yet to be established for either. CP31, a general RNA-binding and highly abundant chloroplast protein, is required for editing of 2 different tobacco sites in vitro (Hirose and Sugiura 2001) and, therefore, potentially represents a general editing factor. The PPR (Pentatricopeptide) protein CRR-4 has been shown to be essential for editing of a specific site in the chloroplasts ndhD mRNA of Arabidopsis thaliana (Kotera et al. 2005) and may be the first representative of the long sought-after site-specific editing factors.
Outside the seed plants, one representative each of ferns and hornworts, Adiantum capillus-veneris and Anthoceros formosae, respectively, have been analyzed in detail for chloroplast RNA editing (Kugita et al. 2003; Wolf et al. 2004). In both species, extensive editing, both C-to-U and—in contrast to seed plants—also U-to-C, has been shown to occur. In the chloroplasts of A. formosae, both types of editing are found to a similar extent, 509 C-to-U and 433 U-to-C editing sites, whereas in the chloroplasts of A. capillus-veneris 315 C-to-U and only 35 U-to-C editing sites have been identified. These data indicate that editing is far more extensive in these lineages than in the seed plants, and it is unknown whether the editing machineries of hornwort, fern, and seed plants are of a monophyletic origin. Only 51 editing events occur at homologous sites in A. formosae and A. capillus-veneris, and 5 events occur at homologous sites in seed plants and A. capillus-veneris (Wolf et al. 2004). This leaves open the possibility that the processes evolved independently. Furthermore, if the "one site one factor" hypothesis established for seed plant chloroplasts is applicable to ferns and hornworts, then we would predict hundreds of site specificity factors encoded in their genomes.
Despite the progress toward understanding the molecular mechanisms of, in particular, chloroplast RNA editing, another challenge is to unravel its raison d'être, that is, to explain its existence in evolutionary terms. This goal is particularly intriguing because, in contrast to other RNA-editing systems, no function, such as regulation of gene expression or generation of functional protein isoforms with different properties (reviewed in Gott and Emeson 2000; Gott 2003), has been attributed to plastid RNA editing yet. For a few chloroplast editing sites, edited partially or in a tissue-dependent manner, a role for the regulation of gene expression has been suggested. Nonediting of internal codons might result into alternative polypeptides (Hirose et al. 1999; Karcher and Bock 2002), and editing events restoring cryptic translational start codons might regulate protein synthesis (Hirose and Sugiura 1997). However, for none of them, a regulating function like, for example, the production of a functional alternative ("unedited") gene product has been demonstrated yet. On the contrary, a study investigating editing efficiency and abundance of maize plastid RNAs in various tissues demonstrated that nearly all editing sites are edited in concert at high efficiency in chloroplasts (Peeters and Hanson 2002). And even if some of the sites are edited at a lower efficiency in some nonphotosynthetic tissues, a biological effect of reduced editing efficiency is expected to be superceded by the much stronger variations in abundance of the respective transcripts (Peeters and Hanson 2002). The main function of chloroplast RNA editing, therefore, appears to be the generation of codons important for protein function. This raises the possibility that a seemingly complex editing mechanism has evolved in the nuclear genome whose function is to neutralize point mutations, or to compensate for the lack thereof at certain sites, in the chloroplast genome. A 3-step model for the evolution of editing systems neutralizing mutations in organellar genomes as a consequence of genetic drift has been proposed by Covello and Gray (1993). In this study, we analyze editing sites from several taxa starting with an analysis of seed plants and then expanding the analysis to include the fern A. capillus-veneris and the hornwort A. formosae. Based on the similarity of context, or surrounding nucleotides, we propose a model for the evolution of RNA editing in land plant chloroplasts. Given the similarities across all land plants, we propose that the extant systems are of monophyletic origin. The context features suggest that the function of the original system was to generate sequence variation at the RNA level, in essence adding to variation generated at the DNA level. Over time, some of these original sites have been lost due to mutations occurring at the DNA level with this loss occurring to a lesser degree at sites with lower mutation rates. We also discuss the possibility that a similar model is applicable to RNA editing in seed plant mitochondria.
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Materials and Methods |
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Lola Software
Lola Software accompanied by documentation is freely available for download at www.indiji.de.
Genome Sequences and Editing Sites
All chloroplast and plant mitochondrial genome sequences used in this study were downloaded from GenBank (chloroplast: A. thaliana [NC_000932], Nicotiana tabacum [NC_001879], Atropa belladonna [NC_004561], Zea mays [NC_001666], Pinus thunbergii [NC_001631], A. capillis-veneris [NC_004766], and A. formosae [NC_004543]; mitochondrial: A. thaliana [NC_001284]). The chloroplast editing sites of A. formosae and A. capillus-veneris and the mitochondrial editing sites of A. thaliana were extracted form the respective GenBank genome entries. Chloroplast editing sites of seed plants were collected from the indicated publications. Codon usages were taken from the Kazusa Codon Usage Database (http://www.kazusa.or.jp/codon/).
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Results and Discussion |
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C-to-U RNA Editing in Seed Plant Chloroplast Occurs Predominately at Positions with Low C-to-T Point Mutation Rates on DNA
It is known from studies on chloroplast RNA editing in seed plants that many editing sites are flanked by a U upstream and an A downstream (what we will call a U_A context). To more fully investigate the context of RNA editing sites, all sites reported for the 5 seed plant species that have been analyzed in detail (N. tabacum, Z. mays, P. thunbergii, A. belladonna, and A. thaliana) were sampled. Altogether 155 C-to-U chloroplast editing events have been described for these 5 species (Maier et al. 1995
; Wakasugi et al. 1996; Hirose et al. 1999; Schmitz-Linneweber et al. 2002; Tillich et al. 2005), and these 155 sites comprise 85 unique positions where RNA editing occurs (table 1). The contexts of these 85 editing sites are shown in figure 1. Overall, 69.4% of sites have a U upstream and 64.7% have an A downstream whereas a total of 40 editing events (47.0%) occur in a U_A context (fig. 2A). The contexts of C-to-U editing sites from A. formosae and A. capillus-veneris show a similar bias toward a U_A context, although it is weaker than in seed plants (figs. 1 and 2).
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As is the case in the chloroplasts of A. formosae and A. capillus-veneris (Kugita et al. 2003
; Wolf et al. 2004; Supplementary Table 1), the codons most frequently affected by RNA editing in seed plant chloroplasts are UCN serine codons (yielding UUR leucine or UUY phenylalanine codons after editing). In all 3 taxa, hornwort, fern, and seed plants, these conversions represent the majority of editing events (Supplementary Table 1). Serine-to-leucine/phenylalanine conversions are expected to have a strong impact on the encoded polypeptide because the involved amino acids differ strongly in their physicochemical properties. In contrast, editing events exchanging codons for amino acids with similar physicochemical properties (such as leucine-to-phenylalanine or alanine-to-valine) or editing at third-codon positions occur rarely (Supplementary Table 1). Although there is a bias in amino acid exchanges, a few of lines of evidence suggest that the bias toward a U upstream and an A downstream from an edited site does not depend on the identity of the encoded amino acid. First, of the 50 serine codons affected by editing, 35 (70%) are UCA codons whereas the mean codon usage of UCA in the analyzed seed plant chloroplast genomes is only 25.4% of the UCN serine codons (fig. 3, top panel). Second, these 35 UCA edits make up 87.5% of the 40 UCR-to-UUR serine-to-leucine conversions, whereas UCA composes just 66.5% of UCR serine codons (fig. 3, top panel). Third, of the 15 CCN proline codons edited at second-codon position, 10 (66.7%) are CCA codons, which make up only 28.1% of CCN proline codons (fig. 3, middle panel). Finally, the U_A bias is also exhibited by editing sites located at first codon positions: 9 of the 12 codons (75.0%) edited at the first position exhibit a U at –1 and 5 of those are CAU codons (fig. 3, bottom panel). Overall, these lines of evidence suggest that the U_A context bias is independent of codon position and is not a function of any targeting of serine codons. Instead, the high proportion of edited serine codons in seed plant chloroplasts seems to be the result of additive selection for 1) replacements involving amino acids with profound differences in their physicochemical properties and 2) bias toward a U_A context.
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The finding that editing sites in seed plant chloroplasts occur predominantly within a U_A context correlates with findings concerning context and variation of point mutation rates. It is well established that in flowering plant organelle DNA, the transition ratio of a given nucleotide depends on the identity of its immediate neighboring bases. In general, the transition rate decreases with an increase in the A/T context (the number of A/T base pairs, 0, 1, or 2, immediately flanking the site) as well as with an increase in the number of 5' pyrimidines (Morton et al. 1997
; Morton 2003). Overall, in flowering plant chloroplast DNA, the lowest transition rate is exhibited by a nucleotide residing in the T_A context, a context that has an A/T context of two and two 5' pyrimidines (Morton 2003). Thus, in seed plant chloroplast RNA, 40 of 85 C-to-U editing sites are biased toward positions with a low C-to-T mutation rate.
A Comparison of Editing Sites in Hornwort, Fern, and Seed Plant Chloroplasts
Another unresolved issue concerning chloroplast RNA editing is the relationships between the systems that exist in various land plant lineages. These relationships are important for establishing when chloroplast RNA editing evolved. To investigate this, the chloroplast editotypes of A. formosae and A. capillus-veneris were compared to seed plants. A total of 18 of the 85 (21.0%) chloroplast editing sites in seed plants are shared with at least one of these two taxa and thus could be remnants of the original editing system of land plants (table 2). As in seed plants, RNA-editing sites seem to evolve rapidly within hornwort and ferns (Freyer et al. 1997; Duff and Moore 2005), so it is likely that even more such sites will be identified when more fern and hornwort species are analyzed for editing. Wolf et al. (2004) reported an overlap of 53 chloroplast editing sites between A. capillus-veneris and A. formosae. The observed distribution of shared editing sites is consistent with an early evolution of RNA editing followed by independent losses of editing sites during seed plant evolution from a common ancestor with many editing sites.
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In the chloroplasts of seed plants, the recognition of editing sites by the corresponding trans-factors is thought to occur via a sequence-specific interaction between the trans-factors and the sequence region immediately upstream from the editing sites. These so-called "cis-elements" have been mapped to a region of about 20 nt upstream of several editing sites. It is probable that sets or clusters of editing sites are recognized by the same, or very similar, trans-factor(s) and that these sites exhibit sequence similarities within their upstream regions (Chateigner-Boutin and Hanson 2002
, 2003; Tillich et al. 2005). We hypothesized that if editing occurs in the chloroplasts of hornwort and fern by a mechanism comparable to the one known from the chloroplasts of seed plants, then we should be able to detect putative cis-elements in A. formosae and A. capillus-veneris by clustering of editing sites with similar upstream elements. To test this, we developed a bioinformatic tool, Lola, which extracts definable sequence regions from a genome and compares them pairwise. Lola was used in this study to extract the regions surrounding editing sites (–100 to +100 exclusive the editing position) and generate all possible pairwise combinations of the extracted sequences with the editing sites aligned at the midpoint. Subsequently, Lola ran a window of 15 nt in size along the aligned sequence pairs in one-nucleotide steps. At each position, the number of sequence fragments exceeding a certain similarity threshold was counted and the cumulative results for all window scans at each position were visualized in diagrams (fig. 4, Supplementary Fig. 1A). For both A. formosae and A. capillus-veneris sequence, similarity was higher in the region between –26 to +12 than it was elsewhere. To exclude the possibility that the observed increase in similarity between the regions upstream of editing sites was simply the result of a nucleotide bias surrounding editing sites (codons preferentially subject to editing, for instance), we performed the same analysis but excluded nucleotide positions –1 and +1 (fig. 4, Supplementary Fig. 1A). This resulted in a reduction, but not elimination, of the observed increase in similarity upstream from –26 to +12 for both A. formosae and A. capillus-veneris. Further analyses revealed that these similarities do not result from a general consensus motif but from individual small sets or clusters of editing sites with similar upstream sequences (data not shown). These increased similarities in the upstream regions between editing sites indicate that, as is the case in seed plants, editing sites in the chloroplasts of hornwort and fern are defined by their upstream regions. Therefore, it is very likely that the recognition of chloroplast editing sites proceeds in a very similar manner in all land plants, further supporting the model that the chloroplast RNA-editing machinery is of a monophyletic origin.
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RNA Editing in Plant Mitochondria
RNA editing is also observed in the mitochondria of land plants. In seed plants, the only clear difference between the editing systems of chloroplasts and mitochondria is the number of editing sites. Whereas seed plant chloroplasts contain about 30 editing sites, seed plant mitochondria usually posses several hundreds, an example being the 411 editing sites that have been reported in the mitochondria of A. thaliana (Giege and Brennicke 1999
). Less is known about the absolute number of editing sites in the mitochondria of hornworts and ferns. However, available data, based on the analysis of single genes or gene segments, indicate that extensive editing may exist in the mitochondria of hornworts and ferns (Steinhauser et al. 1999; Groth-Malonek et al. 2005; Duff 2006).
Apart from this difference, editing in both compartments exhibits many similarities (Maier et al. 1996): First, editing in chloroplasts and mitochondria always coincides phylogenetically (Freyer et al. 1997; Steinhauser et al. 1999). Second, the same nucleotide conversions (solely C-to-U or C-to-U and U-to-C editing events together) always take place in both organelles. Third, available data suggest that cis-acting elements are similar in location and extension to those observed in seed plant chloroplasts (Farre et al. 2001; Choury et al. 2004; Takenaka et al. 2004; Neuwirt et al. 2005; van der Merwe et al. 2006). Finally, the mitochondrial editing sites of Arabidopsis display a bias toward having a U upstream and an A downstream (Giege and Brennicke 1999). These substantial similarities between the 2 plant organellar editing systems point to a common origin of both and hence, studying the 2 systems together may provide insights into the evolution of each.
In order to determine whether or not the regions upstream of mitochondrial RNA-editing sites share similarities, we applied Lola Software on the 411 RNA-editing sites described for the mitochondria of Arabidopsis. An increase in the similarity between the upstream regions was detected by our analysis (Supplementary Fig. 1B). As with the results described above for the chloroplasts of A. formosae and A. capillus-veneris, the similarities between the mitochondrial sites of A. thaliana are located within a sequence window from –23 to +10 with respect to the editing positions. Additionally, these similarities do not result from a general consensus motif but rather from small individual clusters of sites (data not shown). Notably, the position of the similarities detected by our in silico analyses coincides with the location of experimentally determined cis-elements (Farre et al. 2001; Choury et al. 2004; Takenaka et al. 2004; Neuwirt et al. 2005; van der Merwe et al. 2006). These results strongly corroborate the interpretation that the corresponding similarities detected in the chloroplast genomes of A. formosae and A. capillus-veneris (fig. 4; Supplementary Fig. 1A) reflect real cis-elements. Overall, our results indicate a close relationship between chloroplast and mitochondrial RNA editing and suggest that the recognition of editing sites proceeds in a similar fashion in both compartments.
A Model for the Evolution of Plant Organelle RNA Editing
Based on the evidence presented above, the model we propose is that 1) plant chloroplast RNA editing is of monophyletic origin and 2) chloroplast and mitochondrial RNA editing evolved as systems that generated new variation in a manner similar to point mutations. The first aspect of the model is based on the comparison between seed plants, ferns, and hornworts discussed above. The number of edited sites has subsequently been reduced by the occurrence of independent C-to-T and/or T-to-C point mutations with a much larger reduction in seed plants. Independent losses of RNA-editing sites have generated the species-specific patterns of editing sites (the editotypes) found in extant plants. If chloroplast RNA editing is in fact monophyletic, then it would indicate that chloroplast U-to-C editing sites have been eliminated completely in seed plants.
The second aspect of the model is based on the observation that chloroplast RNA-editing sites are predominantly at positions with a low point mutation rate in seed plant chloroplast genomes. The current bias toward T_A contexts is probably the result of some combination of an initial bias toward editing at sites where C-to-T mutations were less frequent, thus in essence compensating for a lack of variation at such sites, and a lower subsequent rate of loss of the need for editing at such sites due to genome mutation; it is probable that over time, some of the edited sites have been lost due to C-to-T point mutations at the appropriate genome site, something that would occur at a lower rate in T_A contexts. This model implies that there are no additional functions for editing such as gene regulation, leading to the prediction that C-to-U editing sites could be replaced by a transition mutation in the genome without any negative impact on plant fitness. This prediction is consistent with the variation of editing sites observed between seed plant species (Funk et al. 2005). Moreover, a C-to-T mutation has been recently set experimentally at an editing site (site atpA-264) in the chloroplast atpA gene of tobacco. Also consistent with the prediction is that mutant plants that are homoplastomic for a T at atpA-264 exhibit a wild-type phenotype (Schmitz-Linneweber et al. 2005). Overall, the data support the model that RNA editing in seed plant chloroplasts functions solely to generate at the RNA level the same effect as a C-to-T point mutation at the DNA level.
One implication of our model is that a decrease in the general mutation rate could result in an increase in the number of editing sites that are retained. Indeed, a correlation between the number of editing sites and the mutation rate is found in several instances in seed plant chloroplasts and mitochondria. First, roughly a quarter of seed plant chloroplast editing sites are located in the ndhB gene. This gene is located in the inverted repeat region of the chloroplast genomes, which evolves about 2.3 times slower than the 2 single-copy regions (Perry and Wolfe 2002). Second, in contrast to chloroplasts, the mitochondria of seed plants posses several hundreds of editing sites and the plant mitochondrial DNA is estimated to evolve about 3 times slower than the chloroplast DNA (reviewed in Palmer 1990). Interestingly, it was recently reported that the mitochondrial genome of Geraniaceae has undergone a period of increased mutation rate that appears to correlate with an unusually low number of editing sites (Parkinson et al. 2005).
No RNA-editing event has yet been identified in the chloroplasts and mitochondria of the marchantiid subclass of liverworts, represented by Marchantia polymorpha (Steinhauser et al. 1999). This suggests that RNA editing was lost in the marchantiid subclass and demonstrates that chloroplast RNA editing is not required in land plants. The chloroplast genome of M. polymorpha exhibits a higher A + T content (71.2%) than A. formosae (67.1%), A. capillis-veneris (58.0%), and the 5 seed plant species investigated here (61.5–63.7%). The increased A + T content of the chloroplast chromosome of M. polymorpha probably indicates different mutational or recombinatorial properties of the chloroplast genome of M. polymorpha that may have contributed to the elimination of RNA-editing sites. Further investigation of this genome should help shed light on this possibility.
At a first glance, it may be difficult to imagine that a complex machinery evolved to, in essence, imitate point mutations at the DNA level, as we have proposed. However, if we consider just the chloroplast genome, a typical leaf cell can contain more than 100 chloroplasts, each of which can contain several hundred copies of its genome. Thus, chloroplasts form a relatively small, asexual, and highly polyploid population within plant cells. Such a population is expected to fix mildly deleterious point mutations (Lynch and Blanchard 1998; Blanchard and Lynch 2000) such as has been described for other endocytobionts, Buchnera (Moran 1996). Also, in contrast to a point mutation occurring in one of the chloroplast chromosomes, an editing factor encoded by the nuclear genome for an organellar site immediately affects the transcripts from all genome copies of the whole organelle population. This would be an important advantage, particularly in cases when a mutation in the chloroplast genome is beneficial for the plant cell but has a negative effect on the organelle population. Such a situation is exemplified by a human mitochondrial mutation associated with the mitochondrial myopathy, encephalopathy, lactic acidosis, and stroke-like episodes syndrome. Here, a mutation in a mitochondrial tRNA gene causes defects in mitochondrial protein synthesis and respiration. However, mutant genomes replace wildtype genomes due to a replication advantage (Yoneda et al. 1992). We propose that a combination of these properties and (possibly) an event inducing point mutations in the early land plant evolution opened the gates for organelle RNA editing to evolve. A similar hypothesis was proposed for the evolution of tRNA editing in metazoan mitochondria (Borner et al. 1997). Another important factor is that among all known RNA-editing systems that affect protein-coding regions, it is only in plants that the factors conferring site specificity to the editing machinery are encoded by a different genome than the target sites. This means that the nuclear encoded editing system might have provided a means to compensate for genetic drift in the chloroplast genome. As suggested recently by Lynch et al. (2006), the different speed of evolution found between the nuclear and organelle genomes of plants, with the organelle genomes evolving much slower than the nuclear genome, might have been a prerequisite for the evolution of plant organellar editing. The relative low mutation rates in the organelle genomes may prevent the mutational decay of cis-elements, what may in turn be required to permit the evolution of the corresponding recognition/editing factors in the nuclear genome (Lynch et al. 2006).
Mechanistically, the editing system could have arisen through proteins with other functions in RNA metabolism. These proteins might have been used to guide the yet unknown RNA-editing activity, a trans-aminase for instance. Once established, these proteins could have been duplicated and adopted to serve different editing sites or sets of sites. Interestingly, the recently identified editing factor for the ndhD message of Arabidopsis, CRR-4, belongs to the PPR family of RNA-binding proteins. The PPR family contains several hundred members in Arabidopsis and rice, the majority of them predicted to be involved in organellar RNA metabolism (Lurin et al. 2004).
The apparent reduction in the number of editing sites during the evolution of higher plants could indicate that editing is disappearing in seed plants as genome mutations eliminate the need for editing at certain sites. This rate of loss of editing sites will be correlated with mutation rate meaning that remaining sites should be predominantly at sites with low point mutation rates as we observe. The appearance of a few new editing sites late in the evolution of flowering plants (Drescher et al. 2002; Tillich et al. 2005) though indicates that this loss is not irreversible. Instead, it could be that the genome evolves toward an equilibrium state in the gain and loss of editing sites. In seed plant mitochondria, RNA-editing activities affecting third-codon positions show a higher evolutionary variability (edited vs. nonedited C) than editing activities affecting nonsynonymous codon position (Shields and Wolfe 1997). This is expected because editing at nonsynonymous codon positions in general generates conserved amino acids and hence should be under positive selection. However, the existence of a high variance of random-like edits at third-codon positions might result from modulations of editing activities that enable editing to extend to novel sites. To clearly distinguish between an "on the way out" model and a balanced gain and loss model, though, more detailed analyses of putative novel editing sites are required.
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Supplementary Material |
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Supplementary Table 1 and Figure 1 are available at Molecular Biology and Evolution online (http://www.mbe.oxfordjournals.org/).
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Acknowledgements |
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TOPAbstractIntroductionMaterials and MethodsResults and DiscussionSupplementary MaterialAcknowledgementsReferences |
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This work was initiated and inspired by Rainer M. Maier, codiscoverer of chloroplast RNA editing, to whose memory it shall be dedicated. We thank Mischa Dieterle and Sebastian Risi for helpful discussions on Lola Software and Christian Schmitz-Linnerweber and Peter Poltnigg for critical reading of the manuscript. U.G.M. and M.T. are supported by the Deutsche Forschungsgemeinschaft via Sonderforschungsbereich Transregio 1.
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1 Present address: Institute for Biology, Humboldt University Berlin, Berlin, Germany.
William Martin, Associate Editor
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References |
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