Department of Biology, National Taiwan Normal University, Taipei,
Laboratory of Molecular Systematics of Fishes, Institute of Zoology, Academia Sinica, Taipei, Taiwan
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Abstract |
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Introduction |
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In addition, the structures of rRNAs are maintained by Watson-Crick base pairing interactions in stem regions, which obviously violate the assumption of nucleotide independence for phylogenetic analyses. The effectiveness of stems for phylogenetic analyses has been discussed in previous studies (Wheeler and Honeycutt 1988
; Smith 1989
; Dixon and Hillis 1993
; Morrison and Ellis 1997
; Mugridge et al. 2000
) and contrary conclusions have been reached. Recognizing this problem, several authors have proposed weighting schemes to account for compensatory substitutions in rRNA genes (Wheeler and Honeycutt 1988
; Dixon and Hillis 1993
; Springer, Hollar, and Burk 1995
). This work cannot be done unless a reliable secondary structure is available.
In the case of rRNAs, comparative sequence analysis has played an important role in establishing secondary structure models because of the difficulty of X-ray crystallography studies on these large RNA species. Thus, rather detailed structures for 5S-, 16S-, and 23S-like rRNAs have now been inferred based primarily on comparative sequence analyses (Gutell et al. 1985
; Ledje and Arnason 1996
; Springer and Douzery 1996
). The secondary structure of the 12S rRNA of fishes was proposed by Peer et al. (1994)
. Their model reveals a set of core pairing interactions common to 16S-like rRNAs. However, that study only included one sequence (Cyprinus carpio) without giving any compensatory evidence for base pairing interactions; so a further revision of the fish 12S rRNA core model is necessary.
Most evidence for compensatory changes was found by comparing distantly related taxa. However, such covariant mutation can also occur within closely related groups (Ortí et al. 1996
). In the present study, we compile a large number of gobioid 12S rRNA sequences, and those from other fish groups (table 1 ), in order to evaluate and improve the model of 12S rRNA set up by Peer et al. (1994)
for establishing a core set of fish base pairing interactions.
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Materials and Methods |
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Different phylogenetic methods, including neighbor-joining (NJ), maximum parsimony (MP), and maximum-likelihood (ML) were carried out using PAUP (Swofford 1999
). On the basis of the morphological studies, Hoese and Gill (1993)
treated Odontobutis as the sister group for the rest of the Gobioidei fishes. We also added Scomber australasicus (Perciformes) as outgroup for the analysis.
To study the impact of base covariance of stems on the phylogenetic analysis, we performed different loop-stem weightings as 1:1 (assumption of nucleotide independence), 1:0.8 (28S rRNA by Dixon and Hillis 1993
), 1:0.6 (12S rRNA by Springer and Douzery 1996
, and this study; see Results), 1:0.5 (strict dependence of nucleotides because of exact compensational changes), 1:0 (loop only), and 0:1 (stem only) when the MP method was performed. Only ratios of 1:1, 0:1, and 1:0 were used for the NJ and ML methods because of the difficulty in incorporating weighting per se into model-based methods (Tillier and Collins 1995
). For each weight used, 500 bootstrap replications were performed for the MP and NJ analyses. We do not carry out bootstrapping for the ML method because of time considerations. We also used the standard-error test of Rzhetsky and Nei (1992)
to estimate confidence probabilities for branches on the NJ tree using MEGA (Kumar, Tamura, and Nei 1993
).
Base compositions and nucleotide substitutions in stems and loops were determined using MEGA. The numbers of different types of substitutions were computed with MacClade (Maddison and Maddison 1992
) with reference to the established phylogeny. Substitutions in stem regions were divided into four types according to Springer, Hollar, and Burk (1995)
, which was in turn modified from Dixon and Hillis (1993)
: Type I (complementary to complementary), Type II (complementary to noncomplementary), Type III (noncomplementary to complementary), and Type IV (noncomplementary to noncomplementary). Each of these is further divided into single and double substitutions, depending on whether one or two substitutions occurred on a particular branch of the tree. The number of substitutions falling into each category listed above was tabulated by MacClade (Maddison and Maddison 1992
). In some cases, the mapped pathways of character evolution were ambiguous. In these instances, each of the alternative pathways was given equal weight in calculating the mean values as recommended by Maddison (1994)
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Results |
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Stem 4 is 8 bp long in the model of Peer et al. (1994, 2000)
and Springer and Douzery (1996)
. The potential base pairings at positions 4-5 and 4-6 of their model (the downstream 1st and 2nd bases of 4-4 in our model) were not found in most of the fish taxa surveyed. We further split this stem into stems 4 and 5, of four and two base pairs in length, respectively.
The region between 10 and 10' is highly variable where Peer et al. (1994, 2000)
recognized only one stem whereas Springer and Douzery (1996)
proposed two stems. When compared to the model of Springer and Douzery (1996)
, we recognized stems 10 and 11 to be three and five base pairings in length, respectively.
Although stem 11 is 6 bp long according to Gutell (1994)
and Springer and Douzery (1996)
, the potential base pairing at 11-6 is low in mammals (only 72% of the suborder-order surveyed). Within the fish group, pairings occur in 72% of sequences within gobioids and 50% in other fish groups examined. Because compensatory and noncompensatory mutations coexist within the same family (Margariscus and Cyprinus in Cyprinidae; Oncorhynchus and Salmo in Salmonidae; data not shown), we omitted this base in stem 11 from our core model.
The Cyprinus model constructed by Peer et al. (1994)
indicated that stem 12 is located between 10' and 7' and is two base pairings in length. This region was recognized as 2 bp long in Homo (Gutell 1994
) but only 1 bp long in the Springer and Douzery (1996)
mammalian model because of the co-occurrence of both compensatory and noncompensatory mutations. Sequences of this stem are almost identical across all taxa examined. The only but compensatory mutation was observed in Latimeria. We, therefore, tentatively retained this 2-bplong stem.
Like in Peer et al. (1994)
, stem 19 in our model is three bases in length, but two bases in the models by Springer and Douzery (1996)
and Peer et al. (2000)
. The additional base pair (19-3) shows 86% of potential base pairing within Gobioidei and 100% in the other fish taxa surveyed, having a positional covariance from guanine-cytosine (G:C) to adenine-thymine (A:T) found in Gadus and gobioids. We also noticed that the potential base pair is held within Carnivores (Ledje and Arnason 1996
).
As in Peer et al. (1994)
, stem 20 in our proposed model is a 6-bp helix against a 7-bp helix in the model by Springer and Douzery (1996)
and Peer et al. (2000)
. The pairing at 20-7 (the downstream 1st base of our model) occurs in 81% of the sequences investigated in gobioids with overwhelming noncompensatory mutations. In addition, because the position is not paired in sequences of most fishes other than gobioids, we removed it from our model. It is noteworthy that Gutell (1994)
proposed an alternative base pairing for this base with stem 23. This is discussed later.
In the model of mammals (Springer and Douzery 1996
), stem 21 is 5 bp in length. This region is highly variable and cannot be aligned reliably. We only recognize a three-base stem because the downstream 1st base was not paired in most of the gobioid sequences. In addition, we also failed to find this stem in Latimeria.
Stem 23 in our proposed model is 2 bp in length, as it was in the models of Peer et al. (1994)
and Springer and Douzery (1996)
, compared to the 3-bplong stem in Gutell (1994)
. The excess of 1 bp (21-3) in the latter conflicts with 20-7 in the model of Springer and Douzery (1996)
with positional covariance supporting both 20-7 and 23-3. This conflict was not observed in fish sequences which are not paired as either 20-7 or 23-3. Consequently, we did not consider this base in our model.
There are four base pairings in stem 27 as proposed by Peer et al. (1994)
, but like Peer et al. (2000)
we only recognized three. The potential base pairing at 27-4 (the downstream 1st base of our model) occurs in only 50% of the sequences analyzed, and was not recognized in the model proposed by Springer and Douzery (1996)
. But consistently, compensatory changes have been found at 27-2 from G:C in fishes to A:T in mammals.
Stem 28 is 4 bp long in our model as it is in the model of Peer et al. (1994)
. Evidence for a potential base pair at position 28-1 is missing in mammals (Springer and Douzery 1996
). In fish, the base pairing occurs across all taxa surveyed, and compensatory substitutions are found in Cyprinus, Crossostoma, and Gadus (see Supplementary Material).
As in the model of Springer and Douzery (1996)
, stem 34 in our model is 16 bp in length, which is 2 bp longer than in the models of Peer et al. (1994, 2000)
and Hickson et al. (1996). The additional two base pairs, 34-15 and 35-16, are almost identical across the fish sequences surveyed, but compensatory base substitutions of 34-15 are found in some invertebrates (fig. 2
of Hickson et al. 1996).
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Stem 39 is a 6-bp (Ledje and Arnason 1996
) or an 8-bp (Springer and Douzery 1996
) helix in mammals. However, we only recognize a 3-bp helix in our proposed model. The region between 39 and 39' is highly variable and difficult to align across diversified fish taxa. An additional three potential base pairs were observed in some fish taxa examined as Hickson et al. (1996) proposed, but both compensatory and noncompensatory mutations coexisted without any strong evidence from positional covariance. We tentatively propose a 3-bp helix for stem 39.
Phylogenetic Analysis
After the sequences were aligned, the regions that could not be aligned reliably were deleted, as indicated by solid black lines in figure 1
. In the 12S rRNAs analyzed, there are 443 bp in loops, 455 bp in stems, and 21 bp in bulges, and the 159 bp in loops, 91 bp in stems, and 4 bp in bulges are phylogenetic informative sites. For further analysis, we count bulges as loops rather than as stems, making a total of 464 bp in the loop set.
A single minimum-length tree derived from the MP method showing the relationships among the Gobioidei is given in figure 2
. The neighbor-joining method based on Kimura's two-parameter distance (Kimura 1980
) yields a tree with the same topology. All the nodes in figure 2
are supported by higher than 50% of both bootstrap replications and the standard-error test, and all but three nodes are supported at the 90% level by at least one of these methods. This result is in good agreement with both traditional (Hoese and Gill 1993
; Pezold 1993
, and references therein) and molecular phylogenetical interpretations (Wang et al. 2001
).
When stems and loops were analyzed separately, the relationships differed dramatically from those shown in figure 2 . A single MP tree based on stems resolved only nodes C, E, and F with low bootstrapping values. The minimum-length tree of loop regions generated by the MP method, in turn, resolved additional three nodes, A, D, and G with the collapse of B and C (table 2 ). The relationships within each supported node are identical with those in figure 2 . The results of different stem-loop weighting schemes generated by the MP method were also given in table 2 , in which increased stem weighting results in the tree topology resembling that in figure 2 . Although the results from the three tree-construction methods differed from each other, the general trend for the loop regions to produce a more constructive topology is the same (table 2 ). In addition, although the loop regions formed more nodes than did stems, stem regions showed better performance in resolving more diverged groups, e.g., node C (table 2 ).
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Discussion |
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Gobioidei Phylogeny
Following the approach of Dixon and Hillis (1993)
, the stem of 12S rRNA should be assigned a weight of 0.66, which is very close to that from mammals (0.61; Springer, Hollar, and Burk 1995
) and Serrasalminae (fishes; 0.63; Ortí et al. 1996
). It is worthy of note that the weighting of mammals was produced by comparing distantly related taxa covering the entire class whereas the latter focused on closely related groups, such as intergeneric comparisons. Because the weightings were transformed from the dependence of covariation (Dixon and Hillis 1993
), similar weightings obtained from a wide-ranging data set may represent the functional constraint(s) for maintaining stem pairings similar to those of the same gene across widely ranging taxa.
Wang et al. (2001)
have used 12S rRNA to study the phylogeny of Gobioidei. In that study, they did not take the different constraints between stems and loops into consideration. As shown in table 2
, it is clear that loops include more phylogenetic information than do stems and provide most of the resolutions in the 12S rRNA gene, especially when the recent divergent groups were considered. The stem regions alone, in turn, can only resolve more distantly related groups. The small number of informative sites is clearly insufficient to demonstrate relationships among most taxa. Nevertheless, loop regions failed to resolve node B and C. A combination of the two data sets shown in figure 2 produces a better resolution of relationships.
We also assigned different weights from 0.5 to 0.8 to the stem. It is clear that difference in stem weighting can be important in phylogenetic inference (table 2A
). When the stems were assigned a weight of 0.5, the monophyly of node B, Eleotrinae, was not resolved and the bootstrap percentage supporting each node was lower. Because the monophyly of Eleotrinae has been supported by osteological study (Hoese and Gill 1993
), this result is less preferred. As the stem weighting was increased to 0.66 and then to 0.8, the resolution of node B became positive, and the bootstrap percentage supporting each node also increased. In addition, there was no obvious difference between the results of the analysis with all characters equally weighted and the results of the analysis with stem characters assigned a weight of 0.8. Thus, increase in stem weighting produced a result closer to the current phylogenetic interpretations.
Phylogenetic Implications
In contrast to our results, Smith (1989)
and Morrison and Ellis (1999)
concluded that stem regions could produce more reliable trees than loop regions of the 18S rRNA gene. In addition, when using the 28S rRNA, Mugridge et al. (2000)
reported that both pairing and nonpairing regions are equally informative. Three reasons, which are not mutually exclusive, could explain these discrepancies. First, 12S rRNA (<1 kb) contains fewer nucleotides, resulting in fewer informative characters as expected. The 18S and 28S rRNAs, in turn, contain more nucleotides which may reveal more phylogenetic information. Second, the difference in length between different rRNAs may not only contribute to their informative accumulations but also influence their covariation dependency. The percentage of dependence (38%, Dixon and Hillis 1993
) for 28S rRNA is much lower than that of 12S rRNA (78%, Springer, Hollar, and Burk 1995
; 74%, Ortí et al. 1996
; 68%, present study). The finding of Stephan and Kirby (1993)
that the number of covariations decreased with physical distance in RNA secondary structures can apply to the above observation. Because 28S rRNA is three times longer than 12S rRNA, the latter is expected to have a higher proportion of covariation, indicating that most stem mutations in 28S rRNA genes lack compensatory substitutions. In other words, the stem regions of 28S rRNA may evolve more freely and independently, which, in turn, accumulate more phylogenetic information than those of 12S rRNA. Therefore, the result of the stems and loops of 28S rRNA being equally informative is not surprising. Third, as shown in table 2
, the degree of divergence among the taxa examined may be influential. Stems gave better results when distantly related taxa were analyzed. In addition, in the study of interordinal relationships within the mammals, Douzery and Catzeflis (1995)
showed that the stem as well as loop regions of 12S rRNA could resolve most of the phylogenetic nodes, although bootstrap replications of some nodes are lower than those from stem sets. Thus, 12S rRNA stem regions may be regarded as being more suitable for distantly related organisms rather than for recently diverged species.
Sequence Compositions and Nucleotide Substitutions
There is a clear violation of strand symmetry (Wu and Maeda 1987
) in the loop regions: the intrastrand equalities of A = T and G = C expected at equilibrium are not obeyed (table 2 ). An excess of adenine is also found in other metazoans. Vawter and Brown (1993)
found higher percentages of A in unpaired than in the paired regions including those of other vertebrates as well as invertebrates. This is presumably caused by A having the least polarity of the four bases, which results in subsequent hydrophobic interactions with proteins (Gutell et al. 1985
). This hypothesis, however, cannot explain the cause of higher C than G (1.5 times). On the other hand, skewness of nucleotide composition (A% > T%, C% > G% or A% + C% > T% + G%) was also found on the fourfold degenerate position of the mammalian (Reyes et al. 1998
) and intergenic regions of the metazoan (Jermiin, Graur, and Crozier 1995
) mitochondrial genome. Because the fourfold degenerate site and intergenic regions of the mtDNA genome are considered as selection-free or -limited positions (Asakawa et al. 1991
; Perna and Kocher 1995
), the violation of strand symmetry in both mitochondrial 12S rRNA loop regions and intergenic regions may reflect an underlying bias for mutations rather than for functional constraints.
Using 25 complete mammalian mitochondrial genomes to study the nucleotide compositions of all three codon positions and fourfold degenerate sites of H-strand genes, Reyes et al. (1998)
found a strong bias toward A and C on the H-strand protein-coding genes and the base composition in fourfold degenerate sites; the numbers of variable sites for each gene are significantly correlated with the duration of the single-stranded state of H-stranded genes during replication. Their main conclusion was that the spontaneous deamination of C and A in the H-strand may be one of the crucial processes for the origin of the asymmetric and biased base composition of mammalian mitochondrial genomes. The same condition is also applicable to the 12S rRNA gene loop regions. Less selective constraint allows the directional mutation pressure of the mtDNA genome to contribute to the biased nucleotide composition in the loop regions of 12S rRNA. In stem regions, in turn, because of the constraint of base pairing (table 5
), the change of A to T on one side and vice versa on the other side must occur simultaneously. The equilibrium frequency of A should be equal to that of T, and likewise, those of C and G should be equal (table 2
). Consequently, the strand symmetry in stem regions is the result of the selective pressure of base pairing.
This hypothesis can also elucidate the higher rate of CT transitions than AG transitions in the loop regions. Although a higher proportion of A% + G% (53.5%) than C% + T% (46.5%) in loop regions was noticed, the transition between C and T is much more profound than that between A and G. The same substitution patterns were also observed in the mammalian counterpart (Douzery and Catzeflis 1995
; Springer and Douzery 1996
). The different transition rates between AG and CT may reflect different deamination rates between C and A. The deamination rate of C estimated by Reyes et al. (1998)
and Tanaka and Ozawa (1994)
is twice as high as that of A. Because of the higher mutation rate from T to C, a greater abundance of CT transitions than AG transitions is expected.
The underlying selective pressure also contributes to different degrees of transitional-transversional bias between stem and loop regions. In stem regions, the base pairing under the A-to-G transition will be retained because both A:T and G:T pairings are allowed in the rRNA secondary structure. This is also true for the C-to-T transition, as the change of G:C to G:T can also be paired. On the other hand, any kind of transversion will destroy base pairing which is subjectively not selectively favored. In loop regions where base pairing is not required, the transition-transversion bias may only reflect the biased mutational pressure of the mtDNA genome.
Compared with its mammalian counterpart, lower proportions of A + T and higher proportions of G + C were found in paired regions of all fish taxa. The nucleotide frequencies of paired regions of mammalian 12S rRNA account only for 50.4%, which is 10% lower than that of fishes in general. The higher G + C composition in paired regions of rRNAs has been predicted based on free energy considerations because G:C pairs have a lower free energy value than G:T or A:T pairs (Turner, Sugimoto, and Freir 1988
). Martin (1995)
found that acceleration in the rate of oxygen consumption is associated with an increase in A + T nucleotides. The lower G + C composition in mammalian 12S rRNA may be caused by higher oxygen metabolism in mammals than in fishes.
Comparisons of substitutions that maintain or destroy base pairings demonstrate the strength of selection pressure for compensatory substitutions along the evolutionary tree. Some positions within stems, however, are characterized by mispairings according to our secondary structure model. Two reasons could explain that. First of all, some sites under study could be of limited functional importance, allowing mispairings to persist. In stem 11, the terminal loop between 11 and 11' is not conserved, ranging from 3 to 11 bases in length. There are two mispairings occurring at position 11-5 (Gadus and Latimeria). This could be caused by the loss of functional constraints in this region. Second, substitutions in one side of the stem are probably not simultaneously compensated for on the other side. This could lead to a time lag in compensation of the mispairing as demonstrated by Kraus et al. (1992)
. In stem 9 of Cyprinus, position 9-3 is not paired, but the compensatory substitutions are otherwise observed in Squalus and Mustelus. This could be because of the time lag of the G-to-C transversion on one side, but compensatory mutation on the other side not yet occurring.
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Supplementary Material |
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Acknowledgements |
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Footnotes |
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Keywords: nucleotide composition
deamination
asymmetric replication
transition-transversion bias
Address for correspondence and reprints: Sin-Che Lee, Laboratory of Molecular Systematics of Fishes, Institute of Zoology, Academia Sinica, Taipei 11529, Taiwan. sclee{at}gate.sinica.edu.tw
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