Replication slippage may cause parallel evolution in the secondary structures of mitochondrial transfer RNAs (original) (raw)
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Journal of Experimental Zoology Part B: Molecular and Developmental Evolution, 2006
Secondary structure stability of mitochondrial origins of light-strand replication (OL) presumably reduces delayed formation of light-strand initiating replication forks on the heavy strand. Delayed replication initiation prolongs single strandedness of the heavy strand. More mutations accumulate during the prolonged time spent single stranded. Presumably, delayed replication initiation and excess mutations affect mitochondrial biochemical processes and ultimately morphological outcomes of development at the whole-organism level. This predicts that developmental stability increases with OL secondary structure stability and with formation of OL-like structures by the five tRNA genes flanking recognized OLs. Stable OLs and high percentages of OL-resembling secondary structures of adjacent tRNA genes (predicted by Mfold) correlate positively with developmental stability in three lizard families (Anguidae, Amphisbaenidae, and Polychrotidae). Accounting for effects of the regular OL, Sfold-predicted OL-like propensity of the entire tRNA gene cluster (not of individual genes) correlates with increased developmental stability in Anguidae, also across the entire free-energy range of Boltzmann's distribution of secondary structures. In the fossorial Amphisbaenidae, the OL-like structure-forming propensity of tRNA genes correlates positively with developmental stability for the distribution's sub-optimally stable regions, and negatively for its optimally stable regions, suggesting the thermoregulated functioning of OL vs. flanking tRNA genes as replication origins. Results for polychrotid tRNA genes are intermediate. Anguid tRNA genes possibly function in addition to the regular OL. Mitochondrial tRNA genes may thus frequently acquire and lose the alternative OL function, without sequence (gene) duplication and loss of their primary function.
Journal of Molecular Evolution, 1997
A phylogenetic tree for major lineages of iguanian lizards is estimated from 1,488 aligned base positions (858 informative) of newly reported mitochondrial DNA sequences representing coding regions for eight tRNAs, ND2, and portions of ND1 and COI. Two well-supported groups are defined, the Acrodonta and the Iguanidae (sensu lato). This phylogenetic hypothesis is used to investigate evolutionary shifts in mitochondrial gene order, origin for light-strand replication, and secondary structure of tRNA Cys . These three characters shift together on the branch leading to acrodont lizards. Plate tectonics and the fossil record indicate that these characters changed in the Jurassic. We propose that changes to the secondary structure of tRNA Cys may destroy function of the origin for light-strand replication which, in turn, may facilitate shifts in gene order.
Molecular systematics of primary reptilian lineages and the tuatara mitochondrial genome
2003
We provide phylogenetic analyses for primary Reptilia lineages including, for the first time, Sphenodon punctatus (tuatara) using data from whole mitochondrial genomes. Our analyses firmly support a sister relationship between Sphenodon and Squamata, which includes lizards and snakes. Using Sphenodon as an outgroup for select squamates, we found evidence indicating a sister relationship, among our study taxa, between Serpentes (represented by Dinodon) and Varanidae. Our analyses support monophyly of Archosauria, and a sister relationship between turtles and archosaurs. This latter relationship is congruent with a growing set of morphological and molecular analyses placing turtles within crown Diapsida and recognizing them as secondarily anapsid (lacking a skull fenestration). Inclusion of Sphenodon, as the only surviving member of Sphenodontia (with fossils from the mid-Triassic), helps to fill a sampling gap within previous analyses of reptilian phylogeny. We also report a unique configuration for the mitochondrial genome of Sphenodon, including two tRNA Lys copies and an absence of ND5, tRNA His , and tRNA Thr genes.
Molecular Biology and Evolution, 1996
DNA (mtDNA) regions corresponding to two major tRNA gene clusters were amplified and sequenced for the Japanese pit viper, himehabu. In one of these clusters, which in most vertebrates characterized to date contains three tightly connected genes for tRNA"', tRNAG1", and tRNAMe', a sequence of approximately 1.3 kb was found to be inserted between the genes for tRNA"" and tRNA G'n. The insert consists of a control-regionlike sequence possessing some conserved sequence blocks, and short flanking sequences which may be folded into tRNAPro, tRNAPhe, and tRNALe" genes. Several other snakes belonging to different families were also found to possess a control-region-like sequence and tRNALe" gene between the tRNA"' and tRNAG'" genes. We also sequenced a region surrounded by genes for cytochrome b and 12s rRNA, where the control region and genes for tRNAPro and tRNAphe are normally located in the mtDNAs of most vertebrates. In this region of three examined snakes, a control-region-like sequence exists that is almost completely identical to the one found between the tRNA"' and tRNAG1" genes. The mtDNAs of these snakes thus possess two nearly identical control-region-like sequences which are otherwise divergent to a large extent between the species. These results suggest that the duplicate state of the control-region-like sequences has long persisted in snake mtDNAs, possibly since the original insertion of the control-region-like sequence and tRNALeu gene into the tRNA gene cluster, which occurred in the early stage of the divergence of snakes. It is also suggested that the duplicated control-region-like sequences at two distant locations of mtDNA have evolved concertedly by a mechanism such as frequent gene conversion. The secondary structures of the determined tRNA genes point to the operation of simplification pressure on the T J, C arm of snake mitochondrial tRNAs.
Genetics, 1998
The 17,191-bp mitochondrial DNA (mtDNA) of a Japanese colubrid snake, akamata (Dinodon semicarinatus), was cloned and sequenced. The snake mtDNA has some peculiar features that were found in our previous study using polymerase chain reaction: duplicate control regions that have completely identical sequences over 1 kbp, translocation of tRNALeu(UUR) gene, shortened TpsiC arm for most tRNA genes, and a pseudogene for tRNAPro. Phylogenetic analysis of amino acid sequences of protein genes suggested an unusually high rate of molecular evolution in the snake compared to other vertebrates. Southern hybridization experiments using mtDNAs purified from multiple akamata individuals showed that the duplicate state of the control region is not a transient or unstable feature found in a particular individual, but that it stably occurs in mitochondrial genomes of the species. This may, therefore, be regarded as an unprecedented example of stable functional redundancy in animal mtDNA. However, s...
Gene, 2007
For the first time the complete mitochondrial genome was sequenced for a member of Lacertidae. Lacerta viridis viridis was sequenced in order to compare the phylogenetic relationships of this family to other reptilian lineages. Using the long-polymerase chain reaction (long PCR) we characterized a mitochondrial genome, 17,156 bp long showing a typical vertebrate pattern with 13 protein coding genes, 22 transfer RNAs (tRNA), two ribosomal RNAs (rRNA) and one major noncoding region. The noncoding region of L. v. viridis was characterized by a conspicuous 35 bp tandem repeat at its 5′ terminus. A phylogenetic study including all currently available squamate mitochondrial sequences demonstrates the position of Lacertidae within a monophyletic squamate group. We obtained a narrow relationship of Lacertidae to Scincidae, Iguanidae, Varanidae, Anguidae, and Cordylidae. Although, the internal relationships within this group yielded only a weak resolution and low bootstrap support, the revealed relationships were more congruent with morphological studies than with recent molecular analyses.
Molecular Biology and Evolution, 2007
A complete mitochondrial DNA (mtDNA) sequence was determined for the lizard Calotes versicolor (Reptilia; Agamidae). The 16,670-bp genome with notable shorter genes for some protein-coding and tRNA genes had the same gene content as that found in other vertebrates. However, a novel gene arrangement was found in which the proline tRNA (trnP) gene is located in the light strand instead of its typical heavy-strand position, providing the first known example of gene inversion in vertebrate mtDNAs. A segment of mtDNA encompassing the trnP gene and its flanking genes and the control region was amplified and sequenced for various agamid taxa to investigate timing and mechanism of the gene inversion. The inverted trnP gene organization was shared by all South Asian draconine agamids examined but by none of the other Asian and African agamids. Phylogenetic analyses including clock-free Bayesian analyses for divergence time estimation suggested a single occurrence of the gene inversion on a lineage leading to the draconine agamids during the Paleogene period. This gene inversion could not be explained by the tandem duplication/random loss model for mitochondrial gene rearrangements. Our available sequence data did not provide evidence for remolding of the trnP gene by an anticodon switch in a duplicated tRNA gene. Based on results of sequence comparisons and other circumstantial evidence, we hypothesize that inversion of the trnP gene was originally mediated by a homologous DNA recombination and that the de novo gene organization that does not disrupt expression of mitochondrial genes has been maintained in draconine mtDNAs for such a long period of time.
The Evolution of tRNA-Leu Genes in Animal Mitochondrial Genomes
2003
Animal mitochondrial genomes usually have two transfer RNAs for Leucine: one, with anticodon UAG, translates the four-codon family CUN, whilst the other, with anticodon UAA, translates the twocodon family UUR. These two genes must differ at the third anticodon position, but in some species the genes differ at many additional sites, indicating that these genes have been independent for a long time. Duplication and deletion of genes in mitochondrial genomes occurs frequently during the evolution of the Metazoa. If a tRNA-Leu gene were duplicated and a substitution occurred in the anticodon, this would effectively turn one type of tRNA into the other. The original copy of the second tRNA type might then be lost by a deletion elsewhere in the genome. There are several groups of species in which the two tRNA-Leu genes occur next to one another (or very close) on the genome, which suggests that tandem duplication has occurred. Here we use RNA-specific phylogenetic methods to determine evolutionary trees for both genes. We present evidence that the process of duplication, anticodon mutation and deletion of tRNA-Leu genes has occurred at least five times during the evolution of the Metazoa -once in the common ancestor of all Protostomes, once in the common ancestor of Echinoderms and Hemichordates, once in the hermit crab, and twice independently in Molluscs.