Tracing plant Mitochondrial DNA evolution: rearrangements of the ancient mitochondrial gene cluster trnA-trnT-nad7 in liverwort phylogeny

Whereas frequent recombination characterizes flowering plant mitochondrial genomes, some mitochondrial gene arrangements may, in contrast, be conserved between streptophyte algae and early land plant clades (bryophytes). Here we explore the evolutionary fate of the mitochondrial gene arrangement trnA-trnT-nad7, which is conserved among the alga Chara, the moss Physcomitrella, and the liverwort Marchantia, although trnT is inverted in orientation in the latter. Surprisingly, we now find that the Chara-type gene arrangement is generally conserved in mosses, but that trnT is lacking between trnA and nad7 in all simple-thalloid and leafy (jungermanniid) liverworts. The ancient gene continuity trnA-trnT-nad7 is, however, conserved in Blasia, representing the sister lineage to all other complex-thalloid (marchantiid) liverworts. The recombinogenic insertion of short sequence stretches, including nad5 and rps7 pseudogene fragments copied from elsewhere in the liverwort mtDNA, likely mediated a subsequent inversion of trnT and flanking sequences in a basal grade of marchantiid liverworts, which was then followed by an independent secondary loss of trnT in derived marchantiid taxa later in evolution. In contrast to the previously observed extreme degree of coding sequence conservation and the assumed absence of active recombination in Marchantia mtDNA, this now reveals a surprisingly dynamic evolution of marchantiid liverwort mitochondrial genomes.     

Mitochondrial gene rearrangements: new paradigm in the evolutionary biology and systematics

Mitochondrial (mt) genomic study may reveal significant insight into the molecular evolution and several other aspects of genome evolution such as gene rearrangements evolution, gene regulation, and replication mechanisms. Other questions such as patterns of gene expression mechanism evolution, genomic variation and its correlation with physiology, and other molecular and biochemical mechanisms can be addressed by the mt genomics. Rare genomic changes have attracted evolutionary biology community for providing homoplasy free evidence of phylogenetic relationships. Gene rearrangements are considered to be rare evolutionary events and are being used to reconstruct the phylogeny of diverse group of organisms. Mt gene rearrangements have been established as a hotspot for the phylogenetic and evolutionary analysis of closely as well as distantly related organisms.     

Mitochondrial gene rearrangements suggest a new genus in the subfamily Cantharinae (Coleoptera)

The Cephalomalthinus semifumatus species group, referred to as the “semifumatus” group henceforth, is interesting because of its heterogeneous morphology resembling either Cephalomalthinus Pic, 1921 or Rhagonycha Eschscholtz, 1830. To elucidate its phylogenetic status, mitochondrial genomes of four species of the “semifumatus” group, 11 Cephalomalthinus species, and 11 Rhagonycha species were sequenced and examined. All analysed mitogenomes were similar with respect to genome size, nucleotide composition, and AT content. Surprisingly, a rearrangement of the trnW-trnC and trnY genes was detected in the “semifumatus” group, presumably caused by tandem duplication and random loss events. Furthermore, genetic distance analyses showed that the proximity of the “semifumatus” group to Cephalomalthinus and to Rhagonycha was comparable to that between the latter two. Moreover, the produced phylogeny strongly supported the monophyly of the “semifumatus” group, and molecular clock analyses dated its divergence from Cephalomalthinus to 32.52 Ma. Thus, the new genus Amphimorphus gen. nov. is suggested to comprise the “semifumatus” group, in which the observed gene rearrangement was a synapomorphy. Moreover, morphological evidence regarding the unique structure of the aedeagus supported this separation. These results indicate that mitochondrial gene rearrangement provide important phylogenetic implications for revising Cephalomalthinus, a speciose genus that is puzzling in the morphology-based taxonomy.     

Mitochondrial genomes of acrodont lizards: timing of gene rearrangements and phylogenetic and biogeographic implications

Background  

Acrodonta consists of Agamidae and Chamaeleonidae that have the characteristic acrodont dentition. These two families and Iguanidae sensu lato are members of infraorder Iguania. Phylogenetic relationships and historical biogeography of iguanian lizards still remain to be elucidated in spite of a number of morphological and molecular studies. This issue was addressed by sequencing complete mitochondrial genomes from 10 species that represent major lineages of acrodont lizards. This study also provided a good opportunity to compare molecular evolutionary modes of mitogenomes among different iguanian lineages.     

Mitochondrial genome of the Komodo dragon: efficient sequencing method with reptile-oriented primers and novel gene rearrangements.

The mitochondrial genome of the Komodo dragon (Varanus komodoensis) was nearly completely sequenced, except for two highly repetitive noncoding regions. An efficient sequencing method for squamate mitochondrial genomes was established by combining the long polymerase chain reaction (PCR) technology and a set of reptile-oriented primers designed for nested PCR amplifications. It was found that the mitochondrial genome had novel gene arrangements in which genes from NADH dehydrogenase subunit 6 to proline tRNA were extensively shuffled with duplicate control regions. These control regions had 99% sequence similarity over 700 bp. Although snake mitochondrial genomes are also known to possess duplicate control regions with nearly identical sequences, the location of the second control region suggested independent occurrence of the duplication on lineages leading to snakes and the Komodo dragon. Another feature of the mitochondrial genome of the Komodo dragon was the considerable number of tandem repeats, including sequences with a strong secondary structure, as a possible site for the slipped-strand mispairing in replication. These observations are consistent with hypotheses that tandem duplications via the slipped-strand mispairing may induce mitochondrial gene rearrangements and may serve to maintain similar copies of the control region.     

Lateral gene transfer and parallel evolution in the history of glutathione biosynthesis genes

Background  

Glutathione is found primarily in eukaryotes and in Gram-negative bacteria. It has been proposed that eukaryotes acquired the genes for glutathione biosynthesis from the alpha-proteobacterial progenitor of mitochondria. To evaluate this, we have used bioinformatics to analyze sequences of the biosynthetic enzymes γ-glutamylcysteine ligase and glutathione synthetase.     

Reverse engineering a gene network using an asynchronous parallel evolution strategy

Background  

The use of reverse engineering methods to infer gene regulatory networks by fitting mathematical models to gene expression data is becoming increasingly popular and successful. However, increasing model complexity means that more powerful global optimisation techniques are required for model fitting. The parallel Lam Simulated Annealing (pLSA) algorithm has been used in such approaches, but recent research has shown that island Evolutionary Strategies can produce faster, more reliable results. However, no parallel island Evolutionary Strategy (piES) has yet been demonstrated to be effective for this task.     

Toxin-resistant sodium channels: parallel adaptive evolution across a complete gene family

Approximately 75% of vertebrate proteins belong to protein families encoded by multiple evolutionarily related genes, a pattern that emerged as a result of gene and genome duplications over the course of vertebrate evolution. In families of genes with similar or related functions, adaptation to a strong selective agent should involve multiple adaptive changes across the entire gene family. However, we know of no evolutionary studies that have explicitly addressed this point. Here, we show how 4 taxonomically diverse species of pufferfishes (Tetraodontidae) each evolved resistance to the guanidinium toxins tetrodotoxin (TTX) and saxitoxin (STX) via parallel amino acid replacements across all 8 sodium channels present in teleost fish genomes. This resulted in diverse suites of coexisting sodium channel types that all confer varying degrees of toxin resistance, yet show remarkable convergence among genes and phylogenetically diverse species. Using site-directed mutagenesis and expression of a vertebrate sodium channel, we also demonstrate that resistance to TTX/STX is enhanced up to 15-fold by single, frequently observed replacements at 2 sites that have not previously been implicated in toxin binding but show similar or identical replacements in pufferfishes and in distantly related vertebrate and nonvertebrate animals. This study presents an example of natural selection acting upon a complete gene family, repeatedly arriving at a diverse but limited number of adaptive changes within the same genome. To be maximally informative, we suggest that future studies of molecular adaptation should consider all functionally similar paralogs of the affected gene family.     

Chromosome rearrangements and the evolution of genome structuring and adaptability

Eukaryotes appear to evolve by micro and macro rearrangements. This is observed not only for long-term evolutionary adaptation, but also in short-term experimental evolution of yeast, Saccharomyces cerevisiae. Moreover, based on these and other experiments it has been postulated that repeat elements, retroposons for example, mediate such events. We study an evolutionary model in which genomes with retroposons and a breaking/repair mechanism are subjected to a changing environment. We show that retroposon-mediated rearrangements can be a beneficial mutational operator for short-term adaptations to a new environment. But simply having the ability of rearranging chromosomes does not imply an advantage over genomes in which only single-gene insertions and deletions occur. Instead, a structuring of the genome is needed: genes that need to be amplified (or deleted) in a new environment have to cluster. We show that genomes hosting retroposons, starting with a random order of genes, will in the long run become organized, which enables (fast) rearrangement-based adaptations to the environment. In other words, our model provides a "proof of principle" that genomes can structure themselves in order to increase the beneficial effect of chromosome rearrangements.     

Large and small rearrangements in the evolution of prokaryotic genomes

Relative frequencies of large and small genome rearrangements (inversions and transpositions) in the evolution of prokaryotic genomes can be evaluated using the ratio between the index S (the ratio of the number of identical pairs of neighboring genes in two genomes to the total number of genes in the sample of interest) and 1 - 6 x L/n, where L is the mean difference in intergenic distances and n is the number of genes in the sample. The S value uniformly decreases with the fixation of genome rearrangements, while the decrease rate of I - 6 x L/n is determined by the rearrangement size. Specifically, large inversions and transpositions lead to a dramatic decrease in the index value, while small rearrangements result in an insignificant decrease. The ratio between these indices was computed for twenty pairs of closely related species belonging to different groups of bacteria and archaea. The pairs examined strongly differed in the relative frequency of large and small rearrangements. However, computer simulation showed that the total variation can be reproduced with the same input parameters of the model. This means that the differences observed can be stochastic and can be interpreted without assuming different mechanisms and factors of genome rearrangements for different groups of prokaryotes. Relative frequencies of large and small rearrangements displayed no noticeable correlations with taxonomic position, total rate of rearrangement fixation, habitation conditions, and the abundance of transposons and repetitive sequences. It is suggested that, in some cases, phage activity increases the frequency of large genome rearrangements.     

Mitochondrial genome evolution in the social amoebae

Most mitochondria contain a core set of genes required for mitochondrial function, but beyond this base there are variable genomic features. The mitochondrial genome of the model species Dictyostelium discoideum demonstrated that the social amoebae mitochondrial genomes have a size between those of metazoans and plants, but no comparative study of social amoebae mitochondria has been performed. Here, we present a comparative analysis of social amoebae mitochondrial genomes using D. discoideum, Dictyostelium citrinum, Dictyostelium fasciculatum, and Polysphondylium pallidum. The social amoebae mitochondria have similar sizes, AT content, gene content and have a high level of synteny except for one segmental rearrangement and extensive displacement of tRNAs. From the species that contain the rearrangement, it can be concluded that the event occurred late in the evolution of social amoebae. A phylogeny using 36 mitochondrial genes produced a well-supported tree suggesting that the pairs of D. discoideum/D. citrinum and D. fasciculatum/P. pallidum are sister species although the position of the root is not certain. Group I introns and endonucleases are variable in number and location in the social amoebae. Phylogenies of the introns and endonucleases suggest that there have been multiple recent duplications or extinctions and confirm that endonucleases have the ability to insert into new areas. An analysis of dN/dS ratios in mitochondrial genes revealed that among groups of genes, adenosine triphosphate synthase complex genes have the highest ratio, whereas cytochrome oxidase and nicotinamide adenine dinucleotide (NADH) dehydrogenase genes had the lowest ratio. The genetic codes of D. citrinum, P. pallidum, and D. fasciculatum are the universal code although D. fasciculatum does not use the TGA stop codon. In D. fasciculatum, we demonstrate for the first time that a mitochondrial genome without the TGA stop codon still uses the release factor RF2 that recognizes TGA. Theories of how the genetic code can change and why RF2 may be a constraint against switching codes are discussed.     

The probability of parallel evolution

Abstract How often will natural selection drive parallel evolution at the DNA sequence level? More precisely, what is the probability that selection will cause two populations that live in identical environments to substitute the same beneficial mutation? Here I show that, under fairly general conditions, the answer is simple: if a wild‐type sequence can mutate to n different beneficial mutations, replicate populations will on average fix the same mutation with probability P= 2/(n + 1). This probability, which is derived using extreme value theory, is independent of most biological details, including the length of the gene in question and the precise distribution of fitness effects among alleles. I conclude that the probability of parallel evolution under natural selection is nearly twice as large as that under neutrality.     

Mitochondrial DNA evolution in the genus Equus

Employing mitochondrial DNA (mtDNA) restriction-endonuclease maps as the basis of comparison, we have investigated the evolutionary affinities of the seven species generally recognized as the genus Equus. Individual species' cleavage maps contained an average of 60 cleavage sites for 16 enzymes, of which 29 were invariant for all species. Based on an average divergence rate of 2%/Myr, the variation between species supports a divergence of extant lineages from a common ancestor approximately 3.9 Myr before the present. Comparisons of cleavage maps between Equus przewalskii (Mongolian wild horse) and E. caballus (domestic horse) yielded estimates of nucleotide sequence divergence ranging from 0.27% to 0.41%. This range was due to intraspecific variation, which was noted only for E. caballus. For pairwise comparisons within this family, estimates of sequence divergence ranged from 0% (E. hemionus onager vs. E. h. kulan) to 7.8% (E. przewalskii vs. E. h. onager). Trees constructed according to the parsimony principle, on the basis of 31 phylogenetically informative restriction sites, indicate that the three extant zebra species represent a monophyletic group with E. grevyi and E. burchelli antiquorum diverging most recently. The phylogenetic relationships of E. africanus and E. hemionus remain enigmatic on the basis of the mtDNA analysis, although a recent divergence is unsupported.      

Large and small rearrangements in the evolution of prokaryotic genomes

Relative frequencies of large and small genome rearrangements (inversions and transpositions) in the evolution of prokaryotic genomes can be evaluated using the ratio between the index S (the ratio of the number of identical pairs of neighboring genes in two genomes to the total number of genes in the sample of interest) and 1–6L/n, where L is the mean difference in intergenic distances and n is the number of genes in the sample. The S value uniformly decreases with the fixation of genome rearrangements, while the decrease rate of 1–6L/n is determined by the rearrangement size. Specifically, large inversions and transpositions lead to a dramatic decrease in the index value, while small rearrangements result in an insignificant decrease. The ratio between these indices was computed for twenty pairs of closely related species belonging to different groups of bacteria and archaea. The pairs examined strongly differed in the relative frequency of large and small rearrangements. However, computer simulation showed that the total variation can be reproduced with the same input parameters of the model. This means that the differences observed can be stochastic and can be interpreted without assuming different mechanisms and factors of genome rearrangements for different groups of prokaryotes. Relative frequencies of large and small rearrangements displayed no noticeable correlations with taxonomic position, total rate of rearrangement fixation, habitation conditions, and the abundance of transposons and repetitive sequences. It is suggested that, in some cases, phage activity increases the frequency of large genome rearrangements.     

Mitochondrial DNA and bindin gene sequence evolution among allopatric species of the sea urchin genus Arbacia

Sea urchins of the genus Arbacia (order Stirodonta) have discontinuous allopatric distributions ranging over thousands of kilometers. Mitochondrial DNA (mtDNA) sequences were used to reconstruct phylogenetic relationships of four Arbacia species and their geographic populations. There is little evidence of genetic structuring of populations within species, except in two cases at range extremes. The mtDNA sequence differentiation between species suggests that divergence occurred about 4-9 MYA. Gene sequences encoding the sperm protein bindin and its intron were obtained and compared with the mtDNA phylogeny. Sea urchins among the well-studied echinoid order Camarodonta, with degrees of mtDNA divergence similar to those of Arbacia species, are known to have remarkable variation in bindin. However, in Arbacia, little variation in deduced amino acid sequences of bindin was found, indicating that purifying selection acts on the protein. In contrast, bindin intron sequences showed much differentiation, including numerous insertion/deletions. Fertilization experiments performed between a divergent pair of Arbacia species from the Atlantic and Pacific Oceans revealed no evidence of blocks to gamete recognition. In Arbacia, fertilization specificities may have evolved relatively slowly as a result of extensive gene flow within species, greater functional constraint on the bindin polypeptide, or reduced selective pressure for species recognition in singly occurring species.      

Effects of chromosomal rearrangements on human-chimpanzee molecular evolution

Many chromosomes are rearranged between humans and chimpanzees while others remain colinear. It was recently observed, based on over 100 genes, that the rates of protein evolution are substantially higher on rearranged than on colinear chromosomes during human-chimpanzee evolution. This finding led to the conclusion, since debated in the literature, that chromosomal rearrangements had played a key role in human-chimpanzee speciation. Here we re-examine this important conclusion by employing larger a data set (over 7000 genes), as well as alternative analyses. We show that the higher rates of protein evolution on rearranged chromosomes observed in the earlier study are not reproduced by our survey of the larger data set. We further show that the conclusion of the earlier study is likely confounded by two factors introduced by the relatively limited sample size: (1) nonuniform distribution of genes in the genome, and (2) stochastic noise in substitution rates inherent to short lineages such as the human-chimpanzee lineage. Our results offer a general cautionary note on the importance of controlling for hidden factors in studies involving bioinformatic surveys.     

Mitochondrial genomes of a bandicoot and a brushtail possum confirm the monophyly of australidelphian marsupials.

Recent molecular analyses suggest that the position of bandicoots is the major difficulty in determining the root of the tree of extant marsupials. To resolve this, we analyse mitochondrial genome sequences of a bandicoot (Isoodon macrourus) and a brushtail possum (Trichosurus vulpecula) together with the previously available marsupial mitochondrial genomes, the Virginia opossum (Didelphis virginiana) and the wallaroo (Macropus robustus). Analyses of mitochondrial protein-coding and RNA genes strongly support the bandicoot as sister to the wallaroo and the brushtail possum. This result, combined with other recent molecular analyses, confirms the monophyly of Australidelphia (Australasian marsupials plus Dromiciops from South America). Further, RY coding was found to nullify AGCT coding nucleotide composition bias.