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A scenario of mitochondrial genome evolution in maize based on rearrangement events.

ABSTRACT: BACKGROUND: Despite their monophyletic origin, animal and plant mitochondrial genomes have been described as exhibiting different modes of evolution. Indeed, plant mitochondrial genomes feature a larger size, a lower mutation rate and more rearrangements than their animal counterparts. Gene order variation in animal mitochondrial genomes is often described as being due to translocation and inversion events, but tandem duplication followed by loss has also been proposed as an alternative process. In plant mitochondrial genomes, at the species level, gene shuffling and duplicate occurrence are such that no clear phylogeny has ever been identified, when considering genome structure variation. RESULTS: In this study we analyzed the whole sequences of eight mitochondrial genomes from maize and teosintes in order to comprehend the events that led to their structural features, i.e. the order of genes, tRNAs, rRNAs, ORFs, pseudogenes and non-coding sequences shared by all mitogenomes and duplicate occurrences. We suggest a tandem duplication model similar to the one described in animals, except that some duplicates can remain. This model enabled us to develop a manual method to deal with duplicates, a recurrent problem in rearrangement analyses. The phylogenetic tree exclusively based on rearrangement and duplication events is congruent with the tree based on sequence polymorphism, validating our evolution model. CONCLUSIONS: This study suggests more similarity than usually reported between plant and animal mitochondrial genomes in their mode of evolution. Further work will consist of developing new tools in order to automatically look for signatures of tandem duplication events in other plant mitogenomes and evaluate the occurrence of this process on a larger scale.

SUBMITTER: Darracq A

PROVIDER: S-EPMC2859866 | biostudies-literature | 2010

REPOSITORIES: biostudies-literature

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A scenario of mitochondrial genome evolution in maize based on rearrangement events.

Darracq Aude A Varré Jean-Stéphane JS Touzet Pascal P

BMC genomics 20100409

<h4>Background</h4>Despite their monophyletic origin, animal and plant mitochondrial genomes have been described as exhibiting different modes of evolution. Indeed, plant mitochondrial genomes feature a larger size, a lower mutation rate and more rearrangements than their animal counterparts. Gene order variation in animal mitochondrial genomes is often described as being due to translocation and inversion events, but tandem duplication followed by loss has also been proposed as an alternative p ...[more]

PMID: 20380689

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Project description:Mitochondrial genome rearrangements that result in control region duplication have been described for a variety of birds, but the mechanisms leading to their appearance and maintenance remain unclear, and their effect on sequence evolution has not been explored. A recent survey of mitochondrial genomes in the Psittaciformes (parrots) found that control region duplications have arisen independently at least six times across the order. We analyzed complete mitochondrial genome sequences from 20 parrot species, including representatives of each lineage with control region duplications, to document the gene order changes and to examine effects of genome rearrangements on patterns of sequence evolution. The gene order previously reported for Amazona parrots was found for four of the six independently derived genome rearrangements, and a previously undescribed gene order was found in Prioniturus luconensis, representing a fifth clade with rearranged genomes; the gene order resulting from the remaining rearrangement event could not be confirmed. In all rearranged genomes, two copies of the control region are present and are very similar at the sequence level, while duplicates of the other genes involved in the rearrangement show signs of degeneration or have been lost altogether. We compared rates of sequence evolution in genomes with and without control region duplications and did not find a consistent acceleration or deceleration associated with the duplications. This could be due to the fact that most of the genome rearrangement events in parrots are ancient, and additionally, to an effect of body size on evolutionary rate that we found for mitochondrial but not nuclear sequences. Base composition analyses found that relative to other birds, parrots have unusually strong compositional asymmetry (AT- and GC-skew) in their coding sequences, especially at fourfold degenerate sites. Furthermore, we found higher AT skew in species with control region duplications. One potential cause for this compositional asymmetry is that parrots have unusually slow mtDNA replication. If this is the case, then any replicative advantage provided by having a second control region could result in selection for maintenance of both control regions once duplicated.

Project description:BackgroundThe mitochondrial (mt) genomes of Sarcoptiformes mites typically contain 37 genes. Although the loss of genes is rare in Sarcoptiformes mite mitogenomes, two of the six previously reported oribatid mites (Acariforms: Sarcoptiformes) are reported to have lost parts of their tRNA genes. To confirm whether the tRNA genes were indeed lost and whether the loss is universal, we re-annotated the available oribatid mite sequences and sequenced the mitogenome of Oribatula sakamorii.MethodsThe mitogenome of O. sakamorii was sequenced using an Illumina HiSeq sequencer. The mt tRNA gene was annotated using multi-software combined with a manual annotation approach. Phylogenetic analyses were performed using the maximum likelihood and Bayesian inference methods with concatenated nucleotide and amino acid sequences.ResultsThe mitogenomes of O. sakamorii contained 37 genes, including 22 tRNA genes. We identified all mt tRNA genes that were reported as "lost" in Steganacarus magnus and Paraleius leontonychus and revealed certain atypical tRNA annotation errors in oribatid mite sequences. Oribatid mite mitogenomes are characterized by low rates of genetic rearrangement, with six or seven gene blocks conserved between the mitogenome of all species and that of ancestral arthropods. Considering the relative order of the major genes (protein-coding genes and rRNAs), only one or two genes were rearranged with respect to their positions in the ancestral genome. We explored the phylogenetic relationships among the available oribatid mites, and the results confirmed the systematic position of Hermannia in the Crotonioidea superfamily. This was also supported by the synapomorphic gene-derived boundaries.ConclusionsThe tRNA "lost" phenomenon is not universal in oribatid mites. Rather, highly atypical secondary structure of the inferred mt tRNA genes made them unidentifiable using a single type of tRNA search program. The use of multi-software combined with a manual annotation approach can improve the accuracy of tRNA gene annotation. In addition, we identified the precise systematic position of Hermannia and validated that Astigmata is nested in Oribatida.

Project description:Despite high pertussis vaccine coverage, reported cases of whooping cough (pertussis) have increased over the last decade in the United States and other developed countries. Although Bordetella pertussis is well known for its limited gene sequence variation, recent advances in long-read sequencing technology have begun to reveal genomic structural heterogeneity among otherwise indistinguishable isolates, even within geographically or temporally defined epidemics. We have compared rearrangements among complete genome assemblies from 257 B. pertussis isolates to examine the potential evolution of the chromosomal structure in a pathogen with minimal gene nucleotide sequence diversity. Discrete changes in gene order were identified that differentiated genomes from vaccine reference strains and clinical isolates of various genotypes, frequently along phylogenetic boundaries defined by single nucleotide polymorphisms. The observed rearrangements were primarily large inversions centered on the replication origin or terminus and flanked by IS481, a mobile genetic element with >240 copies per genome and previously suspected to mediate rearrangements and deletions by homologous recombination. These data illustrate that structural genome evolution in B. pertussis is not limited to reduction but also includes rearrangement. Therefore, although genomes of clinical isolates are structurally diverse, specific changes in gene order are conserved, perhaps due to positive selection, providing novel information for investigating disease resurgence and molecular epidemiology.IMPORTANCE Whooping cough, primarily caused by Bordetella pertussis, has resurged in the United States even though the coverage with pertussis-containing vaccines remains high. The rise in reported cases has included increased disease rates among all vaccinated age groups, provoking questions about the pathogen's evolution. The chromosome of B. pertussis includes a large number of repetitive mobile genetic elements that obstruct genome analysis. However, these mobile elements facilitate large rearrangements that alter the order and orientation of essential protein-encoding genes, which otherwise exhibit little nucleotide sequence diversity. By comparing the complete genome assemblies from 257 isolates, we show that specific rearrangements have been conserved throughout recent evolutionary history, perhaps by eliciting changes in gene expression, which may also provide useful information for molecular epidemiology.

Dataset Information

A scenario of mitochondrial genome evolution in maize based on rearrangement events.

Publications

A scenario of mitochondrial genome evolution in maize based on rearrangement events.

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