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Pause-melting misalignment: a novel model for the birth and motif indel of tandem repeats in the mitochondrial genome.

ABSTRACT: BACKGROUND: Tandem repeats (TRs) in the mitochondrial (mt) genome control region have been documented in a wide variety of vertebrate species. The mechanism by which repeated tracts originate and undergo duplication and deletion, however, remains unclear. RESULTS: We analyzed DNA sequences of mt genome TRs (mtTRs) in the ridged-eye flounder (Pleuronichthys cornutus), and characterized DNA sequences of mtTRs from other vertebrates using the data available in GenBank. Tandem repeats are concentrated in the control regions; however, we found approximately 16.6% of the TRs elsewhere in the mt genome. The flounder mtTRs possess three motif types with hypervariable characteristics at the 3' end of the control region (CR). CONCLUSION: Based on our analysis of this larger dataset of mtTR sequences, we propose a novel model of Pause Melting Misalignment (PMM) to describe the birth and motif indel of tandem repeats. PMM is activated during a pause event in mitochondrial replication in which a dynamic competition between the nascent (N) heavy strand and the displaced (D) heavy strand may lead to the melting of the N-strand from the template (T) light strand. When mispairing occurs during rebinding of the N-strand, one or several motifs can be inserted or deleted in both strands during the next round of mt-replication or repair. This model can explain the characteristics of TRs in available vertebrate mt genomes.

SUBMITTER: Shi W

PROVIDER: S-EPMC3599147 | biostudies-literature | 2013

REPOSITORIES: biostudies-literature

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Pause-melting misalignment: a novel model for the birth and motif indel of tandem repeats in the mitochondrial genome.

Shi Wei W Kong Xiao-Yu XY Wang Zhong-Ming ZM Yu Shan-Shan SS Chen Hai-Xia HX De Stasio Elizabeth A EA

BMC genomics 20130215

<h4>Background</h4>Tandem repeats (TRs) in the mitochondrial (mt) genome control region have been documented in a wide variety of vertebrate species. The mechanism by which repeated tracts originate and undergo duplication and deletion, however, remains unclear.<h4>Results</h4>We analyzed DNA sequences of mt genome TRs (mtTRs) in the ridged-eye flounder (Pleuronichthys cornutus), and characterized DNA sequences of mtTRs from other vertebrates using the data available in GenBank. Tandem repeats a ...[more]

PMID: 23414101

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Project description:BACKGROUND:Tandem repeat sequences are common in the genomes of many organisms and are known to cause important phenomena such as gene silencing and rapid morphological changes. Due to the presence of multiple copies of the same pattern in tandem repeats and their high variability, they contain a wealth of information about the mutations that have led to their formation. The ability to extract this information can enhance our understanding of evolutionary mechanisms. RESULTS:We present a stochastic model for the formation of tandem repeats via tandem duplication and substitution mutations. Based on the analysis of this model, we develop a method for estimating the relative mutation rates of duplications and substitutions, as well as the total number of mutations, in the history of a tandem repeat sequence. We validate our estimation method via Monte Carlo simulation and show that it outperforms the state-of-the-art algorithm for discovering the duplication history. We also apply our method to tandem repeat sequences in the human genome, where it demonstrates the different behaviors of micro- and mini-satellites and can be used to compare mutation rates across chromosomes. It is observed that chromosomes that exhibit the highest mutation activity in tandem repeat regions are the same as those thought to have the highest overall mutation rates. However, unlike previous works that rely on comparing human and chimpanzee genomes to measure mutation rates, the proposed method allows us to find chromosomes with the highest mutation activity based on a single genome, in essence by comparing (approximate) copies of the pattern in tandem repeats. CONCLUSION:The prevalence of tandem repeats in most organisms and the efficiency of the proposed method enable studying various aspects of the formation of tandem repeats and the surrounding sequences in a wide range of settings. AVAILABILITY:The implementation of the estimation method is available at http://ips.lab.virginia.edu/smtr .

Project description:BackgroundTandem repeats are ubiquitous and abundant in higher eukaryotic genomes and constitute, along with transposable elements, much of DNA underlying centromeres and other heterochromatic domains. In maize, centromeric satellite repeat (CentC) and centromeric retrotransposons (CR), a class of Ty3/gypsy retrotransposons, are enriched at centromeres. Some satellite repeats have homology to retrotransposons and several mechanisms have been proposed to explain the expansion, contraction as well as homogenization of tandem repeats. However, the origin and evolution of tandem repeat loci remain largely unknown.ResultsCRM1TR and CRM4TR are novel tandem repeats that we show to be entirely derived from CR elements belonging to two different subfamilies, CRM1 and CRM4. Although these tandem repeats clearly originated in at least two separate events, they are derived from similar regions of their respective parent element, namely the long terminal repeat (LTR) and untranslated region (UTR). The 5' ends of the monomer repeat units of CRM1TR and CRM4TR map to different locations within their respective LTRs, while their 3' ends map to the same relative position within a conserved region of their UTRs. Based on the insertion times of heterologous retrotransposons that have inserted into these tandem repeats, amplification of the repeats is estimated to have begun at least ~4 (CRM1TR) and ~1 (CRM4TR) million years ago. Distinct CRM1TR sequence variants occupy the two CRM1TR loci, indicating that there is little or no movement of repeats between loci, even though they are separated by only ~1.4 Mb.ConclusionsThe discovery of two novel retrotransposon derived tandem repeats supports the conclusions from earlier studies that retrotransposons can give rise to tandem repeats in eukaryotic genomes. Analysis of monomers from two different CRM1TR loci shows that gene conversion is the major cause of sequence variation. We propose that successive intrastrand deletions generated the initial repeat structure, and gene conversions increased the size of each tandem repeat locus.

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Project description:DNA tandem repeats, or satellites, are well described in eukaryotic species, but little is known about their prevalence across prokaryotes. Here, we performed the most complete characterization to date of satellites in bacteria. We identified 121,638 satellites from 12,233 fully sequenced and assembled bacterial genomes with a very uneven distribution. We also determined the families of satellites which have a related sequence. There are 85 genomes that are particularly satellite rich and contain several families of satellites of yet unknown function. Interestingly, we only found two main types of noncoding satellites, depending on their repeat sizes, 22/44 or 52 nucleotides (nt). An intriguing feature is the constant size of the repeats in the genomes of different species, whereas their sequences show no conservation. Individual species also have several families of satellites with the same repeat length and different sequences. This result is in marked contrast with previous findings in eukaryotes, where noncoding satellites of many sizes are found in any species investigated. We describe in greater detail these noncoding satellites in the spirochete Leptospira interrogans and in several bacilli. These satellites undoubtedly play a specific role in the species which have acquired them. We discuss the possibility that they represent binding sites for transcription factors not previously described or that they are involved in the stabilization of the nucleoid through interaction with proteins.IMPORTANCE We found an enigmatic group of noncoding satellites in 85 bacterial genomes with a constant repeat size but variable sequence. This pattern of DNA organization is unique and had not been previously described in bacteria. These findings strongly suggest that satellite size in some bacteria is under strong selective constraints and thus that satellites are very likely to play a fundamental role. We also provide a list and properties of all satellites in 12,233 genomes, which may be used for further genomic analysis.

Dataset Information

Pause-melting misalignment: a novel model for the birth and motif indel of tandem repeats in the mitochondrial genome.

Publications

Pause-melting misalignment: a novel model for the birth and motif indel of tandem repeats in the mitochondrial genome.

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