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Intraspecific rearrangement of mitochondrial genome suggests the prevalence of the tandem duplication-random loss (TDLR) mechanism in Quasipaa boulengeri.

ABSTRACT: Tandem duplication followed by random loss (TDRL) is the most frequently invoked model to explain the diversity of gene rearrangements in metazoan mitogenomes. The initial stages of gene rearrangement are difficult to observe in nature, which limits our understanding of incipient duplication events and the subsequent process of random loss. Intraspecific gene reorganizations may represent intermediate states, and if so they potentially shed light on the evolutionary dynamics of TDRL.Nucleotide sequences in a hotspot of gene-rearrangement in 28 populations of a single species of frog, Quasipaa boulengeri, provide such predicted intermediate states. Gene order and phylogenetic analyses support a single tandem duplication event and a step-by-step process of random loss. Intraspecific gene rearrangements are not commonly found through comparison of all mitochondrial DNA records of amphibians and squamate reptiles in GenBank.The intraspecific variation in Q. boulengeri provides insights into the rate of partial duplications and deletions within a mitogenome, and reveals that fixation and gene-distribution in mitogenomic reorganization is likely non-adaptive.

SUBMITTER: Xia Y

PROVIDER: S-EPMC5122201 | biostudies-literature | 2016 Nov

REPOSITORIES: biostudies-literature

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Intraspecific rearrangement of mitochondrial genome suggests the prevalence of the tandem duplication-random loss (TDLR) mechanism in Quasipaa boulengeri.

Xia Yun Y Zheng Yuchi Y Murphy Robert W RW Zeng Xiaomao X

BMC genomics 20161124 1

<h4>Background</h4>Tandem duplication followed by random loss (TDRL) is the most frequently invoked model to explain the diversity of gene rearrangements in metazoan mitogenomes. The initial stages of gene rearrangement are difficult to observe in nature, which limits our understanding of incipient duplication events and the subsequent process of random loss. Intraspecific gene reorganizations may represent intermediate states, and if so they potentially shed light on the evolutionary dynamics o ...[more]

PMID: 27881087

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Project description:The mitochondrial genomes (mitogenomes) of flatfishes (Pleuronectiformes) exhibit highly diversified types of large-scale gene rearrangements. We have reported that the mitogenomes of Crossorhombus azureus (Bothidae), Samariscus latus (Samaridae) and Cynoglossus fishes (Cynoglossidae) show different types of gene rearrangements.In the present study, the complete mitogenomes of two Symphurus species (Cynoglossidae), Symphurus plagiusa and Symphurus orientalis, were determined. The gene order in the S. plagiusa mitogenome is the same as that of a typical vertebrate (without any gene rearrangements). Surprisingly, large-scale gene rearrangements have occurred in S. orientalis. In the rearranged fragment from the control region (CR) to the WANCY tRNA cluster (tRNA cluster of tRNA-W, tRNA-A, tRNA-N, tRNA-C and tRNA-Y) in the S. orientalis mitogenome, tRNA-V and tRNA-M have been translocated to the 3' end of the 16S rRNA gene, with six large intergenic spacers over 20 bp in length. In addition, an origin for light-strand replication (OL) structure that is typically located in the WANCY region was absent in both the S. plagiusa and S. orientalis mitogenomes. It is generally recognized that a sequence in the WANCY region that encodes tRNAs forms a hairpin structure (OL-like structure) and can act as the OL when the typical locus is lost. Moreover, an additional OL-like structure was identified near the control region in the S. plagiusa mitogenome.The positions of the intergenic spacers and the rearranged genes of the S. orientalis mitogenome strongly indicate that the mechanism underlying the rearrangement of this mitogenome was Tandem Duplication and Random Loss. Additionally, two OL-like regions substituting for the typical locus were found in the S. plagiusa mitogenome. We speculate that the ancestral mitogenomes of S. plagiusa and S. orientalis also had this characteristic, such that if both OL-like structures functioned during mitochondrial replication, they could initiate duplicate replications of the light strand (L-strand), leading to duplication of the region between the two structures. We consider that this mechanism may account for the gene duplication that occurred during the gene rearrangement process in the evolution of the ancestral mitogenome to the S. orientalis mitogenome.

Project description:BackgroundMitochondrial DNA sequences are extensively used as genetic markers not only for studies of population or ecological genetics, but also for phylogenetic and evolutionary analyses. Complete mt-sequences can reveal information about gene order and its variation, as well as gene and genome evolution when sequences from multiple phyla are compared. Mitochondrial gene order is highly variable among mollusks, with bivalves exhibiting the most variability. Of the 41 complete mt genomes sequenced so far, 12 are from bivalves. We determined, in the current study, the complete mitochondrial DNA sequence of Crassostrea hongkongensis. We present here an analysis of features of its gene content and genome organization in comparison with two other Crassostrea species to assess the variation within bivalves and among main groups of mollusks.ResultsThe complete mitochondrial genome of C. hongkongensis was determined using long PCR and a primer walking sequencing strategy with genus-specific primers. The genome is 16,475 bp in length and contains 12 protein-coding genes (the atp8 gene is missing, as in most bivalves), 22 transfer tRNA genes (including a suppressor tRNA gene), and 2 ribosomal RNA genes, all of which appear to be transcribed from the same strand. A striking finding of this study is that a DNA segment containing four tRNA genes (trnk1, trnC, trnQ1 and trnN) and two duplicated or split rRNA gene (rrnL5' and rrnS) are absent from the genome, when compared with that of two other extant Crassostrea species, which is very likely a consequence of loss of a single genomic region present in ancestor of C. hongkongensis. It indicates this region seem to be a "hot spot" of genomic rearrangements over the Crassostrea mt-genomes. The arrangement of protein-coding genes in C. hongkongensis is identical to that of Crassostrea gigas and Crassostrea virginica, but higher amino acid sequence identities are shared between C. hongkongensis and C. gigas than between other pairs. There exists significant codon bias, favoring codons ending in A or T and against those ending with C. Pair analysis of genome rearrangements showed that the rearrangement distance is great between C. gigas-C. hongkongensis and C. virginica, indicating a high degree of rearrangements within Crassostrea. The determination of complete mt-genome of C. hongkongensis has yielded useful insight into features of gene order, variation, and evolution of Crassostrea and bivalve mt-genomes.ConclusionThe mt-genome of C. hongkongensis shares some similarity with, and interesting differences to, other Crassostrea species and bivalves. The absence of trnC and trnN genes and duplicated or split rRNA genes from the C. hongkongensis genome is a completely novel feature not previously reported in Crassostrea species. The phenomenon is likely due to the loss of a segment that is present in other Crassostrea species and was present in ancestor of C. hongkongensis, thus a case of "tandem duplication-random loss (TDRL)". The mt-genome and new feature presented here reveal and underline the high level variation of gene order and gene content in Crassostrea and bivalves, inspiring more research to gain understanding to mechanisms underlying gene and genome evolution in bivalves and mollusks.

Dataset Information

Intraspecific rearrangement of mitochondrial genome suggests the prevalence of the tandem duplication-random loss (TDLR) mechanism in Quasipaa boulengeri.

Publications

Intraspecific rearrangement of mitochondrial genome suggests the prevalence of the tandem duplication-random loss (TDLR) mechanism in Quasipaa boulengeri.

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