Tandem Duplication and Random Loss for mitogenome rearrangement in Symphurus (Teleost: Pleuronectiformes).

BACKGROUND: 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. RESULTS: 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. CONCLUSIONS: 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.

A novel model of double replications and random loss accounts for rearrangements in the Mitogenome of Samariscus latus (Teleostei: Pleuronectiformes).

BACKGROUND: Although more than one thousand complete mitochondrial DNA (mtDNA) sequences have been determined in teleostean fishes, only a few gene rearrangements have been observed, and genome-scale rearrangements are even rarer. However, flatfishes (Pleuronectiformes) have been identified as having diverse types of mitochondrial gene rearrangements. It has been reported that tongue soles and the blue flounder mitogenomes exhibit different types of large-scale gene rearrangements. RESULTS: In the present study, the complete mitochondrial genome of another flatfish, Samariscus latus, was sequenced, and genome-scale rearrangements were observed. The genomic features of this flounder are different from those of any other studied vertebrates, including flatfish species too. The mitogenome of S. latus is characterized by the duplication and translocation of the control region (CR). The genes located between the two CRs are divided into two clusters in which their relative orders are maintained. CONCLUSIONS: We propose a "Double Replications and Random Loss" model to explain the rearrangement events in S. latus mitogenome. This model consists of the following steps. First, the CR was duplicated and translocated. Subsequently, double replications of the mitogenome were successively initiated from the two CRs, leading to the duplication of the genes between the two CRs. Finally, one of each pair of duplicated genes was lost in a random event.

Complete mitogenome sequences of four flatfishes (Pleuronectiformes) reveal a novel gene arrangement of L-strand coding genes.

BACKGROUND: Few mitochondrial gene rearrangements are found in vertebrates and large-scale changes in these genomes occur even less frequently. It is difficult, therefore, to propose a mechanism to account for observed changes in mitogenome structure. Mitochondrial gene rearrangements are usually explained by the recombination model or tandem duplication and random loss model. RESULTS: In this study, the complete mitochondrial genomes of four flatfishes, Crossorhombus azureus (blue flounder), Grammatobothus krempfi, Pleuronichthys cornutus, and Platichthys stellatus were determined. A striking finding is that eight genes in the C. azureus mitogenome are located in a novel position, differing from that of available vertebrate mitogenomes. Specifically, the ND6 and seven tRNA genes (the Q, A, C, Y, S1, E, P genes) encoded by the L-strand have been translocated to a position between tRNA-T and tRNA-F though the original order of the genes is maintained. CONCLUSIONS: These special features are used to suggest a mechanism for C. azureus mitogenome rearrangement. First, a dimeric molecule was formed by two monomers linked head-to-tail, then one of the two sets of promoters lost function and the genes controlled by the disabled promoters became pseudogenes, non-coding sequences, and even were lost from the genome. This study provides a new gene-rearrangement model that accounts for the events of gene-rearrangement in a vertebrate mitogenome.

The complete mitochondrial genome of Zebrias quagga (Pleuronectiformes: Soleidae).

Zebrias quagga (Soleoidei, Soleidae) is a sort of small and medium-sized commercial flatfish, characterized by both eyes on the right side of the body and with a dark brown short tentacle on each eye. In this paper, the complete mitogenome sequence of Z. quagga was first determined, which is 17,045 bp in length and contains 13 protein-coding genes, two rRNA genes, 22 tRNA genes, as well as a control region (CR) and a L-strand replication origin (OL). Gene contents, locations, and orders are identical to those of typical teleostean mtDNA. The nucleotide composition of the whole mitogenome is 28.8%, 29.3%, 15.8%, and 26.1% for A, C, G, and T, respectively, with a slight bias of A+T content (54.9%). This result is expected to contribute to a better understanding the phylogenetic study of Soleidae and Pleuronectiformes.

The complete mitochondrial genome of Cynoglossus puncticeps (Pleuronectiformes: Cynoglossidae).

Cynoglossus puncticeps (Soleoidei Cynoglossidae) is characterized by both eyes on the left side of the body. Here we report the mitogenome of this tonguesole for the first time, which is 17,142 bp in length, and the gene order has been reorganized. The tRNA-Gln gene translocated from the light strand (L-strand) to the heavy strand (H-strand), accompanied by tRNA-Ile gene shuffling. In addition, the putative control region translocated downstream to the position between the ND1 and the tRNA-Gln genes, leaving a 25-bp trace fragment in the original location. In addition, two tandem arrays were found: one was a 17-bp motif with 40.2 copies, and the other was 73-bp with 3.0 copies.

The complete mitochondrial genome sequence of Cynoglossus sinicus (Pleuronectiformes: Cynoglossidae).

Cynoglossidae (tongue soles) mitogenomes have been found to be translocated in their control region and a tRNA gene inversed, but no gene rearrangement in Soleidae, the closest family to Cynoglossidae, has been detected. In order to explore whether or not mitogenomes of tongue soles bear other gene-rearrangement types, we determined another tongue sole mitogenome of Cynoglossus sinicus. The total length of this mitogenome is 16,478 bp, and the tRNA-Gln gene is translocated from the light strand (L-strand) to the heavy strand (H-strand), accompanied by shuffling of tRNA-Gln, Ile and Met genes with a 143 bp intergenic spacer between tRNA-Gln and Ile. The control region (CR) might translocate to the position between the ND1 and the tRNA-Gln genes. The order of the rest genes is identical to that of the typical fish.

The complete mitochondrial genome sequence of Heteromycteris japonicus (Pleuronectiformes: Soleidae).

The bamboo sole Heteromycteris japonicus (Pleuronectiformes: Soleidae) is characterized by both eyes on the right side of the body and a rostral hook. In this article, the complete mitochondrial genome sequence of this sole was first determined. The total length is 17,111 bp, including 13 protein-coding genes, 22 tRNA genes and 2 rRNA genes (12 S and 16 S), as well as a putative control region and a putative L-strand replication origin (OL). Gene contents, locations and arrangements are identical to those of typical bony fishes. Overall base composition of the mitogenome is 29.2%, 27.5%, 16.3% and 27.1% for A, C, G and T, with a high A + T content (56.3%). The determination of H. japonicus mitogenome sequence could contribute to understanding the systematic evolution of the genus Heteromycteris and further phylogenetic study on Soleidae and Pleuronectiformes.

Control region translocation and a tRNA gene inversion in the mitogenome of Paraplagusia japonica (Pleuronectiformes: Cynoglossidae).

Paraplagusia japonica (Cynoglossidae, Soleoidei) is characterized by a bilaterally asymmetrical and a series of fringes on the lips on the ocular side. Here we report for the first time the mitogenome of this tongue sole, which is 16,694 bp in length, and the gene order has been reorganized. The tRNA-Gln gene translocated from the light strand (L-strand) to the heavy strand (H-strand), accompanied by tRNA-Ile gene shuffling. In addition, the putative control region translocated downstream to the place between the ND1 and the tRNA-Gln genes, leaving a 26-bp trace fragment in the original position. Nevertheless, the rest gene order is identical to that of the typical fish. In addition, it is the first report of the rare ATT as an initiation codon for ND3, and the ATP6 (- 26) and ND5 (+26) are unusually shorter or longer than those in other flatfish. These data will provide useful information for better understanding the molecular mechanisms of gene reorganization in fish mitogenome.

The complete mitochondrial genome of a striped sole Zebrias zebrinus (Pleuronectiformes: Soleidae).

Zebrias zebrinus belongs in the family Soleidae of Pleuronectiformes. There are overlaps in the ranges of identification characters between Z. zebrinus and another striped sole Z. fasciatus. In this study, the complete mitochondrial genome of Z. zebrinus was first determined. The total length was 16,758 bp, including 13 protein-coding genes, 22 tRNA genes, and 2 rRNA genes (12S and 16S), as well as a putative control region and a putative L-strand replication origin (O(L)). Gene contents, locations, and arrangements were identical to those of typical bony fishes. The overall base composition of the mitogenome was 28.7%, 30.0%, 15.2%, and 26.1% for A, C, G, and T, respectively, with an A + T content of 54.8%. This result would expect the contribution to the molecular identification of this species and further phylogenetic study of Soleidae and Pleuronectiformes.