Abstract

BackgroundThe 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.ResultsIn 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.ConclusionsThe 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.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-015-1581-6) contains supplementary material, which is available to authorized users.

Highlights

  • The mitochondrial genomes of flatfishes (Pleuronectiformes) exhibit highly diversified types of large-scale gene rearrangements

  • The typical origin for L-strand replication (OL), which is usually located inside the Transfer ribonucleic acid (tRNA) cluster of tRNA-W (WANCY) cluster, was not found in either of the two Symphurus mitogenomes at this location

  • Of the models that have been proposed to explain gene rearrangements in animal mitogenomes, which model most likely applies to the S. orientalis mitogenome? The recombination model is only suitable for block interchanges of small fragments, and this model is quite rare in the mitochondrial genome

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Summary

Introduction

The mitochondrial genomes (mitogenomes) of flatfishes (Pleuronectiformes) exhibit highly diversified types of large-scale gene rearrangements. Vertebrate mitochondrial genomes (mitogenomes) typically contain the same 37 genes [1] The order of these genes is generally considered conservative in most vertebrate genomes; gene rearrangements have been found in many taxa, such as birds [2,3,4], reptiles [5,6], amphibians [7,8], and fishes [9,10,11]. Shi et al [20] proposed the Dimer-Mitogenome and Non-Random Loss model (DMNR), which inferred the course of gene rearrangements in C. azureus. For the rearrangement events in the S. latus mitogenome, Shi et al [21] proposed the Double Replications and Random Loss model

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