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Open Access Highly Accessed Research article

Transfer RNA gene arrangement and codon usage in vertebrate mitochondrial genomes: a new insight into gene order conservation

Takashi P Satoh1, Yukuto Sato2, Naoharu Masuyama34, Masaki Miya5 and Mutsumi Nishida3*

Author Affiliations

1 Collection Center, National Museum of Nature and Science, 3-23-1 Hyakunincho, Shinjuku-ku, Tokyo 169-0073, Japan

2 Division of Population Genetics, National Institute of Genetics, 1111 Yata, Mishima, Shizuoka 411-8540, Japan

3 Department of Marine Bioscience, Atmosphere and Ocean Research Institute, The University of Tokyo, 5-1-5 Kashiwanoha, Kashiwa-shi, Chiba 277-8564, Japan

4 Resonarch Co., Ltd., 2-2-23 Josui-shinmachi, Kodaira, Tokyo 187-0023, Japan

5 Department of Zoology, Natural History Museum and Institute, 955-2 Aoba-cho, Chuo-ku, Chiba 260-8682, Japan

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BMC Genomics 2010, 11:479  doi:10.1186/1471-2164-11-479

Published: 19 August 2010

Abstract

Background

Mitochondrial (mt) gene arrangement has been highly conserved among vertebrates from jawless fishes to mammals for more than 500 million years. It remains unclear, however, whether such long-term persistence is a consequence of some constraints on the gene order.

Results

Based on the analysis of codon usage and tRNA gene positions, we suggest that tRNA gene order of the typical vertebrate mt-genomes may be important for their translational efficiency. The vertebrate mt-genome encodes 2 rRNA, 22 tRNA, and 13 transmembrane proteins consisting mainly of hydrophobic domains. We found that the tRNA genes specifying the hydrophobic residues were positioned close to the control region (CR), where the transcription efficiency is estimated to be relatively high. Using 47 vertebrate mt-genome sequences representing jawless fishes to mammals, we further found a correlation between codon usage and tRNA gene positions, implying that highly-used tRNA genes are located close to the CR. In addition, an analysis considering the asymmetric nature of mtDNA replication suggested that the tRNA loci that remain in single-strand for a longer time tend to have more guanine and thymine not suffering deamination mutations in their anticodon sites.

Conclusions

Our analyses imply the existence of translational constraint acting on the vertebrate mt-gene arrangement. Such translational constraint, together with the deamination-related constraint, may have contributed to long-term maintenance of gene order.