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Gene Rearrangements and Evolution of tRNA Pseudogenes in the Mitochondrial Genome of the Parrotfish (Teleostei: Perciformes: Scaridae)

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Abstract

Genomic size of animal mitochondrial DNA is usually minimized over time. Thus, when regional duplications occur, they are followed by a rapid elimination of redundant material. In contrast to this general view, we report here long-sustained tRNA pseudogenes in the mitochondrial genome (mitogenome) of teleost fishes of the family Scaridae (parrotfishes). During the course of a molecular phylogenetic study of the suborder Labroidei, we determined the complete nucleotide sequence of the mitogenome for a parrotfish, Chlorurus sordidus, and found a gene rearrangement accompanied by a tRNA pseudogene. In the typical gene order of vertebrates, a tRNA-gene cluster between ND1 and ND2 genes includes tRNAIle (I), tRNAGln (Q), and tRNAMet (M) genes in this order (IQM). However, in the mitogenome of the parrotfish, the tRNAMet gene was inserted between the tRNAIle and the tRNAGln genes, and the tRNAGln gene was followed by a putative tRNAMet pseudogene (ψM). Such a tRNA gene rearrangement including a pseudogene (IMQψM) was found in all of the 10 examined species, representing 7 of the 10 currently recognized scarid genera. All sister groups examined (20 species of Labridae and a single species of Odacidae) had the typical gene order of vertebrate mitogenomes. Phylogenetic analysis of the tRNAMet genes and the resulting pseudogenes demonstrated that the ancestral tRNAMet gene was duplicated in a common ancestor of the parrotfish. Based on the fossil record, these results indicate that the pseudogenes have survived at least 14 million years. Most of the vertebrate mitochondrial gene rearrangements involving the IQM region have held the tRNAMet gene just upstream of the ND2 gene, and even in a few exceptional cases, including the present ones, the tRNA pseudogenes have been found in that position. In addition, most of these tRNAMet pseudogenes maintained clover-leaf secondary structures, with the remainder sustaining the clover-leaf structure in the „top half (TψC and acceptor arms). Considering their potential secondary structures (holding “top halves” of the clover-leaf structures), locations within mitogenomes (flanking the 5′ ends of the ND2 genes) and stabilities over time (survived at least 14 Myr), it is likely that the tRNA pseudogenes retain function as punctuation marks for mitochondrial ND2 mRNA processing.

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Acknowledgments

We wish to thank H. Ikeda, Y. Yamanoue, K. Kuriiwa, T. Kudo, K. Matsumoto, Weekly Sunday Fishing, Tokyo Sea Life Park, and Australian Museum for providing tissue or fresh whole specimens. We also thank Y. Azuma, T. Mukai, S. Nakamura, and Y. Kozaki for field assistance and Y. Yanagisawa, Ogasawara Fisheries Center, for generously allowing us to use their laboratories. We are grateful to J.G. Inoue and Y. Futamura for critical comment on this study. This study was supported partly by Research Fellowships of the Japan Society for the Promotion of Science for Young Scientists (No. 72503) and Grants-in-Aid from the Ministry of Education, Culture, Sports, Science, and Technology, Japan (12NP0201).

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Authors and Affiliations

  1. Ocean Research Institute, University of Tokyo, 1-15-1 Minamidai, Nakano-ku, Tokyo, 164-8639, Japan

    Kohji Mabuchi, Takashi P. Satoh & Mutsumi Nishida

  2. Department of Zoology, Natural History Museum & Institute, Chiba, Chiba, 260-8682, Japan

    Masaki Miya

  3. Department of Zoology, Field Museum of Natural History, Chicago, IL, 60605–2496, USA

    Mark W. Westneat

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  1. Kohji Mabuchi
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Correspondence to Kohji Mabuchi.

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Mabuchi, K., Miya, M., Satoh, T.P. et al. Gene Rearrangements and Evolution of tRNA Pseudogenes in the Mitochondrial Genome of the Parrotfish (Teleostei: Perciformes: Scaridae). J Mol Evol 59, 287–297 (2004). https://doi.org/10.1007/s00239-004-2621-z

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