Sequence Evolution of Mitochondrial TRNA Genes and Deep-branch Animal Phylogenetics

Overview

Journal J Mol Evol

Specialty Biochemistry

Date 1993 Oct 1

PMID 7508516

Citations 61

Authors

Y Kumazawa

M Nishida

Affiliations

Soon will be listed here.

Abstract

Mitochondrial DNA sequences are often used to construct molecular phylogenetic trees among closely related animals. In order to examine the usefulness of mtDNA sequences for deep-branch phylogenetics, genes in previously reported mtDNA sequences were analyzed among several animals that diverged 20-600 million years ago. Unambiguous alignment was achieved for stem-forming regions of mitochondrial tRNA genes by virtue of their conservative secondary structures. Sequences derived from stem parts of the mitochondrial tRNA genes appeared to accumulate much variation linearly for a long period of time: nearly 100 Myr for transition differences and more than 350 Myr for transversion differences. This characteristic could be attributed, in part, to the structural variability of mitochondrial tRNAs, which have fewer restrictions on their tertiary structure than do nonmitochondrial tRNAs. The tRNA sequence data served to reconstruct a well-established phylogeny of the animals with 100% bootstrap probabilities by both maximum parsimony and neighbor-joining methods. By contrast, mitochondrial protein genes coding for cytochrome b and cytochrome oxidase subunit I did not reconstruct the established phylogeny or did so only weakly, although a variety of fractions of the protein gene sequences were subjected to tree-building. This discouraging phylogenetic performance of mitochondrial protein genes, especially with respect to branches originating over 300 Myr ago, was not simply due to high randomness in the data. It may have been due to the relative susceptibility of the protein genes to natural selection as compared with the stem parts of mitochondrial tRNA genes. On the basis of these results, it is proposed that mitochondrial tRNA genes may be useful in resolving deep branches in animal phylogenies with divergences that occurred some hundreds of Myr ago. For this purpose, we designed a set of primers with which mtDNA fragments encompassing clustered tRNA genes were successfully amplified from various vertebrates by the polymerase chain reaction.

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References

Gadaleta G, Pepe G, DE CANDIA G, Quagliariello C, Sbisa E, Saccone C . The complete nucleotide sequence of the Rattus norvegicus mitochondrial genome: cryptic signals revealed by comparative analysis between vertebrates. J Mol Evol. 1989; 28(6):497-516. DOI: 10.1007/BF02602930. View

Cedergren R, Sankoff D, Larue B, Grosjean H . The evolving tRNA molecule. CRC Crit Rev Biochem. 1981; 11(1):35-104. DOI: 10.3109/10409238109108699. View

Anderson S, Bankier A, Barrell B, de Bruijn M, Coulson A, Drouin J . Sequence and organization of the human mitochondrial genome. Nature. 1981; 290(5806):457-65. DOI: 10.1038/290457a0. View

Cantatore P, Gadaleta M, Roberti M, Saccone C, Wilson A . Duplication and remoulding of tRNA genes during the evolutionary rearrangement of mitochondrial genomes. Nature. 1987; 329(6142):853-5. DOI: 10.1038/329853a0. View

Reeves J . Heterogeneity in the substitution process of amino acid sites of proteins coded for by mitochondrial DNA. J Mol Evol. 1992; 35(1):17-31. DOI: 10.1007/BF00160257. View

Kocher T, Thomas W, Meyer A, Edwards S, Paabo S, Villablanca F . Dynamics of mitochondrial DNA evolution in animals: amplification and sequencing with conserved primers. Proc Natl Acad Sci U S A. 1989; 86(16):6196-200. PMC: 297804. DOI: 10.1073/pnas.86.16.6196. View

Saitou N, Nei M . The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol. 1987; 4(4):406-25. DOI: 10.1093/oxfordjournals.molbev.a040454. View

Cedergren R, Gray M, Abel Y, Sankoff D . The evolutionary relationships among known life forms. J Mol Evol. 1988; 28(1-2):98-112. DOI: 10.1007/BF02143501. View

Brown W, Prager E, Wang A, Wilson A . Mitochondrial DNA sequences of primates: tempo and mode of evolution. J Mol Evol. 1982; 18(4):225-39. DOI: 10.1007/BF01734101. View

10.

Hasegawa M, Yano T, Miyata T . Evolutionary implications of error amplification in the self-replicating and protein-synthesizing machinery. J Mol Evol. 1984; 20(1):77-85. DOI: 10.1007/BF02101989. View

11.

Hein J . A new method that simultaneously aligns and reconstructs ancestral sequences for any number of homologous sequences, when the phylogeny is given. Mol Biol Evol. 1989; 6(6):649-68. DOI: 10.1093/oxfordjournals.molbev.a040577. View

12.

Desjardins P, Morais R . Sequence and gene organization of the chicken mitochondrial genome. A novel gene order in higher vertebrates. J Mol Biol. 1990; 212(4):599-634. DOI: 10.1016/0022-2836(90)90225-B. View

13.

Miyata T, Hayashida H, Kikuno R, Hasegawa M, Kobayashi M, Koike K . Molecular clock of silent substitution: at least six-fold preponderance of silent changes in mitochondrial genes over those in nuclear genes. J Mol Evol. 1982; 19(1):28-35. DOI: 10.1007/BF02100221. View

14.

Thomas W, Maa J, Wilson A . Shifting constraints on tRNA genes during mitochondrial DNA evolution in animals. New Biol. 1989; 1(1):93-100. View

15.

WOLSTENHOLME D, Macfarlane J, Okimoto R, Clary D, Wahleithner J . Bizarre tRNAs inferred from DNA sequences of mitochondrial genomes of nematode worms. Proc Natl Acad Sci U S A. 1987; 84(5):1324-8. PMC: 304420. DOI: 10.1073/pnas.84.5.1324. View

16.

Edwards S, Arctander P, Wilson A . Mitochondrial resolution of a deep branch in the genealogical tree for perching birds. Proc Biol Sci. 1991; 243(1307):99-107. DOI: 10.1098/rspb.1991.0017. View

17.

Neefs J, Van de Peer Y, De Rijk P, Goris A, De Wachter R . Compilation of small ribosomal subunit RNA sequences. Nucleic Acids Res. 1991; 19 Suppl:1987-2015. PMC: 331343. DOI: 10.1093/nar/19.suppl.1987. View

18.

Felsenstein J . CONFIDENCE LIMITS ON PHYLOGENIES: AN APPROACH USING THE BOOTSTRAP. Evolution. 2017; 39(4):783-791. DOI: 10.1111/j.1558-5646.1985.tb00420.x. View

19.

Gyllensten U, Erlich H . Generation of single-stranded DNA by the polymerase chain reaction and its application to direct sequencing of the HLA-DQA locus. Proc Natl Acad Sci U S A. 1988; 85(20):7652-6. PMC: 282250. DOI: 10.1073/pnas.85.20.7652. View

20.

Thomas W, Beckenbach A . Variation in salmonid mitochondrial DNA: evolutionary constraints and mechanisms of substitution. J Mol Evol. 1989; 29(3):233-45. DOI: 10.1007/BF02100207. View