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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Abbreviations
- AA stem:
-
amino acid-acceptor stem
- AC stem:
-
anticodon stem
- COI:
-
cytochrome oxidase subunit I
- cytb:
-
cytochrome b
- D stem:
-
dihydrouridine stem
- MP:
-
maximum parsimony
- mtDNA:
-
mitochondrial DNA
- Myr:
-
million years
- NJ:
-
neighbor joining
- PCR:
-
polymerase chain reaction
- Ti:
-
transition
- T stem:
-
tψC stem
- Tv:
-
transversion
References
Anderson S, Bankier AT, Barrell BG, de Bruijn MHL, Coulson AR, Drouin J, Eperon IC, Nierlich DP, Roe BA, Sanger F, Schreier PH, Smith AJH, Staden R, Young IG (1981) Sequence and organization of the human mitochondrial genome. Nature 290:457–465
Anderson S, de Bruijn MHL, Coulson AR, Eperon IC, Sanger F, Young IG (1982) Complete sequence of bovine mitochondrial DNA. Conserved features of the mammalian mitochondrial genome. J Mol Biol 156:683–717
Aquadro CF, Greenberg BD (1983) Human mitochondrial DNA variation and evolution: analysis of nucleotide sequences from seven individuals. Genetics 103:287–312
Asakawa S, Kumazawa Y, Araki T, Himeno H, Miura K, Watanabe K (1991) Strand-specific nucleotide composition bias in echinoderm and vertebrate mitochondrial genomes. J Mol Evol 32:511–520
Avise JC (1989) Gene trees and organismal histories: a phylogenetic approach to population biology. Evolution 43:1192–1208
Bibb MJ, Van Etten RA, Wright CT, Walberg MW, Clayton DA (1981) Sequence and gene organization of mouse mitochondrial DNA. Cell 26:167–180
Brown WM, Prager EM, Wang A, Wilson AC (1982) Mitochondrial DNA sequences of primates: tempo and mode of evolution. J Mol Evol 18:225–239
Cantatore P, Gadaleta MN, Roberti M, Saccone C, Wilson AC (1987) Duplication and remoulding of tRNA genes during the evolutionary rearrangement of mitochondrial genomes. Nature 329:853–855
Cantatore P, Roberti M, Rainaldi G, Gadaleta MN, Saccone C (1989) The complete nucleotide sequence, gene organization, and genetic code of the mitochondrial genome of Paracentrotus lividus. J Biol Chem 264:10965–10975
Cedergren RJ, Sankoff D, LaRue B, Grosjean H (1981) The evolving tRNA molecule. CRC Crit Rev Biochem 11:35–104
Cedergren R, Gray MW, Abel Y, Sankoff D (1988) The evolutionary relationships among known life forms. J Mol Evol 28:98–112
Clayton DA, Doda JN, Friedberg EC (1974) The absence of a pyrimidine dimer repair mechanism in mammalian mitochondria. Proc Natl Acad Sci USA 71:2777–2781
de Bruijn MHL, Klug A (1983) A model for the tertiary structure of mammalian mitochondrial transfer RNAs lacking the entire ‘dihydrouridine’ loop and stem. EMBO J 2:1309–1321
Desjardins P, Morais R (1990) Sequence and gene organization of the chicken mitochondrial genome. A novel gene order in higher vertebrates. J Mol Biol 212:599–634
Edwards SV, Arctander P, Wilson AC (1991) Mitochondrial resolution of a deep branch in the genealogical tree for perching birds. Proc R Soc Lond B 243:99–107
Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791
Felsenstein J (1988) Phylogenies from molecular sequences: inference and reliability. Annu Rev Genet 22:521–565
Gadaleta G, Pepe G, De Candia G, Quagliariello C, Sbisà E, Saccone C (1989) The complete nucleotide sequence of the Rattus norvegicus mitochondrial genome: cryptic signals revealed by comparative analysis between vertebrates. J Mol Evol 28:497–516
Gutell RR, Weiser B, Woese CR, Noller HF (1985) Comparative anatomy of 16-S-like ribosomal RNA. Prog Nucleic Acid Res Mol Biol 32:155–216
Gyllensten UB, Erlich HA (1988) 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 USA 85:7652–7656
Hall BD, Clarkson SG, Tocchini-Valentini G (1982) Transcription initiation of eucaryotic transfer RNA genes. Cell 29:3–5
Hasegawa M, Yano T, Miyata T (1981) Phylogeny of transfer RNA and origins of organelles. Precambrian Res 14:81–98
Hasegawa M, Yano T, Miyata T (1984) Evolutionary implications of error amplification in the self-replicating and protein-synthesizing machinery. J Mol Evol 20:77–85
Hein J (1989) A new method that simultaneously aligns and reconstructs ancestral sequences for any number of homologous sequences, when the phylogeny is given. Mol Biol Evol 6:649–668
Hillis DM (1991) Discriminating between phylogenetic signal and random noise in DNA sequences. In: Miyamoto MM, Cracraft J (eds) Phylogenetic analysis of DNA sequences. Oxford University Press, New York, pp 278–294
Himeno H, Masaki H, Kawai T, Ohta T, Kumagai I, Miura K, Watanabe K (1987) Unusual genetic codes and a novel gene structure for tRNAsSerAGY in starfish mitochondrial DNA. Gene 56:219–230
Irwin DM, Kocher TD, Wilson AC (1991) Evolution of the cytochrome b gene of mammals. J. Mol. Evol.32:128–144
Jacobs HT, Elliott DJ, Math VB, Farquharson A (1988) Nucleotide sequence and gene organization of sea urchin mitochondrial DNA. J Mol Biol 202:185–217
Jacobs HT, Asakawa S, Araki T, Miura K, Smith MJ, Watanabe K (1989) Conserved tRNA gene cluster in starfish mitochondrial DNA. Curr Genet 15:193–206
Kimura M (1980) A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120
Kocher TD, Thomas WK, Meyer A, Edwards SV, Pääbo S., Villablanca FX, Wilson AC (1989) Dynamics of mitochondrial DNA evolution in animals: amplification and sequencing with conserved primers. Proc Natl Acad Sci USA 86:6196–6200
Kumazawa Y, Yokogawa T, Hasegawa E, Miura K, Watanabe K (1989) The aminoacylation of structurally variant phenylalanine tRNAs from mitochondria and various nonmitochondrial sources by bovine mitochondrial phenylalanyl-tRNA synthetase. J Biol Chem 264:13005–13011
Kumazawa Y, Himeno H, Miura K, Watanabe K (1991a) Unilateral aminoacylation specificity between bovine mitochondria and eubacteria. J Biochem 109:421–427
Kumazawa Y, Schwartzbach CJ, Liao H-X, Mizumoto K, Kaziro Y, Miura K, Watanabe K, Spremulli LL (1991b) Interactions of bovine mitochondrial phenylalanyl-tRNA with ribosomes and elongation factors from mitochondria and bacteria. Biochim Biophys Acta 1090:167–172
Martin AP, Naylor GJP, Palumbi SR (1992) Rates of mitochondrial DNA evolution in sharks are slow compared with mammals. Nature 357:153–155
Meyer A, Wilson AC (1990) Origin of tetrapods inferred from their mitochondrial DNA affiliation to lungfish. J Mol Evol 31:359–364
Mindell DP, Honeycutt RL (1990) Ribosomal RNA in vertebrates: evolution and phylogenetic applications. Annu Rev Ecol Syst 21:541–566
Miyamoto MM, Boyle SM (1989) The potential importance of mitochondrial DNA sequence data to eutherian mammal phylogeny. In: Fernholm B, Bremer K, Jörnvall H (eds) The hierarchy of life. Elsevier, Amsterdam, pp 437–450
Miyata T, Hayashida H, Kikuno R, Hasegawa M, Kobayashi M, Koike K (1982) Molecular clock of silent substitution: at least six-fold preponderance of silent changes in mitochondrial genes over those in nuclear genes. J Mol Evol 19:28–35
Moritz C, Dowling TE, Brown WM (1987) Evolution of animal mitochondrial DNA: relevance for population biology and systematics. Annu Rev Ecol Syst 18:269–292
Neefs J-M, Van de Peer Y, De Rijk P, Goris A, De Wachter R (1991) Compilation of small ribosomal subunit RNA sequences. Nucleic Acids Res 19:1987–2015
Nei M (1991) Relative efficiencies of different tree-making methods for molecular data. In: Miyamoto MM, Cracraft J (eds) Phylogenetic analysis of DNA sequences. Oxford University Press, New York, pp 90–128
Pääbo S, Thomas WK, Whitfield KM, Kumazawa Y, Wilson AC (1991) Rearrangements of mitochondrial transfer RNA genes in marsupials. J Mol Evol 33:426–430
Reeves JH (1992) Heterogeneity in the substitution process of amino acid sites of proteins coded for by mitochondrial DNA. J Mol Evol 35:17–31
Rich A, RajBhandary UL (1976) Transfer RNA: molecular structure, sequence, and properties. Annu Rev Biochem 45:805–860
Robinson DF, Foulds LR (1981) Comparison of phylogenetic trees. Math Biosci 53:131–147
Roe BA, Ma D-P, Wilson RK, Wong JF-H (1985) The complete nucleotide sequence of the Xenopus laevis mitochondrial genome. J Biol Chem 260:9759–9774
Saitou N, Nei M (1987) The neighbor joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425
Sampson JR, DiRenzo AB, Behlen LS, Uhlenbeck OC (1990) Role of the tertiary nucleotides in the interaction of yeast phenylalanine tRNA with its cognate synthetase. Biochemistry 29:2523–2532
Schulman LH (1991) Recognition of tRNAs by aminoacyl-tRNA synthetases. Prog Nucleic Acid Res Mol Biol 41:23–87
Sokal RR, Rohlf FJ (1981) Biometry, 2nd ed. WH Freeman, New York
Sommer R, Tautz D (1989) Minimal homology requirements for PCR primers. Nucleic Acids Res 17:6749
Sprinzl M, Dank N, Nock S, Schön A (1991) Compilation of tRNA sequences and sequences of tRNA genes. Nucleic Acids Res 19:2127–2171
Swofford DL (1991) PAUP: phylogenetic analysis using parsimony, version 3.0s. Illinois Natural History Survey, Champaign, IL
Tamura K (1992) NJBOOT2, version 1.06. Pennsylvania State University, PA
Thomas WK, Beckenbach AT (1989) Variation in salmonid mitochondrial DNA: evolutionary constraints and mechanisms of substitution. J Mol Evol 29:233–245
Thomas WK, Maa J, Wilson AC (1989) Shifting constraints on tRNA genes during mitochondrial DNA evolution in animals. New Biol 1:93–100
Ueda T, Ohta T, Watanabe K (1985) Large scale isolation and some properties of AGY-specific serine tRNA from bovine heart mitochondria. J Biochem 98:1275–1284
Van de Peer Y, Neefs J-M, De Wachter R (1990) Small ribosomal subunit RNA sequences, evolutionary relationships among different life forms, and mitochondrial origins. J Mol Evol 30:463–476
Wilson AC, Cann RL, Carr SM, George M, Gyllensten UB, Helm-Bychowski KM, Higuchi RG, Palumbi SR, Prager EM, Sage RD, Stoneking M (1985) Mitochondrial DNA and two perspectives on evolutionary genetics. Biol J Linn Soc 26: 375–400
Wolstenholme DR, Macfarlane JL, Okimoto R, Clary DO, Wahleithner JA (1987) Bizarre tRNAs inferred from DNA sequences of mitochondrial genomes of nematode worms. Proc Natl Acad Sci USA 84:1324–1328
Yokogawa T, Kumazawa Y, Miura K, Watanabe K (1989) Purification and characterization of two serine isoacceptor tRNAs from bovine mitochondria by using a hybridization assay method. Nucleic Acids Res 17:2623–2638
Yokogawa T, Watanabe Y, Kumazawa Y, Ueda T, Hirao I, Miura K, Watanabe K (1991) A novel cloverleaf structure found in mammalian mitochondrial tRNAsSer(UCN). Nucleic Acids Res 19:6101–6105
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Correspondence to: Y. Kumazawa
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Kumazawa, Y., Nishida, M. Sequence evolution of mitochondrial tRNA genes and deep-branch animal phylogenetics. J Mol Evol 37, 380–398 (1993). https://doi.org/10.1007/BF00178868
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DOI: https://doi.org/10.1007/BF00178868