Phylogeny, recombination, and mechanisms of stepwise mitochondrial genome reorganization in mantellid frogs from Madagascar

Molecular Biology and Evolution

Volumn 25, Issue 5, 2008, Pages 874-891

  Kurabayashi, Atsushi ^a   Sumida, Masayuki ^a   Yonekawa, Hiromichi ^b   Glaw, Frank ^c   Vences, Miguel ^d   Hasegawa, Masami ^e,f  

^a HIROSHIMA UNIVERSITY   (Japan)

^b TOKYO METROPOLITAN INSTITUTE OF MEDICAL SCIENCE   (Japan)

^c ZOOLOGISCHE STAATSSAMMLUNG MÜNCHEN   (Germany)

^d TECHNICAL UNIVERSITY OF BRAUNSCHWEIG   (Germany)

^e INSTITUTE OF STATISTICAL MATHEMATICS   (Japan)

^f FUDAN UNIVERSITY   (China)

Author keywords

Concerted evolution; Gene rearrangement; Mantellidae; Mitochondrial genome; Recombination

Indexed keywords

ANIMAL TISSUE; ARTICLE; BLOMMERSIA; CONTROLLED STUDY; DNA FLANKING REGION; FROG; GENE DELETION; GENE DUPLICATION; GENE REARRANGEMENT; GENE STRUCTURE; GENETIC RECOMBINATION; GENETIC VARIABILITY; GUIBEMANTIS; MADAGASCAR; MANTELLA; MITOCHONDRIAL GENE; MOLECULAR EVOLUTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; SPINOMANTIS; WAKEA; ANIMAL; CHEMISTRY; CLASSIFICATION; FROGS AND TOADS; GENETICS; GENOME; MITOCHONDRION; REGULATORY SEQUENCE;

ANURA; MANTELLA; MANTELLINAE;

CYTOCHROME B; MITOCHONDRIAL DNA; NUCLEOSIDE; TRANSFER RNA;

ANIMALS; ANURA; CYTOCHROMES B; DNA, MITOCHONDRIAL; EVOLUTION, MOLECULAR; GENE REARRANGEMENT; GENOME; MADAGASCAR; MITOCHONDRIA; NUCLEOSIDES; PHYLOGENY; RECOMBINATION, GENETIC; REGULATORY SEQUENCES, NUCLEIC ACID; RNA, TRANSFER;

EID: 50949133166     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/msn031     Document Type: Article

References (96)

1. Arndt A, Smith MJ. 1998. Mitochondrial gene rearrangement in the sea cucumber genus Cucumaria. Mol Biol Evol. 15:1009-1016.
2. Bierne H, Ehrlich SD, Michel B. 1997. Deletions at stalled replication forks occur by two different pathways. EMBO J. 2:3332-3340.
3. Black WCIV, Roehrdanz RL. 1998. Mitochondrial gene order is not conserved in arthropods: prostriate and metastriate tick mitochondrial genomes. Mol Biol Evol. 15:1772-1785.
4. Boore JL. 1999. Survey and summary: animal mitochondrial genomes. Nucleic Acids Res. 27:1767-1780.
5. Boore JL. 2000. The duplication/random loss model for gene rearrangement exemplified by mitochondrial genomes of deuterostome animals. In: Sankoff D, Nadeau J, editors. Computational biology series. Vol. 1. Dordrecht (The Netherlands): Kluwer Academic Publishers. p. 133-147.
6. Boore JL, Brown WM. 1994. Mitochondrial genomes and the phylogeny of mollusks. Nautilus. 108(Suppl 2):61-78.
7. Boore JL, Brown WM. 1998. Big trees from little genomes. Mitochondrial gene order as a phylogenetic tool. Curr Opin Genet Dev. 8:668-674.
8. Boore JL, Macey JR, Medina M. 2005. Sequencing and comparing whole mitochondrial genomes of animals. Methods Enzymol. 395:311-348.
9. Bossuyt F, Milinkovitch MC. 2000. Convergent adaptive radiations in Madagascan and Asian ranid frogs reveal covariation between larval and adult traits. Proc Natl Acad Sci USA. 97:6585-6590.
10. Bossuyt F, Milinkovitch MC. 2001. Amphibians as indicators of early tertiary "out-of-India" dispersal of vertebrates. Science. 292:93-95.
11. Bowmaker M, Yang MY, Yasukawa T, Reyes A, Jacobs HT, Huberman JA, Holt IJ. 2003. Mammalian mitochondrial DNA replicates bidirectionally from an initiation zone. J Biol Chem. 278:50961-50969.
12. Brandley MC, Schmitz A, Reeder TW. 2005. Partitioned Bayesian analyses, partition choice, and the phylogenetic relationships of scincid lizards. Syst Biol. 54:373-390.
13. Brown WM. 1985. Evolution of the animal mitochondrial DNA genome. In: MacIntyre R, editor. Molecular evolutionary genetics. New York: Plenum Press. p. 95-130.
14. Cairns SS, Bogenhagen DF. 1986. Mapping of the displacement loop within the nucleotide sequence of Xenopus laevis mitochondrial DNA. J Biol Chem. 25:8481-8487.
15. Campbell NJ, Barker SC. 1999. The novel mitochondrial gene arrangement of the cattle tick, Boophilus microplus: fivefold tandem repetition of a coding region. Mol Biol Evol. 16:732-740.
16. Castresana J. 2000. Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol. 17:540-552.
17. Clayton DA. 1982. Replication of animal mitochondrial DNA. Cell. 28:693-705.
18. Dowton M, Campbell NJH. 2001. Intramitochondrial recombination: is it why some mitochondrial genes sleep around? Trends Ecol Evol. 16:269-271.
19. Eberhard JR, Wright TF, Bermingham E. 2001. Duplication and concerted evolution of the mitochondrial control region in the parrot genus Amazona. Mol Biol Evol. 18:1330-1342.
20. Endo K, Noguchi Y, Ueshima R, Jacobs HT. 2005. Novel repetitive structures, deviant protein-encoding sequences and unidentified ORFs in the mitochondrial genome of the brachiopod Lingula anatina. J Mol Evol. 61:36-53.
21. Frost DR, Grant T, Faivovich J, et al. (19 co-authors). 2006. The amphibian tree of life. Bull Am Mus Nat Hist. 297:1-371.
22. Gissi C, San Mauro D, Pesole G, Zardoya R. 2006. Mitochondrial phylogeny of Anura (Amphibia): a case study of congruent phylogenetic reconstruction using amino acid and nucleotide characters. Gene. 366:228-237.
23. Glaw F, Hoegg S, Vences M. 2006. Discovery of a new basal relict lineage of Madagascan frogs and its implications for mantellid evolution. Zootaxa. 1334:27-43.
24. Glaw F, Vences M. 2006. Phylogeny and genus-level classification of mantellid frogs. Org Divers Evol. 6:236-253.
25. Glaw F, Vences M. 2007. A field guide to the amphibians and reptiles of Madagascar, 3rd ed. Köln (Germany): Vences & Glaw Verlag. p. 496.
26. Guindon S, Gascuel O. 2003. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol. 52:696-704.
27. Hasegawa M, Kishino H. 1994. Accuracies of the simple methods for estimating the bootstrap probability of a maximum likelihood tree. Mol Biol Evol. 11:142-145.
28. Henikoff S. 1987. Exonuclease III generated deletions for DNA sequence analysis. Promega Notes No 8: 1-3.
29. Hoegg S, Vences M, Brinkmann H, Meyer A. 2004. Phylogeny and comparative substitution rates of frogs inferred from sequences of three nuclear genes. Mol Biol Evol. 21:1188-1200.
30. Hoffmann RJ, Boore JL, Brown WM. 1992. A novel mitochondrial genome organization for the blue mussel, Mytilus edulis. Genetics. 131:397-412.
31. Holliday R. 1964. The induction of mitotic recombination by mitomycin C in Ustilago and Saccharomyces. Genetics. 50:323-335.
32. Holt IJ, Dunbar DR, Jacobs HT. 1997. Behaviour of a population of partially duplicated mitochondrial DNA molecules in cell culture: segregation, maintenance and recombination dependent upon nuclear background. Hum Mol Genet. 6:1251-1260.
33. Holt IJ, Lorimer HE, Jacobs HT. 2000. Coupled leading- and lagging-strand synthesis of mammalian mitochondrial DNA. Cell. 100:515-524.
34. Howell N. 1997. mtDNA recombination: what do in vitro data mean? Am J Hum Genet. 61:19-22.
35. Igawa T, Kurabayashi A, Usuki C, Fujii T, Sumida M. 2008. Complete mitochondrial genomes of three neobatrachian anurans: a case study of divergence time estimation using different data and calibration settings. Gene. 407:116-129.
36. Inoue JG, Miya M, Tsukamoto K, Nishida M. 2003. Evolution of the deep-sea gulper eel mitochondrial genomes: large-scale gene rearrangements originated within the eels. Mol Biol Evol. 20:1917-1924.
37. Kajander OA, Karhunen PJ, Holt IJ, Jacobs HT. 2001. Prominent mitochondrial DNA recombination intermediates in human heart muscle. EMBO Rep. 2:1007-1012.
38. Kajander OA, Rovio AT, Majamaa K, Poulton J, Spelbrink JN, Holt IJ, Karhunen PJ, Jacobs HT. 2000. Human mtDNA sublimons resemble rearranged mitochondrial genomes found in pathological states. Hum Mol Genet. 9:2821-2835.
39. Kogoma T. 1997. Stable DNA replication: interplay between DNA replication, homologous recombination, and transcription. Microbiol Mol Biol Rev. 61:212-238.
40. Kraytsberg Y, Schwartz M, Brown TA, Ebralidse K, Kunz WS, Clayton DA, Vissing J, Khrapko K. 2004. Recombination of human mitochondrial DNA. Science. 304:981.
41. Kumar S. 1996. Phyltest: phylogeny hypothesis testing software. Philadelphia (PA): The Pennsylvania State University.
42. Kumazawa Y, Endo H. 2004. Mitochondrial genome of the Komodo dragon: efficient sequencing method with reptile-oriented primers and novel gene rearrangements. DNA Res. 11:115-125.
43. Kumazawa Y, Ota H, Nishida M, Ozawa T. 1996. Gene rearrangements in snake mitochondrial genomes: highly concerted evolution of control-region-like sequences duplicated and inserted into a tRNA gene cluster. Mol Biol Evol. 13:1242-1254.
44. Kumazawa Y, Ota H, Nishida M, Ozawa T. 1998. The complete nucleotide sequence of a snake (Dinodon semicarinatus) mitochondrial genome with two identical control regions. Genetics. 150:313-329.
45. Kurabayashi A, Ueshima R. 2000. Complete sequence of the mitochondrial DNA of the primitive opisthobranch gastropod Pupa strigosa: systematic implication of the genome organization. Mol Biol Evol. 17:266-277.
46. Kurabayashi A, Usuki C, Mikami N, Fujii T, Yonekawa H, Sumida M, Hasegawa M. 2006. Complete nucleotide sequence of the mitochondrial genome of a Malagasy poison frog Mantella madagascariensis: evolutionary implications on mitochondrial genomes of higher anuran groups. Mol Phylogenet Evol. 39:223-236.
47. Ladoukakis ED, Zouros E. 2001. Recombination in animal mitochondrial DNA: evidence from published sequences. Mol Biol Evol. 18:2127-2131.
48. Lavrov DV, Boore JL, Brown WM. 2002. Complete mtDNA sequences of two millipedes suggest a new model for mitochondrial gene rearrangements: duplication and non-random loss. Mol Biol Evol. 19:163-169.
49. Lee JS, Miya M, Lee YS, Kim CG, Park EH, Aoki Y, Nishida M. 2001. The complete DNA sequence of the mitochondrial genome of the self-fertilizing fish Rivulus marmoratus (Cyprinodontiformes, Rivulidae) and the first description of duplication of a control region in fish. Gene. 280:1-7.
50. Lewin G. 2003. Genes VIII. Princeton (NJ): Pearson Prentice Hall.
51. Lunt DF, Hyman BC. 1997. Animal mitochondrial DNA recombination. Nature. 387:247.
52. Mabuchi K, Miya M, Sato TP, Westneat MW, Nishida M. 2004. Gene rearrangements and evolution of tRNA pseudogenes in the mitochondrial genome of the parrotfish (Teleostei: Perciformes: Scaridae). J Mol Evol. 59:287-297.
53. Macey JR, Larson A, Ananjeva NB, Fang Z, Papenfuss TJ. 1997. Two novel gene orders and the role of light-strand replication in rearrangement of the vertebrate mitochondrial genome. Mol Biol Evol. 14:91-104.
54. Mindell DP, Sorenson MD, Dimcheff DE. 1998. Multiple independent origins of mitochondrial gene order in birds. Proc Natl Acad Sci USA. 95:10693-10697.
55. Moritz C, Dowling TE, Brown WM. 1987. Tandem duplications in animal mitochondrial DNAs: variation in incidence and gene content among lizards. Proc Natl Acad Sci USA. 84:7183-7187.
56. Mueller RL, Boore JL. 2005. Molecular mechanisms of extensive mitochondrial gene rearrangement in plethodontid salamanders. Mol Biol Evol. 22:2104-2112.
57. Noguchi Y, Endo K, Tajima F, Ueshima R. 2000. The mitochondrial genome of the brachiopod Laqueus rubellus. Genetics. 155:245-259.
58. Ogoh K, Ohmiya Y. 2007. Concerted evolution of duplicated control regions within an ostracod mitochondrial genome. Mol Biol Evol. 24:74-78.
59. Pääbo S, Irwin DM, Wilson AC. 1990. DNA damage promotes jumping between templates during enzymatic amplification. J Biol Chem. 265:4718-4721.
60. Posada D, Crandall KA. 1998. Modeltest: testing the model of DNA substitution. Bioinformatics. 14:817-818.
61. Rawson PD. 2005. Nonhomologous recombination between the large unassigned region of the male and female mitochondrial genomes in the mussel, Mytilus trossulus. J Mol Evol. 61:717-732.
62. Reyes A, Yang MY, Bowmaker M, Holt IJ. 2005. Bidirectional replication initiates at sites throughout the mitochondrial genome of birds. J Biol Chem. 280:3242-3250.
63. Richards CM, Nussbaum RA, Raxworthy J. 2000. Phylogenetic relationships within Madagascan boophids and mantellids as elucidated by mitochondrial ribosomal genes. Afr J Herpetol. 49:23-32.
64. Roe BA, Ma DP, Wilson RK, Wong JFH. 1985. The complete nucleotide sequence of the Xenopus laevis mitochondrial genome. J Biol Chem. 260:9759-9774.
65. Roelants K, Gower DJ, Wilkinson M, Loader SP, Biju SD, Guillaume K, Moriau L, Bossuyt F. 2007. Global patterns of diversification in the history of modern amphibians. Proc Natl Acad Sci USA. 104:887-892.
66. Roelants K, Jiang J, Bossuyt F. 2004. Endemic ranid (Amphibia: Anura) genera in southern mountain ranges of the Indian subcontinent represent ancient frog lineages: evidence from molecular data. Mol Phylogenet Evol. 31:730-740.
67. Ronquist F, Huelsenbeck JP. 2003. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics. 19:1572-1574.
68. San Mauro D, García-París M, Zardoya R. 2004. Phylogenetic relationships of discoglossid frogs (Amphibia: Anura: Discoglossidae) based on complete mitochondrial genomes and nuclear genes. Gene. 343:357-366.
69. San Mauro D, Gower DJ, Zardoya R, Wilkinson M. 2006. A hotspot of gene order rearrangement by tandem duplication and random loss in the vertebrate mitochondrial genome. Mol Biol Evol. 23:227-234.
70. San Mauro D, Vences M, Alcobendas M, Zardoya R, Meyer A. 2005. Initial diversification of living amphibians predated the breakup of Pangaea. Am Nat. 165:590-599.
71. Sano N, Kurabayashi A, Fujii T, Yonekawa H, Sumida M. 2004. Complete nucleotide sequence and gene rearrangement of the mitochondrial genome of the bell-ring frog, Buergeria buergeri (family Rhacophoridae). Genes Genet Syst. 79:151-163.
72. Sano N, Kurabayashi A, Fujii T, Yonekawa H, Sumida M. 2005. Complete nucleotide sequence of the mitochondrial genome of Schlegel's tree frog Rhacophorus schlegelii (family Rhacophoridae): duplicated control regions and gene rearrangements. Genes Genet Syst. 80:213-224.
73. Sato A, Nakada K, Akimoto M, Ishikawa K, Ono T, Shitara H, Yonekawa H, Hayashi J. 2005. Rare creation of recombinant mtDNA haplotypes in mammalian tissues. Proc Natl Acad Sci USA. 102:6057-6062.
74. Shadel GS, Clayton DA. 1997. Mitochondrial DNA maintenance in vertebrates. Annu Rev Biochem. 66:409-435.
75. Shao R, Dowton M, Murrell A, Barker SC. 2003. Rates of gene rearrangement and nucleotide substitution are correlated in the mitochondrial genomes of insects. Mol Biol Evol. 20:1612-1619.
76. Shimodaira H, Hasegawa M. 2001. CONSEL: a program for assessing the confidence of phylogenetic tree selection. Bioinformatics. 17:1246-1247.
77. Smith MJ, Arndt A, Gorski S, Fajber E. 1993. The phylogeny of echinoderm classes based on mitochondrial gene arrangements. J Mol Evol. 36:545-554.
78. Sumida M, Kanamori Y, Kaneda H, Kato Y, Nishioka M, Hasegawa M, Yonekawa H. 2001. Complete nucleotide sequence and gene rearrangement of the mitochondrial genome of the Japanese pond frog Rana nigromaculata. Genes Genet Syst. 76:311-325.
79. Swofford DL. 2003. PAUP*: phylogenetic analysis using parsimony (*and other methods). Version 4. Sunderland (MA): Sinauer Associates.
80. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG. 1997. The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 24:4876-4882.
81. Thorne JL, Kishino H. 2002. Divergence time and evolutionary rate estimation with multilocus data. Syst Biol. 51:689-702.
82. Thyagarajan B, Padua RA, Campbell C. 1996. Mammalian mitochondria possess homologous DNA recombination activity. J Biol Chem. 271:27536-27543.
83. Tsaousis AD, Martin DP, Ladoukakis ED, Posada D, Zouros E. 2005. Widespread recombination in published animal mtDNA sequences. Mol Biol Evol. 22:925-933.
84. Van Bocxlaer I, Roelants K, Biju SD, Nagaraju J, Bossuyt F. 2006. Late Cretaceous vicariance in Gondwanan amphibians. PLoS ONE. 1:e74.
85. Van der Meijden A, Vences M, Hoegg S, Boistel R, Channing A, Meyer A. 2007. Nuclear gene phylogeny of narrow-mouthed toads (family Microhylidae) and a discussion of competing hypotheses concerning their biogeographical origins. Mol Phylogenet Evol. 44:1017-1030.
86. Van der Meijden A, Vences M, Hoegg S, Meyer A. 2005. A previously unrecognized radiation of ranid frogs in southern Africa revealed by nuclear and mitochondrial DNA sequences. Mol Phylogenet Evol. 37:674-685.
87. Vences M, Andreone F, Glaw F, Kosuch J, Meyer A, Schaefer HC, Veith M. 2002. Exploring the potential of life-history key innovation: brook breeding in the radiation of the Malagasy treefrog genus Boophis. Mol Ecol. 11:1453-1463.
88. Vences M, Andreone F, Glaw F, Randrianirina JE. 2003. Molecular and bioacoustic divergence in Mantidactylus granulatus and M. zavona sp. n. (Anura: Mantellidae): bearings for the biogeography of northern Madagascar. Afr Zool. 38:67-78.
89. Vences M, Vieites DR, Glaw F, Brinkmann H, Kosuch J, Veith M, Meyer A. 2003. Multiple overseas dispersal in amphibians. Proc R Soc Lond Ser B. 270:2435-2442.
90. Vences M, Wahl-Boos G, Hoegg S, Glaw F, Spinelli O, Meyer A, Perry S. 2007. Molecular systematics of mantelline frogs from Madagascar and evolution of their femoral glands. Biol J Linn Soc. 92:529-539.
91. Wolstenholme DR. 1992. Animal mitochondrial DNA: structure and evolution. In: Wolstenholme DR, Jeon KW, editors. Mitochondrial genomes. New York: Academic Press. p. 173-216.
92. Xu W, Jameson D, Tang B, Higgs PG. 2006. The relationship between the rate of molecular evolution and the rate of genome rearrangement in animal mitochondrial genomes. J Mol Evol. 63:375-392.
93. Yang MY, Bowmaker M, Reyes A, Vergani L, Angeli P, Gringeri E, Jacobs HT, Holt IJ. 2002. Biased incorporation of ribonucleotides on the mitochondrial L-strand accounts for apparent strand-asymmetric DNA replication. Cell. 111:495-505.
94. Yasukawa T, Reyes A, Cluett TJ, Yang MY, Bowmaker M, Jacobs HT, Holt IJ. 2006. Replication of vertebrate mitochondrial DNA entails transient ribonucleotide incorporation throughout the lagging strand. EMBO J. 25:5358-5371.
95. Yokobori S, Fukuda N, Nakamura M, Aoyama T, Oshima T. 2004. Long-term conservation of six duplicated structural genes in cephalopod mitochondrial genomes. Mol Biol Evol. 21:2034-2046.
96. Yokobori S, Oshima T, Wada H. 2005. Complete nucleotide sequence of the mitochondrial genome of Doliolum nationalis with implications for evolution of urochordates. Mol Phylogenet Evol. 34:273-283.