The complete maternal and paternal mitochondrial genomes of the Mediterranean mussel Mytilus galloprovincialis: Implications for the doubly uniparental inheritance mode of mtDNA

Molecular Biology and Evolution

Volumn 22, Issue 4, 2005, Pages 952-967

  Mizi, Athanasia ^a   Zouros, Eleftherios ^b   Moschonas, Nicholas ^b   Rodakis, George C ^a  

^a UNIVERSITY OF ATHENS   (Greece)

^b UNIVERSITY OF CRETE   (Greece)

Author keywords

Maternally or paternally inherited mtDNA; Mitochondrial genome; Mytilus

Indexed keywords

ADENOSINE TRIPHOSPHATASE; CELL PROTEIN; METHIONINE; MITOCHONDRIAL DNA; PROTEIN COX3; PROTEIN NAD3; TRANSFER RNA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BIODIVERSITY; CLAM; CODON USAGE; CONTROLLED STUDY; EXTRACHROMOSOMAL INHERITANCE; FEMALE; GENE IDENTIFICATION; GENE REPLICATION; GENETIC COMPLEMENTATION; GENETIC TRANSCRIPTION; INHERITANCE; MALE; MEDITERRANEAN SEA; MITOCHONDRIAL GENETICS; MUSSEL; MYTILUS GALLOPROVINCIALIS; NONHUMAN; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; PATERNALISM; PHYLOGENY; SEQUENCE HOMOLOGY; STOP CODON; VENERUPIS PHILIPPINARUM;

ANIMALS; BASE SEQUENCE; BIVALVIA; DNA, MITOCHONDRIAL; FEMALE; GENOME; GENOMIC IMPRINTING; MALE; MOLECULAR SEQUENCE DATA; NUCLEIC ACID CONFORMATION; RNA, RIBOSOMAL; RNA, TRANSFER; SPECIES SPECIFICITY;

EID: 16344377703     PISSN: 07374038     EISSN: None     Source Type: Journal    
DOI: 10.1093/molbev/msi079     Document Type: Article

References (82)

1. Altschul, S. F., W. Gish, W. Miller, E. W. Myers, and D. J. Lipman. 1990. Basic local alignment search tool. J. Mol. Biol. 215:403-410.
2. Asakawa, S., H. Himeno, K. Miura, and K. Watanabe. 1995. Nucleotide sequence and gene organization of the starfish Asterina pectinifera mitochondrial genome. Genetics 140:1047-1060.
3. Asakawa, S., Y. Kumazawa, T. Araki, H. Himeno, K. Miura, and K. Watanabe. 1991. Strand-specific nucleotide composition bias in echinoderm and vertebrate mitochondrial genomes. J. Mol. Evol. 32:511-520.
4. Ballard, J. W. 2004. Sequential evolution of a symbiont inferred from the host: Wolbachia and Drosophila simulans. Mol. Biol. Evol. 21:428-442.
5. Ser(UCN) gene. Genetics 152:641-652.
6. Bibb, M. J., R. A. Van Etten, C. T. Wright, M. W. Walberg, and D. A. Clayton. 1981. Sequence and gene organization of mouse mitochondrial DNA. Cell 26:167-180.
7. Boore, J. L. 1999. Animal mitochondrial genomes. Nucleic Acids Res. 27:1767-1780.
8. Boore, J. L., and W. M. Brown. 1994. Complete DNA sequence of the mitochondrial genome of the black chiton Katharina tunicata. Genetics 138:423-443.
9. -. 1995. Complete sequence of the mitochondrial DNA of the annelid worm Lumbricus terrestris. Genetics 141: 305-319.
10. -. 2000. Mitochondrial genomes of Galathealinum, Helobdella, and Platynereis: sequence and gene arrangement comparisons indicate that Pogonophora is not a phylum and Annelida and Arthropoda are not sister taxa. Mol. Biol. Evol. 17:87-106.
11. Boore, J. L., M. Medina, and L. A. Rosenberg. 2004. Complete sequences of the highly rearranged molluscan mitochondrial genomes of the scaphopod Graptacme eborea and the bivalve Mytilus edulis. Mol. Biol. Evol. 21:1492-1503.
12. Broughton, R. E., J. E. Milam, and B. A. Roe. 2001. The complete sequence of the zebrafish (Danio rerio) mitochondrial genome and evolutionary patterns in vertebrate mitochondrial DNA. Genome Res. 11:1958-1967.
13. Burzynski, A., M. Zbawicka, D. O. F. Skibinski, and R. Wenne. 2003. Evidence for recombination of mtDNA in the marine mussel Mytilus trossulus from the Baltic. Mol. Biol. Evol. 20:388-392.
14. Cantatore, P., M. Roberti, G. Rainaldi, M. N. Gadaleta, and C. Saccone. 1989. The complete nucleotide sequence, gene organization, and genetic code of the mitochondrial genome of Paracentrotus lividus. J. Biol. Chem. 264:10965-10975.
15. Cao, L., E. Kenchington, and E. Zouros. 2004. Differential segregation patterns of sperm mitochondria in embryos of the blue mussel (Mytilus eduiis). Genetics 166:883-894.
16. Cao, L., E. Kenchington, E. Zouros, and G. C. Rodakis. 2004. Evidence that the large noncoding sequence is the main control region of maternally and paternally transmitted mitochondrial genomes of the marine mussel (Mytilus spp.). Genetics 167:835-850.
17. Carter, J. G., Campbell, D. C., and M. R. Campbell. 2000. Cladistic perspectives on early bivalve evolution. Pp. 47-79 In E. M. Harper, J. D. Taylor, and J. A. Crame, eds. The evolutionary biology of the bivalvia. Special Publications 177. Geological Society, London.
18. Chang, Y. S., F. L. Huang, and T. B. Lo. 1994. The complete nucleotide sequence and gene organization of carp (Cyprinus carpio) mitochondrial genome. J. Mol. Evol. 38:138-155.
19. Clary, D. O., and D. R. Wolstenholme. 1985. The mitochondrial DNA molecule of Drosophila yakuba: nucleotide sequence, gene organization, and genetic code. J. Mol. Evol. 22:252-271.
20. Crease, T. J. 1999. The complete sequence of the mitochondrial genome of Daphnia pulex (Cladocera: Crustacea). Gene 233:89-99.
21. Curole, J. P., and T. D. Kocher. 2002. Ancient sex-specific extension of the cytochrome c oxidase II gene in bivalves and the fidelity of doubly-uniparental inheritance. Mol. Biol. Evol. 19:1323-1328.
22. De Giorgi, C., A. Martiradonna, C. Lanave, and C. Saccone. 1996. Complete sequence of the mitochondrial DNA in the sea urchin Arbacia lixula: conserved features of the echinoid mitochondrial genome. Mol. Phylogenet. Evol. 5:323-332.
23. DeJong, R. J., A. M. Emery, and C. M. Adema. 2004. The mitochondrial genome of Biomphalaria glabrata (gastropoda, basommatophora), intermediate host of Schistosoma mansoni. J. Parasitol. 90:991-997.
24. Diaz, F., M. P. Bayona-Bafaluy, M. Rana, M. Mora, H. Hao, and C. T. Moraes. 2002. Human mitochondrial DNA with large deletions repopulates organelles faster than full-length genomes under relaxed copy number control. Nucleic Acids Res. 30:4626-4633.
25. Dirheimaer, G., G. Keith, P. Dumas, and E. Westhof. 1995. Primary, secondary, and tertiary structures of tRNAs. Pp. 93-126 in D. Söll and U. L. RajBahandary, eds. tRNA: structure, biosynthesis and function. ASM Press, Washington, DC.
26. Dreyer, H., and G. Steiner. 2004. The complete sequence and gene organization of the mitochondrial genome of the gadilid scaphopod Siphonodentalium lobatum (Mollusca). Mol. Phylogenet. Evol. 31:605-617.
27. Garesse, R. 1988. Drosophila melanogaster mitochondrial DNA: gene organization and evolutionary considerations. Genetics 118:649-663.
28. Garrido-Ramos, M. A., D. T. Stewart, B. W. Sutherland, and E. Zouros. 1998. The distribution of male-transmitted and female-transmitted mitochondrial DNA types in somatic tissues of blue mussels: implications for the operation of doubly uniparental inheritance of mitochondrial DNA. Genome 41:818-824.
29. Gossling, E. 1992. Systematics and geographic distribution of Mytilus. Pp. 1-20 in E. Gossling, ed. The mussel Mytilus: ecology, physiology, genetics and aquaculture. Elsevier, Amsterdam.
30. Grande, C., J. Templado, J. L. Cervera, and R. Zardoya. 2002. The complete mitochondrial genome of the nudibranch Roboastra europaea (Mollusca: Gastropoda) supports the monophyly of opisthobranchs. Mol. Biol. Evol. 10:1672-1685.
31. Hatzoglou, E., G. C. Rodakis, and R. Lecanidou. 1995. Complete sequence and gene organization of the mitochondrial genome of the land snail Albinaria coerulea. Genetics 140:1353-1366.
32. Helfenbein, K. G., W. M. Brown, and J. L. Boore. 2001. The complete mitochondrial genome of the articulate brachiopod Terebratalia transversa. Mol. Biol. Evol. 18:1734-1744.
33. Hoeh, W. R., D. T. Stewart, and S. I. Guttman. 2002. High fidelity of mitochondrial genome transmission under the doubly uniparental mode of inheritance in freshwater mussels (Bivalvia: Unionoidea). Evol. Int. J. Org. Evol. 56:2252-2261.
34. Hoeh, W. R., D. T. Stewart, C. Saavedra, B. W. Sutherland, and E. Zouros. 1997. Phylogenetic evidence for role-reversals of gender-associated mitochondrial DNA in Mytilus (Bivalvia: Mytilidae). Mol. Biol. Evol. 14:959-967.
35. Hoeh, W. R., D. T. Stewart, B. W. Sutherland, and E. Zouros. 1996. Cytochrome c oxidase sequence comparisons suggest an unusually high rate of mitochondrial DNA evolution in Mytilus (Mollusca: Bivalvia). Mol. Biol. Evol. 13:418-421.
36. Hoffmann, R. J., J. L. Boore, and W. M. Brown. 1992. A novel mitochondrial genome organization for the blue mussel Mytilus edulis. Genetics 131:397-412.
37. Hurst, L. D., and R. F. Hoekstra. 1994. Evolutionary genetics. Shellfish genes kept in line. Nature 368:811-812.
38. Ingman, M., H. Kaessmann, S. Pääbo, and U. Gyllensten. 2000. Mitochondrial genome variation and the origin of modern humans. Nature 408:708-713.
39. Jermiin, L. S., and R. H. Crozier. 1994. The cytochrome b region in the mitochondrial DNA of the ant Tetraponera rufoniger: sequence divergence in Hymenoptera may be associated with nucleotide content. J. Mol. Evol. 38:282-294.
40. Jermiin, L. S., P. G. Foster, D. Graur, R. M. Lowe, and R. H. Crozier. 1996. Unbiased estimation of symmetrical directional mutation pressure from protein-coding DNA. J. Mol. Evol. 42:476-480.
41. Jermiin, L. S., D. Graur, R. M. Lowe, and R. H. Crozier. 1994. Analysis of directional mutation pressure and nucleotide content in mitochondrial cytochrome b genes. J. Mol. Evol. 39:160-173.
42. Kimura, M. 1980. A simple method for estimating evolutionary rates of base substitution through comparative studies of nucleotide sequences. J. Mol. Evol. 16:111-120.
43. Kumar, S. 1996. PHYLTEST: a program for testing phylogenetic hypotheses. Pennsylvania State University, University Park.
44. Kumar, S., K. Tamura, I. B. Jakobsen, and M. Nei. 2001. MEGA2: molecular evolutionary genetics analysis software. Bioinformatics 17:1244-1245.
45. Kurabayashi, A., and R. Ueshima. 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. Ladoukakis, E. D., C. Saavedra, A. Magoulas, and E. Zouros. 2002. Mitochondrial DNA variation in a species with two mitochondrial genomes: the case of Mytilus galloprovincialis from the Atlantic, the Mediterranean and the Black Sea. Mol. Ecol. 11:755-769.
47. Ladoukakis, E. D., and E. Zouros. 2001. Direct evidence for homologous recombination in mussel (Mytilus galloprovincialis) mitochondrial DNA. Mol. Biol. Evol. 18:1168-1175.
48. Le, T. H., D. Blair, T. Agatsuma et al. (14 co-authors). 2000. Phylogenies inferred from mitochondrial gene orders - a cautionary tale from the parasitic flatworms. Mol. Biol. Evol. 17:1123-1125.
49. Liu, H.-R, J. B. Mitton, and S. K. Wu. 1996. Paternal mitochondrial DNA differentiation far exceeds maternal DNA and allozyme differentiation in the fresh water mussel Anodonda grantis grantis. Evolution 50:952-957.
50. Noguchi, Y., K. Endo, F. Tajima, and R. Ueshima. 2000. The mitochondrial genome of the brachiopod Laqueus rubellus. Genetics 155:245-259.
51. Ojala, D., J. Montoya, and G. Attardi. 1981. tRNA punctuation model of RNA processing in human mitochondria. Nature 290:470-474.
52. Okimoto, R., J. L. Macfarlane, D. O. Clary, and D. R. Wolstenholme. 1992. The mitochondrial genomes of two nematodes, Caenorhabditis elegans and Ascaris suum. Genetics 130:471-498.
53. Passamonti, M., and V. Skali. 2001. Gender-associated mitochondrial DNA heteroplasmy in the venerid clam Tapes philippinarum (Mollusca: Bivalvia). Curr. Genet. 39:117-124.
54. Perna, N. T., and T. D. Kocher. 1995. Patterns of nucleotide composition at fourfold degenerate sites of animal mitochondrial genomes. J. Mol. Evol. 41:353-358.
55. Pesole, G., C. Gissi, A. De Chirico, and C. Saccone. 1999. Nucleotide substitution rate of mammalian mitochondrial genomes. J. Mol. Evol. 48:427-434.
56. Quesada, H., D. A. Skibinski, and D. O. Skibinski. 1996. Sex-biased heteroplasmy and mitochondrial DNA inheritance in the mussel Mytilus galloprovincialis Lmk. Curr. Genet. 29:423-426.
57. Quesada, H., M. Warren, and D. O. Skibinski. 1998. Nonneutral evolution and differential mutation rate of gender-associated mitochondrial DNA lineages in the marine mussel Mytilus. Genetics 149:1511-1526.
58. Quesada, H., R. Wenne, and D. O. Skibinski. 1999. Interspecies transfer of female mitochondrial DNA is coupled with role-reversals and departure from neutrality in the mussel Mytilus trossulus. Mol. Biol. Evol. 16: 655-665.
59. Rand, D. M., and L. M. Kann. 1998. Mutation and selection at silent and replacement sites in the evolution of animal mitochondrial DNA. Genetica 102/103:393-407.
60. Rawson, P. D., and T. J. Hilbish. 1995. Evolutionary relationships among the male and female mitochondrial DNA lineages in the Mytilus edulis species complex. Mol. Biol. Evol. 12:893-901.
61. Roe, B. A., D. P. Ma, R. K. Wilson, and J. F. Wong. 1985. The complete nucleotide sequence of the Xenopus laevis mitochondrial genome. J. Biol. Chem. 260:9759-9774.
62. Rozas, J., and R. Rozas. 1999. DnaSP version3: an integrated program for molecular population genetics and molecular evolution analysis. Bioinformatics 15:174-175.
63. Rzhetsky A., Kumar S., and M. Nei. 1995. Four-cluster analysis: a simple method to test phylogenetic hypotheses. Mol. Biol. Evol. 12:163-167.
64. Saavedra, C., M. I. Reyero, and E. Zouros. 1997. Male-dependent doubly uniparental inheritance of mitochondrial DNA and female-dependent sex-ratio in the mussel Mytilus galloprovincialis. Genetics 145:1073-1082.
65. Saccone, C., C. De Giorgi, C. Gissi, G. Pesole, and A. Reyes. 1999. Evolutionary genomics in Metazoa: the mitochondrial DNA as a model system. Gene 238:195-209.
66. Sanger, F., S. Nicklen, and A. R. Coulson. 1977. DNA sequencing with chain-terminating inhibitors. Proc. Natl. Acad. Sci. USA 74:5463-5467.
67. Serb, J. M., and C. Lydeard. 2003. Complete mtDNA sequence of the North American freshwater mussel, Lampsilis ornata (Unionidae): an examination of the evolution and phylogenetic utility of mitochondrial genome organization in Bivalvia (Mollusca). Mol. Biol. Evol. 20:1854-1866.
68. Skibinski, D. O. F., C. Gallagher, and C. M. Beynon. 1994a. Mitochondrial DNA inheritance. Nature 368:817-818.
69. -. 1994b. Sex limited mitochondrial DNA transmission in the marine mussel Mytilus edulis. Genetics 138:801-809.
70. Spruyt, N., C. Delarbre, G. Gachelin, and V. Laudet. 1998. Complete sequence of the amphioxus (Branchiostoma lanceolatum) mitochondrial genome: relations to vertebrates. Nucleic Acids Res. 26:3279-3285.
71. Stechmann, A., and M. Schlegel. 1999. Analysis of the complete mitochondrial DNA sequence of the brachiopod Terebratulina retusa places Brachiopoda within the protostomes. Proc. R. Soc. Lond. B Biol. Sci. 266:2043-2052.
72. Stewart, D. T., E. R. Kenchington, R. K. Singh, and E. Zouros. 1996. Degree of selective constraint as an explanation of the different rates of evolution of gender-specific mitochondrial DNA lineages in the mussel Mytilus. Genetics 143:1349-1357.
73. Stewart, D. T., C. Saavedra, R. R. Stanwood, A. O. Ball, and E. Zouros. 1995. Male and female mitochondrial lineages in the blue mussel (Mytilus edulis) species group. Mol. Biol. Evol. 12:735-747.
74. Sueoka, N. 1962. On the genetic basis of variation and heterogeneity of DNA base composition. Proc. Natl. Acad. Sci. USA 48:582-592.
75. Terrett, J. A., S. Miles, and R. H. Thomas. 1996. Complete DNA sequence of the mitochondrial genome of Cepaea nemoralis (Gastropoda: Pulmonata). J. Mol. Evol. 42:160-168.
76. Thompson, J. D., T. J. Gibson, F. Plewniak, F. Jeanmougin, and D. G. Higgins. 1997. The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 24:4876-4882.
77. Tomita, K., S. Yokobori, T. Oshima, T. Ueda, and K. Watanabe. 2002. The cephalopod Loligo bleekeri mitochondrial genome: multiplied noncoding regions and transposition of tRNA genes. J. Mol. Evol. 54:486-500.
78. Wolstenholme, D. R. 1992. Animal mitochondrial DNA: structure and evolution. Int. Rev. Cytol. 141:173-216.
79. Yamazaki, N., R. Ueshima, J. A. Terrett et al. (12 co-authors). 1997. Evolution of pulmonate gastropod mitochondrial genomes: comparisons of gene organizations of Euhadra, Cepaea and Albinaria and implications of unusual tRNA secondary structures. Genetics 145:749-758.
80. Zouros, E., A. O. Ball, C. Saavedra, and K. R. Freeman. 1994a. Mitochondrial DNA inheritance. Nature 368:818.
81. -. 1994b. An unusual type of mitochondrial DNA inheritance in the blue mussel Mytilus. Proc. Natl. Sci. USA 91:7463-7467.
82. Zuker, M. 2003. Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res. 31:3406-3415.