Characteristics of mitochondrial DNA of unionid bivalves (Mollusca: Bivalvia: Unionidae). II. Comparison of complete sequences of maternally inherited mitochondrial genomes of Sinanodonta woodiana and Unio pictorum
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Department of Genetics, University of Szczecin, Poland
Submission date: 2010-09-21
Acceptance date: 2010-11-04
Publication date: 2020-05-14
Corresponding author
Marianna Soroka   

Department of Genetics, University of Szczecin, Felczaka 3c, 71-412 Szczecin, Poland
Folia Malacol. 2010;18(4):189-209
The objective of the study was to sequence the complete female mitochondrial genomes of Sinanodonta woodiana and Unio pictorum, and to ascertain their intra- and inter-specific variation within all the genes and non-coding regions. Complete sequence of maternally inherited mitochondrial genome of Sinanodonta woodiana is 16,243 bp long and is one of the three longest mt genomes in unionids; mt genome of Unio pictorum with its 15,761 bp is one of the smallest in the family. Each genome includes 14 protein-coding genes (13 as in most Metazoa, plus one open reading frame F ORF), 2 ribosomal RNA genes and 22 genes fortransfer RNA with typical secondary structures, except for tRNA for serine1. S. woodiana has 25, and U. pictorum 27 non-coding sequences, which constitute 7.8 and 4.9% of mt genome, respectively. The content of A+T bases is 65.8% in S. woodiana and 65.1% in U. pictorum; the difference between the two species is 21%. Intra-specific variation in S. woodiana is three times greater than in U. pictorum. Lower nucleotide diversity within the second species suggests a small effective population size of the Polish U. pictorum. The two species show a similar usage of the most frequent and least frequent codons; the differences pertain to the usage of both stop codons. Gene trnS1 (serine, UGA) in unionids is very little variable with respect to tRNA secondary structure (absence of DHU arm), and nucleotide composition, while its inter-specific variation is half lower than in other mt-tRNAs.
Anderson S., Bankier A. T., Barrell B. G., De Bruijn M. H., Coulson A. R., Drouin J., Eperon I. C., Nierlich D. P., Roe B. A., Sanger F., Schreier P. H., Smith A. J., Staden R., Young I. G. 1981. Sequence and organization of the human mitochondrial genome. Nature 290: 457-465.
Avise J. C. 1986. Mitochondrial DNA and the evolutionary genetics of higher animals. Phil. Trans. R. Soc. Lond. B 312: 325-342.
Avise J. C., Arnold J., Ball R. M., Bermingham E., Lamb T., Neigel J. E., Reeb A. C., Saunders N. C. 1987. Intra-specific phylogeography: The mitochondrial DNA bridge between population genetics and systematics. Ann. Rev. Ecol. Syst. 18: 489-522.
Avise J. C., Lansman R. A., Shade R. O. 1979. The use of restriction endonucleases to measure mitochondrial DNA sequence relatedness in natural populations. I. Population structure and evolution in the genus Peromyscus. Genetics 92: 279-295.
Beagley C. T., Okimoto R., Wolstenholme D. R. 1998. The mitochondrial genome of the sea anemone Metridium senile (Cnidaria): introns, a paucity of tRNA genes, and a near-standard genetic code. Genetics 148: 1091-1108.
Bleidorn C., Podsiadlowski L., Bartolomaeus T. 2006. The complete mitochondrial genome of the orbiniid polychaete Orbinia latreillii (Annelida, Orbiniidae) - A novel gene order for Annelida and implications for annelid phylogeny. Gene 370: 96-103.
Bogan A. E. 2008. Global diversity of freshwater mussels (Mollusca, Bivalvia) in freshwater. Hydrobiologia 595: 139-147.
Bogan A. E., Roe K. J. 2008. Freshwater bivalve (Unioniformes) diversity, systematics, and evolution: status and future directions. J. N. Am. Benthol. Soc. 27: 349-369.
Boore J. L. 1999. Animal mitochondrial genomes. Nucleic Acids Res. 27: 1767-1780.
Boore J. L., Brown W. M. 1994a. Complete DNA sequence of the mitochondrial genome of the black chiton, Katharina tunicata. Genetics 138: 423-443.
Boore J. L., Brown W. M. 1994b. Mitochondrial genomes and the phylogeny of Mollusks. The Nautilus Spp. 2: 61-78.
Boore J. L., Medina M., Rosenberg L. A. 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.
Breton S., Burger G., Stewart D. T., Blier P. U. 2006. Comparative analysis of gender-associated complete mitochondrial genomes in marine mussels (Mytilus spp.). Genetics 172: 1107-1119.
Breton S., Beaupré H. D., Stewart D. T., Piontkivska H., Karmakar M., Bogan A. E., Blier P. U., Hoeh W. R. 2009. Comparative mitochondrial genomics of freshwater mussels (Bivalvia: Unionoida) with doubly uniparental inheritance of mtDNA: gender-specific open reading frames and putative origins of replication. Genetics 183: 1575-1589.
Broughton R. E., Milam J. E., Roe B. A. 2001. The complete sequence of the zebrafish (Danio rerio) mitochondrial genome and evolutionary patterns in vertebrate mitochondrial DNA. Genome Res. 11: 1958-1967.
Brugler M. R., France S. C. 2008. The mitochondrial genome of a deep-sea bamboo coral (Cnidaria, Anthozoa, Octocorallia, Isididae): genome structure and putative origins of replication are not conserved among octocorals. J. Mol. Evol. 67: 125-136.
Cao L., Kenchington E., Zouros E., Rodakis G. C. 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.
Cao L., Ort B. S., Mizi A., Pogson G., Kenchington E., Zouros E., Rodakis G. C. 2009. The control region of maternally and paternally inherited mitochondrial genomes of three species of the sea mussel genus Mytilus. Genetics 181: 1045-1056.
Chang Y. S., Huang F. L., Lo T. B. 1994. The complete nucleotide sequence and gene organization of carp (Cyprinus carpio) mitochondrial genome. J. Mol. Evol. 38: 138-155.
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.
Doucet-Beaupré H., Breton S., Chapman E., Blier P., Bogan A., Stewart D., Hoeh W. 2010. Mitochondrial phylogenomics of the Bivalvia (Mollusca): searching for the origin and mitogenomic correlates of doubly uniparental inheritance of mtDNA. BMC Evol. Biol. 10: 50 doi: 10.1186/1471-2148-10-50.
Dreyer H., Steiner G. 2006. The complete sequences and gene organisation of the mitochondrial genomes of the heterodont bivalves Acanthocardia tuberculata and Hiatella arctica -and the first record for a putative ATPase subunit 8 gene in marine bivalves. Frontiers in Zoology 3: 13.
Gissi C., Iannelli F., Pesole G. 2008. Evolution of the mitochondrial genome of Metazoa as exemplified by comparison of congeneric species. Heredity 101: 301-320.
Graf D. L., Cummings K. S. 2007. Review of the systematics and global diversity of freshwater mussel species (Bivalvia: Unionoida). J. Moll. Stud. 73: 291-314.
Hatzoglou E., Rodakis G. C., Lecanidou R. 1995. Complete sequence and gene organization of the mitochondrial genome of the land snail Albinaria coerulea. Genetics 140: 1353-1366.
Hoffmann R. J., Boore J. L., Brown W. M. 1992. A novel mitochondrial genome organization for the blue mussel, Mytilus edulis. Genetics 131: 397-412.
Ingman M., Kaessmann H., Pääbo S., Gyllensten U. 2000. Mitochondrial genome variation and the origin of modern humans. Nature 408: 708-713.
Källersjo M., Von Proschwitz T., Lundberg S., Eldenäs P., Erséus C. 2005. Evaluation of ITS rDNA as a complement to mitochondrial gene sequences for phylogenetic studies in freshwater mussels: an example using Unionidae from north-western Europe. Zool. Scr. 34: 415-424.
Kimura M. 1980. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J. Mol. Evol. 16: 111-120.
Kuhn K., Streit B., Schwenk K. 2006. Conservation of structural elements in the mitochondrial control region of Daphnia. Gene 420: 101-112.
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.
La Roche J., Snyder M., Cook D. I., Fuller K., Zouros E. 1990. Molecular characterization of a repeat element causing large-scale size variation in the mitochondrial DNA of the sea scallop Placopecten magellanicus. Mol. Biol. Evol. 7: 45-64.
Liu H., Mitton J., Herrmann J. 1996a. Genetic differentiation in and managment recommendations for the freshwater mussel, Pyganodon grandis (Say, 1829). Am. Malacol. Bull. 13: 117-124.
Liu H., Mitton J., Wu S. 1996b. Paternal mitochondrial DNA differentiation far exceeds maternal mitochondrial DNA and allozyme differentiation in the fresh-water mussel, Anodonta grandis grandis. Evolution 50: 952-957.
Milbury C. A., Gaffney P. M. 2005. Complete mitochondrial DNA sequence of the eastern oyster Crassostrea virginica. Mar. Biotechnol. (NY) 7: 697-712.
Mizi A., Zouros E., Moschonas N., Rodakis G. C. 2005. The complete maternal and paternal mitochondrial genomes of the Mediterranean mussel Mytilus galloprovincialis: implications for the doubly uniparental inheritance mode of mtDNA. Mol. Biol. Evol. 22: 952-967.
Moritz C., Dowling T., Brown W. 1987. Evolution of animal mitochondrial DNA: Relevance for population biology and systematics. Annu. Rev. Ecol. Systematics 18: 269-292.
Mueller R. L., Boore J. L. 2005. Molecular mechanisms of extensive mitochondrial gene rearrangement in plethodontid salamanders. Mol. Biol. Evol. 22: 2104-2112.
Nei M., Gojobori T. 1986. Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol. Biol. Evol. 3: 418-426.
Okimoto R., Macfarlane J. L., Clary D. O., Wolstenholme D. R. 1992. The mitochondrial genomes of two nematodes, Caenorhabditis elegans and Ascaris suum. Genetics 130: 471-498.
Piechocki A., Dyduch-Falniowska A. 1993. Mięczaki (Mollusca). Małże (Bivalvia). Fauna Słodkowodna Polski 7A, PWN, Warszawa.
Podsiadlowski L. 2006. The mitochondrial genome of the bristletail Petrobius brevistylis (Archaeognatha: Machilidae). Insect Mol. Biol. 15: 253-258.
Podsiadlowski L., Carapelli A., Nardi F., Dallai R., Koch M., Boore J. L., Frati F. 2006. The mitochondrial genomes of Campodea fragilis and Campodea lubbocki (Hexapoda: Diplura): High genetic divergence in a morphologically uniform taxon. Gene 381: 49-61.
Pruitt K. D., Tatusova T., Klimke W., Maglott D. R. 2009. NCBI Reference Sequences: current status, policy and new initiatives. Nucleic Acids Res. 37: D32-36.
Ren J., Liu X., Zhang G., Liu B., Guo X. 2009. "Tandem duplication-random loss" is not a real feature of oyster mitochondrial genomes. BMC Genomics 10: 84.
Roe B. A., Ma D. P., Wilson R. K., Wong J. F. 1985. The complete nucleotide sequence of the Xenopus laevis mitochondrial genome. J. Biol. Chem. 260: 9759-9774.
Sato M., Nagashima K. 2001. Molecular characterization of a mitochondrial DNA segment from the Japanese scallop (Patinopecten yessoensis): demonstration of a region showing sequence polymorphism in the population. Mar. Biotechnol. (NY) 3: 370-379.
Seligmann H. 2008. Hybridization between mitochondrial heavy strand tDNA and expressed light strand tRNA modulates the function of heavy strand tDNA as light strand replication origin. J. Mol. Biol. 379: 188-199.
Seligmann H., Krishnan N. M., Rao B. J. 2006. Possible multiple origins of replication in primate mitochondria: Alternative role of tRNA sequences. J. Theor. Biol. 241: 321-332.
Serb J. M., Lydeard C. 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.
Soroka M. 2005. Genetic variability among freshwater mussel Anodonta woodiana (Lea, 1834) (Bivalvia: Unionidae) populations recently introduced in Poland. Zool. Sci. 22: 1137-1144.
Soroka M. 2008. Doubly uniparental inheritance of mitochondrial DNA in the freshwater bivalve Anodonta woodiana (Bivalvia: Unionidae). Folia Biol. (Krakow) 56: 91-95.
Soroka M. 2010. Characteristics of mitochondrial DNA of unionid bivalves (Mollusca: Bivalvia: Unionidae). I. Detection and characteristics of doubly uniparental inheritance (DUI) of unionid mitochondrial DNA. Folia Malacol. 18: 147-188.
Soroka M., Burzyński A. 2010. Complete sequences of maternally inherited mitochondrial genomes in mussels Unio pictorum (Bivalvia, Unionidae). J. Appl. Genet. 51: 469-476.
Tamura K., Dudley J., Nei M., Kumar S. 2007. MEGA4: Molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol. Biol. Evol. 24: 1596-1599.
Terrett J. A., Miles S., Thomas R. H. 1996. Complete DNA sequence of the mitochondrial genome of Cepaea nemoralis (Gastropoda: Pulmonata). J. Mol. Evol. 42: 160-168.
Theologidis I., Fodelianakis S., Gaspar M. B., Zouros E. 2008. Doubly uniparental inheritance (DUI) of mitochondrial DNA in Donax trunculus (Bivalvia: Donacidae) and the problem of its sporadic detection in Bivalvia. Evolution 62: 959-970.
Tomita K., Yokobori S., Oshima T., Ueda T., Watanabe K. 2002. The cephalopod Loligo bleekeri mitochondrial genome: Multiplied noncoding regions and transposition of tRNA genes. J. Mol. Evol. 54: 486-500.
Wenne R. 1993. Zróżnicowanie przestrzenne i ewolucja wybranych gatunków małży morskich. Wydawnictwo Uniwersytetu Gdańskiego, Gdańsk.
Werle E., Schneider C., Renner M., Volker M., Fiehn W. 1994. Convenient single-step, one tube purification of PCR products for direct sequencing. Nucleic Acids Res. 22: 4354-4355.
Wu X., Xu X., Yu Z., Kong X. 2009. Comparative mitogenomic analyses of three scallops (Bivalvia: Pectinidae) reveal high level variation of genomic organization and a diversity of transfer RNA gene sets. BMC Research Notes 2: 69.
Xu K., Kanno M., Yu H., Li Q., Kijima A. 2010. Complete mitochondrial DNA sequence and phylogenetic analysis of Zhikong scallop Chlamys farreri (Bivalvia: Pectinidae). Mol. Biol. Rep. Doi: 10.1007/s11033-010-9974-8.
Yamazaki N. R., Ueshima J. A., Terrett S. I., Yokobori M., Kaifu R., Segawa T., Kobayashi K. I., Numachi T., Ueda K., Nishikawa K., Watanabe K., Thomas R. H. 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.
Yu Z., Wei Z., Kong X., Shi W. 2008. Complete mitochondrial DNA sequence of oyster Crassostrea hongkongensis - a case of Tandem duplication-random loss for genome rearrangement in Crassostrea? BMC Genomics 9: 477.
Zbawicka M., Burzyński A., Skibinski D., Wenne R. 2010. Scottish Mytilus trossulus mussels retain ancestral mitochondrial DNA: complete sequences of male and female mtDNA genomes. Gene 456: 45-53.
Zbawicka M., Burzyński A., Wenne R. 2007. Complete sequences of mitochondrial genomes from the Baltic mussel Mytilus trossulus. Gene 406: 191-198.
Zheng R., Li J., Niu D. 2010. The complete DNA sequence of the mitochondrial genome of Sinonovacula constricta (Bivalvia: Solecurtidae). Acta Oceanol. Sin. 9: 88-92.
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