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. 1992 Jun;131(2):397–412. doi: 10.1093/genetics/131.2.397

A Novel Mitochondrial Genome Organization for the Blue Mussel, Mytilus Edulis

R J Hoffmann 1, J L Boore 1, W M Brown 1
PMCID: PMC1205014  PMID: 1386586

Abstract

The sequence of 13.9 kilobases (kb) of the 17.1-kb mitochondrial genome of Mytilus edulis has been determined, and the arrangement of all genes has been deduced. Mytilus mitochondrial DNA (mtDNA) contains 37 genes, all of which are transcribed from the same DNA strand. The gene content of Mytilus is typically metazoan in that it includes genes for large and small ribosomal RNAs, for a complete set of transfer RNAs and for 12 proteins. The protein genes encode the cytochrome b apoenzyme, cytochrome c oxidase (CO) subunits I-III, NADH dehydrogenase (ND) subunits 1-6 and 4L, and ATP synthetase (ATPase) subunit 6. No gene for ATPase subunit 8 could be found. The reading frames for the ND1, COI, and COIII genes contain long extensions relative to those genes in other metazoan mtDNAs. There are 23 tRNA genes, one more than previously found in any metazoan mtDNA. The additional tRNA appears to specify methionine, making Mytilus mtDNA unique in having two tRNA(Met) genes. Five lengthy unassigned intergenic sequences are present, four of which vary in length from 79 to 119 nucleotides and the largest of which is 1.2 kb. The base compositions of these are unremarkable and do not differ significantly from that of the remainder of the mtDNA. The arrangement of genes in Mytilus mtDNA is remarkably unlike that found in any other known metazoan mtDNA.

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Selected References

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  1. Anderson S., de Bruijn M. H., Coulson A. R., Eperon I. C., Sanger F., Young I. G. Complete sequence of bovine mitochondrial DNA. Conserved features of the mammalian mitochondrial genome. J Mol Biol. 1982 Apr 25;156(4):683–717. doi: 10.1016/0022-2836(82)90137-1. [DOI] [PubMed] [Google Scholar]
  2. Auerbach S., Brinster R. L. Lactate dehydrogenase isozymes in the early mouse embryo. Exp Cell Res. 1967 Apr;46(1):89–92. doi: 10.1016/0014-4827(67)90411-9. [DOI] [PubMed] [Google Scholar]
  3. Batuecas B., Garesse R., Calleja M., Valverde J. R., Marco R. Genome organization of Artemia mitochondrial DNA. Nucleic Acids Res. 1988 Jul 25;16(14A):6515–6529. doi: 10.1093/nar/16.14.6515. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Beutler E., Mathai C. K., Smith J. E. Biochemical variants of glucose-6-phosphate dehydrogenase giving rise to congenital nonspherocytic hemolytic disease. Blood. 1968 Feb;31(2):131–150. [PubMed] [Google Scholar]
  5. Bibb M. J., Van Etten R. A., Wright C. T., Walberg M. W., Clayton D. A. Sequence and gene organization of mouse mitochondrial DNA. Cell. 1981 Oct;26(2 Pt 2):167–180. doi: 10.1016/0092-8674(81)90300-7. [DOI] [PubMed] [Google Scholar]
  6. Britton-Davidian J., Ruiz Bustos A., Thaler L., Topal M. Lactate dehydrogenase polymorphism in Mus musculus L. and Mus spretus Lataste. Experientia. 1978 Sep 15;34(9):1144–1145. doi: 10.1007/BF01922920. [DOI] [PubMed] [Google Scholar]
  7. Brown W. M., George M., Jr, Wilson A. C. Rapid evolution of animal mitochondrial DNA. Proc Natl Acad Sci U S A. 1979 Apr;76(4):1967–1971. doi: 10.1073/pnas.76.4.1967. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Cattanach B. M., Perez J. N. A genetically determined variant of the A-subunit of lactic dehydrogenase in the deer mouse. Biochem Genet. 1969 Oct;3(5):499–506. doi: 10.1007/BF00485610. [DOI] [PubMed] [Google Scholar]
  9. Charles D. J., Pretsch W. Linear dose-response relationship of erythrocyte enzyme-activity mutations in offspring of ethylnitrosourea-treated mice. Mutat Res. 1987 Jan;176(1):81–91. doi: 10.1016/0027-5107(87)90255-7. [DOI] [PubMed] [Google Scholar]
  10. Clary D. O., Wolstenholme D. R. The mitochondrial DNA molecular of Drosophila yakuba: nucleotide sequence, gene organization, and genetic code. J Mol Evol. 1985;22(3):252–271. doi: 10.1007/BF02099755. [DOI] [PubMed] [Google Scholar]
  11. Clayton D. A. Replication of animal mitochondrial DNA. Cell. 1982 Apr;28(4):693–705. doi: 10.1016/0092-8674(82)90049-6. [DOI] [PubMed] [Google Scholar]
  12. Clough J. R., Whittingham D. G. Metabolism of [14C]glucose by postimplantation mouse embryos in vitro. J Embryol Exp Morphol. 1983 Apr;74:133–142. [PubMed] [Google Scholar]
  13. Desjardins P., Morais R. Nucleotide sequence and evolution of coding and noncoding regions of a quail mitochondrial genome. J Mol Evol. 1991 Feb;32(2):153–161. doi: 10.1007/BF02515387. [DOI] [PubMed] [Google Scholar]
  14. Desjardins P., Morais R. Sequence and gene organization of the chicken mitochondrial genome. A novel gene order in higher vertebrates. J Mol Biol. 1990 Apr 20;212(4):599–634. doi: 10.1016/0022-2836(90)90225-B. [DOI] [PubMed] [Google Scholar]
  15. Devereux J., Haeberli P., Smithies O. A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res. 1984 Jan 11;12(1 Pt 1):387–395. doi: 10.1093/nar/12.1part1.387. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Dubin D. T., HsuChen C. C., Tillotson L. E. Mosquito mitochondrial transfer RNAs for valine, glycine and glutamate: RNA and gene sequences and vicinal genome organization. Curr Genet. 1986;10(9):701–707. doi: 10.1007/BF00410919. [DOI] [PubMed] [Google Scholar]
  17. Ehling U. H., Machemer L., Buselmaier W., Dýcka J., Frohberg H., Kratochvilova J., Lang R., Lorke D., Müller D., Peh J. Standard protocol for the dominant lethal test on male mice set up by the work group "Dominant Lethal Mutations of the ad hoc Committe Chemogenetics". Arch Toxicol. 1978 Jan 25;39(3):173–185. doi: 10.1007/BF00368226. [DOI] [PubMed] [Google Scholar]
  18. Ellington S. K. In vitro analysis of glucose metabolism and embryonic growth in postimplantation rat embryos. Development. 1987 Jul;100(3):431–439. doi: 10.1242/dev.100.3.431. [DOI] [PubMed] [Google Scholar]
  19. Engel W., Kreutz R., Wolf U. Studies on the genetic polymorphism of lactate dehydrogenase B (phenotype B - ) in rodent erythrocytes. Biochem Genet. 1972 Aug;7(1):45–55. doi: 10.1007/BF00487009. [DOI] [PubMed] [Google Scholar]
  20. Engel W., Petzoldt U. Early developmental changes of the lactate dehydrogenase isoenzyme pattern in mouse, rat, guinea-pig, Syrian hamster and rabbit. Humangenetik. 1973;20(2):125–131. doi: 10.1007/BF00284847. [DOI] [PubMed] [Google Scholar]
  21. Favor J. Characterization of dominant cataract mutations in mice: penetrance, fertility and homozygous viability of mutations recovered after 250 mg/kg ethylnitrosourea paternal treatment. Genet Res. 1984 Oct;44(2):183–197. doi: 10.1017/s0016672300026380. [DOI] [PubMed] [Google Scholar]
  22. Foran D. R., Hixson J. E., Brown W. M. Comparisons of ape and human sequences that regulate mitochondrial DNA transcription and D-loop DNA synthesis. Nucleic Acids Res. 1988 Jul 11;16(13):5841–5861. doi: 10.1093/nar/16.13.5841. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Gardner D. K., Leese H. J. The role of glucose and pyruvate transport in regulating nutrient utilization by preimplantation mouse embryos. Development. 1988 Nov;104(3):423–429. doi: 10.1242/dev.104.3.423. [DOI] [PubMed] [Google Scholar]
  24. Gossen J. A., de Leeuw W. J., Tan C. H., Zwarthoff E. C., Berends F., Lohman P. H., Knook D. L., Vijg J. Efficient rescue of integrated shuttle vectors from transgenic mice: a model for studying mutations in vivo. Proc Natl Acad Sci U S A. 1989 Oct;86(20):7971–7975. doi: 10.1073/pnas.86.20.7971. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Gupta R. Halobacterium volcanii tRNAs. Identification of 41 tRNAs covering all amino acids, and the sequences of 33 class I tRNAs. J Biol Chem. 1984 Aug 10;259(15):9461–9471. [PubMed] [Google Scholar]
  26. Guthrie C., McClain W. H. Rare transfer ribonucleic acid essential for phage growth. Nucleotide sequence comparison of normal and mutant T4 isoleucine-accepting transfer ribonucleic acid. Biochemistry. 1979 Aug 21;18(17):3786–3795. doi: 10.1021/bi00584a023. [DOI] [PubMed] [Google Scholar]
  27. Himeno H., Masaki H., Kawai T., Ohta T., Kumagai I., Miura K., Watanabe K. Unusual genetic codes and a novel gene structure for tRNA(AGYSer) in starfish mitochondrial DNA. Gene. 1987;56(2-3):219–230. doi: 10.1016/0378-1119(87)90139-9. [DOI] [PubMed] [Google Scholar]
  28. Hoeh W. R., Blakley K. H., Brown W. M. Heteroplasmy suggests limited biparental inheritance of Mytilus mitochondrial DNA. Science. 1991 Mar 22;251(5000):1488–1490. doi: 10.1126/science.1672472. [DOI] [PubMed] [Google Scholar]
  29. HsuChen C. C., Kotin R. M., Dubin D. T. Sequences of the coding and flanking regions of the large ribosomal subunit RNA gene of mosquito mitochondria. Nucleic Acids Res. 1984 Oct 25;12(20):7771–7785. doi: 10.1093/nar/12.20.7771. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Jacobs H. T., Elliott D. J., Math V. B., Farquharson A. Nucleotide sequence and gene organization of sea urchin mitochondrial DNA. J Mol Biol. 1988 Jul 20;202(2):185–217. doi: 10.1016/0022-2836(88)90452-4. [DOI] [PubMed] [Google Scholar]
  31. Johansen S., Guddal P. H., Johansen T. Organization of the mitochondrial genome of Atlantic cod, Gadus morhua. Nucleic Acids Res. 1990 Feb 11;18(3):411–419. doi: 10.1093/nar/18.3.411. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Kanno T., Sudo K., Takeuchi I., Kanda S., Honda N., Nishimura Y., Oyama K. Hereditary deficiency of lactate dehydrogenase M-subunit. Clin Chim Acta. 1980 Dec 8;108(2):267–276. doi: 10.1016/0009-8981(80)90013-3. [DOI] [PubMed] [Google Scholar]
  33. Kashdan M. A., Dudock B. S. The gene for a spinach chloroplast isoleucine tRNA has a methionine anticodon. J Biol Chem. 1982 Oct 10;257(19):11191–11194. [PubMed] [Google Scholar]
  34. Kitamura M., Iijima N., Hashimoto F., Hiratsuka A. Hereditary deficiency of subunit H of lactate dehydrogenase. Clin Chim Acta. 1971 Oct;34(3):419–423. doi: 10.1016/0009-8981(71)90095-7. [DOI] [PubMed] [Google Scholar]
  35. LOWRY O. H., ROSEBROUGH N. J., FARR A. L., RANDALL R. J. Protein measurement with the Folin phenol reagent. J Biol Chem. 1951 Nov;193(1):265–275. [PubMed] [Google Scholar]
  36. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  37. Leese H. J., Barton A. M. Pyruvate and glucose uptake by mouse ova and preimplantation embryos. J Reprod Fertil. 1984 Sep;72(1):9–13. doi: 10.1530/jrf.0.0720009. [DOI] [PubMed] [Google Scholar]
  38. Maekawa M., Sudo K., Kanno T. Immunochemical studies on lactate dehydrogenase A subunit deficiencies. Am J Hum Genet. 1986 Aug;39(2):232–238. [PMC free article] [PubMed] [Google Scholar]
  39. McCracken A., Uhlenbusch I., Gellissen G. Structure of the cloned Locusta migratoria mitochondrial genome: restriction mapping and sequence of its ND-1 (URF-1) gene. Curr Genet. 1987;11(8):625–630. doi: 10.1007/BF00393926. [DOI] [PubMed] [Google Scholar]
  40. Merkle S., Pretsch W. Characterization of triosephosphate isomerase mutants with reduced enzyme activity in Mus musculus. Genetics. 1989 Dec;123(4):837–844. doi: 10.1093/genetics/123.4.837. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Mohrenweiser H. W., Novotny J. E. An enzymatically inactive variant of human lactate dehydrogenase-LDHBGUA-1. Study of subunit interaction. Biochim Biophys Acta. 1982 Mar 18;702(1):90–98. doi: 10.1016/0167-4838(82)90030-9. [DOI] [PubMed] [Google Scholar]
  42. Monk M., Ansell J. Patterns of lactic dehydrogenase isozymes in mouse embryos over the implantation period in vivo and in vitro. J Embryol Exp Morphol. 1976 Dec;36(3):653–662. [PubMed] [Google Scholar]
  43. Montoya J., Gaines G. L., Attardi G. The pattern of transcription of the human mitochondrial rRNA genes reveals two overlapping transcription units. Cell. 1983 Aug;34(1):151–159. doi: 10.1016/0092-8674(83)90145-9. [DOI] [PubMed] [Google Scholar]
  44. Moritz C., Brown W. M. Tandem duplication of D-loop and ribosomal RNA sequences in lizard mitochondrial DNA. Science. 1986 Sep 26;233(4771):1425–1427. doi: 10.1126/science.3018925. [DOI] [PubMed] [Google Scholar]
  45. Moritz C., Brown W. M. Tandem duplications in animal mitochondrial DNAs: variation in incidence and gene content among lizards. Proc Natl Acad Sci U S A. 1987 Oct;84(20):7183–7187. doi: 10.1073/pnas.84.20.7183. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. NISSELBAUM J. S., PACKER D. E., BODANSKY O. COMPARISON OF THE ACTIONS OF HUMAN BRAIN, LIVER, AND HEART LACTIC DEHYDROGENASE VARIANTS ON NUCLEOTIDE ANALOGUES AND ON SUBSTRATE ANALOGUES IN THE ABSENCE AND IN THE PRESENCE OF OXALATE AND OXAMATE. J Biol Chem. 1964 Sep;239:2830–2834. [PubMed] [Google Scholar]
  47. Okimoto R., Chamberlin H. M., Macfarlane J. L., Wolstenholme D. R. Repeated sequence sets in mitochondrial DNA molecules of root knot nematodes (Meloidogyne): nucleotide sequences, genome location and potential for host-race identification. Nucleic Acids Res. 1991 Apr 11;19(7):1619–1626. doi: 10.1093/nar/19.7.1619. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Okimoto R., Macfarlane J. L., Wolstenholme D. R. Evidence for the frequent use of TTG as the translation initiation codon of mitochondrial protein genes in the nematodes, Ascaris suum and Caenorhabditis elegans. Nucleic Acids Res. 1990 Oct 25;18(20):6113–6118. doi: 10.1093/nar/18.20.6113. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Okimoto R., Wolstenholme D. R. A set of tRNAs that lack either the T psi C arm or the dihydrouridine arm: towards a minimal tRNA adaptor. EMBO J. 1990 Oct;9(10):3405–3411. doi: 10.1002/j.1460-2075.1990.tb07542.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Pastink A., Vreeken C., Nivard M. J., Searles L. L., Vogel E. W. Sequence analysis of N-ethyl-N-nitrosourea-induced vermilion mutations in Drosophila melanogaster. Genetics. 1989 Sep;123(1):123–129. doi: 10.1093/genetics/123.1.123. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Peebles C. L., Gegenheimer P., Abelson J. Precise excision of intervening sequences from precursor tRNAs by a membrane-associated yeast endonuclease. Cell. 1983 Feb;32(2):525–536. doi: 10.1016/0092-8674(83)90472-5. [DOI] [PubMed] [Google Scholar]
  52. Pretsch W. Eight independent Ldh-1 mutations of the mouse recovered in mutagenicity experiments: biochemical characteristics and chromosomal localization. Genet Res. 1989 Apr;53(2):101–104. doi: 10.1017/s001667230002797x. [DOI] [PubMed] [Google Scholar]
  53. Päbo S., Thomas W. K., Whitfield K. M., Kumazawa Y., Wilson A. C. Rearrangements of mitochondrial transfer RNA genes in marsupials. J Mol Evol. 1991 Nov;33(5):426–430. doi: 10.1007/BF02103134. [DOI] [PubMed] [Google Scholar]
  54. Rapola J., Koskimies O. Embryonic enzyme patterns: characterization of the single lactate dehydrogenase isozyme in preimplanted mouse ova. Science. 1967 Sep 15;157(3794):1311–1312. doi: 10.1126/science.157.3794.1311. [DOI] [PubMed] [Google Scholar]
  55. Rauch N. A mutant form of lactate dehydrogenase in the horse. Ann N Y Acad Sci. 1968 Jun 14;151(1):672–677. doi: 10.1111/j.1749-6632.1968.tb11927.x. [DOI] [PubMed] [Google Scholar]
  56. Roe B. A., Ma D. P., Wilson R. K., Wong J. F. The complete nucleotide sequence of the Xenopus laevis mitochondrial genome. J Biol Chem. 1985 Aug 15;260(17):9759–9774. [PubMed] [Google Scholar]
  57. SHAW C. R., BARTO E. GENETIC EVIDENCE FOR THE SUBUNIT STRUCTURE OF LACTATE DEHYDROGENASE ISOZYMES. Proc Natl Acad Sci U S A. 1963 Aug;50:211–214. doi: 10.1073/pnas.50.2.211. [DOI] [PMC free article] [PubMed] [Google Scholar]
  58. Sankoff D., Cedergren R., Abel Y. Genomic divergence through gene rearrangement. Methods Enzymol. 1990;183:428–438. doi: 10.1016/0076-6879(90)83028-8. [DOI] [PubMed] [Google Scholar]
  59. Sederoff R. R. Structural variation in mitochondrial DNA. Adv Genet. 1984;22:1–108. doi: 10.1016/s0065-2660(08)60038-3. [DOI] [PubMed] [Google Scholar]
  60. Smith M. J., Banfield D. K., Doteval K., Gorski S., Kowbel D. J. Gene arrangement in sea star mitochondrial DNA demonstrates a major inversion event during echinoderm evolution. Gene. 1989 Mar 15;76(1):181–185. doi: 10.1016/0378-1119(89)90022-x. [DOI] [PubMed] [Google Scholar]
  61. Smith M. J., Banfield D. K., Doteval K., Gorski S., Kowbel D. J. Nucleotide sequence of nine protein-coding genes and 22 tRNAs in the mitochondrial DNA of the sea star Pisaster ochraceus. J Mol Evol. 1990 Sep;31(3):195–204. doi: 10.1007/BF02109496. [DOI] [PubMed] [Google Scholar]
  62. Snyder M., Fraser A. R., Laroche J., Gartner-Kepkay K. E., Zouros E. Atypical mitochondrial DNA from the deep-sea scallop Placopecten magellanicus. Proc Natl Acad Sci U S A. 1987 Nov;84(21):7595–7599. doi: 10.1073/pnas.84.21.7595. [DOI] [PMC free article] [PubMed] [Google Scholar]
  63. Sprinzl M., Dank N., Nock S., Schön A. Compilation of tRNA sequences and sequences of tRNA genes. Nucleic Acids Res. 1991 Apr 25;19 (Suppl):2127–2171. doi: 10.1093/nar/19.suppl.2127. [DOI] [PMC free article] [PubMed] [Google Scholar]
  64. Sternberger L. A., Hardy P. H., Jr, Cuculis J. J., Meyer H. G. The unlabeled antibody enzyme method of immunohistochemistry: preparation and properties of soluble antigen-antibody complex (horseradish peroxidase-antihorseradish peroxidase) and its use in identification of spirochetes. J Histochem Cytochem. 1970 May;18(5):315–333. doi: 10.1177/18.5.315. [DOI] [PubMed] [Google Scholar]
  65. Stormo G. D., Schneider T. D., Gold L. M. Characterization of translational initiation sites in E. coli. Nucleic Acids Res. 1982 May 11;10(9):2971–2996. doi: 10.1093/nar/10.9.2971. [DOI] [PMC free article] [PubMed] [Google Scholar]
  66. Towbin H., Staehelin T., Gordon J. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci U S A. 1979 Sep;76(9):4350–4354. doi: 10.1073/pnas.76.9.4350. [DOI] [PMC free article] [PubMed] [Google Scholar]
  67. Uhlenbusch I., McCracken A., Gellissen G. The gene for the large (16S) ribosomal RNA from the Locusta migratoria mitochondrial genome. Curr Genet. 1987;11(8):631–638. doi: 10.1007/BF00393927. [DOI] [PubMed] [Google Scholar]
  68. Vesell E. S. Genetic control of isozyme patterns in human tissues. Prog Med Genet. 1965;4:128–175. [PubMed] [Google Scholar]
  69. Weber F., Dietrich A., Weil J. H., Maréchal-Drouard L. A potato mitochondrial isoleucine tRNA is coded for by a mitochondrial gene possessing a methionine anticodon. Nucleic Acids Res. 1990 Sep 11;18(17):5027–5030. doi: 10.1093/nar/18.17.5027. [DOI] [PMC free article] [PubMed] [Google Scholar]
  70. West J. D., Flockhart J. H., Peters J., Ball S. T. Death of mouse embryos that lack a functional gene for glucose phosphate isomerase. Genet Res. 1990 Oct-Dec;56(2-3):223–236. doi: 10.1017/s0016672300035321. [DOI] [PubMed] [Google Scholar]
  71. Wolstenholme D. R., Macfarlane J. L., Okimoto R., Clary D. O., Wahleithner J. A. Bizarre tRNAs inferred from DNA sequences of mitochondrial genomes of nematode worms. Proc Natl Acad Sci U S A. 1987 Mar;84(5):1324–1328. doi: 10.1073/pnas.84.5.1324. [DOI] [PMC free article] [PubMed] [Google Scholar]
  72. Wong T. W., Clayton D. A. In vitro replication of human mitochondrial DNA: accurate initiation at the origin of light-strand synthesis. Cell. 1985 Oct;42(3):951–958. doi: 10.1016/0092-8674(85)90291-0. [DOI] [PubMed] [Google Scholar]
  73. Zevering C. E., Moritz C., Heideman A., Sturm R. A. Parallel origins of duplications and the formation of pseudogenes in mitochondrial DNA from parthenogenetic lizards (Heteronotia binoei; Gekkonidae). J Mol Evol. 1991 Nov;33(5):431–441. doi: 10.1007/BF02103135. [DOI] [PubMed] [Google Scholar]
  74. Zuker M., Stiegler P. Optimal computer folding of large RNA sequences using thermodynamics and auxiliary information. Nucleic Acids Res. 1981 Jan 10;9(1):133–148. doi: 10.1093/nar/9.1.133. [DOI] [PMC free article] [PubMed] [Google Scholar]

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