Abstract
The nucleotide sequences of two segments of 6,737 ntp and 258 ntp of the 18.4-kb circular mitochondrial (mt) DNA molecule of the soft coral Sarcophyton glaucum (phylum Cnidaria, class Anthozoa, subclass Octocorallia, order Alcyonacea) have been determined. The larger segment contains the 3′ 191 ntp of the gene for subunit 1 of the respiratory chain NADH dehydrogenase (ND1), complete genes for cytochrome b (Cyt b), ND6, ND3, ND4L, and a bacterial MutS homologue (MSH), and the 5’ terminal 1,124 ntp of the gene for the large subunit rRNA (1-rRNA). These genes are arranged in the order given and all are transcribed from the same strand of the molecule. The smaller segment contains the 3′ terminal 134 ntp of the ND4 gene and a complete tRNAf-Met gene, and these genes are transcribed in opposite directions. As in the hexacorallian anthozoan, Metridium senile, the mt-genetic code of S. glaucum is near standard: that is, in contrast to the situation in mt-genetic codes of other invertebrate phyla, AGA and AGG specify arginine, and ATA specifies isoleucine. However, as appears to be universal for metazoan mt-genetic codes, TGA specifies tryptophan rather than termination. Also, as in M. senile the mt-tRNAf-Met gene has primary and secondary structural features resembling those of Escherichia coli initiator tRNA, including standard dihydrouridine and Tv(iC loop sequences, and a mismatched nucleotide pair at the top of the amino-acyl stem. The presence of a mutS gene homologue, which has not been reported to occur in any other known mtDNA, suggests that there is mismatch repair activity in S. glaucum mitochondria. In support of this, phylogenetic analysis of MutS family protein sequences indicates that the S. glaucum mtMSH protein is more closely related to the nuclear DNA-encoded mitochondrial mismatch repair protein (MSH1) of the yeast Saccharomyces cerevisiae than to eukaryotic homologues involved in nuclear function, or to bacterial homologues. Regarding the possible origin of the S. glaucum mtMSH gene, the phylogenetic analysis results, together with comparative base composition considerations, and the absence of an MSH gene in any other known mtDNA best support the hypothesis that S. glaucum mtDNA acquired the mtMSH gene from nuclear DNA early in the evolution of octocorals. The presence of mismatch repair activity in S. glaucum mitochondria might be expected to influence the rate of evolution of this organism’s mtDNA.
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Alani E, Reenan RAG, Kolodner RD (1994) Interactions between mismatch repair and genetic recombination. Genetics 137:19–39
Arnason U, Xu X, Gullberg A (1996) Comparison between the complete mitochondrial DNA sequences of Homo and the common chimpanzee based on nonchimeric sequences. J Mol Evol 42:145–152
Baker SM, Bronner CE, Zhang L, Plug AW, Robatzek M, Warren G, Elliott EA, Yu J, Ashley T, Arnheim N, Glavell RA, Liskay RM (1995) Male mice defective in the DNA mismatch repair gene PMS2 exhibit abnormal chromosome synapsis in meiosis. Cell 82: 309–319
Bibb MJ, Van Etten RA, Wright CT, Walberg MW, Clayton DA (1981) Sequence and gene organization of mouse mitochondrial DNA. Cell 26:167–180
Boore JL, Brown WM (1994) Complete DNA sequence of the mitochondrial genome of the black chiton Katharina tunicata. Genetics 138:423–43
Boore JL, Brown WM (1995) Complete sequence of the mitochondrial DNA of the annelid worm Lumbricus terrestris. Genetics 141:305- 319
Bridge D, Cunningham CW, DeSalle R, Buss LW (1995) Class level relationships in the phylum Cnidaria: molecular and morphological evidence. Mol Biol Evol 12:679–689
Bronner CE, Baker SM, Morrison PT, Warren G, Smith LG, Lescoe MK, Kane M, Earabino C, Lipford J, Lindblom A, Tannergård P, Bollag RJ, Godwin AR, Ward DC, Nordenskjøld M, Fishel R, Kolodner R, Liskay RM (1994) Mutation in the DNA mismatch repair gene homologue hMLHl is associated with hereditary nonpolyposis colon cancer. Nature 368:258–261
Brown WM (1983) Evolution of animal mitochondrial DNA. In: Nei M, Koehn RK (eds) Evolution of genes and proteins. Sinauer, Sutherland, MA, pp 62–88
Brown WM (1985) The mitochondrial genomes in animals. In: Maclntyre RJ (ed) Molecular evolutionary genetics. Plenum, New York, pp 95–130
Brown WM, George M Jr, Wilson AC (1979) Rapid evolution of animal mitochondrial DNA. Proc Natl Acad Sci USA 76:1967- 1971
Brown WM, Prager EM, Wang A, Wilson AC (1982) Mitochondrial DNA sequences in primates: tempo and mode of evolution. J Mol Evol 18:225–239
Buddemeier RW, Fautin DG (1993) Coral bleaching as an adaptive mechanism. Bioscience 43:320–326
Casane D, Dennebouy N, deRochanbeau H, Mounolou JC, Monnerot M (1994) Genetic analysis of systematic mitochondrial heteroplasmy in rabbits. Genetics 138:471–80
Chi NW, Kolodner RD (1994a) Purification and characterization of MSH1, a yeast mitochondrial protein that binds to DNA mismatches. J Biol Chem 269: (47)29984–29992
Chi NW, Kolodner RD (1994b) The effect of DNA mismatches on the ATPase activity of MSH1, a protein in yeast mitochondria that recognizes DNA mismatches. J Biol Chem 269:(47)29993–29997
Clark-Walker GD (1991) Contrasting mutation rates in mitochondrial and nuclear genes of yeasts versus mammals. Curr Genet 20:195- 198
Clark-Walker GD, McArthur CR, Daley DJ (1981) Does mitochondrial DNA length influence the frequency of spontaneous petite mutants in yeasts? Curr Genet 4:7–12
Clary DO, Wolstenholme DR (1985) The mitochondrial DNA molecule of Drosophila yakuba: nucleotide sequence, gene organization, and genetic code. J Mol Evol 22:252–271
Clayton DA (1991) Replication and transcription of vertebrate mitochondrial DNA. Annu Rev Cell Biol 7:453–478
Clayton DA (1992) Transcription and replication of animal mitochondrial DNAs. In: Wolstenholme DR, Jeon KW (eds) Mitochondrial genomes. International review of cytology, vol 141. Academic Press, New York, pp 217–232
DeSalle R, Greedman T, Prager EM, Wilson AC (1987) Tempo and mode of sequence evolution in mitochondrial DNA of Hawaiian Drosophila. J Mol Evol 26:157–164
deWind ND, Dekker M, Berns A, Radman M, teRiele H (1995) Inactivation of the mouse MSH2 gene results in mismatch repair deficiency, methylation tolerance, hyperrecombination, and predisposition to cancer. Cell 82:321–330
Dirheimer G, Keith G, Sibler A-P, Martin RP (1979) The primary structure of tRNAs and their rare nucleosides. In: Schimmel PR, Soil D, Abelson JN (eds) Transfer RNA: structure, properties and recognition. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY, pp 19–41
Fang W-H, Modrich P (1993) Human strand-specific mismatch repair occurs by a bidirectional mechanism similar to that of the bacterial reaction. J Biol Chem 268:11838–11844
Felsenstein J (1978) Cases in which parsimony or compatability methods will be positively misleading. Syst Zool 27:401–410
Felsenstein J (1993) PHYLIP version 3.5.1. University of Washington, Seattle, WA
Fishel R, Lescoe MK, Rao MRS, Copeland NG, Jenkins NA, Garber J, Kane M, Kolodner R (1993) The human mutator gene homolog MSH2 and its association with hereditary nonpolyposis colon cancer. Cell 75:1027–1038
Fleck O, Michael H, Heim L (1992) The swi4 gene of Schizosaccharomyces pombe encodes a homologue of mismatch repair enzymes. Nucleic Acids Res 20:2271–2278
Fujii H, Shimada T (1989) Isolation and characterization of cDNA clones derived from the divergently transcribed gene in the region upstream from the human dihydrofolate reductase gene. J Biol Chem 264:10057–10064
Garey JR, Wolstenholme DR (1989) Platyhelminth mitochondrial DNA: evidence for early evolutionary origin of a tRNASer(AGN) that contains a dihydrouridine-arm replacement loop, and of serinespecifying AGA and AGG codons. J Mol Evol 28:374–387
Gorbalenya AE, Koonin EV (1990) Superfamily of UvrA-related NTP- binding proteins: implications for rational classification of recombination/repair systems. J Mol Biol 213:583–591
Haber LT, Pang PP, Sobell DI, Mankovich JA, Walker GC (1988) Nucleotide sequence of the Salmonella typhimurium mutS gene required for mismatch repair: homology of MutS and HexA of Streptococcus pneumoniae. J Bacteriol 170:197–202
Hatzoglou E, Rodakis GC, Lecanidou R (1995) Complete sequence and gene organization of the mitochondrial genome of the land snail Albinaria coerulea. Genetics 140:1353–1366
Hoffmann RJ, Boore JL, Brown WM (1992) A novel mitochondrial genome organization for the blue mussell, Mytilus edulis. Genetics 131:397–312
Hong GF (1982) A systematic DNA sequencing strategy. J Mol Biol 158:539–549
Janke A, Gemmell NJ, Feldmaier-Fuchs G, von Haeseler A, Pääbo S (1996) The mitochondrial genome of a monotreme-the platypus (Ornithorhynchus anatinus). J Mol Evol 42:153–159
Kolodner RD, Alani E (1994) Mismatch repair and cancer susceptibility. Curr Opin Biotechnol 5:585–594
Krettek A, Gullberg A, Arnason U (1995) Sequence analysis of the complete mitochondrial DNA molecule of the hedgehog, Erinaceus europaeus, and the phylogenetic position of the Lipotyphla. J Mol Evol 441:952–957
Lahue RS, Au KG, Moderich P (1989) DNA mismatch correction in a defined system. Science 245:160–164
Lang BF, Burger G, O’Kelly CJ, Cedergren R, Golding GB, Lemieux C, Sankoff D, Turmel M, Gray MW (1997) An ancestral mitochondrial DNA resembling a eubacterial genome in miniature. Nature 387:493–97
Le O, Shen B, Iismaa SE, Burgess BK (1993) Azotobacter vinelandii mutS: nucleotide sequence and mutant analysis. J Bacteriol 175: 7707–7710
Leach FS, Nicolaides NC, Papadopoulos N, Liu B, Jen J, Parsons R, Peltomäki P, Sistonen P, Aaltonen LA, Nyström-Lahti M, Guan X-Y, Zhang J, Meltzer PS, Yu J-W, Kao F-T, Chen DJ, Cerosaletti KM, Fournier REK, Todd S, Lewis T, Leach RJ, Naylor SL, Weissenbach J, Mecklin J-P, Järvinen H, Petersen GM, Hamilton SR, Green J, Jass J, Watson P, Lynch HT, Trent JM, de la Chapelle A, Kinzler KW, Vogelstein B (1993) Mutations of a mutS homolog in hereditary nonpolyposis colorectal cancer. Cell 75:1215–1225
Lee WJ, Kocher TD (1995) Complete sequence of a sea lamprey (Petromyzon marinus) mitochondrial genome: early establishment of the vertebrate genome organization. Genetics 139:873–887
Linton JP, Jong-Young JY, Selby E, Chen Z, Chinsky JM, Liu K, Kellems RE, Crouse GF (1989) Dual bidirectional promoters at the mouse dhfr locus: cloning and characterization of two mRNA classes of the divergently transcribed rep-l gene. Mol Cell Biol 9:3058–3072
Modrich P (1991) Mechanisms and biological effects of mismatch repair. Annu Rev Genet 25:229–253
Modrich P (1994) Mismatch repair, genetic stability, and cancer. Science 266:1959–1960
Moritz C (1991) Evolutionary dynamics of mitochondrial DNA duplication in parthenogenetic geckos, Heteronotia binoei. Genetics 129:221–230
Moritz C, Dawling T, Brown WM (1987) Evolution of animal mitochondrial DNA: relevance for population biology and systematics. Annu Rev Ecol Syst 18:269–292
Monnerot M, Solignac M, Wolstenholme DR (1990) Discrepancy in divergence of the mitochondrial and nuclear genes of Drosophila teissieri and Drosophila yakuba. J Mol Evol 30:500–508
New L, Liu K, Crouse GF (1993) The yeast gene MSH3 defines a new class of eukaryotic MutS homologs. Mol Gen Genet 239:91–108
Nicolaides NC, Papadopoulos N, Liu B, Wei Y-F, Carter KC, Ruben SM, Rosen CA, Haseltine WA, Fleischmann RD, Fraser CM, Adams MD, Venter JC, Dunlop MG, Hamilton SR, Petersen GM, de la Chapelle A, Vogelstein B, Kinzler KW (1994) Mutation of two PMS homologues in hereditary nonpolyposis colon cancer. Nature 371:75–80
Okimoto R, Chamberlin HM, Macfarlane JL, Wolstenholme DR (1991) 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 19:1619–1626
Okimoto R, Macfarlane JL, Clary DO, Wolstenholme DR (1992) The mitochondrial genomes of two nematodes, Caenorhabdidis elegans and Ascaris suum. Genetics 130:471–498
Papadopoulos N, Nicolaides NC, Wei Y-F, Ruben SM, Carter KC, Rosen CA, Haseltine WA, Fleischmann RD, Fraser CM, Adams MD, Venter JC, Hamilton SR, Petersen GM, Watson P, Lynch HT, Peltomäki P, Mecklin J-P, de la Chapelle A, Kinzler KW, Vogel-stein B (1994) Mutation of a mutL homolog in hereditary colon cancer. Science 263:1625–1629
Pont-Kingdon GA, Beagley CT, Okimoto R, Wolstenholme DR (1994) Mitochondrial DNA of the sea anemone, Metridium senile (Cnidaria): prokaryote-like genes for tRNAf-Met and small subunit ribosomal RNA, and standard genetic code specificities for AGR and ATA codons. J Mol Evol 39:387–399
Pont-Kingdon GA, Okada NA, Macfarlane JL, Beagley CT, Wolstenholme DR, Cavalier-Smith T, Clark-Walker GD (1995) A coral mitochondrial MutS gene. Nature 375:109–111
Priebe SD, Hadi SM, Greenberg B, Lacks SA (1988) Nucleotide sequence of the hexA gene for DNA mismatch repair in Streptococcus pneumoniae and homology of hexA to mutS of Escherichia coli and Salmonella typhimurium. J Bacteriol 170:190–196
Prolla TA, Pang Q, Alani E, Kolodner RD, Liskay RM (1994) MLH1, PMS 1 and MSH2 interactions during the initiation of DNA mismatch repair in yeast. Science 265:1091–1093
Prudhomme M, Martin B, Mejean V, Claverys J-P (1989) Nucleotide sequence of the Streptococcus pneumoniae hexB mismatch repair gene: homology of HexB and MutL of Salmonella typhimurium and to PMS 1 of Saccharomyces cerevisiae. J Bacteriol 171:5332–5338
Reenan RAG, Kolodner RD (1992a) Isolation and characterization of two Saccharomyces cerevisiae genes encoding homologs of the bacterial HexA and MutS mismatch repair proteins. Genetics 132: 963–973
Reenan RAG, Kolodner RD (1992b) Characterization of insertion mutations in the Saccharomyces cerevisiae MSH1 and MSH2 genes: evidence for separate mitochondrial and nuclear function. Genetics 132:975–985
Rich A, RajBhandary UL (1976) Transfer RNA: molecular structure, sequence and properties. Annu Rev Biochem 45:805–860
Ross-Macdonald P, Roeder GS (1994) Mutation of a meiosis-specific MutS homolog decreases crossing over but not mismatch correction. Cell 79:1069–1080
Sänger F, Nicklen S, Coulson AR (1977) DNA sequencing with chainterminating inhibitors. Proc Natl Acad Sci USA 74:5463–5467
Schlensog V, Böck A (1991) The Escherichia coli fdv gene probably encodes MutS and is located at minute 58.8 adjacent to the hyc-hyp gene cluster. J Bacteriol 173:7414–7415
Schuster W, Brennicke A (1987) Plastid, nuclear and reverse transcriptase sequences in the mitochondrial genome of Oenothera: is genetic information transferred between organelles via RNA? EMBO J 6:2857–2863
Singhal RP, Fallis PAM (1979) Structure, function, and evolution of transfer RNAs. Prog Nucleic Acids Res Mol Biol 23:227–290
Sprinzl M, Hartmann T, Weber J, Blank J, Zeidler R. (1989) Compilation of tRNA sequences and sequences of tRNA genes. Nucleic Acids Res 17(Suppl):rl-r72
Stanton DJ, Daehler LL, Moritz CC, Brown WM (1994) Sequences with the potential to form stem-and-loop structures are associated with coding-region duplications in animal mitochondrial DNA. Genetics 137:233–241
Stern DB, Palmer JD (1984) Extensive and widespread homologies between mitochondrial DNA and chloroplast DNA of plants. Proc Natl Acad Sci USA 81:1946–1950
Tomkinson AE, Bonk RT, Kim J, Bartfeld N, Linn S (1990) Mammalian mitochondrial endonuclease activities specific for ultraviolet irradiated DNA. Nucleic Acids Res 18(4):929–935
Upholt WB, David IB (1977) Mapping of mitochondrial DNA of individual sheep and goats: rapid evolution of the D-loop region. Cell 11:571–583
Varlet I, Pallard C, Radman M, Moreau J, deWind N (1994) Cloning and expression of the Xenopus and mouse MSH2 DNA mismatch repair genes. Nucleic Acids Res 22:5723–5728
Vawter L, Brown WM (1986) Nuclear and mitochondrial DNA comparisons reveal extreme rate variation in the molecular clock. Science 234:194–196
Wallace DC, Ye J, Neckelmann SN, Singh G, Webster KA, Greenberg BD (1987) Sequence analysis of cDNAs for the human and bovine ATP synthase b subunit: mitochondrial DNA genes sustain seventeen times more mutations. Curr Genet 12:81–90
Wolstenholme DR (1992a) Animal mitochondrial DNA: structure and evolution. In: Wolstenholme DR, Jeon KW (eds) Mitochondrial genomes. International review of cytology, vol 141. Academic Press, New York, NY, pp 173–216
Wolstenholme DR (1992b) Genetic novelties in mitochondrial genomes of multicellular animals. Curr Opin Genet Dev 2:918–925
Wolstenholme DR, Fauron CM-R (1995) Mitochondrial genome organization. In: Levings CS III, Vasil IK, (eds) Advances in cellular and molecular biology of plants, vol. 3: The molecular biology of plant mitochondria. Kluwer Academic, Dordrecht, The Netherlands, pp 1–59
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 Sci USA 84: 1324–1328
Worth L, Clark S, Radman M, Modrich P. (1994) Mismatch repair proteins MutS and MutL inhibit RecA-catalyzed strand transfer between diverged DNAs. Proc Natl Acad Sci USA 91:3238–3241
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Pont-Kingdon, G., Okada, N.A., Macfarlane, J.L. et al. Mitochondrial DNA of the coral sarcophyton glaucum contains a gene for a homologue of bacterial muts: A possible case of gene transfer from the nucleus to the mitochondrion. J Mol Evol 46, 419–431 (1998). https://doi.org/10.1007/PL00006321
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DOI: https://doi.org/10.1007/PL00006321