Summary
Three genes for the subunits of the NADH dehydrogenase (nad5, nad4, and nad2) are tandemly clustered on the liverwort mitochondrial genome. Their gene products showed high levels of amino acid sequence identity with the corresponding subunits from higher plant mitochondria (82.8–84.4%), and significant levels of identity with those from liverwort chloroplast (32.0–33.5%), Podospora anserina mitochondria (21.4–45.9%), and human mitochondria (18.4–27.9%). In addition, these three subunits from liverwort mitochondria have conserved amino acid residues in their central regions. The gene nad5 is interrupted by a 672 by group I intron, while genes nad4 and nad2 are interrupted by group II introns of 899 by and 1418 bp, respectively. Northern blot analysis using exon-intron specific probes indicated that these three genes are transcribed as a single precursor mRNA of 9.6 kb in length and are processed into mature mRNA molecules in liverwort mitochondria. Several regions of this nad gene cluster are repeated in the liverwort mitochondrial genome.
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Binder S, Marchfelder A, Brennicke A, Wissinger B (1992) RNA editing in trans-splicing intron sequences of nad2 mRNAs in Oenothera mitochondria. J Biol Chem 267:7615–7623
Bland MM, Levings CS III, Matzinger DF (1986) The tobacco mitochondrial ATPase subunit 9 gene is closely linked to an open reading frame for a ribosomal protein. Mol Gen Genet 204:8–16
Chapdelaine Y, Bonen L (1991) The wheat mitochondrial gene for subunit I of the NADH dehydrogenase complex: A trans-splicing model for this gene-in-pieces. Cell 65:465–472
Chomyn A, Mariottini P, Cleeter MWJ, Ragan CI, Matsuno-Yagi A, Hatefi Y, Doolittle RF, Attardi G (1985) Six unidentified reading frames of human mitochondrial DNA encode components of the respiratory-chain NADH dehydrogenase. Nature 314:592–597
Chomyn A, Cleeter MWJ, Ragan CI, Riley M, Doolittle RF, Attardi G (1986) URF6, last unidentified reading frame of human mtDNA, codes for an NADH dehydrogenase subunit. Science 234:614–618
Cummings DJ, McNally KL, Domenico JM, Matsuura ET (1990) The complete DNA sequence of the mitochondrial genome of Podospora anserina. Curr Genet 17:375–402
de Souza AP, Jubier MF, Delcher E, Lancelin D, Lejeune B (1991) A trans-splicing model for the expression of the tripartite nad5 gene in wheat and maize mitochondria. Plant Cell 3:1363–1378
Dupuis A, Skehel JM, Walker JE (1991) A homologue of a nuclear-coded iron-sulfur protein subunit of bovine mitochondrial complex I is encoded in chloroplast genomes. Biochemistry 30:2954–2960
Ecke W, Schmitz U, Michaelis G (1990) The mitochondrial nad5 gene of sugar beet (Beta vulgaris) encoding a subunit of the respiratory NADH dehydrogenase. Curr Genet 18:133–139
Gass DA, Makaroff CA, Palmer JD (1992) Variable intron content of the NADH dehydrogenase subunit 4 gene of plant mitochondria. Curr Genet 21:423–430
Gualberto JM, Wintz H, Weil JH, Grienenberger JM (1988) The genes coding for subunit 3 of NADH dehydrogenase and for ribosomal protein S12 are present in the wheat and maize mitochondrial genomes and are co-transcribed. Mol Gen Genet 215:118–127
Hiratsuka J, Shimada H, Whittier R, Ishibashi T, Sakamoto M, Mori M, Kondo C, Honji Y, Sun CR, Meng BY, Li YQ, Kanno A, Nishizawa Y, Hirai A, Shinozaki K, Sugiura M (1989) The complete sequence of the rice (Oryza sativa) chloroplast genome: Intermolecular recombination between distinct tRNA genes accounts for a major plastid DNA inversion during the evolution of the cereals. Mol Gen Genet 217:185–194
Knoop V, Schuster W, Wissinger B, Brennicke A (1991) Trans splicing integrates an exon of 22 nucleotides into the nad5 mRNA in higher plant mitochondria. EMBO J 10:3483–3493
Lamattina L, Weil LH, Grienenberger JM (1989) RNA editing at a splicing site of NADH dehydrogenase subunit IV gene transcript in wheat mitochondria. FEBS Lett 258:79–83
Lamattina L, Grienenberger JM (1991) RNA editing of the transcript coding for subunit 4 of NADH dehydrogenase in wheat mitochondria: uneven distribution of the editing sites among the four exons. Nucleic Acids Res 19:3275–3282
Michel F, Dujon B (1983) Conservation of RNA secondary structures in two intron families including mitochondrial-, chloroplast- and nuclear-encoded members. EMBO J 2:33–38
Nixon PJ, Gounaris K, Coomber SA, Hunter CN, Dyer TA, Barber J (1989) psbG is not a photosystem two gene but may be a ndh gene. J Biol Chem 264:14129–14135
Oda K, Kohchi T, Ohyama K (1992a) Mitochondrial DNA of Marchantia polymorpha as a single circular form with no incorporation of foreign DNA. Biosci Biotech Biochem 56:132–135
Oda K, Yamato K, Ohta E, Nakamura Y, Takemura M, Nozato N, Akashi K, Kanegae T, Ogura Y, Kohchi T, Ohyama K (1992b) Gene organization deduced from the complete sequence of liverwort Marchantia polymorpha mitochondrial DNA: A primitive form of plant mitochondrial genome. J Mol Biol 223:1–7
Oda K, Yamato K, Ohta E, Nakamura Y, Takemura M, Nozato N, Akashi K, Kanegae T, Ogura Y, Kohchi T, Ohyama K (1992c) Complete nucleotide sequence of the mitochondrial DNA from a liverwort, Marchantia polymorpha. Plant Mol Biol Rep 10:105–163
Ohyama K, Fukuzawa H, Kohchi T, Shirai H, Sano T, Sano S, Umesono K, Shiki K, Takeuchi M, Chang Z, Aota S, Inokuchi H, Ozeki H (1986) Chloroplast gene organization deduced from complete sequence of liverwort Marchantia polymorpha chloroplast DNA. Nature 322:571–574
Ohyama K, Fukuzawa H, Kohchi T, Sano T, Sano S, Shirai H, Umesono K, Shiki K, Takeuchi M, Chang Z, Aota S, Inokuchi H, Ozeki H (1988) Structure and organization of Marchantia polymorpha chloroplast genome I. Cloning and gene identification. J Mol Biol 203:281–298
Rasmussen J, Hanson MR (1989) A NADH dehydrogenase subunit gene is co-transcribed with the abnormal Petunia mitochondrial gene associated with cytoplasmic male sterility. Mol Gen Genet 215:332–336
Schuster W, Wissinger B, Unseld M, Brennicke A (1990) Transcripts of the NADH-dehydrogenase subunit 3 gene are differentially edited in Oenothera mitochondria. EMBO J 9:263–269
Shinozaki K, Ohme M, Tanaka M, Wakasugi T, Hayashida N, Matsubayashi T, Zaita N, Chunwongse J, Obokata J, Yamaguchi-Shinozaki K, Ohto C, Torazawa K, Meng BY, Sugita M, Deno H, Kamogashira T, Yamada K, Kusuda J, Takaiwa F, Kato A, Tohdoh N, Shimada H, Sugiura M (1986) The complete nucleotide sequence of the tobacco chloroplast genome: its gene organization and expression. EMBO J 5:2043–2049
Stern DB, Bang AG, Thompson WF (1986) The watermelon mitochondrial URF-1 gene: evidence for a complex structure. Curr Genet 10:857–869
Wahleithner JA, Macfarlane JL, Wolstenholme DR (1990) A sequence encoding a maturase-related protein in a group II intron of a plant mitochondrial nad1 gene. Proc Natl Acad Sci USA 87:548–552
Wintz H, Chen HC, Pillay DTN (1989) Partial characterization of the gene coding for subunit IV of soybean mitochondrial NADH dehydrogenase. Curr Genet 15:155–160
Wissinger B, Hiesel R, Schuster W, Brennicke A (1988) The NADH dehydrogenase subunit 5 gene in Oenothera mitochondria contains two introns and is co-transcribed with the 5S rRNA gene. Mol Gen Genet 212:56–65
Wissinger B, Schuster W, Brennicke A (1991) Trans splicing in Oenothera mitochondria: nad1 mRNAs are edited in exon and trans-splicing group II intron sequences. Cell 65:473–482
Xue Y, Davies DR, Thomas CM (1990) Sugarbeet mitochondria contain an open reading frame showing extensive sequence homology to the subunit 2 gene of the NADH: ubiquinone reductase complex. Mol Gen Genet 221:195–198
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Communicated by R.G. Herrmann
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Nozato, N., Oda, K., Yamato, K. et al. Cotranscriptional expression of mitochondrial genes for subunits of NADH dehydrogenase, nad5, nad4, nad2, in Marchantia polymorpha . Molec. Gen. Genet. 237, 343–350 (1993). https://doi.org/10.1007/BF00279437
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DOI: https://doi.org/10.1007/BF00279437