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Gene organization and newly identified groups of genes of the chloroplast genome from a liverwort, Marchantia polymorpha

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Abstract

The complete nucleotide sequence of chloroplast DNA from a liverwort, Marchantia polymorpha has made clear the entire gene organization of the chloroplast genome. Quite a few genes encoding components of photosynthesis and protein synthesis machinery have been identified by comparative computer analysis. Other genes involved in photosynthesis, respiratory electron transport, and membrane-associated transport in chloroplasts were predicted by the amino acid sequence homology and secondary structure of gene products. Thirty-three open reading frames in the liverwort chloroplast genome remain unidentified. However, most of these open reading frames are also conserved in the chloroplast genomes of two species, a liverwort, Marchantia polymorpha, and tobacco, Nicotiana tabacum, indicating their active functions in chloroplasts.

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Abbreviations

bp:

base pair

kDa:

kilodalton

IR:

inverted repeat

ORF:

open reading frame

DALA:

δ-aminolevulinate

References

  • Alt J and Herrmann RG (1984) Nucleotide sequence of the gene for preapocytochrome f in the spinach plastid chromosome. Curr Genet 8: 551–557

    Google Scholar 

  • Alt J, Morris J, Westhoff P and Herrmann RG (1984) Nucleotide sequence of the clustered genes for the 44kkd chlorophyll a apoprotein and the ‘32 kd’-like protein of the photosystem II reaction center in the spinach plastid chromosome. Curr Genet 8: 597–606

    Google Scholar 

  • Anderson S, Bankier AT, Barrell BG, deBruijn MHL, Coulson AR, Drouin J, Eperon IC, Nierlich DP, Roe BA, Sanger F, Schreier PH, Smith AJH, Staden R and Young IG (1981) Sequence and organization of the human mitochondrial genome. Nature 290: 457–465

    Google Scholar 

  • Bedwell D, Davis G, Gosink M, Post L, Nomura M, Kestler H, Zengel JM and Lindahl L (1985) Nucleotide sequence of the alpha ribosomal protein operon of Escherichia coli. Nucl Acids Res 13: 3891–3903

    Google Scholar 

  • Bennoun P (1982) Evidence for a respiratory chain in the chloroplast. Proc Natl Acad Sci USA 79: 4352–4356

    Google Scholar 

  • Bonitz SG, Berlani R, Coruzzi G, Li M, Nobrega FG, Nobrega MP, Thalenfeld BE and Tzagoloff A (1980) Codon recognition rules in yeast mitochondria. Proc Natl Acad Sci USA 77: 3167–3170

    Google Scholar 

  • Cerretti DP, Dean D, Davis GP, Bedwell DM and Nomura M (1983) The spc ribosomal protein operon of Escherichia coli: sequence and cotranscription of the ribosomal protein genes and a protein export gene. Nucl Acids Res 11: 2599–2616

    Google Scholar 

  • Chomyn A, Mariottini P, Cleeter MWJ, Ragan CI, Matsuno-Yagi A, Hatefi Y, Doolittle RF and Attardi G (1985) Six unidentified reading frames of human mitochondrial DNA encode components of the respiratory-chain NADH dehydrogenase. Nature 314: 592–597

    Google Scholar 

  • Chomyn A, Cleeter MWJ, Ragan CI, Riley M, Doolittle RF and Attardi G (1986) URF6, last unidentified reading frame of human mtDNA, codes for an NADH dehydrogenase subunit. Science 234: 614–618

    Google Scholar 

  • Cozens AL, Walker JE, Phillips AL, Huttly AK and Gray JC (1986) A sixth subunit of ATP synthase, an F0 component, is encoded in the pea chloroplast genome. EMBO J 5: 217–222

    Google Scholar 

  • Crick FHC (1966) The genetic code: III. Sci Amer 254(4): 55–62.

    Google Scholar 

  • Crouse EJ, Schmitt JM and Bohnert HJ (1985) Chloroplast and cyanobacterial genomes, genes and RNAs: a compilation. Plant Mol Biol Reporter 3: 43–89

    Google Scholar 

  • Deno H and Sugiura M (1983) The nucleotide sequences of tRNASer (GCU) and tRNAGln (UUG) genes from tobacco chloroplasts. Nucl Acids Res 11: 2185–2192

    Google Scholar 

  • Dorne AM, Lescure AM and Mache R (1984) Site of synthesis of spinach chloroplast ribosomal proteins and formation of incomplete ribosomal particles in isolated chloroplasts. Plant Mol Biol 3: 83–90

    Google Scholar 

  • Ellis RJ (1981) Chloroplast proteins: synthesis, transport and assembly. Ann Rev Plant Physiol 32: 111–137

    Google Scholar 

  • Fish LE, Kuck U and Bogorad L (1985) Two partially homologous adjacent light-inducible maize chloroplast genes encoding polypeptides of the p700 chlorophyll a-protein complex of photosystem I. J Biol Chem 260: 1413–1421

    Google Scholar 

  • Fournier MJ and Ozeki H (1985) Structure and organization of the transfer ribonucleic acid genes of Escherichia coli K-12. Microbiol Rev 49: 379–397

    Google Scholar 

  • Froshauer S and Beckwith J (1984) The nucleotide sequence of the gene for malF protein, an inner membrane component of the maltose transport system of Escherichia coli. J Biol Chem 259: 10896–10903

    Google Scholar 

  • Fukuzawa H, Kohchi T, Shirai H, Ohyama K, Umesono K, Inokuchi H and Ozeki H (1986) Coding sequences for chloroplast ribosomal protein S12 from the liverwort, Marchantia polymorpha, are separated far apart on the different DNA strands. FEBS Lett 198: 11–15

    Google Scholar 

  • Fukuzawa H, Yoshida T, Kohchi T, Okumura T, Sawano Y and Ohyama K (1987) Splicing of group II introns in mRNAs coding cytochrome b 6 and subunit IV in the liverwort Marchantia polymorpha chloroplast genome: Exon specifying a region coding for two genes with the spacer region. FEBS Lett 220: 61–66

    Google Scholar 

  • Gilson E, Nikaido H and Hofnung M (1982) Sequence of the malK gene in E. coli K12. Nucl Acids Res 10: 7449–7458

    Google Scholar 

  • Hausinger RP and Howard JB (1982) The amino acid sequence of the nitrogenase iron protein from Azotobacter vinelandii. J Biol Chem 257: 2483–2487

    Google Scholar 

  • Hayashida N, Matsubayashi T, Shinozaki M, Inoue K and Hiyama T (1987) The gene for the 9 kd polypeptide, a possible apoprotein for the iron-sulfur centers A and B of the photosystem I complex, in tobacco chloroplast DNA. Curr Genet 12: 247–250

    Google Scholar 

  • Hearst JE, Alberti M and Doolittle RF (1985) A putative nitrogenase reductase gene found in the nucleotide sequences from the photosynthetic gene cluster of R. capsulata. Cell 40: 219–220

    Google Scholar 

  • Heinemeyer W, Alt J and Herrmann RG (1984) Nucleotide sequence of the clustered genes for apocytochrome b6 and subunit 4 of the cytochrome b/f complex in the spinach plastid chromosome. Curr Genet 8: 543–549

    Google Scholar 

  • Henning J and Herrmann RG (1986) Chloroplast ATP synthase of spinach contains nine nonidentical subunit species, six of which are encoded by plastid chromosomes in two operons in a phylogenetically conserved arrangement. Mol Gen Genet 203: 117–128

    Google Scholar 

  • Herrmann RG, Alt J, Schiller B, Widger WR and Cramer WA (1984) Nucleotide sequence of the gene for apocytochrome b-559 on the spinach plastid chromosome: implications for the structure of the membrane protein. FEBS Lett 176: 239–244

    Google Scholar 

  • Higgins CF, Haag PD, Nikaido K, Ardeshir F, Garcia G and Ames GFL (1982) Complete nucleotide sequence and identification of membrane components of the histidine transport operon of S. typhimurium. Nature 298: 723–727

    Google Scholar 

  • Higgins CF, Hiles ID, Whalley K and Jamieson DJ (1985) Nucleotide binding by membrane components of bacterial periplasmic binding protein-dependent transport systems. EMBO J 4: 1033–1040

    Google Scholar 

  • Higgins CF, Hiles ID, Salmond GPC, Gill DR, Downie JA, Evans IJ, Holland IB, Gray L, Buckel SD, Bell AW and Hermodson MA (1986) A family of related ATP-binding subunits coupled to many distinct biological processes in bacteria. Nature 323: 448–450

    Google Scholar 

  • Hirschberg J and McIntosh L (1983) Molecular basis of herbicide resistance in Amaranthus hybridus. Science 222: 1346–1349

    Google Scholar 

  • Høj PB, Svendsen I, Scheller HV and Moller BL (1987) Identification of a chloroplastencoded 9-kDa polypeptide as a 2[4Fe-4S] protein carrying centers A and B of photosystem I. J Biol Chem 262: 12676–12684

    Google Scholar 

  • Holschuh K, Bottomley W and Whitfeld PR (1984) Structure of the spinach chloroplast genes for the D2 and 44 kd reaction-center proteins of photosystem II and for tRNASer (UGA). Nucl Acids Res 12: 8819–8834

    Google Scholar 

  • Howard JB, Lorsbach TW, Ghosh D, Melis K and Stout CD (1983) Structure of Azotobacter vinelandii 7Fe ferredoxin. J Biol Chem 258: 508–522

    Google Scholar 

  • Klein P, Kanehisa M and DeLisi C (1985) The detection and classification of membrane-spanning proteins. Biochim Biophys Acta 815: 468–476

    Google Scholar 

  • Maione TE and Gibbs M (1986) Association of the chloroplastic respiratory and photosynthetic electron transport chains of Chlamydomonas reinhardtii with photoreduction and the oxyhydrogen reaction. Plant Physiol 80: 364–368

    Google Scholar 

  • Minami Y, Wakabayashi S, Wada K, Matsubara H, Kerscher L and Oesterhelt D (1985) Amino acid sequence of a ferredoxin from thermoacidophilic Archaebacterium, Sulfolobus acidocaldarius. Presence of an N6-monomethyllysine and phyletic consideration of Archaebacteria. J Biochem 97: 745–753

    Google Scholar 

  • Montandon PE and Stutz E (1983) Nucleotide sequence of a Euglena gracilis chloroplast genome region coding for the elongation factor Tu; evidence for a spliced mRNA. Nucl Acids Res 11: 5877–5891

    Google Scholar 

  • Morris J and Herrmann RG (1984) Nucleotide sequence of the gene for the P680 chlorophyll a apoprotein of the photosystem II reaction center from spinach. Nucl Acids Res 12: 2837–2850

    Google Scholar 

  • Oh-oka H, Takahashi Y, Wada K, Matsubara H, Ohyama K and Ozeki H (1987) The 8 kDa polypeptide in photosystem I is a probable candidate of an iron-sulfur center protein coded by the chloroplast gene frxA. FEBS Lett 218: 52–54

    Google Scholar 

  • Ohyama K, Fukuzawa H, Kohchi T, Shirai H, Sano T, Sano S, Umesono K, Shiki Y, Takeuchi M, Chang Z, Aota S, Inokuchi H and Ozeki H (1986) Chloroplast gene organization deduced from complete sequence of liverwort Marchantia polymorpha chloroplast DNA. Nature 322: 572–574

    Google Scholar 

  • Phillips AL and Gray JC (1984) Location and nucleotide sequence of the gene for the 15.2 kDa polypeptide of the cytochrome b-f complex from pea chloroplasts. Mol Gen Genet 194: 477–484

    Google Scholar 

  • Quigley F and Weil JH (1985) Organization and sequence of five tRNA genes and of an unidentified reading frame in the wheat chloroplast genome: evidence for gene rearrangements during the evolution of chloroplast genomes. Curr Genet 9: 495–503

    Google Scholar 

  • Schon A, Krupp G, Gough S, Berry-Lowe S, Kannangara CG and Soll D (1986) The RNA required in the first step of chlorophyll biosynthesis is a chloroplast glutamate tRNA. Nature 322: 281–284

    Google Scholar 

  • 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 and Sugiura M (1986) The Complete nucleotide sequence of the tobacco chloroplast genomes: its gene organization and expression. EMBO J 5: 2043–2049

    Google Scholar 

  • Steinback KE, Bonitz S, Arntzen CJ and Bogorad L (1985) (eds) Molecular Biology of the Photosynthetic Apparatus. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY

    Google Scholar 

  • Steinmetz AA, Castroviejo M, Sayre RT and Bogorad L (1986) Protein PSII-G: An additional component of photosystem II identified through its plasmid gene in maize. J Biol Chem 261: 2485–2488

    Google Scholar 

  • Stern DB, Bang AG and Thompson WF (1986) The watermelon mitochondrial URF-1 gene: evidence for a complex structure. Curr Genet 10: 857–869

    Google Scholar 

  • Sugita M, Shinozaki K and Sugiura M (1985) Tobacco chloroplast tRNALys(UUU) conserved boundary sequence in the intron. Proc Natl Acad Sci USA 82: 3557–3561

    Google Scholar 

  • Wada A and Sako T (1987) Primary structures of and genes for new ribosomal proteins A and B in Escherichia coli. J Biochem 101: 817–820

    Google Scholar 

  • Westhoff P (1985) Transcription of the gene encoding the 51 kd chlorophyll a-apoprotein of the photosystem II reaction center from spinach. Mol Gen Genet 201: 115–123

    Google Scholar 

  • Westhoff P, Farchaus JW and Herrmann RG (1986) The gene for the M r 10,000 phosphoprotein associated with photosystem II is part of the psbB operon of the spinach plastid chromosome. Curr Genet 11: 165–169

    Google Scholar 

  • Wittmann HG (1983) Architecture of prokaryotic ribosomes. Ann Rev Biochem 52: 35–65

    Google Scholar 

  • Youvan DC, Bylina EJ, Alberti M, Begusch H and Hearst JE (1984) Nucleotide and deduced polypeptide sequences of the photosynthetic reaction-center, B8970 antenna, and flanking polypeptides from R. capsulata. Cell 37: 949–957

    Google Scholar 

  • Zurawski G, Bohnert HJ, Whitfeld PR and Bottomley W (1982) Nucleotide sequence of the gene for the M r 32,000 thylakoid membrane protein from Spinacia oleracea and Nicotiana debneyi predicts a totally conserved primary translation product of M r 38,950. Proc Natl Acad Sci USA 79: 7699–7703

    Google Scholar 

  • Zurawski G and Zurawski SM (1985) Structure of the Escherichia coli S10 ribosomal protein operon. Nucl Acids Res 13: 4521–4526

    Google Scholar 

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Ohyama, K., Kohchi, T., Fukuzawa, H. et al. Gene organization and newly identified groups of genes of the chloroplast genome from a liverwort, Marchantia polymorpha . Photosynth Res 16, 7–22 (1988). https://doi.org/10.1007/BF00039483

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  • DOI: https://doi.org/10.1007/BF00039483

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