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Nucleotide sequence and phylogenetic implication of the ATPase subunits β and ε encoded in the chloroplast genome of the brown alga Dictyota dichotoma

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Abstract

We have cloned and sequenced the genes atpB and atpE, coding for CF1 subunits β and ε, respectively, of the chloroplast genome of the brown alga Dictyota dichotoma. Although the coding site of atpE cannot be demonstrated by heterologous Southern hybridizations, a 417 bp reading frame 3′ to atpB was identified as the gene atpE by sequence similarities with atpE genes from other sources. A maximum sequence identity of 30% is found between the predicted amino acid sequence of the Dictyota subunit ε and the corresponding cyanobacterial subunits. Including conserved amino acid replacements, the Dictyota ε subunit exhibits about 70% sequence similarity with the cyanobacterial and land plant subunits. As in cyanobacteria, the atpE gene does not overlap the preceding gene atpB. The deduced amino acid sequence of atpB is 74–79% identical to the corresponding cyanobacterial and chloroplast subunits. Entirely conserved are regions referred to as the catalytic and/or regulatory sites of ATP formation, including interacting regions between subunits α and β. A phylogram predicted from F1/CF1-β subunits of eleven different organisms suggests a common evolutionary origin of plastids from chlorophytes and brown algae.

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References

  1. Andrews WW, Hill FC, Allison WS: Identification of the Lys residue to which the 4-nitrobenzofuran group migrates after the bovine mitochondrial F1-ATPase is inactivated with 7-chloro-4-nitro [14C] benzofuran. J Biol Chem 259: 14378–14382 (1984).

    PubMed  Google Scholar 

  2. Bickel S: Katalytische und regulatorische Wechsel-wirkungen von Adeninnukleotiden mit der H+ ATPase des Chloroplasten. Thesis, University Düsseldorf, FRG (1988).

    Google Scholar 

  3. Cozens AL, Walker JE: The organization and sequence of the genes for ATP synthase subunits in the cyanobacterium Synechococcus 6301. J Mol Biol 194: 359–383 (1987).

    Article  PubMed  Google Scholar 

  4. Cross RL, Cunningham D, Miller CG, Xue Z, Zhou J, Boyer PD: Adenine nucleotide binding sites on beef heart F1 ATPase: Photoaffinity labeling of β-subunit Tyr-368 at a noncatalytic site and β Tyr-345 at a catalytic site. Proc Natl Acad Sci USA 84: 5715–5719 (1987).

    PubMed  Google Scholar 

  5. Curtis SE: Genes encoding the β and ε subunits of the proton-translocating ATPase from Anabaena sp. strain PCC 7120. J Bact 169: 80–86 (1987).

    PubMed  Google Scholar 

  6. Falk G, Hampe A, Walker JE: Nucleotide sequence of the Rhodospirillum rubrum atp operon. Biochem J 228: 391–407 (1985).

    PubMed  Google Scholar 

  7. Falk G, Walker JE: DNA sequence of a gene cluster coding for subunits of the F0 membrane sector of ATP synthase in Rhodospirillum rubrum. Biochem J 254: 109–122 (1988).

    PubMed  Google Scholar 

  8. Fry DC, Kuby SA, Mildvan AS: NMR studies of the MgATP binding site of adenylate kinase and of a 45-residue peptide fragment of the enzyme. Biochemistry 24: 4680–4694 (1985).

    PubMed  Google Scholar 

  9. Futai M, Kanazawa H: Structure and function of proton-translocating adenosine triphosphatase (F0F1): Biochemical and molecular biological approaches. Microbiol Rev 47: 285–312 (1983).

    PubMed  Google Scholar 

  10. Garboczi DN, Fox AH, Gerring SL, Pedersen PL: β subunit of rat liver mitochondrial ATP synthase: cDNA cloning, amino acid sequence, expression in Escherichia coli and structural relationship to adenylate kinase. Biochemistry 27: 553–560 (1988).

    PubMed  Google Scholar 

  11. Gibbs SP: The chloroplasts of some algal groups may have evolved from endosymbiotic eukaryotic algae. Ann NY Acad Sci 361: 193–208 (1981).

    PubMed  Google Scholar 

  12. Gibbs SP: The chloroplast endoplasmic reticulum: Structure, function and evolutionary significance. Int Rev Cytol 72: 49–99 (1981).

    Google Scholar 

  13. Giovannoni SJ, Turner S, Olsen GJ, Barns S, Lane DJ, Pace NR: Evolutionary relationships among cyanobacteria and green chloroplasts. J Bact 170: 3584–3592 (1988).

    PubMed  Google Scholar 

  14. Gunderson JH, Elwood H, Ingold A, Kindle K, Sogin ML: Phylogenetic relationships between chlorophytes, chrysophytes and oomycetes. Proc Natl Acad Sci USA 84: 5823–5827 (1987).

    PubMed  Google Scholar 

  15. Hennig J, Herrmann RG: 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 (1986).

    Article  Google Scholar 

  16. Higgins DG, Sharp PM: Clustal: a package for performing multiple sequence alignments on a microcomputer. Gene 73: 237–244 (1988).

    Article  PubMed  Google Scholar 

  17. Horbach M, Meyer HE, Bickel-Sandkötter S: Inactivation of chloroplast H+-ATPase by modification of Lysβ359, Lysα176 and Lysα266. Eur J Biochem, 200: 449–456 (1991).

    PubMed  Google Scholar 

  18. Howe CJ, Fearnley IM, Walker JE, Dyer TA, Gray JC: Nucleotide sequences of the genes for the alpha, beta and epsilon subunits of wheat chloroplast ATP synthase. Plant Mol Biol 4: 333–345 (1985).

    Google Scholar 

  19. Inatomi K, Eya S, Maeda M, Futai M: Amino acid sequence of the α and β subunits of Methanosarcina barkeri ATPase deduced from cloned genes. J Biol Chem 264: 10954–10959 (1989).

    PubMed  Google Scholar 

  20. Kobayashi K, Nakamura K, Asahi T: CF1ATPase β- and ε-genes are separated in the sweet potato chloroplast genome. Nucl Acids Res 15: 7177 (1987).

    PubMed  Google Scholar 

  21. Kowallik KV: Molecular aspects and phylogenetic implications of plastid genomes of certain chromophytes. In: Green JC, Leadbeater BSC, Diver WL (eds) The Chromophyte Algae, pp. 101–123. Clarendon Press, Oxford 1989.

    Google Scholar 

  22. Krebbers ET, Larrinua IM, McIntosh L, Bogorad L: The maize chloroplast genes for the β and ε subunits of the photosynthetic coupling factor CF1 are fused. Nucl Acids Res 10: 4958–5002 (1982).

    Google Scholar 

  23. Kuby SA, Palmieri RH, Frischat A, Fischer AH, Wu LH, Maland L, Manship M: Studies on adenosine triphosphate transphosphorylases. Amino acid sequence of rabbit muscle ATP-AMP transphosphorylase. Biochemistry 23: 2393–2399 (1984).

    PubMed  Google Scholar 

  24. Kuhsel M: Molekulare Charakterisierung des Plastiden-gemoms der Braunalge Dictyota dichotoma (Huds.) Lamour. PhD Thesis, University Düsseldorf, FRG (1988).

    Google Scholar 

  25. Ludwig W, Weizenegger M, Kirchhof G, Köhler G, Klugbauer N, Dorn S, Schleifer KH: Phylogenetic relationships of prokaryotes analyzed by comparative sequencing of genes encoding 23S rRNA, elongation factor Tu and beta subunit of ATP-synthase. Abstract ICSEB IV, College Park, University of Maryland USA, 1990.

  26. McCarn DF, Whitaker RA, Alman J, Vrba JM, Curtis SE: Genes encoding the alpha, gamma, delta, and four F0 subunits of ATP synthase constitute an operon in the cyanobacterium Anabaena PCC 7120. J Bact 170: 3448–3458 (1988).

    PubMed  Google Scholar 

  27. Mordon CW, Golden SS: psbA genes indicate common ancestry of prochlorophytes and chloroplasts. Nature 337: 382–385 (1989).

    Article  PubMed  Google Scholar 

  28. Nelson N: Structure, function, and evolution of proton ATPases. Plant Physiol 86: 1–3 (1988).

    Google Scholar 

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

    Google Scholar 

  30. Olsen GJ: The earliest phylogenetic branchings: comparing rRNA-based evolutionary trees inferred with various techniques. Cold Spring Harbor Symp Quant Biol 52: 825–838 (1987).

    PubMed  Google Scholar 

  31. Pai EF, Sachsenheimer W, Schirmer RH, Schulz GE: Substrate positions and induced-fit in crystalline adenylate kinase. J Mol Biol 114: 37–45 (1977).

    PubMed  Google Scholar 

  32. Pancic PG, Strotmann H, Kowallik KV: The δ subunit of the chloroplast ATPase is plastid-encoded in the diatom Odontella sinensis. FEBS Lett 280: 387–392 (1991).

    Article  PubMed  Google Scholar 

  33. Pougeois R, Satre M, Vignais PV: N-ethoxycarbonyl-2-ethoxy-1,2-dihydroquinoline, a new inhibitor of the mitochondrial F1-ATPase. Biochemistry 17: 3018–3023 (1978).

    PubMed  Google Scholar 

  34. Reith M, Cattolico RA: Inverted repeat of Olisthodiscus luteus chloroplast DNA contains genes for both subunits of ribulose-1,5-bisphosphate carboxylase and the 32,000-dalton QB protein: Phylogenetic implications. Proc Natl Acad Sci USA 83: 8599–8603 (1986).

    Google Scholar 

  35. Rothschild LJ, Ragan MA, Coleman AW, Heywood P, Gerbi SA: Are rRNA sequence comparisons the rosetta stone of phylogenetics? Cell 47: 640 (1986).

    Article  PubMed  Google Scholar 

  36. Runswick MJ, Walker JE: The amino acid sequence of the β-subunit of ATP synthase from bovine heart mitochondria. J Biol Chem 258: 3081–3083 (1983).

    PubMed  Google Scholar 

  37. Saraste M, Gay NJ, Eberle A, Runswick MJ, Walker JE: The atp operon: nucleotide sequence of the genes for the γ, β and ε subunits of Escherichia coli ATP synthase. Nucl Acids Res 9: 5287–5296 (1981).

    PubMed  Google Scholar 

  38. Shine J, Dalgarno L: The 3′ terminal sequence of Escherichia coli 16S ribosomal RNA: complementary to nonsense triplets and ribosome binding sites. Proc Natl Acad Sci USA 71: 1342–1346 (1974).

    PubMed  Google Scholar 

  39. Shinozaki K, Deno H, Kato A, Sugiura M: Overlap and cotranscription of the genes for the beta and epsilon subunit of the tobacco chloroplast ATPase. Gene 24: 147–155 (1983).

    Article  PubMed  Google Scholar 

  40. Sogin ML, Gunderson JH, Elwood HJ, Alonso RA, Peattie DA: Phylogenetic meaning of the kingdom concept: An unusual ribosomal RNA from Giardia lamblia. Science 243: 75–77 (1989).

    PubMed  Google Scholar 

  41. Strotmann H, Bickel-Sandkötter S: Structure, function and regulation of the chloroplast ATPase. Annu Rev Plant Physiol 35: 97–120 (1984).

    Google Scholar 

  42. Swofford DL: PAUP 3.0 User's Manual (Draft 12/11/89). Illinois Natural History Survey, Illinois, 1989.

    Google Scholar 

  43. Turmel M, Lemieux B, Lemieux C: The chloroplast genome of the green alga Chlamydomonas moewusii: Localisation of protein coding genes and transcriptionally active regions. Mol Gen Genet 214: 412–419 (1988).

    Article  PubMed  Google Scholar 

  44. Walker JE, Saraste M, Runswick MJ, Gay NJ: Distantly related sequences in the α- and β-subunits of ATP synthase, myosin, kinase and other ATP-requiring enzymes and a common nucleotide binding fold. EMBO J 1: 945–951 (1982).

    PubMed  Google Scholar 

  45. Walker JE, Saraste M, Gay NJ: The unc operon. Nucleotide sequence, regulation and structure of ATP-synthase. Biochim Biophys Acta 168: 164–200 (1984).

    Google Scholar 

  46. Westhoff P, Alt J, Nelson N, Herrmann RG: Genes and transcripts for ATP synthase CF0 subunits I and II from spinach thylakoid membranes. Mol Gen Genet 199: 290–299 (1985).

    Article  Google Scholar 

  47. Whatley JM, Whatley FR: Chloroplast evolution. New Phytol 87: 233–247 (1981).

    Google Scholar 

  48. Wilbur WJ, Lipman DJ: Rapid similarity searches of nucleic acid and protein data banks. Proc Natl Acad Sci USA 80: 726–730 (1983).

    PubMed  Google Scholar 

  49. Winnacker E: From Genes to Clones. Introduction to Gene Technology. Verlag Chemie, Weinheim, 634 pp. (1987).

    Google Scholar 

  50. Woese CR: Archaebacteria. Sci Am 224: 94–106 (1981).

    Google Scholar 

  51. Woessner JP, Gilham NW, Boynton JE: The sequence of the chloroplast atpB gene and its flanking regions in Chlamydomonas reinhardtii. Gene 44: 17–28 (1986).

    Article  PubMed  Google Scholar 

  52. Woessner JP, Gilham NW, Boynton JE: Chloroplast genes encoding subunits of the H+-ATPase complex of Chlamydomonas reinhardtii are rearranged compared to higher plants: sequence of the atpE gene and location of the atpF and atpI genes. Plant Mol Biol 8: 151–158 (1987).

    Google Scholar 

  53. Xue Z, Miller CG, Zhou JM, Boyer PD: Catalytic and noncatalytic nucleotide binding sites of chloroplast F1 ATPase. Photoaffinity labeling and peptide sequencing. FEBS Lett 223: 391–394 (1987).

    Article  PubMed  Google Scholar 

  54. Zurawski G, Bottomley W, Whitfeld PR: Structures of the genes for the β and ε subunits of spinach chloroplast ATPase indicate a dicistronic mRNA and an overlapping translation stop/start signal. Proc Natl Acad Sci USA 79: 6260–6264 (1982).

    Google Scholar 

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Leitsch, C.E.W., Kowallik, K.V. Nucleotide sequence and phylogenetic implication of the ATPase subunits β and ε encoded in the chloroplast genome of the brown alga Dictyota dichotoma . Plant Mol Biol 19, 289–298 (1992). https://doi.org/10.1007/BF00027350

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