Advertisement

Plant Molecular Biology

, Volume 18, Issue 1, pp 83–95 | Cite as

Structural organization of the chloroplast genome of the chromophytic algaVaucheria bursata

  • Karl-Heinz Linne von Berg
  • Klaus V. Kowallik
Article

Abstract

The chloroplast genome of the chromophytic algaVaucheria bursata has been characterized by restriction site and gene mapping analysis. It is represented by a circular molecule 124.6 kb in size. An inverted sequence duplication (IR) not larger than 5.85 kb carries the rRNA genes and separates two single-copy regions of 64.6 kb and 48.3 kb from one another. TheVaucheria plastid genome exists in two equimolar isomers which is due to intramolecular flip-flop recombination within the IR sequences. The coding sites for 21 structural and soluble proteins have been mapped on both single-copy regions using heterologous gene sequences as probes. Although the overall gene order is found to be rearranged when compared with other chromophytic algal and land plant chloroplast genomes, most of the transcriptional units of cyanobacteria and land plant chloroplast genomes appear to be conserved. The phylogenetic implications of these findings are further discussed.

Key words

chloroplast genome gene mapping inverted repeat flip-flop recombination Chromophyta Vaucheria bursata 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Alt J, Herrmann RG: Nucleotide sequence of the gene for pre-apocytochromefin the spinach plastid chromosome. Curr Genet 8: 551–557 (1984).Google Scholar
  2. 2.
    Alt J, Morris J, Westhoff P, Herrmann RG: Nucleotide sequence of the clustered genes for the 44 kd chlorophylla apoprotein and the ‘32 kd’-like protein of the photosystem II reaction center in the plastid chromosome. Curr Genet 8: 597–606 (1984).Google Scholar
  3. 3.
    Bourne CM, Stoermer EF, Palmer JD: Structure of the chloroplast genome in closely related species ofCyclotella (Bacillariophyceae). J Phycol 25 (Suppl): 5 (1989).Google Scholar
  4. 4.
    Cantrell A, Bryant DA: Molecular cloning and nucleotide sequence of thepsaA andpsaB genes of the cyanobacteriumSynechococcus sp. PCC 7002. Plant Mol Biol 9: 453–468 (1987).Google Scholar
  5. 5.
    Cattolico RA, Loiseaux-de Goer S: Analysis of chloroplast evolution and phylogeny: a molecular approach. In: Green JC, Leadbeater BSC, Diver WL (eds) The Chromophyte Algae. Problems and Perspectives, vol 38, pp. 85–100. The Systematics Association/Clarendon Press, Oxford (1989).Google Scholar
  6. 6.
    Cozens AL, Walker JE: Pea chloroplast DNA encodes homologues ofEscherichia coli ribosomal subunit S2 and the β′ subunit of RNA polymerase. Biochem J 236: 453–460 (1986).PubMedGoogle Scholar
  7. 7.
    Cozens AL, Walker JE: The organization and sequence of the genes for ATP synthase subunits in the cyanobacteriumSynechococcus 6301. Support for an endosymbiotic origin of chloroplasts. J Mol Biol 194: 359–383 (1987).CrossRefPubMedGoogle Scholar
  8. 8.
    Dente L, Cesareni G, Cortese R: pEMBL: a new family of single stranded plasmids. Nucl Acids Res 11: 1645–1655 (1983).PubMedGoogle Scholar
  9. 9.
    Douglas SE: Physical mapping of the plastid genome from the chlorophyllc-containing algaCryptomonas Φ. Curr Genet 14: 591–598 (1988).Google Scholar
  10. 10.
    Fish LE, Kück U, Bogorad L: Two partially homologous adjacent light-inducible maize chloroplast genes encoding polypeptides of the P700 chlorophylla-protein complex of photosystem I. J Biol Chem 260: 1413–1421 (1985).PubMedGoogle Scholar
  11. 11.
    Gibbs SP: Chloroplasts of some algae groups may have evolved from endosymbiotic eucaryotic algae. Ann N Y Acad Sci 361: 193–207 (1981).PubMedGoogle Scholar
  12. 12.
    Golden SS, Stearns GW: Nucleotide sequence and transcript analysis of three photosystem II genes from the cyanobacteriumSynechococcus sp. PCC 7942. Gene 67: 85–96 (1988).CrossRefPubMedGoogle Scholar
  13. 13.
    Heinemeyer W, Alt J, Herrmann RG: Nucleotide sequence of the clustered genes for apocytochromeb6 and subunit 4 of the cytochromeb/f complex in the spinach plastid chromosome. Curr Genet 8: 543–549 (1984).Google Scholar
  14. 14.
    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).CrossRefGoogle Scholar
  15. 15.
    Herrmann RG, Alt J, Schiller B, Widger WR, Cramer WA: 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 (1984).CrossRefGoogle Scholar
  16. 16.
    Kirsch W, Seyer P, Herrmann RG: Nucleotide sequence of the clustered genes for two P700 chlorophylla apoproteins of the photosystem I reaction center and the ribosomal protein S14 of the spinach plastid chromosome. Curr Genet 10: 843–855 (1986).Google Scholar
  17. 17.
    Kowallik KV. Molecular aspects and phylogenetic implications of plastid genomes of certain chromophytes. In: Green JC, Leadbeater BSC, Diver WL (eds) The Chromophyte Algae, Problems and Perspectives, vol. 38, pp. 101–124. The Systematics Association/Clarendon Press, Oxford (1989).Google Scholar
  18. 18.
    Kuhsel M, Kowallik KV: The plastome of a brown alga,Dictyota dichotoma I. Physical properties and theBam HI/Sal I/Bgl II cleavage site map. Plant Mol Biol 4: 365–376 (1985).Google Scholar
  19. 19.
    Kuhsel M, Kowallik KV: The plastome of a brown alga,Dictyota dichotoma. II. Localization of structural genes coding for ribosomal RNAs, the large subunit of ribulose-1,5-biphosphate carboxylase/oxygenase and for polypeptides of photosystems I and II. Mol Gen Genet 207: 361–368 (1987).CrossRefGoogle Scholar
  20. 20.
    Lawn RM, Fritsch EF, Parker RC, Blake G, Maniatis T: The isolation and characterization of linked α- and β globin genes from a cloned library of human DNA. Cell 15: 1157–1174 (1978).CrossRefPubMedGoogle Scholar
  21. 21.
    Linne von Berg K-H, Schmid M, Linne von Berg G, Sturm K, Hennig A, Kowallik KV: The chloroplast genome (plastome) from algae of different phylogenetic relationships. Br Phycol J 17: 235 (1982).Google Scholar
  22. 22.
    Linne von Berg K-H, Kowallik KV: Structural organization and evolution of the plastid genome ofVaucheria sessilis (Xanthophyceae). BioSystems 21: 239–247 (1988).CrossRefPubMedGoogle Scholar
  23. 23.
    Loiseaux-de Goer S, Markowicz Y, Dalmon J, Audren H: Physical maps of the two circular plastid DNA modules of the brown algaPylaiella littoralis (L.) Kjellm. Location of the rRNA genes and of several protein-coding regions on both molecules. Curr Genet 14: 155–162 (1988).Google Scholar
  24. 24.
    Maniatis T, Fritsch EF, Sambrook J: Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY (1982).Google Scholar
  25. 25.
    Margulis L, Obar R:Heliobacterium and the origin of chrysoplasts. BioSystems 17: 317–325 (1985).CrossRefPubMedGoogle Scholar
  26. 26.
    Milligan BG: Differentiation of chloroplast DNA within populations ofTrifolium pratense. Fourth International Congress of Systematics and Evolution Biology, College Park, Maryland, USA (1990).Google Scholar
  27. 27.
    Milligan BG, Hampton JN, Palmer JD: Dispersed repeats and structural reorganization in subclover chloroplast DNA. Mol Biol Evol 6: 355–368 (1989).PubMedGoogle Scholar
  28. 28.
    Morris J, Herrmann RG: Nucleotide sequence of the gene for the P680 chlorophylla apoprotein of the photosystem II reaction center from spinach. Nucl Acids Res 12: 2837–2850 (1984).PubMedGoogle Scholar
  29. 29.
    Ohme M, Tanaka M, Chunwongse J, Shinozaki K, Sugiura M: A tobacco chloroplast DNA sequence possibly coding for a polypeptide similar toE. coli RNA polymerase β subunit. FEBS Lett 200: 87–90 (1986).CrossRefPubMedGoogle Scholar
  30. 30.
    Palmer JD: Chloroplast DNA exists in two orientations. Nature 301: 92–93 (1983).Google Scholar
  31. 31.
    Palmer JD: Plastid chromosomes: Structure and Evolution. In: Bogorad L, Vasil IK (eds) The Molecular Biology of Plastids, vol 7. In: Cell Culture and Somatic Cell Genetics in Plants, in press.Google Scholar
  32. 32.
    Palmer JD: Comparison of chloroplast and mitochondrial genome evolution in plants. In: Herrmann RG (ed.) Plant Gene Research, vol. 6: Organelles. Springer-Verlag, Heidelberg/New York, in press.Google Scholar
  33. 33.
    Palmer JD, Boynton JE, Gillham NW, Harris EH: Evolution and recombination of the large inverted repeat inChlamydomonas chloroplast DNA. In: Molecular Biology of the Photosynthetic Apparatus, pp. 269–278 Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.Google Scholar
  34. 34.
    Palmer JD, Herbon LA: Tricircular mitochondrial genomes ofBrassica andRaphanus: Reversal of repeat configurations by inversion. Nucl Acids Res 14: 9755–9764 (1986).PubMedGoogle Scholar
  35. 35.
    Palmer JD, Nugent JM, Herbon LA: Unusual structure ofGeranium chloroplast DNA: A triple-sized inverted repeat, extensive gene duplications, multiple inversions, and two repeat families. Proc Natl Acad Sci USA 84: 769–773 (1987).Google Scholar
  36. 36.
    Pancic PG, Strotmann H, Kowallik KV: The δ-subunit of the chloroplast ATPase is plastid-encoded in the diatomOdontella sinensis. FEBS Lett 280: 387–392 (1991).CrossRefPubMedGoogle Scholar
  37. 37.
    Reith M, Cattolico RA: Inverted repeat ofOlisthodiscus 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
  38. 38.
    Rieth A: Xanthophyceae. In: Ettl H, Gerloff J, Heynig H (eds) Süsswasserflora von Mitteleuropa, Band 4. Gustav Fischer Verlag, Stuttgart/New York (1980).Google Scholar
  39. 39.
    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: The complete nucleotide sequence of the tobacco chloroplast genome: its gene organization and expression. EMBO J 5: 2043–2049 (1986).Google Scholar
  40. 40.
    Sijben-Müller G, Hallick RB, Alt J, Westhoff P, Herrmann RG: Spinach plastid genes coding for initiation factor IF-1, ribosomal protein S11 and RNA polymerase α-subunit. Nucl Acids Res 14: 1029–1044 (1986).PubMedGoogle Scholar
  41. 41.
    Stosch HAvon, Drebes G: Entwicklungsgeschichtliche Untersuchungen an zentrischen Diatomeen IV. Die PlanktonalgeStephanopyxis turris — ihre Behandlung und Entwicklungsgeschichte. Helgol Wiss Meersunters 11: 209–257 (1964).Google Scholar
  42. 42.
    Tanaka M, Obokata J, Chunwongse J, Shinozaki K, Sugiura M: Rapid splicing and stepwise processing of a transcript from thepsbB operon in tobacco chloroplasts: Determination of the intron sites inpetB andpetD. Mol Gen Genet 209: 427–431 (1987).CrossRefGoogle Scholar
  43. 43.
    Waris H: The significance for algae of chelating substances in the nutrient solutions. Physiol Plant 6: 538–543 (1953).Google Scholar
  44. 44.
    Watson JC, Surzycki SJ: Extensive sequence homology in the DNA coding for elongation factor Tu fromEscherichia coli and theChlamydomonas reinhardtii chloroplast. Proc Natl Acad Sci USA 79: 2264–2267 (1982).PubMedGoogle Scholar
  45. 45.
    Westhoff P, Nelson N, Bünemann H, Herrmann RG: Localization of genes for coupling factor subunits on the spinach plastid chromosome. Curr Genet 4: 109–120 (1981).Google Scholar
  46. 46.
    Westhoff P, Herrmann RG: Complex RNA maturation in chloroplasts. ThepsbB operon from spinach. Eur J Biochem 171: 551–564 (1988).PubMedGoogle Scholar
  47. 47.
    Whatley JM, Whatley FR: Chloroplast evolution. New Phytol 87: 233–247 (1981).Google Scholar
  48. 48.
    Zurawski G, Perrot B, Bottomley W, Whitfeld PR: The structure of the gene for the large subunit of ribulose 1,5-bisphosphate carboxylase from spinach chloroplast DNA. Nucl Acids Res 9: 3251–3270 (1981).PubMedGoogle Scholar
  49. 49.
    Zurawski G, Bohnert HJ, Whitfeld PR, Bottomley W: Nucleotide sequence of the gene for theM r 32,000 thylakoid membrane protein fromSpinacia oleracea andNicotiana debneyi predicts a totally conserved primary translation product ofM r 38,950. Proc Natl Acad Sci USA 79: 7699–7703 (1982).Google Scholar
  50. 50.
    Zurawski G, Bottomley W, Whitfeld PR: Structure 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

Copyright information

© Kluwer Academic Publishers 1992

Authors and Affiliations

  • Karl-Heinz Linne von Berg
    • 1
  • Klaus V. Kowallik
    • 1
  1. 1.Institut für Botanik der Heinrich-Heine-UniversitätUniversitätsstrasse 1DüsseldorfFRG

Personalised recommendations