Skip to main content
SpringerLink
Log in

Structural organization of the chloroplast genome of the chromophytic algaVaucheria bursata

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  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. 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. 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. 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. 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. 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).

    PubMed  Google Scholar 

  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).

    Article  PubMed  Google Scholar 

  8. Dente L, Cesareni G, Cortese R: pEMBL: a new family of single stranded plasmids. Nucl Acids Res 11: 1645–1655 (1983).

    PubMed  Google Scholar 

  9. Douglas SE: Physical mapping of the plastid genome from the chlorophyllc-containing algaCryptomonas Φ. Curr Genet 14: 591–598 (1988).

    Google Scholar 

  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).

    PubMed  Google Scholar 

  11. Gibbs SP: Chloroplasts of some algae groups may have evolved from endosymbiotic eucaryotic algae. Ann N Y Acad Sci 361: 193–207 (1981).

    PubMed  Google Scholar 

  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).

    Article  PubMed  Google Scholar 

  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. 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 

  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).

    Article  Google Scholar 

  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. 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. 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. 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).

    Article  Google Scholar 

  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).

    Article  PubMed  Google Scholar 

  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. Linne von Berg K-H, Kowallik KV: Structural organization and evolution of the plastid genome ofVaucheria sessilis (Xanthophyceae). BioSystems 21: 239–247 (1988).

    Article  PubMed  Google Scholar 

  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. Maniatis T, Fritsch EF, Sambrook J: Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY (1982).

    Google Scholar 

  25. Margulis L, Obar R:Heliobacterium and the origin of chrysoplasts. BioSystems 17: 317–325 (1985).

    Article  PubMed  Google Scholar 

  26. Milligan BG: Differentiation of chloroplast DNA within populations ofTrifolium pratense. Fourth International Congress of Systematics and Evolution Biology, College Park, Maryland, USA (1990).

  27. Milligan BG, Hampton JN, Palmer JD: Dispersed repeats and structural reorganization in subclover chloroplast DNA. Mol Biol Evol 6: 355–368 (1989).

    PubMed  Google Scholar 

  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).

    PubMed  Google Scholar 

  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).

    Article  PubMed  Google Scholar 

  30. Palmer JD: Chloroplast DNA exists in two orientations. Nature 301: 92–93 (1983).

    Google Scholar 

  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.

  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.

  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.

  34. Palmer JD, Herbon LA: Tricircular mitochondrial genomes ofBrassica andRaphanus: Reversal of repeat configurations by inversion. Nucl Acids Res 14: 9755–9764 (1986).

    PubMed  Google Scholar 

  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. 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).

    Article  PubMed  Google Scholar 

  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. 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. 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. 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).

    PubMed  Google Scholar 

  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. 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).

    Article  Google Scholar 

  43. Waris H: The significance for algae of chelating substances in the nutrient solutions. Physiol Plant 6: 538–543 (1953).

    Google Scholar 

  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).

    PubMed  Google Scholar 

  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. Westhoff P, Herrmann RG: Complex RNA maturation in chloroplasts. ThepsbB operon from spinach. Eur J Biochem 171: 551–564 (1988).

    PubMed  Google Scholar 

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

    Google Scholar 

  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).

    PubMed  Google Scholar 

  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. 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 

Download references

Author information

Author notes

  1. Karl-Heinz Linne von Berg

    Present address: Botanisches Institut der Universität Köln, Gyrhofstrasse 15, D-5000, Köln 41, FRG

Authors and Affiliations

  1. Institut für Botanik der Heinrich-Heine-Universität, Universitätsstrasse 1, D-4000, Düsseldorf, FRG

    Karl-Heinz Linne von Berg & Klaus V. Kowallik

Authors
  1. Karl-Heinz Linne von Berg
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Klaus V. Kowallik
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Linne von Berg, KH., Kowallik, K.V. Structural organization of the chloroplast genome of the chromophytic algaVaucheria bursata . Plant Mol Biol 18, 83–95 (1992). https://doi.org/10.1007/BF00018459

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00018459

Key words

Search

Navigation