Plant Molecular Biology

, Volume 24, Issue 4, pp 585–602

Conserved gene clusters in the highly rearranged chloroplast genomes of Chlamydomonas moewusii and Chlamydomonas reinhardtii

  • Eric Boudreau
  • Christian Otis
  • Monique Turmel
Research Articles

Abstract

We have extended to about 75 the number of genes mapped on the Chlamydomonas moewusii and Chlamydomonas reinhardtii chloroplast DNAs (cpDNAs) by partial sequencing of the very closely related C. eugametos and C. moewusii cpDNAs and by hybridizations with Chlamydomonas chloroplast gene-specific sequences. Only four of these genes (tscA and three reading frames) have not been identified in any other algal cpDNAs and thus may be specific to Chlamydomonas. Although the C. moewusii and C. reinhardtii cpDNAs differ by complex sequence rearrangements, 38 genes scattered throughout the genome define 12 conserved clusters of closely linked loci. Aside from the rRNA operon, four of these gene clusters share similarity to evolutionarily primitive operons found in other cpDNAs, representing in fact remnants of these operons. Our results thus indicate that most of the ancestral bacterial operons that characterize the chloroplast genome organization of land plants and early-diverging photosynthetic eukaryotes have been disrupted before the emergence of the polyphyletic genus Chlamydomonas. All gene rearrangements between the C. moewusii and C. reinhardtii cpDNAs, with the exception of those accounting for the relocations of atpA, psbI and rbcL, occurred within corresponding regions of the genome. One of these rearrangements seems to have led to disruption of the ancestral region containing rpl23, rpl2, rps19, rpl16, rpl14, rpl5, rps8 and the psaA exon 1. This gene cluster, which bears striking similarity to the Escherichia coli S10 and spc operons, spans a continuous DNA segment in C. reinhardtii, while it maps to two separate fragments in C. moewusii.

Key words

Chlamydomonas chloroplast DNA chloroplast gene organization genome evolution green algae multicistronic operons 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Arizmendi JM, Runswick MJ, Skehel JM, Walker JE: NADH:ubiquinone oxidoreductase from bovine heart mitochondria. A fourth nuclear encoded subunit with a homologue encoded in chloroplast genomes. FEBS Lett 301: 237–242 (1992).CrossRefPubMedGoogle Scholar
  2. 2.
    Bergeron A: Analyse structurale d'un ADN linéaire de 6 kilopaires de bases chez Chlamydomonas moewusii. M.Sc. thesis, Université Larval (1990).Google Scholar
  3. 3.
    Bergeron A, Boulanger J, Turmel M: Nucleotide sequence of the chloroplast petD gene of Chlamydomonas eugametos. Nucl Acids Res 17: 3593 (1989).PubMedGoogle Scholar
  4. 4.
    Berry-Lowe SL, Johnson CH, Schmidt GW: Nucleotide sequence of the psbB gene of Chlamydomonas reinhardtii chloroplasts. Plant Physiol 98: 1541–1543 (1992).Google Scholar
  5. 5.
    Birnboim HC, Doly J: A rapid alkaline extraction procedure for screening recombinant plasmid DNA. Nucl Acids Res 7: 1513–1523 (1979).PubMedGoogle Scholar
  6. 6.
    Boynton JE, Gillham NW, Newman SM, Harris EH: Organelle genetics and transformation of Chlamydomonas. In: Hermann RG (ed) Plant Gene Research, vol VI, pp. 3–64, Springer-Verlag, Vienna (1992).Google Scholar
  7. 7.
    Bryant DA, Stirewalt VT: The cyanelle genome of Cyanophora paradoxa encodes ribosomal proteins encoded by the chloroplast genome of higher plants. FEBS Lett 259: 273–280 (1990).CrossRefPubMedGoogle Scholar
  8. 8.
    Buchheim MA, Turmel M, Zimmer EA, Chapman RL: Phylogeny of Chlamydomonas (Chlorophyta) based on cladistic analysis of nuclear 18S rRNA sequence data. J Phycol 26: 689–699 (1990).CrossRefGoogle Scholar
  9. 9.
    Buchheim MA, Chapman RL: Phylogeny of Carteria (Chlorophyceae) inferred from molecular and organismal data. J Phycol 28: 362–374 (1992).CrossRefGoogle Scholar
  10. 10.
    Christopher DA, Hallick RB: Euglena gracilis chloroplast ribosomal protein operon: A new chloroplast gene for ribosomal protein L5 and description of a novel organelle intron category designated group III. Nucl Acids Res 17: 7591–7608 (1989).PubMedGoogle Scholar
  11. 11.
    Devereux J, Haeberli P, Smithies O: A comprehensive set of sequence analysis programs for the VAX. Nucl Acids Res 12: 387–395 (1984).PubMedGoogle Scholar
  12. 12.
    Durocher V, Gauthier A, Bellemare G, Lemieux C: An optional group I intron between the chloroplast small subunit rRNA genes of Chlamydomonas moewusii and C. eugametos. Curr Genet 15: 277–282 (1989).PubMedGoogle Scholar
  13. 13.
    Fong SE, Surzycki SJ: Chloroplast RNA polymerase genes of Chlamydomonas reinhardtii exhibit an unusual structure and arrangement. Curr Genet 21: 485–497 (1992).PubMedGoogle Scholar
  14. 14.
    Fong SE, Surzycki SJ: Organization and structure of plastome psbF, psbL, petG and ORF712 genes in Chlamydomonas reinhardtii. Curr Genet 21: 527–530 (1992).PubMedGoogle Scholar
  15. 15.
    Goldschmidt-Clermont M: Transgenic expression of aminoglycoside adenine transferase in the chloroplast: a selectable marker for site-specific directed transformation of Chlamydomonas. Nucl Acids Res 19: 4083–4089 (1991).PubMedGoogle Scholar
  16. 16.
    Goldschmidt-Clermont M, Choquet Y, Girard-Bascou J, Michel F, Schirmer-Rahire M, Rochaix J-D: A small chloroplast RNA may be required for trans-splicing in Chlamydomonas reinhardtii. Cell 65: 135–143 (1991).CrossRefPubMedGoogle Scholar
  17. 17.
    Gowans CS: Genetics of Chlamydomonas moewusii and Chlamydomonas eugametos. In: Lewin RA (ed) The Genetics of Algae, Botanical Monographs, vol. 12, pp. 145–173. Blackwell Scientific Publications, Oxford (1976).Google Scholar
  18. 18.
    Grant DM, Gillham NW, Boynton JE: Inheritance of chloroplast DNA in Chlamydomonas reinhardtii. Proc Natl Acad Sci USA 77: 6067–6071 (1980).Google Scholar
  19. 19.
    Gray MW: The endosymbiont hypothesis revisited. Int Rev Cytol 141: 233–257 (1992).PubMedGoogle Scholar
  20. 20.
    Hallick RB, Hong L, Drager RG, Favreau MR, Monfort A, Orsat B, Spielmann A, Stutz E: Complete sequence of Euglena gracilis chloroplast DNA. Nucl Acids Res 21: 3537–3544 (1993).PubMedGoogle Scholar
  21. 21.
    Harris EH: Chlamydomonas reinhardtii chloroplast genome. In: O'Brien SJ (ed) Genetic Maps, 6th ed., Book 2, pp. 165–168. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY (1993).Google Scholar
  22. 22.
    Hess WR, Prombona A, Fieder B, Subramanian AR, Börner T: Chloroplast rps15 and the rpoB/C1/C2 gene cluster are strongly transcribed in ribosome-deficient plastids: evidence for a functioning non-chloroplast-encoded RNA polymerase. EMBO J 12: 563–571 (1993).PubMedGoogle Scholar
  23. 23.
    Hiratsuka J, Shimada H, Whittier R, Ishibashi T, Sakamoto M, Mori M, Kondo C, Honji Y, Sun C-R, Meng B-Y, Li Y-Q, Kanno A, Nishizawa Y, Harai A, Shinozaki K, Sugiura M: 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 (1989).PubMedGoogle Scholar
  24. 24.
    Huang C, Liu X-Q: Nucleotide sequence of the frxC, petB and trnL genes in the chloroplast genome of Chlamydomonas reinhardtii. Plant Mol Biol 18: 985–988 (1992).PubMedGoogle Scholar
  25. 25.
    Johnson CH, Schmidt GW: Nucleotide sequence of the psbH gene of Chlamydomonas reinhardtii. Accession number Z15133.Google Scholar
  26. 26.
    Kück U: The intron of a plastid gene from a green alga contains an open reading frame for a reverse transcriptase-like enzyme. Mol Gen Genet 218: 257–267 (1989).CrossRefPubMedGoogle Scholar
  27. 27.
    Kück U, Godehardt I, Schmidt U: A self-splicing group II intron in the mitochondrial large subunit rRNA (LSUrRNA) gene of the eukaryotic alga Scenedesmus obliquus. Nucl Acids Res 18: 2691–2697 (1990).PubMedGoogle Scholar
  28. 28.
    Lemieux B, Lemieux C: Extensive sequence rearrangements in the chloroplast genomes of the green algae Chlamydomonas eugametos and Chlamydomonas reinhardtii. Curr Genet 10: 213–219 (1985).Google Scholar
  29. 29.
    Lemieux C, Turmel M, Seligy VL, Lee RW: The large subunit of ribulose-1,5-bisphosphate carboxylase-oxygenase is encoded in the inverted repeat sequence of the Chlamydomonas eugametos chloroplast genome. Curr Genet 9: 139–145 (1985).Google Scholar
  30. 30.
    Leu S, Schlesinger J, Micheals A, Shavit N: Complete DNA sequence of the Chlamydomonas reinhardtii chloroplast atpA gene. Plant Mol Biol 18: 613–616 (1992).PubMedGoogle Scholar
  31. 31.
    Liu X-Q, Gillham NW, Boynton JE: Chloroplast ribosomal protein gene rps12 of Chlamydomonas reinhardtii: wild-type sequence, mutation to streptomycin resistance and dependence, and function in Escherichia coli. J Biol Chem 264: 16100–16108 (1989).PubMedGoogle Scholar
  32. 32.
    Mattox K, Stewart K: Classification of the green algae: a concept based on comparative cytology. In: Irvine DEG, John DM (eds) Systematics of the Green Algae, pp. 29–72, Academic Press, London (1984).Google Scholar
  33. 33.
    Monod C, Goldschmidt-Clermont M, Rochaix J-D: Accumulation of chloroplast psbB RNA requires a nuclear factor in Chlamydomonas reinhardtii. Mol Gen Genet 231: 449–459 (1992).CrossRefPubMedGoogle Scholar
  34. 34.
    Ohyama K, Fukuzawa H, Kohchi T, Shirai H, Sano T, Sano S, Umesono K, Shiki Y, Takeuchi M, Chang Z, Aota S, Inokuchi H, Ozeki H: Chloroplast gene organization deduced from complete sequence of liverwort Marchantia polymorpha. Nature 322: 572–574 (1986).Google Scholar
  35. 35.
    O'Neill GP, Schön A, Chow H, Chen M-W, Kim Y-C, Söll D: Sequence of tRNAGlu and its genes from the chloroplast genome of Chlamydomonas reinhardtii. Nucl Acids Res 18: 5893 (1990).PubMedGoogle Scholar
  36. 36.
    Palmer JD: Plastid chromosomes: structure and evolution. In: Bogorad L, Vasil IK (eds) Cell Culture and Somatic Cell Genetics of Plants, vol 7a: The Molecular Biology of Plastids, pp. 5–53, Academic Press, San Diego (1991).Google Scholar
  37. 37.
    Reith M, Munholland J: A high-resolution gene map of the chloroplast genome of the red alga Porphyra purpurea. Plant Cell 5: 465–475 (1993).CrossRefPubMedGoogle Scholar
  38. 38.
    Richard M, Bellemare G: Nucleotide sequence of Chlamydomonas moewusii chloroplastic tRNA-Thr. Nucl Acids Res 18: 3061 (1990).Google Scholar
  39. 39.
    Robertson D, Boynton JE, Gillham NW: Cotranscription of the wild-type chloroplast atpE gene encoding the CF1/CF0 epsilon subunit with the 3′ half of the rps7 gene in Chlamydomonas reinhardtii and characterization of frameshift mutations in atpE. Mol Gen Genet 221: 155–163 (1990).CrossRefPubMedGoogle Scholar
  40. 40.
    Rochaix J-D: Post-transcriptional steps in the expression of chloroplast genes. Annu Rev Cell Biol 8: 1–28 (1992).PubMedGoogle Scholar
  41. 41.
    Rochaix J-D, Kuchka M, Mayfield S, Schirmer-Rahire M, Girard-Bascou J, Bennoun P: Nuclear and chloroplast mutations affect the synthesis or stability of the chloroplast psbC gene product in Chlamydomonas reinhardtii. EMBO J 8: 1013–1021 (1989).PubMedGoogle Scholar
  42. 42.
    Sakamoto W, Kindle KL, Stern DB: In vivo analysis of Chlamydomonas chloroplast petD gene expression using stable transformation of β-glucuronidase translational fusions. Proc Natl Acad Sci USA 90: 497–501 (1993).PubMedGoogle Scholar
  43. 43.
    Schlösser UG: Species-specific sporangium autolysins (cell-wall-dissolving enzymes) in the genus Chlamydomonas. In: Irvine DEG, John DM (eds) Systematics of the Green Algae, pp. 409–418. Academic Press, London (1984).Google Scholar
  44. 44.
    Schmidt RJ, Hosler JP, Gillham NW, Boynton JE: Biogenesis and evolution of chloroplast ribosomes: cooperation of nuclear and chloroplast genes. In: Steinbeck KE, Bonitz S, Arntzen CJ, Bogorad L (eds) Molecular Biology of the Photosynthetic Apparatus, pp. 417–427, Cold Spring Harbor Laboratory, Cold Spring Harbor, NY (1985).Google Scholar
  45. 45.
    Shinozaki N, 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
  46. 46.
    Silk GW, Dela Cruz F, Wu M: Nucleotide sequence of the chloroplast gene for the 4 kD K polypeptide of photosystem II (psbK) and the psbK-tufA intergenic region of Chlamydomonas reinhardtii. Nucl Acids Res 18: 4930 (1990).PubMedGoogle Scholar
  47. 47.
    Siemeister DA, Buchholz C, Hachtel W: Genes for the ribosomal proteins are retained on the 73 kb DNA from Astasia longa that resembles Euglena chloroplast DNA. Curr Genet 18: 457–464 (1990).CrossRefPubMedGoogle Scholar
  48. 48.
    Sprinzl M, Hartmann T, Weber J, Blank J, Zeidler R: Compilation of tRNA sequences and sequences of tRNA genes. Nucl Acids Res 17 (suppl): r1-r172 (1989).Google Scholar
  49. 49.
    Takahashi Y, Goldschmidt-Clermont M, Soen S-Y, Franzén LG, Rochaix J-D: Directed chloroplast transformation in Chlamydomonas reinhardtii: insertional inactivation of the psaC gene encoding the iron sulfur protein destabilizes photosystem I. EMBO J 10: 2033–2040 (1991).PubMedGoogle Scholar
  50. 50.
    Turmel M, Bellemare G, Lemieux C: Physical mapping of differences between the chloroplast DNAs of the interfertile algae Chlamydomonas eugametos and Chlamydomonas moewusii. Curr Genet 11: 543–552 (1987).Google Scholar
  51. 51.
    Turmel M, Lemieux B, Lemieux C: The chloroplast genome of the green alga Chlamydomonas moewusii: localization of protein-coding genes and transcriptionally active regions. Mol Gen Genet 214: 412–419 (1988).CrossRefPubMedGoogle Scholar
  52. 52.
    Turmel M, Boulanger J, Lemieux C: Two group I introns with long open reading frames in the chloroplast psbA gene of Chlamydomonas moewusii. Nucl Acids Res 17: 3875–3887 (1989).PubMedGoogle Scholar
  53. 53.
    Turmel M, Boulanger J, Schnare MN, Gray MW, Lemieux C: Six group I introns and three internal transcribed spacers in the chloroplast large subunit ribosomal RNA gene of the green alga Chlamydomonas eugametos. J Mol Biol 218: 293–311 (1991).CrossRefPubMedGoogle Scholar
  54. 54.
    Turmel M, Gutell RR, Mercier J-P, Otis C, Lemieux C: Analysis of the chloroplast large subunit ribosomal RNA gene from 17 Chlamydomonas taxa: three internal transcribed spacers and 12 group I intron insertion sites. J Mol Biol 232, 446–467 (1993).CrossRefPubMedGoogle Scholar
  55. 55.
    Turmel M, Mercier J-P, Côté M-J: Group I introns interrupt the chloroplast psaB and psbC and the mitochondrial rrnL gene in Chlamydomonas. Nucl Acids Res 21: 5242–5250 (1993).PubMedGoogle Scholar
  56. 56.
    Vallet J-M, Rahire M, Rochaix J-D: Localization and sequence analysis of chloroplast DNA sequences of Chlamydomonas reinhardtii that promote autonomous replication in yeast. EMBO J 3: 415–421 (1984).Google Scholar
  57. 57.
    Weeks DP: Chlamydomonas: an increasingly powerful model plant cell system. Plant Cell 4: 871–878 (1992).CrossRefGoogle Scholar
  58. 58.
    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).CrossRefPubMedGoogle Scholar
  59. 59.
    Yan RCA, Dove M, Seligy VL, Lemieux C, Turmel M, Narang SA: Complete nucleotide sequence and mRNA-mapping of the large subunit of ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco) from Chlamydomonas moewusii. Gene 50: 259–270 (1986).CrossRefPubMedGoogle Scholar
  60. 60.
    Yu W, Spreitzer RJ: Sequences of the trnR-ACG and petD that contain a tRNA-like element within the chloroplast genome of Chlamydomonas reinhardtii. Nucl Acids Res 19: 957 (1992).Google Scholar
  61. 61.
    Yu W, Zhang D, Spreitzer RJ: Sequences of the Chlamydomonas reinhardtii chloroplast genes encoding tRNASer and ribosomal protein L20. Plant Physiol 100: 1079–1080 (1992).Google Scholar
  62. 62.
    Zhang D, Spreitzer RJ: Nucleotide sequences of the Chlamydomonas reinhardtii chloroplast genes for tryptophan and glycine transfer RNAs. Nucl Acids Res 17: 8873 (1989).PubMedGoogle Scholar

Copyright information

© Kluwer Academic Publishers 1994

Authors and Affiliations

  • Eric Boudreau
    • 1
  • Christian Otis
    • 1
  • Monique Turmel
    • 1
  1. 1.Département de biochimie, Faculté des sciences et de génieUniversité LavalQuébecCanada

Personalised recommendations