Plant Molecular Biology

, Volume 45, Issue 3, pp 307–315 | Cite as

The plastid chromosome of spinach (Spinacia oleracea): complete nucleotide sequence and gene organization

  • Christian Schmitz-Linneweber
  • Rainer M. Maier
  • Jean-Pierre Alcaraz
  • Annick Cottet
  • Reinhold G. Herrmann
  • Regis Mache

Abstract

The chloroplast chromosome of spinach (Spinacia oleracea) is a double-stranded circular DNA molecule of 150 725 nucleotide pairs. A comparison of this chromosome with those of the three other autotrophic dicotyledons for which complete DNA sequences of plastid chromosomes are available confirms a conserved overall structure. Three classes of open reading frames were distinguished: (1) genes of known function which include 108 unique loci, (2) three hypothetical chloroplast reading frames (ycfs) that are highly conserved interspecifically, and (3) species-specific or rapidly diverging 'open reading frames'. A detailed transcript study of one of the latter (ycf15) shows that these loci may be transcribed, but do not constitute protein-coding genes.

chloroplast open reading frames plastid chromosome spinach Spinacia oleracea,ycf15 

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References

  1. Altschul, F.A., Gish, W., Miller, W., Myers, E.W. and Lipman G.J. 1990. Basic local alignment search tool. J. Mol. Biol. 215: 403–410.Google Scholar
  2. Altschul, F.A., Madden, T.L., Schäffer, A.A., Zhang, J., Miller, W. and Lipman, D.J. 1997. Gapped Blast and Psi-Blast: a new generation of protein database search programs. Nucl. Acids Res. 25: 3389–3402.Google Scholar
  3. Boer, P.H. and Gray M.W. 1988. Genes encoding a subunit of the respiratory NADH dehydrogenase (ND1) and a reverse transcriptase-like protein (rtl) are linked to ribosomal RNA gene pieces in Chlamydomonas rheinhardii. EMBO J. 7: 3501–3508.Google Scholar
  4. Burger, G., Saint-Louis, D., Gray, M.W. and Lang, B.F. 1999. Complete sequence of the mitochondrial DNA of red alga Porphyra purpurea. Cyanobacterial introns and shared ancestry of red and green algae. Plant Cell 11: 1675–1694.Google Scholar
  5. Butterfass T. 1979. Patterns of Chloroplast Reproduction. Cell Biology Monographs, vol. 6, Springer-Verlag, Wien/New York.Google Scholar
  6. Downie, S.R., Olmstead, R.G., Zurawski, G., Soltis, D.E., Soltis, P.S., Watson, J.C. and Palmer J.D. 1991. Six independent losses of the chloroplast DNA rpl2 intron in dicotyledons: molecular and phylogenetic implications. Evolution 45: 1245–1259.Google Scholar
  7. Drescher, A., Ruf, S., Calsa, T., Carrer, H. and Bock, R. 2000. The two largest chloroplast genome-encoded open reading frames of higher plants are essential genes. Plant J. 22: 97–104.Google Scholar
  8. Hallick, R.B. 1989. Proposals for the naming of chloroplast genes. II. Update to the nomenclature of genes for thylakoid membrane polypeptides. Plant Mol. Biol. Rep. 7: 266–275.Google Scholar
  9. Hallick, R.B. and Bottomley, W. 1983. Proposals for the naming of chloroplast genes. Plant Mol. Biol. Rep. 1: 38–43.Google Scholar
  10. Herrmann, R.G. 1982. The preparation of circular DNA from plastids. In: M. Edelman, R. Hallick and N.-H. Chua (eds.) Methods of Chloroplast Molecular Biology, Elsevier/North Holland Press, Amsterdam, pp. 254–279.Google Scholar
  11. Herrmann, R.G., Bohnert, H.J., Kowallik, K.V. and Schmitt, J.M. 1975. Size, conformation and purity of chloroplast DNA of some higher plants.Biochim. Biophys. Acta 378: 305–317.Google Scholar
  12. Herrmann, R.G., Oelmüller, R., Bichler, J., Schneiderbauer, A., Steppuhn, J., Wedel, N., Tyagi, A.K. and Westhoff, P. 1991. The thylakoid membrane of higher plants: genes, their expression and interaction. In: R.G. Herrmann and B.A. Larkins (eds.) Plant Molecular Biology 2, NATO ASI Series A: Life Sciences, vol. 212, Plenum, New York, pp. 411–427.Google Scholar
  13. Hupfer, H., Swiatek, M., Hornung, S., Herrmann, R.G., Maier, R.M., Chiu, W.-L. and Sears, B. 2000. Complete nucleotide sequence of the Oenothera elata plastid chromosome, representing plastome I of the five distinguishable Euoenothera plastomes. Mol. Gen. Genet. 263: 581–585.Google Scholar
  14. Jeanmougin, F., Thompson, J.D., Gouy, M., Higgins, D.G. and Gibson, T.J. 1998. Multiple sequence alignment with Clustal X. Trends Biochem. Sci. 23: 403–405.Google Scholar
  15. Mache, R.1990. Chloroplast ribosomal proteins and their genesaa. Plant Sci. 72: 1–12.Google Scholar
  16. Maier, R.M., Hoch, B., Zeltz, P. and Koessel, H. 1992. Internal editing of the maize chloroplast ndhA transcript restores codons for conserved amino acids. Plant Cell 4: 609–616.Google Scholar
  17. Maier, R.M., Neckermann, K., Igloi, G.L. and Koessel, H. 1995. Complete sequence of the maize chloroplast genome: gene content, hotspots of divergence and fine tuning of genetic information by transcript editing. J. Mol. Biol. 251: 614–628.Google Scholar
  18. Martin, W., Stoebe, B., Goremykin, V., Hansmann, S., Hasegawa, M. and Kowallik, K.V. 1998. Gene transfer to the nucleus and the evolution of chloroplasts. Nature 393: 162–165.Google Scholar
  19. Michel, F. and Ferat, J.L. 1995. Structure and activities of group II introns. Annu. Rev. Biochem. 64: 435–461.Google Scholar
  20. Murray, M.G. and Thompson, W.F. 1980. Rapid isolation of high molecular weight plant DNA. Nucl. Acids Res. 8: 4321–4325.Google Scholar
  21. Nimzyk, R., Schondorf, T. and Hachtel, W. 1995. In-frame length mutations associated with short tandem repeats are located in unassigned open reading frames of Oenothera chloroplast DNA. Curr. Genet. 23: 265–270.Google Scholar
  22. Rosenblum, B.B., Lee, L.G., Spurgeon, S.L., Khan, S.H., Menchen, S.M., Heiner, C.R. and Chen, S.M. 1997. New dye-labelled terminators for improved DNA sequencing patterns. Nucl. Acids Res.25: 4500–4504.Google Scholar
  23. Sanger, F., Nicklen, S. and Coulsen, A.R. 1977. DNA sequencing with chain terminating inhibitors. Proc. Natl. Acad. Sci. USA 74: 5463–5467.Google Scholar
  24. 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, B.Y., Sugita, M., Deno, H., Kamogashira, T., Yamada, K., Kusuda, J., Takaiwa, F., Kato, A., Thodo, N., Shimada, H. and Sugiura, M. 1986. The complete nucleotide sequence of the tobacco chloroplast genome: its gene organization and expression. EMBO J. 5: 2043–2049.Google Scholar
  25. Siegenthaler, P.A. and Depery, F. 1976. Influence of unsaturated fatty acids in chloroplasts. Eur. J. Biochem. 61: 573–580.Google Scholar
  26. Sijben-Muller, G., Hallick, R.B., Alt, J., Westhoff, P. and Herrmann, R.G. 1986. Spinach plastid genes coding for initiation factor IF-1, ribosomal protein S11 and RNA polymerase α-subunit. Nucl. Acids Res. 24: 1029–1044.Google Scholar
  27. Soltis, P.S., Soltis, D.E. and Chase, M.W. 1999. Angiosperm phylogeny inferred from multiple genes as a tool for comparative biology. Nature 25: 402–404.Google Scholar
  28. Stoebe, B., Martin, W. and Kowallik, K.V. 1998. Distribution and nomenclature of protein-coding genes in 12 sequenced chloroplast genomes. Plant Mol. Biol. Rep. 16: 243–255.Google Scholar
  29. Sugita, M., Svab, Z., Maliga, P. and Sugiura, M. 1997. Targeted deletion of sprA from the tobacco plastid genome indicates that the encoded small RNA is not essential for pre-16S rRNA maturation in plastids. Mol. Gen. Genet. 257: 23–27.Google Scholar
  30. Sugiura, M. 1995. The chloroplast genome. Essays Biochem. 30: 49–57.Google Scholar
  31. Tewari, K.K. 1971. Genetic autonomy of extranuclear organelles. Annu. Rev. Plant Physiol. 22: 141–168.Google Scholar
  32. Thomas, F., Massenet, O., Dorne, A.M., Briat, J.F. and Mache, R. 1988. Expression of the rpl23, rpl2 and rps19 genes in spinach chloroplasts. Nucl. Acids Res. 25: 2461–2472.Google Scholar
  33. Walker, D.A. 1971. Chloroplasts (and Grana): Aqueous (Including High Carbon Fixation Ability). Meth. Enzymol. 23: 211–220.Google Scholar
  34. Wolfe, K.H., Li, W.H. and Sharp, P.M. 1987. Rates of nucleotide substitution vary greatly among mitochondrial, chloroplast, and nuclear DNAs. Proc. Natl. Acad. Sci. USA 84: 9054–9058.Google Scholar

Copyright information

© Kluwer Academic Publishers 2001

Authors and Affiliations

  • Christian Schmitz-Linneweber
    • 1
  • Rainer M. Maier
    • 1
  • Jean-Pierre Alcaraz
    • 2
  • Annick Cottet
    • 2
  • Reinhold G. Herrmann
    • 1
  • Regis Mache
    • 2
  1. 1.Botanisches Institut der Ludwig-Maximilians-UniversitätMünchenGermany
  2. 2.Laboratoire de Génétique Moléculaire des PlantesUniversité Joseph Fourier and CNRSGrenobleFrance

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