Widespread Occurrence of Small Inversions in the Chloroplast Genomes of Land Plants

  • Kim, Ki-Joong (School of Life Sciences and Biotechnology, Korea University) ;
  • Lee, Hae-Lim (School of Life Sciences and Biotechnology, Korea University)
  • Received : 2004.09.30
  • Accepted : 2004.12.14
  • Published : 2005.02.28

Abstract

Large inversions are well characterized in the chloroplast genomes of land plants. In contrast, reports of small inversions are rare and involve limited plant groups. In this study, we report the widespread occurrence of small inversions ranging from 5 to 50 bp in fully and partially sequenced chloroplast genomes of both monocots and dicots. We found that small inversions were much more common than large inversions. The small inversions were scattered over the chloroplast genome including the IR, SSC, and LSC regions. Several small inversions were uncovered in chloroplast genomes even though they shared the same overall gene order. The majority of these small inversions were located within 100 bp downstream of the 3' ends of genes. All had inverted repeat sequences, ranging from 11 to 24 bp, at their ends. Such small inversions form stem-loop hairpin structures that usually have the function of stabilizing the corresponding mRNA molecules. Intra-molecular recombination between the inverted sequences in the stem-forming regions are responsible for generating flip-flop orientations of the loops. The presence of two different orientations of the stem-loop in the trnL-F noncoding region of a single species of Jasminum elegans suggests that a short inversion can be generated within a short period of time. Small inversions of non-coding sequences may influence sequence alignment and character interpretation in phylogeny reconstructions, as shown in nine species of Jasminum. Many small inversions may have been generated by parallel or back mutation events during chloroplast genome evolution. Our data indicate that caution is needed when using chloroplast non-coding sequences for phylogenetic analysis.

Keywords

Acknowledgement

Supported by : Korea University, Korea Science and Engineering Foundation

References

  1. Asano, T., Tsudzuki, T., Takahashi, S., Shimada, H., and Kadowaki, K. (2004) Complete nucleotide sequence of the surgacane (Saccharum officinarum) chloroplast genome: a comparative analysis of four monocot chloroplast genomes. DNA Res. 11, 93-.99 https://doi.org/10.1093/dnares/11.2.93
  2. Baas, P., Esser, P. M., van der Western, M.E.T., and Zandee, M. (1988) Wood anatomy of the Oleaceae. IAWA Bull. 9, 103-.182
  3. Doyle, J. J. and Doyle, J. L. (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem. Bull. 19, 11-.15
  4. Doyle, J. J., Davis, J. I., Soreng, R. J., Garvin, D., and Anderson, M. J. (1992) Chloroplast DNA inversions and the origin of the grass family (Poaceae). Proc. Natl. Acad. Sci. USA 89, 7722-.7726
  5. Doyle, J. J., Doyle, J. L., Ballenger, J. A., and Palmer, J. D. (1996) The distribution and phylogenetic significance of a 50-kb chloroplast DNA inversion in the flowering plant family Leguminosae. Mol. Phylog. Evol. 5, 429-.438 https://doi.org/10.1006/mpev.1996.0038
  6. Graham, S. W. and Olmstead, R. G. (2000) Evolutionary significance of an unusual chloroplast DNA inversion found in two basal angiosperm lineages. Curr. Genet. 37, 183-.188 https://doi.org/10.1007/s002940050517
  7. Hiratsuka, J., Shimada, H., Whittier, R., Ishibashi, T., Sakamota, M., et al. (1989) 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 https://doi.org/10.1007/BF02464880
  8. Howe, C. J., Barker, R. F., Bowman, C. M., and Dyer, T. A. (1988) Common features of three inversions in wheat chloroplast DNA. Curr. Genet. 13, 343-.349 https://doi.org/10.1007/BF00424430
  9. Hupfer, H., Swiatek, M., Hornung, S., Herrmann, R. G., Maier, Ki-Joong Kim & Hae-Lim Lee 113 R. M., et al. (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
  10. Jansen, K. R. and Palmer, J. D. (1987) A chloroplast DNA inversion marks an ancient evolutionary split in the sunflower family (Asteraceae). Proc. Natl. Acad. Sci. USA 84, 5818-.5822
  11. Kanno, A. and Hirai, A. (1993) A transcription map of the chloroplast genome from rice (Oryza sativa). Curr. Genet. 23, 166-.174 https://doi.org/10.1007/BF00352017
  12. Kato, T., Kaneko, T., Sato, S., Nakamura, Y., and Tabata, S. (2000) Complete structure of the chloroplast genome of a legume, Lotus japonicus. DNA Res. 7, 323-.330 https://doi.org/10.1093/dnares/7.6.323
  13. Kelchner, S. A. and Wendel, J. F. (1996) Hairpins create minute inversions in non-coding regions of chloroplast DNA. Curr. Genet. 30, 259-.262 https://doi.org/10.1007/s002940050130
  14. Kim, K.-J. and Lee, H.-L. (2004) Complete chloroplast genome sequences from Korean ginseng (Panax schinseng Nees) and comparative analysis of sequence evolution among 17 vascular plants. DNA Res. 11, 247-.261 https://doi.org/10.1093/dnares/11.4.247
  15. Kim, K.-J. and Jansen, R. K. (1994) Comparisions of phylogenetic hypotheses among different data sets in dwarf dandelions (Krigia): additional information from internal transcribed spacer sequences of nuclear ribosomal DNA. Pl. Syst. Evol. 190, 157-.185 https://doi.org/10.1007/BF00986191
  16. Kimura, M. (1980) A simple model for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J. Mol. Evol. 16, 111-.120 https://doi.org/10.1007/BF01731581
  17. Kumar, S., Tamura, K., Jakobsen, I. B., and Nei, M. (2001) MEGA2: molecular evolutionary genetics analysis software. Bioinformatics 17, 1244-.1245 https://doi.org/10.1093/bioinformatics/17.12.1244
  18. Kurtz, S., Choudhuri, J. V., Ohlebusch, E., Schleiermacher, C., Stoye, J., et al. (2001) REPuter: the manifold applications of repeat analysis on a genomic scale. Nucleic Acids Res. 29, 4633-.4642 https://doi.org/10.1093/nar/29.22.4633
  19. Lee, S. S., Jeong W. J., Bae J. M., Bang J. W., Liu J. R., et al. (2004) Characterization of the plastid-encoded carboxyltransferase subunit (accD) gene of potato. Mol. Cells 17, 423-.429
  20. Maier, R. M., Neckermann, K., Igloi, G. L., and Kossel, 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 https://doi.org/10.1006/jmbi.1995.0460
  21. Mast, A. R., Feller, D. M., Kelso, S., and Conti, E. (2004) Buzzpollinated Dodecatheon originated from within the heterostylous Primula subgenus Auriculastrum (Primulaceae): a seven-region cpDNA phylogeny and its implications for floral evolution. Am. J. Bot. 91, 926-.942 https://doi.org/10.3732/ajb.91.12.2004
  22. Milligan, B. G., Hampton, J. N., and Palmer, J. D. (1989) Dispersed repeats and structural reorganization in subclover chloroplast DNA. Mol. Biol. Evol. 6, 355-.368
  23. Ogihara, Y., Isono, K., Kojima, T., Endo, A., Hanaoka, M., et al. (2002) Structural features of a wheat plastome as revealed by complete sequencing of chloroplast DNA. Mol. Genet. Genomics 266, 740-.746 https://doi.org/10.1007/s00438-001-0606-9
  24. Ogihara, Y., Terachi, T., and Sasakuma, T. (1988) Intramolecular recombination of chloroplast genome mediated by short direct-repeat sequences in wheat species. Proc. Natl. Acad. Sci. USA 85, 8573-.8577
  25. Palmer, J. D. (1986) Isolation and structural analysis of chloroplast DNA; in Methods in Enzymology, Vol. 118, Weissbach, A. and Weissbach, H. (eds.), pp. 167-.186, Academic Press, New York
  26. Palmer, J. D. (1990) Contrasting modes and tempos of genome evolution in land plant organelles. Trends Genet. 6, 115-.120 https://doi.org/10.1016/0168-9525(90)90125-P
  27. Palmer, J. D. (1991) Plastid chromosomes: structure and evolution;in Cell Culture and Somatic Cell Genetics in Plants, Vol. 7A, The Molecular Biology of Plastids, Vasil, I. K. and Bogorad, L. (eds.), pp. 5-.53, Academic Press, San Diego
  28. Raubeson, L. A. and Jansen R. K. (1992) Chloroplast DNA evidence on the ancient evolutionary split in vascular land plants. Science 255, 1697-.1699 https://doi.org/10.1126/science.255.5052.1697
  29. Rohwer, J. G. (1994) Seed characters in Jasminum (Oleaceae):unexpected support for De Candolle's sections. Bot. Jahrb. Syst. 116, 299-.319
  30. Schmitz-Linneweber, C., Regel, R., Du, T. G., Hupfer, H., Herrmann, R. G., et al. (2002) The Plastid Chromosome of Atropa belladonna and its comparison with that of Nicotiana tabacum: the role of RNA editing in generating divergence in the process of plant speciation. Mol. Biol. Evol. 19, 1602-.1612
  31. Shimada, H. and Sugiura, M. (1989) Pseudogenes and short repeated sequences in the rice chloroplast genome. Curr. Genet. 16, 293-.301 https://doi.org/10.1007/BF00422116
  32. Shinozaki, K., Hayashida, N., and Sugiura, M. (1988) Nicotiana chloroplast genes for components of the photosynthetic apparatus. Photosynthesis Res. 18, 7-.31 https://doi.org/10.1007/BF00042978
  33. Shinozaki, K., Ohme, M., Tanaka, M., Wakasugi, T., Hayashida, N., et al. (1986) The complete nucleotide sequence of tobacco chloroplast genome: its gene organization and expression. EMBO J. 5, 2043-.2049
  34. Sugiura, M. (1989) The chloroplast chromosomes in land plants. Annu. Rev. Cell Biol. 5, 51-.70 https://doi.org/10.1146/annurev.cb.05.110189.000411
  35. Swofford, D. L. (2002) PAUP 4.0. Computer program and documentation. Sinauer Asso., Suderland Massachusetts
  36. Taberlet, P., Gielly, L., Pautou, G., and Bouvet, J. (1991) Universal primers for amplification of three non-coding regions of chloroplast DNA. Pl. Mol. Biol. 17, 1105-.1109 https://doi.org/10.1007/BF00037152
  37. Thompson, J. D., Gibson, T. J., Plewniak, F., Jeanmougin, F., and Higgins, D. G. (1997) The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 24, 4876-.4882
  38. Wakasugi, T., Tsudzuki, J., Ito, S., Nakashima, K., Tsudzuki, T., et al. (1994) Loss of all ndh genes as determined by sequencing the entire chloroplast genome of the black pine Pinus thunbergii. Proc. Natl. Acad. Sci. USA 91, 9794-.9798
  39. Zuker, M. (2003) Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res. 31, 3406-.3415 https://doi.org/10.1093/nar/gkg595