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The chloroplast genome arrangement ofLobelia thuliniana (Lobeliaceae): Expansion of the inverted repeat in an ancestor of theCampanulales

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Abstract

A clone-bank ofSac I restriction fragments was constructed from the chloroplast DNA (cpDNA) ofLobelia thuliniana E. B. Knox (Lobeliaceae). These cloned fragments and a set of 106 clones spanning the tobacco chloroplast genome were used as probes to determine the cpDNA restriction fragment arrangement forSac I and six other restriction enzymes (BamH I,EcoR V,Hind III,Nci I,Pst I, andXho I) and the chloroplast genome arrangement ofL. thuliniana relative to tobacco, which has been fully sequenced and is collinear with the hypothesized ancestral genome arrangement of angiosperms. The results confirm and refine our previous understanding of the chloroplast genome arrangement in the large single-copy region (LSC) and reveal (1) a roughly 11 kilobase (kb) expansion of the inverted repeat (IR) into the small single-copy region (SSC) and (2) apparent sequence divergence of the DNA segment inL. thuliniana that corresponds to ORF1901 in tobacco. The expansion of the IR into the SSC is present in all other examined members ofLobeliaceae, Cyphiaceae, andCampanulaceae, which indicates that the IR expansion was an early event in the cpDNA evolution of theCampanulales. The IR expansion into the SSC was not present inSphenoclea, which additionally supports exclusion of this genus from theCampanulaceae.

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References

  • Bruneau, A., Doyle, J. J., Palmer, J. D., 1990: A chloroplast DNA inversion as a subtribal character in thePhaseoleae (Leguminosae). — Syst. Bot.15: 378–386.

    Google Scholar 

  • Chase, M. W., Soltis, D. E., Olmstead, R. G., Morgan, D., Les, D. H., Mishler, B. D., Duvall, M. R., Price, R. A., Hills, H. G., Qiu, Y.-L., Kron, K. A., Rettig, J. H., Conti, E., Palmer, J. D., Manhart, J. R., Sytsma, K. J., Michaels, H. J., Kress, W. J., Karol, K. G., Clark, W. D., Hedrén, M., Gaut, B. S., Jansen, R. K., Kim, K.-J., Wimpee, C. F., Smith, J. F., Furnier, G. R., Strauss, S. H., Xiang, Q.-Y., Plunkett, G. M., Soltis, P. S., Swensen, S. M., Williams, S. E., Gadek, P. A., Quinn, C. J., Eguiarte, L. E., Golenberg, E., Learn, G. H., Jr.,Graham, S. W., Barrett, S. C. H., Dayanandan, S., Albert, V. A., 1993: Phylogenetics of seed plants: an analysis of nucleotide sequences from the plastid generbcL. — Ann. Missouri Bot. Gard.80: 528–580.

    Google Scholar 

  • Cosner, M. E., 1993: Phylogenetic and molecular evolutionary studies of chloroplast DNA variation in theCampanulaceae. — Ph.D. Thesis, The Ohio State University, Columbus.

    Google Scholar 

  • —, 1994: Phylogenetic relationships in theCampanulaceae based onrbcL sequences. — Pl. Syst. Evol.190: 79–95.

    Google Scholar 

  • —, 1997: The highly rearranged chloroplast genome ofTrachelium caeruleum (Campanulaceae): multiple inversions, inverted repeat expansion and contraction, transposition, insertions/deletions, and several repeat families. — Curr. Genet.31: 419–429.

    Google Scholar 

  • Downie, S. R., Palmer, J. D., 1992a: Use of chloroplast DNA rearrangements in reconstructing plant phylogeny. — InSoltis, P. S., Soltis, D. E., Doyle, J. J., (Eds): Molecular systematics of plants, pp. 14–35. — New York: Chapman & Hall.

    Google Scholar 

  • —, 1992b: Restriction site mapping of the chloroplast DNA inverted repeat: a molecular phylogeny of theAsteridae. — Ann. Missouri Bot. Gard.79: 266–283.

    Google Scholar 

  • —, 1994: A chloroplast DNA phylogeny of theCaryophyllales based on structural and inverted repeat restriction site variation. — Syst. Bot.19: 236–252.

    Google Scholar 

  • Doyle, J. J., Davis, J. I., Soreng, R. J., Garvin, D., Anderson, M. J., 1992: Chloroplast DNA inversions and the origin of the grass family (Poaceae). — Proc. Natl. Acad. Sci. USA89: 7722–7726.

    Google Scholar 

  • —, 1995: Multiple independent losses of two genes and one intron from legume chloroplast genomes. — Syst. Bot.20: 272–294.

    Google Scholar 

  • Goulding, S. E., Olmstead, R. G., Morden, C. W., Wolfe, K. H., 1996: Ebb and flow of the chloroplast inverted repeat. — Molec. Gen. Genet.252: 195–206.

    Google Scholar 

  • Gustafsson, M. H. G., 1996: Phylogenetic hypotheses forAsteraceae relationships. — InHind, D. J. H., Beentje, H. J., (Eds):Compositae: systematics. Proceedings of the InternationalCompositae Conference, Kew, 1994,1, pp. 9–19. — Richmond: Royal Botanic Gardens, Kew.

    Google Scholar 

  • —, 1996: Phylogeny of theAsterales sensu lato based onrbcL sequences with particular reference to theGoodeniaceae. — Pl. Syst. Evol.199: 217–242.

    Google Scholar 

  • Herdenberger, F., Pillay, D. T. N., Steinmetz, A., 1990: Sequence of thetrnH gene and the inverted repeat structure deletion site of the broad bean chloroplast genome. — Nucl. Acids Res.18: 1297.

    Google Scholar 

  • 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., Hirai, A., Shinozaki, K., Sugiura, M., 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. — Molec. Gen. Genet.217: 185–194.

    Google Scholar 

  • Hoot, S. B., Palmer, J. D., 1994: Structural rearrangements, including parallel inversions, within the chloroplast genome ofAnemone and related genera. — J. Molec. Evol.38: 274–281.

    Google Scholar 

  • Jansen, R. K., Palmer, J. D., 1987: A chloroplast DNA inversion marks an ancient evolutionary split in the sunflower family (Asteraceae). — Proc. Natl. Acad. Sci. USA84: 5818–5822.

    Google Scholar 

  • Johansson, J. T., Jansen, R. K., 1993: Chloroplast DNA variation and phylogeny of theRanunculaceae. — Pl. Syst. Evol.187: 29–49.

    Google Scholar 

  • Katayama, H., Ogihara, Y., 1996: Phylogenetic affinities of the grasses to other monocots as revealed by molecular analysis of chloroplast DNA. — Curr. Genet.29: 572–581.

    Google Scholar 

  • Kim, Y.-D., Jansen, R. K., 1994: Characterization and phylogenetic distribution of a chloroplast DNA rearrangement in theBerberidaceae. — Pl. Syst. Evol.193: 107–114.

    Google Scholar 

  • Kishima, Y., Ogura, K., Mizukami, K., Mikami, T., Adachi, T., 1995: Chloroplast DNA analysis in buckwheat species: phylogenetic relationships, origin of the reproductive systems and extended inverted repeats. — Pl. Sci.108: 173–179.

    Google Scholar 

  • Knox, E. B., Palmer, J. D., 1998: Chloroplast DNA evidence on the origin and radiation of the giant lobelias in eastern Africa. — Syst. Bot.23 (in press).

  • —, 1993: Chloroplast genome rearrangements and the evolution of giant lobelias from herbaceous ancestors. — Molec. Biol. Evol.10: 414–430.

    Google Scholar 

  • Konishi, T., Sasaki, Y., 1994: Compartmentalization of two forms of acetyl-CoA carboxylase in plants and the origin of their tolerance towards herbicides. — Proc. Natl. Acad. Sci. USA91: 3598–3601.

    Google Scholar 

  • Lammers, T. G., 1992: Circumscription and phylogeny of theCampanulales. — Ann. Missouri Bot. Gard.79: 388–413.

    Google Scholar 

  • —, 1998:Nemacladoideae, a new subfamily ofCampanulaceae. — Novon8: 36–37.

    Google Scholar 

  • Lavin, M., Doyle, J. J., Palmer, J. D., 1990: Evolutionary significance of the loss of the chloroplast-DNA inverted repeat in theLeguminosae subfamilyPapilionoideae. — Evolution44: 390–402.

    Google Scholar 

  • Lidholm, J., Szmidt, A. E., Hällgren, J.-E., Gustafsson, P., 1988: The chloroplast genomes of conifers lack one of the rRNA-encoding inverted repeats. — Molec. Gen. Genet.212: 6–10.

    Google Scholar 

  • Maier, R. M., Neckermann, K., Igloi, G. L., Kössel, H., 1995: Complete sequence of the maize chloroplast genome: gene content, hotspots of divergence and fine tuning of genetic information by transcript editing. — J. Molec. Biol.251: 614–628.

    Google Scholar 

  • Milligan, B. G., Hampton, J. N., Palmer, J. D., 1989: Dispersed repeats and structural reorganization in subclover chloroplast DNA. — Molec. Biol. Evol.6: 355–368.

    Google Scholar 

  • O'Kane, S. L., 1995: Clone bank and physical map ofLopezia miniata Lag. ex DC. ssp.miniata (Onagraceae) chloroplast DNA. — Biochem. Syst. Ecol.25: 507–516.

    Google Scholar 

  • Olmstead, R. G., Sweere, J. A., Wolfe, K. H., 1993: Ninety extra nucleotides inndhF gene of tobacco chloroplast DNA: a summary of revisions to the 1986 genome sequence. — Pl. Molec. Biol.22: 1191–1193.

    Google Scholar 

  • Palmer, J. D., 1983: Chloroplast DNA exists in two orientations. — Nature301: 92–93.

    Google Scholar 

  • —, 1985: Comparative organization of chloroplast genomes. — Annual Rev. Genet.19: 325–354.

    Google Scholar 

  • —, 1986: Isolation and structural analysis of chloroplast DNA. — Meth. Enzymol.118: 167–186.

    Google Scholar 

  • —, 1991: Plastid chromosomes: structure and evolution. — InBogorad, L., Vasil, I. K., (Eds): The molecular biology of plastids. — InVasil, I. K., (Ed.): Cell culture and somatic genetics of plants,7A, pp. 5–53. — New York: Academic Press.

    Google Scholar 

  • —, 1986: Conservation of chloroplast genome structure among vascular plants. — Curr. Genet.10: 823–833.

    Google Scholar 

  • —, 1981: Rearrangements in the chloroplast genomes of mung bean and pea. — Proc. Natl. Acad. Sci. USA78: 5533–5537.

    Google Scholar 

  • —, 1987: Unusual structure of geranium chloroplast DNA: a triple-sized inverted repeat, extensive gene duplications, multiple inversions, and two repeat families. — Proc. Natl. Acad. Sci. USA84: 769–773.

    Google Scholar 

  • —, 1988a: Chloroplast DNA variation and plant phylogeny. — Ann. Missouri Bot. Gard.75: 1180–1206.

    Google Scholar 

  • —, 1988b: Chloroplast DNA evolution among legumes: loss of a large inverted repeat occurred prior to other sequence rearrangements. — Curr. Genet.11: 275–286.

    Google Scholar 

  • —, 1994: Chloroplast and mitochondrial DNAs ofArabidopsis thaliana: conventional genomes in an unconventional plant. — InMeyerowitz, E. M., Somerville, C. R., (Eds):Arabidopsis, pp. 37–62. — Plainview, New York: Cold Spring Harbor Laboratory Press.

    Google Scholar 

  • Raubeson, L. A., Jansen, R. K., 1992a: A rare chloroplast-DNA structural mutation is shared by all conifers. — Biochem. Syst. Ecol.20: 17–24.

    Google Scholar 

  • —, 1992b: Chloroplast DNA evidence on the ancient evolutionary split in vascular land plants. — Science255: 1697–1699.

    Google Scholar 

  • Sasaki, Y., Nagano, Y., Morioka, S., Ishikawa, H., Matsuno, R., 1989: A chloroplast gene encoding a protein with one zinc finger. — Nucl. Acids Res.17: 6217–6228.

    Google Scholar 

  • Shen, G. F., Chen, K., Wu, M., Kung, S. D., 1982:Nicotiana chloroplast genome IV.N. acuminata has larger inverted repeats and genome size. — Molec. Gen. Genet.187: 12–18.

    Google Scholar 

  • 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., Thodoh, N., Shimada, H., Sugiura, M., 1986: The complete nucleotide sequence of the tobacco chloroplast genome: its gene organization and expression. — EMBO J.5: 2043–2049.

    Google Scholar 

  • Smith, A. G., Wilson, R. M., Kaethner, T. M., Willey, D. L., Gray, J. C., 1991: Pea chloroplast genes encoding a 4 kDa polypeptide of photosystem I and a putative enzyme of C1 metabolism. — Curr. Genet.19: 403–410.

    Google Scholar 

  • Stein, D. B., Conant, D. S., Ahearn, M. E., Jordan, E. T., Kirch, S. A., Hasebe, M., Iwatsuki, K., Tan, M. K., Thomson, J. A., 1992: Structural rearrangements of the chloroplast genome provide an important phylogenetic link in ferns. — Proc. Natl. Acad. Sci. USA89: 1856–1860.

    Google Scholar 

  • Strauss, S. H., Palmer, J. D., Howe, G. T., Doerksen, A. H., 1988: Chloroplast genomes of two conifers lack a large inverted repeat and are extensively rearranged. — Proc. Natl. Acad. Sci. USA85: 3898–3902.

    Google Scholar 

  • Tsudzuki, J., Nakashima, K., Tsudzuki, T., Hiratsuka, J., Shibata, M., Wakasugi, T., Sugiura, M., 1992: Chloroplast DNA of black pine retains a residual inverted repeat lacking rRNA genes: nucleotide sequences oftrnQ,trnK,psbA,trnI andtrnH and the absence ofrps16. — Molec. Gen. Genet.232: 206–214.

    Google Scholar 

  • Wakasugi, T., Tsudzuki, J., Ito, S., Nakashima, K., Tsudzuki, T., Sugiura, M., 1994: Loss of allndh genes as determined by sequencing the entire chloroplast genome of the black pinePinus thunbergii. — Proc. Natl. Acad. Sci. USA91: 9794–9798.

    Google Scholar 

  • Wimmer, F. E., 1943:Campanulaceae Lobelioideae. I. Teil. — InStubbe, H., Noack, K. I., (Eds): Das Pflanzenreich. IV, 267 b (106. Heft), pp. i-viii + 1-260. — Leipzig: Engelmann.

    Google Scholar 

  • —, 1953:Campanulaceae Lobelioideae. II. Teil. — InStubbe, H., Noack, K. I., (Eds): Das Pflanzenreich. IV, 267 b (107. Heft), pp. i-viii + 261-813. — Berlin: Akademie-Verlag.

    Google Scholar 

  • —, 1968:Campanulaceae — Lobelioideae Supplementum etCampanulaceae — Cyphioideae. — InStubbe, H., (Ed.): Das Pflanzenreich IV, 267 c (108. Heft), pp. i-x + 815-1024. — Berlin: Akademie-Verlag.

    Google Scholar 

  • Wolfe, K. H., 1988: The site of deletion of the inverted repeat in pea chloroplast DNA contains duplicated gene fragments. — Curr. Genet.13: 97–99.

    Google Scholar 

  • —, 1987: Rates of nucleotide substitution vary greatly among mitochondrial, chloroplast, and nuclear DNAs. — Proc. Natl. Acad. Sci. USA84: 9054–9058.

    Google Scholar 

  • —, 1992: Function and evolution of a minimal plastid genome from a nonphotosynthetic parasitic plant. — Proc. Natl. Acad. Sci. USA89: 10648–10652.

    Google Scholar 

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  1. Department of Biological Sciences, Rutgers University, 101 Warren Street, 07102, Newark, New Jersey, USA

    Eric B. Knox

  2. Department of Biology, Jordan Hall Indiana University, 47405, Bloomington, Indiana, USA

    Jeffrey D. Palmer

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  1. Eric B. Knox
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Knox, E.B., Palmer, J.D. The chloroplast genome arrangement ofLobelia thuliniana (Lobeliaceae): Expansion of the inverted repeat in an ancestor of theCampanulales . Pl Syst Evol 214, 49–64 (1999). https://doi.org/10.1007/BF00985731

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