Skip to main content
SpringerLink
Log in

Extensive Rearrangements in the Chloroplast Genome of Trachelium caeruleum Are Associated with Repeats and tRNA Genes

  • Published:
Journal of Molecular Evolution Aims and scope Submit manuscript

Abstract

Chloroplast genome organization, gene order, and content are highly conserved among land plants. We sequenced the chloroplast genome of Trachelium caeruleum L. (Campanulaceae), a member of an angiosperm family known for highly rearranged genomes. The total genome size is 162,321 bp, with an inverted repeat (IR) of 27,273 bp, large single-copy (LSC) region of 100,114 bp, and small single-copy (SSC) region of 7,661 bp. The genome encodes 112 different genes, with 17 duplicated in the IR, a tRNA gene (trnI-cau) duplicated once in the LSC region, and a protein-coding gene (psbJ) with two duplicate copies, for a total of 132 putatively intact genes. ndhK may be a pseudogene with internal stop codons, and clpP, ycf1, and ycf2 are so highly diverged that they also may be pseudogenes. ycf15, rpl23, infA, and accD are truncated and likely nonfunctional. The most conspicuous feature of the Trachelium genome is the presence of 18 internally unrearranged blocks of genes inverted or relocated within the genome relative to the ancestral gene order of angiosperm chloroplast genomes. Recombination between repeats or tRNA genes has been suggested as a mechanism of chloroplast genome rearrangements. The Trachelium chloroplast genome shares with Pelargonium and Jasminum both a higher number of repeats and larger repeated sequences in comparison to eight other angiosperm chloroplast genomes, and these are concentrated near rearrangement endpoints. Genes for tRNAs occur at many but not all inversion endpoints, so some combination of repeats and tRNA genes may have mediated these rearrangements.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Achaz G, Coissac E, Netter P, Rocha EPC (2003) Associations between inverted repeats and the structural evolution of bacterial genomes. Genetics 164:1279–1289

    PubMed  CAS  Google Scholar 

  • Bowman CM, Barker RF, Dyer TA (1988) In wheat ctDNA, segments of ribosomal-protein genes are dispersed repeats, probably conserved by nonreciprocal recombination. Curr Genet 14:127–136

    Article  PubMed  CAS  Google Scholar 

  • Bowman CM, Dyer TA (1986) The location and possible evolutionary significance of small dispersed repeats in wheat ctDNA. Curr Genet 10:931–941

    Article  CAS  Google Scholar 

  • Chang CC, Lin HC, Lin IP, Chow TY, Chen HH, Chen WH, Cheng CH, Lin CY, Lieu SM, Chang CC Chaw SM (2006) The chloroplast genome of Phalaenopsis aphrodite Orchidaceae: comparative analysis of evolutionary rate with that of grasses and its phylogenetic implications. Mol Biol Evol 23:279–291

    Article  PubMed  CAS  Google Scholar 

  • Chumley TW, Palmer JD, Mower JP, Fourcade HM, Callie PJ, Boore JL, Jansen RK (2006) The complete chloroplast genome sequence of Pelargonium × hortorum: organization and evolution of the largest and most highly rearranged chloroplast genome of land plants. Mol Biol Evol 23:2175–2190

    Article  PubMed  CAS  Google Scholar 

  • Cosner ME (1993) Phylogenetic and molecular evolutionary studies of chloroplast DNA variation in the Campanulaceae. Ph.D. thesis. The Ohio State University, Columbus

  • Cosner ME, Jansen RK, Palmer JD, Downie SR (1997) The highly rearranged chloroplast genome of Trachelium caeruleum Campanulaceae: multiple inversions, inverted repeat expansion and contraction, transposition, insertions/deletions, and several repeat families. Curr Genet 31:419–429

    Article  PubMed  CAS  Google Scholar 

  • Cosner ME, Raubeson LA, Jansen RK (2004) Chloroplast DNA rearrangements in Campanulaceae: phylogenetic utility of highly rearranged genomes. BMC Evol Biol 4:27

    Article  PubMed  CAS  Google Scholar 

  • Downie SR, Palmer JD (1992) Use of chloroplast DNA rearrangements in reconstructing plant phylogeny. In: Soltis PS, Soltis DE, Doyle JJ (eds) Molecular systematics of plants. Chapman and Hall, London, UK, pp 14–35

    Google Scholar 

  • Ewing B, Green P (1998) Base-calling of automated sequencer traces using phred. II. error probabilities. Genome Res 8:186–194

    PubMed  CAS  Google Scholar 

  • Fan WH, Woelfle MA, Mosig G (1995) Two copies of a DNA element, Wendy, in the chloroplast chromosome of Chlamydomonas-reinhardtii between rearranged gene clusters. Plant Mol Biol 29:63–80

    Article  PubMed  CAS  Google Scholar 

  • Fiebig A, Stegemann S, Bock R (2004) Rapid evolution of RNA editing sites in a small non-essential plastid gene. Nucleic Acids Res 32:3615–3622

    Article  PubMed  CAS  Google Scholar 

  • Gordon D, Abajian C, Green P (1998) Consed: a graphical tool for sequence finishing. Genome Res 8:195–202

    PubMed  CAS  Google Scholar 

  • Hipkins VD, Marshall KA, Neale DB, Rottmann WH, Strauss SH (1995) A mutation hotspot in the chloroplast genome of a conifer Douglas-fir, Pseudotsuga is caused by variability in the number of direct repeats derived from a partially duplicated transfer-RNA gene. Curr Genet 27:572–579

    Article  PubMed  CAS  Google Scholar 

  • Hiratsuka J, Shimada H, Whittier R, Ishibashi T, Sakamoto M, Mori M, Kondo C, Honji Y, Sun CR, Meng BY, Li YQ, 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 transfer-RNA genes accounts for a major plastid DNA inversion during the evolution of the cereals. Mol Gen Genet 217:185–194

    Article  PubMed  CAS  Google Scholar 

  • Hirose T, Kusemegi T, Tsudzuki T, Sugiura M (1999) RNA editing sites in tobacco chloroplast transcripts: editing as a possible regulator of chloroplast RNA polymerase activity. Mol Gen Genet 262:452–467

    Google Scholar 

  • Hoot SB, Palmer JD (1994) Structural rearrangements, including parallel inversions, within the chloroplast genome of Anemone and related genera. J Mol Evol 383:274–281

    Google Scholar 

  • Howe CJ (1985) The endpoints of an inversion in wheat chloroplast DNA are associated with short repeated sequences containing homology to att-lambda. Curr Genet 102:139–145

    Article  Google Scholar 

  • Hupfer H, Swiatek M, Hornung S, Herrmann RG, Maier RM, Chiu WL, 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

    PubMed  CAS  Google Scholar 

  • Jansen RK, Raubeson LA, Boore JL, dePamphilis CW, Chumley TW, Haberle RC, Wyman SK, Alverson A, Peery R, Herman SJ, Fourcade HM, Kuehl JV, McNeal JR, Leebens-Mack J, Cui L (2005) Methods for obtaining and analyzing whole chloroplast genome sequences. Molecular evolution: producing the biochemical data, part B. Methods Enzymol 395:348–384

    PubMed  CAS  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 296:572–581

    Article  Google Scholar 

  • Kelchner SA (2000) The evolution of non-coding chloroplast DNA and its application in plant systematics. Ann Mo Bot Gard 87:482–498

    Article  Google Scholar 

  • Kelchner SA, Wendel JF (1996) Hairpins create minute inversions in non-coding regions of chloroplast DNA. Curr Genet 303:259–262

    Article  Google Scholar 

  • Kim K-J, Choi KS, Jansen RK (2005) Two chloroplast DNA inversions originated simultaneously during early evolution in the sunflower family. Mol Biol Evol 22:1783–1792

    Article  PubMed  CAS  Google Scholar 

  • Kim K-J, Lee HL (2005) Widespread occurrence of small inversions in the chloroplast genomes of land plants. Mol Cells 19:104–113

    PubMed  CAS  Google Scholar 

  • Knox EB, Palmer JD (1999) The chloroplast genome arrangement of Lobelia thuliniana Lobeliaceae: expansion of the inverted repeat in an ancestor of the Campanulales. Plant Syst Evol 214:49–64

    Article  Google Scholar 

  • Knox EB, Downie SR, Palmer JD (1993) Chloroplast genome rearrangements and the evolution of giant lobelias from herbaceous ancestors. Mol Biol Evol 10:414–430

    CAS  Google Scholar 

  • Koch MA, Dobes C, Matschinger M, Bleeker W, Vogel J, Kiefer J, Mitchell-Olds T (2005) Evolution of the trnF-gaa gene in Arabidopsis relatives and the Brassicaceae family: monophyletic origin and subsequent diversification of a plastid pseudogene. Mol Biol Evol 22:1032–1043

    Article  PubMed  CAS  Google Scholar 

  • Kolodner R, Tewari KK (1975) Chloroplast DNA from higher-plants replicates by both cairns and rolling circle mechanism. Nature 256:708–711

    Article  PubMed  CAS  Google Scholar 

  • Kurtz S, Choudhuri JV, Ohlebusch E, Schleiermacher C, Stoye J, Giegerich R (2001) REPuter: the manifold applications of repeat analysis on a genomic scale. Nucleic Acids Res 29:4633–4642

    Article  PubMed  CAS  Google Scholar 

  • Lee H-L, Jansen RK, Chumley TW, Kim K-J (2007) Gene relocations within chloroplast genomes of Jasminum and Menodora (Oleaceae) are due to multiple, overlapping inversions. Mol Biol Evol 24:1161–1180

    Article  PubMed  CAS  Google Scholar 

  • Maier RM, Neckermann K, Igloi GL, 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

    Article  PubMed  CAS  Google Scholar 

  • Marshall HD, Newton C, Ritland K (2001) Sequence-repeat polymorphisms exhibit the signature of recombination in lodgepole pine chloroplast DNA. Mol Biol Evol 11:2136–2138

    Google Scholar 

  • Maul JE, Lilly JW, Cui L, dePamphilis CW, Miller W, Harris EH, Stern DB (2002) The Chlamydomonas reinhardtii plastid chromosome: islands of genes in a sea of repeats. Plant Cell 14:2659–2679

    Article  PubMed  CAS  Google Scholar 

  • Millen RS, Olmstead RG, Adams KL, Palmer JD, Lao NT, Heggie L, Kavanagh TA, Hibberd JM, Giray JC, Morden CW, Calie PJ, Jermiin LS, Wolfe KH (2001) Many parallel losses of infA from chloroplast DNA during angiosperm evolution with multiple independent transfers to the nucleus. Plant Cell 13:645–658

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Morton BR, Clegg MT (1993) A chloroplast DNA mutational hotspot and gene conversion in a non-coding region near rbcL in the grass family Poaceae. Curr Genet 244:357–365

    Article  Google Scholar 

  • Ogihara Y, Isono K, Kojima T, Endo A, Hanaoka M, Shiina T, Terachi T, Utsugi S, Murata M, Mori N, Takumi S, Ikeo K, Gojobori T, Murai R, Murai K, Matsuoka Y, Ohnishi Y, Tajiri H, Tsunewaki K (2002) Structural features of a wheat plastome as revealed by complete sequencing of chloroplast DNA. Mol Gen Genom 266:740–746

    Article  CAS  Google Scholar 

  • Ogihara Y, Terachi T, 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

    Article  PubMed  CAS  Google Scholar 

  • Oldenburg DJ, Bendich AJ (2004a) Most chloroplast DNA of maize seedlings in linear molecules with defined ends and branched forms. J Mol Biol 335:953–970

    Article  PubMed  CAS  Google Scholar 

  • Oldenburg DJ, Bendich AJ (2004b) Changes in the structure of DNA molecules and the amount of DNA per plastid during chloroplast development in maize. J Mol Biol 344:1311–1330

    Article  PubMed  CAS  Google Scholar 

  • Palmer JD (1986) Isolation and structural analysis of chloroplast DNA. Methods Enzymol 118:167–186

    Article  CAS  Google Scholar 

  • Palmer JD (1991) Plastid chromosomes: structure and evolution. In: Bogorad L (ed) Molecular biology of plastids. Academic Press, San Diego, CA, pp 5–53

    Google Scholar 

  • Palmer JD, Nugent JM, Herbon LA (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 USA 843:769–773

    Article  Google Scholar 

  • Pombert J-F, Lemieux C, Turmel M (2006) The complete chloroplast DNA sequence of the green alga Oltmannsiellopsis viridis reveals a distinctive quadripartite architecture in the chloroplast genome of early diverging ulvophytes. BMC Biol 4:3

    Article  PubMed  CAS  Google Scholar 

  • Pombert J-F, Otis C, Lemieux C, Turmel M (2005) The chloroplast genome sequence of the green alga Pseudendoclonium akinetum Ulvophyceae reveals unusual structural features and new insights into the branching order of chlorophyte lineages. Mol Biol Evol 22:1903–1918

    Article  PubMed  CAS  Google Scholar 

  • Provan J, Powell W, Hollingsworth PM (2001) Chloroplast microsatellites: new tools for studies in plant ecology and evolution. Trends Ecol Evol 16:142–147

    Article  PubMed  Google Scholar 

  • Quigley F, Weil JH (1985) Organization and sequence of 5 transfer-RNA genes and of an unidentified reading frame in the wheat chloroplast genome—evidence for gene rearrangements during the evolution of chloroplast genomes. Curr Genet 96:495–503

    Article  Google Scholar 

  • Raubeson LA, Jansen RK (1992) Chloroplast DNA evidence on the ancient evolutionary split in vascular land plants. Science 255:1697–1699

    Article  PubMed  CAS  Google Scholar 

  • Raubeson LA, Jansen RK (2005) Chloroplast genomes of plants. In: Henry RJ (ed) Plant diversity and evolution: genotypic and phenotypic variation in higher plants. CABI, Cambridge, MA, pp 45–68

    Google Scholar 

  • Raubeson LA, Peery R, Chumley T, Dziubek C, Fourcade HM, Boore JL, Jansen RK (2007) Comparative chloroplast genomics: Analyses including new sequences from the angiosperms Nuphar advena and Ranunculus macranthus. BMC Genom 8:174

    Article  CAS  Google Scholar 

  • Rocha EPC (2003) DNA repeats lead to the accelerated loss of gene order in bacteria. Trends Genet 19:600–603

    Article  PubMed  CAS  Google Scholar 

  • Saski C, Lee S-B, Daniell H, Wood TC, Tomkins J, Kim H-G, Jansen RK (2005) Complete chloroplast genome sequence of Glycine max and comparative analyses with other legume genomes. Plant Mol Biol 59:309–322

    Article  PubMed  CAS  Google Scholar 

  • Schmitz-Linneweber C, Maier RM, Alcaraz J-P, Cottet A, Herrmann RG, Mache R (2001) The plastid chromosome of spinach Spinacia oleracea: complete nucleotide sequence and gene organization. Plant Mol Biol 45:307–315

    Article  PubMed  CAS  Google Scholar 

  • Schwartz S, Elnitski L, Li M, Weirauch M, Riemer C, Smit A, Program NCS, Green ED, Hardison RC, Miller W (2003) MultiPipMaker and supporting tools: alignments and analysis of multiple genomic DNA sequences. Nucleic Acids Res 31:3518–3524

    Article  PubMed  CAS  Google Scholar 

  • Shimada H, Sugiura M (1989) Pseudogenes and short repeated sequences in the rice chloroplast genome. Curr Genet 164:293–301

    Article  Google Scholar 

  • Simpson L, Sbicego S, Aphsizhev R (2003) Uridine insertion/deletion RNA editing in trypanosome mitochondria: a complex business. RNA 9:265–276

    Article  PubMed  CAS  Google Scholar 

  • Steane DA (2005) Complete nucleotide sequence of the chloroplast genome from the Tasmanian blue gum, Eucalyptus globules Myrtacaceae. DNA Res 12:215–220

    Article  PubMed  CAS  Google Scholar 

  • Stein DB, Conant DS, Ahearn ME, Jordan ET, Kirch SA, Hasebe M, Iwatsuki K, Tan MK, Thomson JA (1992) Structural rearrangements of the chloroplast genome provide an important phylogenetic link in ferns. Proc Natl Acad Sci USA 89:1856–1860

    Article  PubMed  CAS  Google Scholar 

  • Sugiura M (1989) The chloroplast chromosomes in land plants. Annu Rev Cell Biol 5:51–70

    Article  PubMed  CAS  Google Scholar 

  • Thomas F, Massenet O, Dorne AM, Briat JF, Mache R (1988) Expression of the rp123, rp12 and rps19 genes in spinach chloroplasts. Nucleic Acids Res 16:2461–2472

    Article  PubMed  CAS  Google Scholar 

  • Timme RE, Kuehl JV, Boore JL, Jansen RK (2007) A comparison of the first two sequenced chloroplast genomes in Asteraceae: lettuce and sunflower. Am J Bot 94:302–312

    Article  CAS  Google Scholar 

  • Tsai CH, Strauss SH (1989) Dispersed repetitive sequences in the chloroplast genome of Douglas-fir. Curr Genet 163:211–218

    Article  Google Scholar 

  • Turmel M, Otis C, Lemieux C (2002) The chloroplast and mitochondrial genome sequences of the charophyte Chaetosphaeridium globosum: insights into the timing of the events that restructured organelle DNAs within the green algal lineage that led to land plants. Proc Natl Acad Sci USA 99:11275–11280

    Article  PubMed  CAS  Google Scholar 

  • Wakasugi T, Tsudzuki J, Ito S, Nakashima K, Tsudzuki T, Sugiura M (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

    Article  PubMed  CAS  Google Scholar 

  • Wolfe KH (1988) The site of deletion of the inverted repeat in pea chloroplast DNA contains duplicated gene fragments. Curr Genet 131:97–99

    Article  Google Scholar 

  • Wolfe KH, Morden CW, Palmer JD (1992) Function and evolution of a minimal plastid from a nonphotosynthetic parasitic plant. Proc Natl Acad Sci USA 89:10648–10652

    Article  PubMed  CAS  Google Scholar 

  • Wyman SK, Jansen RK, Boore JL (2004) Automatic annotation of organellar genomes with DOGMA. Bioinformatics 20:3252–3255

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

Funding for this project was provided by a grant from the NSF (DEB 0120709) to R.K.J. and J.L.B. Part of this work was performed under the auspices of the U.S. Department of Energy, Office of Biological and Environmental Research, by the University of California, Lawrence Berkeley National Laboratory, under contract No. DE-AC02-05CH11231. The authors thank Stacia Wyman for computational assistance and Tim Chumley and Gwen Gage for technical assistance in generating figures. We also thank Andrew Alverson, Katie Hansen, Paul Wolf, and Elizabeth Ruck for their helpful comments and suggestions on an early version of the manuscript. This paper represents a portion of R.C.H.’s Ph.D. thesis in botany at the University of Texas at Austin.

Author information

Authors and Affiliations

  1. Section of Integrative Biology and Institute of Cellular and Molecular Biology, University of Texas, Austin, TX, 78712, USA

    Rosemarie C. Haberle & Robert K. Jansen

  2. Department of Plant Sciences, Mail Stop 2, University of California, Davis, CA, 95616, USA

    Rosemarie C. Haberle

  3. DOE Joint Genome Institute, Walnut Creek, CA, 94598, USA

    H. Matthew Fourcade & Jeffrey L. Boore

  4. Genome Project Solutions, 1024 Promenade Street, Hercules, CA, 94547, USA

    Jeffrey L. Boore

Authors
  1. Rosemarie C. Haberle
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. H. Matthew Fourcade
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jeffrey L. Boore
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Robert K. Jansen
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Rosemarie C. Haberle.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Haberle, R.C., Fourcade, H.M., Boore, J.L. et al. Extensive Rearrangements in the Chloroplast Genome of Trachelium caeruleum Are Associated with Repeats and tRNA Genes. J Mol Evol 66, 350–361 (2008). https://doi.org/10.1007/s00239-008-9086-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00239-008-9086-4

Keywords

Search

Navigation