Journal of Molecular Evolution

, Volume 38, Issue 3, pp 274–281

Structural rearrangements, including parallel inversions, within the chloroplast genome of Anemone and related genera

  • Sara B. Hoot
  • Jeffrey D. Palmer
Article

Abstract

Chloroplast DNA cleavage sites for 10 restriction enzymes were mapped for 46 species representing all sections of Anemone, four closely related genera (Clematis, Pulsatilla, Hepatica, and Knowltonia), and three more distantly related outgroups (Caltha, Ranunculus, and Adonis). Comparison of the maps revealed that the chloroplast genomes of Anemone and related genera have sustained an unusual number and variety of rearrangements. A single inversion of a 42-kb segment was found in the large single-copy region of Adonis aestivalis. Two types of rearrangements were found in the chloroplast genome of Clematis, Anemone, Pulsatilla, Hepatica, and Knowltonia: An approximately 4-kb expansion of the inverted repeat and four inversions within the large single-copy region. These rearrangements support the monophyletic status of these genera, clearly separating them from Caltha, Ranunculus, and Adonis. Two further inversions were found in two Clematis species and three Anemone species. While appearing to support a monophyletic grouping for these taxa, these two inversions conflict with data from both chloroplast restriction sites and morphology and are better interpreted as having occurred twice independently. These are the first two documented cases of homoplastic inversions in chloroplast DNA. Finally, the second intron of the chloroplast rps12 gene was shown to have been lost in the common ancestor of the same three Anemone species that feature the two homoplastic inversions.

Key words

Chloroplast DNA Rearrangements Inversions Intron loss Homoplasy Ranunculaceae Anemone complex 

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References

  1. Bruneau A, Doyle JJ, Palmer JD (1990) A chloroplast DNA inversion as a subtribal character in the Phaseoleae (Leguminosae). Syst Bot 15:378–386Google Scholar
  2. Collins ML, Hunsaker WR (1985) Improved hybridization assays employing tailed oligonucleotide probes: a direct comparison with 5′-end-labeled oligonucleotide probes and nick-translated plasmid probes. Anal Biochem 151:211–224Google Scholar
  3. 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, New York, p 14–35Google Scholar
  4. Downie SR, Palmer JD (1994) A chloroplast DNA phylogeny of the Caryophyllales based on structural and inverted repeat restriction site variation. Syst Bet 19(2)Google Scholar
  5. Downie SR, Olmstead RG, Zurawski G, Soltis DE, Soltis PS, Watson JC, Palmer JD (1991) Six independent losses of the chloroplast DNA rpl2 intron in dicotyledons: molecular and phylogenetic implications. Evolution 45:1245–1259Google Scholar
  6. Doyle JJ, Davis GI, Soreng RJ, Garvin D, Anderson MJ (1992) Chloroplast DNA inversions and the origin of the grass family (Poaceae). Proc Natl Acad Sci USA 89:7722–7726Google Scholar
  7. Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small quantities of fresh tissue. Phytochem Bull 19:11–15Google Scholar
  8. Giese K, Subramanian AR, Larrinua IG, Bogarad L (1987) Nucleotide sequence, promoter analysis, and linkage mapping of the unusually organized operon encoding ribosomal proteins S7 and S12 in maize chloroplast. J Biol Chem 262:15251–15255Google Scholar
  9. Gregory WC (1941) Phylogenetic and cytological studies in the Ranunculaceae Juss. Trans Am Phil Soc, NS 31:441–520Google Scholar
  10. 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 plastic DNA inversion during the evolution of the cereals. Mol Gen Genet 217:85–194Google Scholar
  11. Hoot SB (1991) Phylogeny of the Ranunculaceae based on epidermal microcharacters and macromorphology. Syst Bot 16:741–755Google Scholar
  12. Hoot SB, Reznicek AA, Palmer JD (1994) Phylogenetic relationships in Anemone (Ranunculaceae) based on morphology and chloroplast DNA. Syst Bot 19:172–203Google Scholar
  13. Howe CJ, Barker RF, Bowman CM, Dyer TA (1988) Common features of three inversions in wheat chloroplast DNA. Curr Genet 13:343–349Google Scholar
  14. Jansen RK, Palmer JD (1987) A chloroplast DNA inversion marks an ancient evolutionary split in the sunflower family (Asteraceae). Proc Natl Acad Sci USA 84:5818–5822Google Scholar
  15. Johansson JT, Jansen RK (1993) Chloroplast DNA variation and phylogeny of the Ranunculaceae. Plant Syst Evol 187:29–49Google Scholar
  16. Knox E, Downie SR, Palmer JD (1993) Chloroplast genome rearrangements and the evolution of giant lobelias from herbaceous ancestors. Mol Biol Evol 10:414–430Google Scholar
  17. Kuhsel MG, Strickland R, Palmer JD (1990) An ancient group I intron shared by eubacteria and chloroplasts. Science 250:1570–1573Google Scholar
  18. Milligan BG, Hampton JN, Palmer JD (1989) Dispersed repeats and structural reorganization in subclover chloroplast DNA. Mol Biol Evol 6:355–368PubMedGoogle Scholar
  19. Moon E, Kao T-H, Wu R (1988) Rice mitochondrial genome contains a rearranged chloroplast gene cluster. Mol Gen Genet 213:247–253Google Scholar
  20. Olmstead R, Palmer JD (1992) A chloroplast DNA phylogeny of the Solanaceae: subfamilial relationships and character evolution. Ann Missouri Bot Gard 79:346–360Google Scholar
  21. Palmer JD (1991) Plastid Chromosomes: Structure and Evolution. In: Bogarad L, Vasil IK (eds) Cell culture and somatic cell genetics of plants 7A. Academic, San Diego, p 5Google Scholar
  22. Palmer JD, Thompson WF (1982) Chloroplast DNA inversions are more frequent when a large inverted repeat is lost. Cell 29:537–550Google Scholar
  23. Palmer JD, Nugent JM, Herbon LA (1987a) 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 84:769–773Google Scholar
  24. Palmer JD, Osorio B, Thompson WF (1988a) Evolutionary significance of inversions in legume chloroplast DNAs. Curr Genet 14:65–74Google Scholar
  25. Palmer JD, Osorio B, Aldrich J, Thompson WF (1987b) Chloroplast DNA evolution among legumes: loss of a large inverted repeat occurred prior to other sequence rearrangements. Curr Genet 11:275–286Google Scholar
  26. Palmer JD, Jansen RK, Michaels HJ, Chase MW, Manhart JR (1988b) Chloroplast DNA variation and plant phylogeny. Ann Missouri Bot Gard 75:1180–1206Google Scholar
  27. Quigley F, Weil JH (1985) Organization and sequence of five tRNA genes and of an unidentified reading frame in the wheat chloroplast genome: evidence for gene rearrangements during the evolution of chloroplast genomes. Curr Genet 9:495–503PubMedGoogle Scholar
  28. Raubeson LA, Jansen RK (1992) Chloroplast DNA evidence on the ancient evolutionary split in vascular land plants. Science 255: 1697–1699Google Scholar
  29. Shinozaki K, Ohme M, Tanaka M, Wakasugi T, Hayashida N, Matsubayashi T, Zaita N, Chunwongse J, Obokata J, YamaguchiShinozaki K, Ohto C, Torazawa K, Meng B-Y, Sugita M, Deno H, Kamogashira T, Yamada K, Kusuda J, Takaiwa F, Kato A, Tohdoh N, Shimada H, Sugiura M (1986) The complete nucleotide sequence of the tobacco chloroplast genome: its gene organization and expression. EMBO J 5:2043–2049Google Scholar
  30. Stein DB, Palmer JD, Thompson WF (1986) Structural evolution and flip-flop recombination of chloroplast DNA in the fern genus Osmunda. Curt Genet 10:835–841Google Scholar
  31. Strauss SH, Palmer JD, Howe GT, Doerksen AH (1988) Chloroplast genomes of two conifers lack a large inverted repeat and are extensively rearranged. Proc Natl Acad Sci USA 85:3898–3902Google Scholar
  32. Swofford DL (1990) PAUP: Phylogenetic analysis using parsimony, version 3.0. Illinois Natural History Survey, Champaign, ILGoogle Scholar
  33. Tamura M (1967) Morphology, ecology and phylogeny of the Ranunculaceae VII. Sci Repts Osaka Univ 17:41–56Google Scholar
  34. von Allmen JM, Stutz E (1987) Complete sequence of “divided” rps12 (r-protein S12) and rps7 (r-protein S7) gene in soybean chloroplast DNA. Nucleic Acids Res 15:2387Google Scholar

Copyright information

© Springer-Verlag New York Inc 1994

Authors and Affiliations

  • Sara B. Hoot
    • 1
  • Jeffrey D. Palmer
    • 2
  1. 1.University of Michigan HerbariumNorth University BuildingAnn ArborUSA
  2. 2.Department of BiologyIndiana UniversityBloomingtonUSA
  3. 3.Field Museum of Natural HistoryChicagoUSA

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