Skip to main content
Log in

Analysis of nrDNA polymorphism in closely related diploid sexual, tetraploid sexual and polyploid agamospermous species

  • Original Article
  • Published:
Plant Systematics and Evolution Aims and scope Submit manuscript

Abstract

Nuclear sequences of ITS1-5.8S-ITS2 region of rDNA may be an important source of phylogenetically informative data provided that nrDNA is cloned and the character of sequence variation of clones is properly analyzed. nrDNA of selected Taraxacum sections was studied to show sequence variation differences among diploid sexual, tetraploid sexual and polyploid agamospermous species. We examined nucleotide characteristics, substitution pattern, secondary structure, and the phylogenetic utility of ITS1-5.8S-ITS2 from 301 clones of 32 species representing 11 sections. The most divergent sequences of ITS1&2 differed by 17.1% and in 5.8S only by 3.7%. The ITS1-5.8S-ITS2 characteristics, integrity and also stability of secondary structures confirmed that pseudogenes are not responsible for the above variation. The within-individual polymorphism of clones implies that the concerted evolution of ITS cistron of agamospermous polyploid Taraxacum is remarkably suppressed. Sequences of ITS clones proved to be a useful tool for mapping pathways of complex reticulation (polyploid hybridity) in agamospermous Taraxacum.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Álvarez I, Wendel JF (2003) Ribosomal ITS sequences and plant phylogenetic inference. Mol Phylog Evol 29:417–434

    Article  Google Scholar 

  • Baldwin BG (1992) Phylogenetic utility of internal transcribed spacer of nuclear DNA in plants: an example from the Compositae. Mol Phylog Evol 1:3–16

    Article  CAS  Google Scholar 

  • Baldwin BG, Sanderson MJ, Porter JM, Wojciechowski MF, Campbell CS, Donoghue MJ (1995) The ITS region of nuclear ribosomal DNA: a valuable source of evidence on angiosperm phylogeny. Ann Missouri Bot Gard 82:247–277

    Article  Google Scholar 

  • Bailey CD, Carr TG, Harris SA, Hughes CE (2003) Characterization of angiosperm nrDNA polymorphism: paralogy and pseudogenes. Mol Phylog Evol 29:435–455

    Article  CAS  Google Scholar 

  • Bandelt H-J, Forster P, Röhl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16(1):37–48

    PubMed  CAS  Google Scholar 

  • Battjes J, Menken SBJ, den Nijs JCM (1992) Clonal diversity in some microspecies of Taraxacum sect. Palustria (Lindb. fil.) Dahlst. from Czechoslovakia. Bot Jb Syst 114:315–328

    Google Scholar 

  • Bremer K (1994) Asteraceae: cladistics and classification. Timber Press, Portland

    Google Scholar 

  • Buckler ESI, Holtsford TP (1996) Zea ribosomal repeat evolution and substitutional pattern. Mol Biol Evol 13:623–632

    PubMed  CAS  Google Scholar 

  • Buckler ESI, Ippolito A, Holtsford TP (1997) The evolution of ribosomal DNA: divergent paralogues and phylogenetic implications. Genetics 145:821–832

    PubMed  CAS  Google Scholar 

  • Campbell CS, Wojciechowski MF, Baldwin BG, Alice LA, Donoghue MJ (1997) Persistent nuclear ribosomal DNA sequence polymorphism in the Amelanchier agamic complex (Rosaceae). Mol Phylog Evol 14(1):81–90

    CAS  Google Scholar 

  • Cronn R, Cedroni M, Haselkorn T, Grover C, Wendel JF (2002) PCR-mediated recombination in amplification products derived from polyploid cotton. Theor Appl Gen 104:482–489

    Article  CAS  Google Scholar 

  • den Nijs JCM, Kirschner J, Štěpánek J, van der Hulst A (1990) Distribution of diploid sexual plants of Taraxacum sect. Ruderalia in east-Central Europe, with special reference to Czechoslovakia. Pl Syst Evol 170:71–84

    Article  Google Scholar 

  • den Nijs JCM, Sterk AA (1980) Cytogeography of Taraxacum sectio Taraxacum and sectio Alpestria in France and adjacent parts of Italy and Switzerland, including some taxonomic remarks. Acta Bot Neerl 33(1):1–24

    Google Scholar 

  • Dobeš C, Mitchell-Olds T, Koch MA (2004) Intraspecific diversification in North American Boechera stricta (=Arabis drummondii), Boechera × divaricarpa, and Boechera holboellii (Brassicaceae) inferred from nuclear and chloroplast molecular markers—an integrative approach. Amer J Bot 91:2087–2101

    Article  Google Scholar 

  • Doll R (1982) Grundriss der Evolution der Gattung Taraxacum Zinn. Feddes Repert 93:426–481

    Google Scholar 

  • Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull 19:11–15

    Google Scholar 

  • Felsenstein J (1993) PHYLIP (Phylogeny inference package), 3.0. Distributed by the author, Seattle

  • Ferguson D, Sang T (2001) Speciation through homoploid hybridization between allotetraploids in peonies (Paeonia). Proc Natl Acad Sci USA 98:3915–3919

    Article  PubMed  CAS  Google Scholar 

  • Fürnkranz D (1969) Eine neue mediterrane Reliktart der Gattung Taraxacum. Österr Bot Z 117:149–156

    Article  Google Scholar 

  • Glémin S, Bazin E, Charlesworth D (2006) Impact of mating systems on patterns of sequence polymorphism in flowering plants. Proc Roy Soc B 273:3011–3019

    Article  Google Scholar 

  • Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  • Harpke D, Peterson A (2006) Non-concerted evolution in Mammillaria (Cactaceae). Mol Phylog Evol 41:579–593

    Article  CAS  Google Scholar 

  • Jobes DV, Thien B (1997) A conserved motif in the 5.8S ribosomal RNA (rRNA) gene is a useful diagnostic marker for plant internal transcribed spacer (ITS) sequences. Pl Mol Biol Rep 15:326–334

    Article  CAS  Google Scholar 

  • Kiers AM, Mes THM, Van der Meijden R, Bachmann K (1999) Morphologically defined Cichorium (Asteraceae) species reflect lineages based on chloroplast and nuclear (ITS) DNA data. Syst Bot 24(4):645–659

    Article  Google Scholar 

  • Kim K-J, Jansen RK (1994) Phylogenetic implications of rbcL and ITS sequence variation in the Berberidaceae. Syst Bot 21:381–396

    Article  Google Scholar 

  • King LM (1993) Origins of genotypic variation in North American dandelions inferred from ribosomal DNA and chloroplast DNA restriction enzyme analysis. Evolution 47(1):136–151

    Article  CAS  Google Scholar 

  • King LM, Schaal BA (1990) Genotypic variation within asexual lineages of Taraxacum officinale. Proc Natl Acad Sci USA 87:998–1002

    Article  PubMed  CAS  Google Scholar 

  • Kirschner J, Štěpánek J (1993) The genus Taraxacum in the Caucasus. 1, Introduction. 2, The section Porphyrantha. Folia Geobot Phytotax 28:295–320

    Google Scholar 

  • Kirschner J, Štěpánek J (1996) Modes of speciation and evolution of the sections in Taraxacum. Folia Geobot Phytotax 31:415–426

    Article  Google Scholar 

  • Kirschner J, Štěpánek J (1998) A monograph of Taraxacum sect. Palustria. Institute of Botany, Průhonice. 281

  • Kirschner J, Štěpánek J (1998b) A revision of Taraxacum sect. Piesis (Compositae). Folia Geobot 33:391–414

    Article  Google Scholar 

  • Kirschner J, Štěpánek J (2004) New sections in Taraxacum. Folia Geobot 39:259–274

    Article  Google Scholar 

  • Kirschner J, Štěpánek J (2005) Dandelions in Central Asia: Taraxacum sect. Suavia. Preslia 77:263–276

    Google Scholar 

  • Kirschner J, Štěpánek J, Tichý M, Krahulcová A, Kirschnerová L, Pellar L (1994) Variation in Taraxacum bessarabicum and allied taxa of the section Piesis (Compositae): allozyme diversity, karyotypes and breeding behaviour. Folia Geobot Phytotax 29:61–83

    Article  Google Scholar 

  • Kirschner J, Štěpánek J, Mes THM, den Nijs JCM, Oosterveld P, Štorchová H, Kuperus P (2003) Principal features of the cpDNA evolution in Taraxacum (Asteraceae, Lactuceae): a conflict with taxonomy. Pl Syst Evol 239:231–255

    Article  CAS  Google Scholar 

  • Kirschner J, Štěpánek J, Klimeš L (2006) Dandelions in Central Asia: a taxonomic revision of Taraxacum section Leucantha. Preslia 78:27–65

    Google Scholar 

  • Koch MA, Dobeš C, Mitchell-Olds T (2003) Multiple hybrid formation in natural populations: concerted evolution of the internal transcribed spacer of nuclear ribosomal DNA (ITS) in North American Arabis divaricarpa (Brassicaceae). Mol Biol Evol 20:338–350

    Article  PubMed  CAS  Google Scholar 

  • Li W (1997) Molecular evolution. Sinauer Associates, Sunderland

    Google Scholar 

  • Liston A, Robinson WA, Oliphant JM, Alvarez-Buylla E (1996) Length variation in the nuclear ribosomal DNA internal transcribed spacer region of non-flowering seed plants. Syst Bot 21:109–120

    Article  Google Scholar 

  • Liu JS, Schardl CL (1994) A conserved sequence in internal transcribed spacer–1 of plant nuclear ribosomal–RNA genes. Pl Mol Biol 26(2):775–778

    Article  CAS  Google Scholar 

  • Logacheva MD, Valiejo-Roman CM, Pimenov MG (2008) ITS phylogeny of West Asian Heracleum species and related taxa of Umbelliferae-Tordylieae W.D.J. Koch, with notes on evolution of their psbA-trnH sequences. Pl Syst Evol 270:139–157

    Article  CAS  Google Scholar 

  • Małecka J (1964) Multinucleate pollen grains in Taraxacum serotinum. Acta Biol Cracov 7:108–116

    Google Scholar 

  • Manen J-F (2004) Are both sympatric species Ilex perado and Ilex canariensis secretly hybridizing? Indication from nuclear markers collected in Tenerife. BMC Evol. Biol. 4, Art. No. 46

  • Menken SBJ, Morita T (1989) Uniclonal population structure in the pentaploid obligate agamosperm Taraxacum albidum Dahlst. Pl Species Biol 4:29–36

    Article  Google Scholar 

  • Mes THM, Kuperus P, Kirschner J et al (2002) Detection of genetically divergent clone mates in apomictic dandelions. Mol Ecol 11(2):253–265

    Article  PubMed  CAS  Google Scholar 

  • Nieto Feliner G, Larena BG, Aguilar JF (2004) Fine-scale geographic structure, intra-individual polymorphism and recombination in nuclear ribosomal internal transcribed spacers in Armeria (Plumbaginaceae). Ann Bot 93:189–200

    Article  PubMed  Google Scholar 

  • Nixon KC (1999) The parsimony ratchet, a new method for rapid phylogenetic analysis. Cladistics 15:407–414

    Article  Google Scholar 

  • Nixon KC (2002) WinClada ver. 1.00.08. Published by the author, Ithaca

  • Rauschler JT, Doyle JJ, Brown HD (2004) Multiple origins and nrDNA internal transcribed spacer homeologue evolution in the Glycine tomentella (Leguminosae) allopolyploid complex. Genetics 166:987–998

    Article  Google Scholar 

  • Razafimandimbison SG, Kellog EA, Bremer B (2004) Recent origin and phylogenetic utility of divergent ITS putative pseudogenes: a case study from Naucleeae (Rubiaceae). Syst. Biol. 53:177–192

    Article  PubMed  Google Scholar 

  • Richards AJ (1969) Chromosome numbers in Taraxacum. Taxon 18:560–562

    Google Scholar 

  • Rieseberg LH, Beckstrom-Sternberg S, Doan K (1990) Helianthus annus ssp. texanus has chloroplast DNA and nuclear ribosomal RNA genes of Helianthus debilis ssp. cucumerifolius. Proc Natl Acad Sci USA 87:593–597

    Article  PubMed  CAS  Google Scholar 

  • Roalson EH, Columbus JT, Friar EA (2001) Phylogenetic relationships in Cariceae (Cyperaceae) based on ITS (nrDNA) and trnT-L-F (cpDNA) region sequences: assessment of suprageneric and sectional relationships in Carex with emphasis on section Acrocystic. Syst Bot 26(2):318–341

    Google Scholar 

  • Rooney AP, Ward TJ (2005) Evolution of large ribosomal RNA multigene family in filamentous fungi: birth and death of concerted evolution paradigm. Proc Natl Acad Sci USA 102(14):5084–5089

    Article  PubMed  CAS  Google Scholar 

  • Rosselló JA, Lázaro A, Cosín R, Molins A (2007) A phylogenetic split in Buxus balearica (Buxaceae) as evidenced by nuclear ribosomal markers: when ITS paralogs are welcome. J Mol Evol 64:143–157

    Article  PubMed  Google Scholar 

  • Rozas J, Sánchez-Delbarrio JC, Messeguer X, Rozas R (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496–2497

    Article  PubMed  CAS  Google Scholar 

  • Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual. Cold Spring Laboratory Press, New York

    Google Scholar 

  • Sang T, Crawford DJ, Stuessy TF (1995) Documentation of reticulate evolution in peonies (Paeonia) using internal transcribed spacer sequences of nuclear ribosomal DNA: implications for biogeography and concerted evolution. Proc Natl Acad Sci USA 92:6813–6817

    Article  PubMed  CAS  Google Scholar 

  • Stace CA (2005) Plant taxonomy and biosystematics—does DNA provide all the answers? Taxon 54(4):999–1007

    Google Scholar 

  • van Dijk PJ, Bakx-Schotman JMT (2004) Formation of unreduced megaspores (diplospory) in apomictic dandelions (Taraxacum officinale s.l.) is controlled by a sex specific dominant locus. Genetics 166(1):483–492

    Article  PubMed  Google Scholar 

  • van den Hulst RGM, Mes THM, Nijs JCM, Bachmann K (2000) Amplified fragment length polymorphism (AFLP) markers reveal that population structure of triploid dandelions (Taraxacum officinale) exhibits both clonality and recombination. Mol Evol 9(1):1–8

    Article  Google Scholar 

  • Van Oostrum H, Sterk AA, Wijsman HJW (1985) Genetic variation in agamospermous microspecies of Taraxacum sect. Erythrosperma and sect. Obliqua. Heredity 55:223–228

    Article  Google Scholar 

  • Verduijn MH, van Dijk P, Van Damme JMM (2004) The role of tetraploids in the sexual–asexual cycle in dandelions (Taraxacum). Heredity 93:390–398

    Article  PubMed  CAS  Google Scholar 

  • Wendel JF, Schnabel A, Seelanan T (1995) Bidirectional interlocus concerted evolution following allopolyploid speciation in cotton (Gossypium). Proc Natl Acad Sci USA 92:280–284

    Article  PubMed  CAS  Google Scholar 

  • White TJ, Bruns TD, Lee S, Taylor JW (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ (eds) PCR protocols: a guide to methods and amplifications. Academic Press, Inc, San Diego, pp 315–322

    Google Scholar 

  • Wittzell H (1999) Chloroplast DNA variation and reticulate evolution in sexual and apomictic sections of dandelions. Mol Ecol 8:2023–2035

    Article  PubMed  CAS  Google Scholar 

  • Wei X-X, Wang X-Q, Hong D-Y (2003) Marked intragenomic heterogeneity and geographical differentiation of nrDNA ITS in Larix potaninii (Pinaceae). J Mol Evol 57:623–635

    Article  PubMed  CAS  Google Scholar 

  • Záveský L, Jarolímová V, Štěpánek J (2005) Nuclear DNA content variation within the genus Taraxacum (Asteraceae). Folia Geobot 40:91–104

    Article  Google Scholar 

  • Zuker M (2003) Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res 31(13):3406–3415

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

The study was performed in the DNA Laboratory, Institute of Botany ASCR and Laboratory of the Centre for Integrated Genomics and Institute (1M6837805002) of Molecular Genetics ASCR and was supported by grants GACR 206/02/0346 and 206/05/0970. The study was also supported by the institutional Research Plan AV0Z60050516. We thank Šárka Pinkasová for invaluable help during the work in the laboratory, and Věra Matějovičová for help with cultivation and sample preparation. We are particularly indebted to L. Klimeš for important samples collected in Ladakh, NW India. P. Trávníček was so kind as to screen selected herbarium samples for flow-cytometry estimates.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jan Kirschner.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material (DOC 872 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Záveská Drábková, L., Kirschner, J., Štěpánek, J. et al. Analysis of nrDNA polymorphism in closely related diploid sexual, tetraploid sexual and polyploid agamospermous species. Plant Syst Evol 278, 67–85 (2009). https://doi.org/10.1007/s00606-008-0134-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00606-008-0134-8

Keywords

Navigation