Skip to main content
SpringerLink
Log in

Extensive 5.8S nrDNA polymorphism in Mammillaria (Cactaceae) with special reference to the identification of pseudogenic internal transcribed spacer regions

  • Regular Paper
  • Published:
Journal of Plant Research Aims and scope Submit manuscript

Abstract

The internal transcribed spacer (ITS) region (ITS1, 5.8S rDNA, ITS2) represents the most widely applied nuclear marker in eukaryotic phylogenetics. Although this region has been assumed to evolve in concert, the number of investigations revealing high degrees of intra-individual polymorphism connected with the presence of pseudogenes has risen. The 5.8S rDNA is the most important diagnostic marker for functionality of the ITS region. In Mammillaria, intra-individual 5.8S rDNA polymorphisms of up to 36% and up to nine different types have been found. Twenty-eight of 30 cloned genomic Mammillaria sequences were identified as putative pseudogenes. For the identification of pseudogenic ITS regions, in addition to formal tests based on substitution rates, we attempted to focus on functional features of the 5.8S rDNA (5.8S motif, secondary structure). The importance of functional data for the identification of pseudogenes is outlined and discussed. The identification of pseudogenes is essential, because they may cause erroneous phylogenies and taxonomic problems.

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.

Fig. 1
Fig. 2

Similar content being viewed by others

References

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

    Article  PubMed  Google Scholar 

  • Andreasen K, Baldwin BG (2003) Nuclear ribosomal DNA sequence polymorphism and hybridization in checker mallows (Sidalcea, Malvaceae). Mol Phylogenet Evol 29:563–581

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Baker WJ, Hedderson TA, Dransfield JU (2000) Molecular phylogentics of subfamily Calamoideae (Palmae) based on nrDNA ITS and cpDNA rps16 intron sequence data. Mol Phylogenet Evol 14:195–217

    Article  PubMed  CAS  Google Scholar 

  • Blattner FR (2004) Phylogeny of Hordeum (Poaceae) as inferred by nuclear rDNA ITS sequences. Mol Phylogenet Evol 33:289–299

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Cannone JJ, Subramanian S, Schnare MN, Collett JR, D’Souza LM, Du YS, Feng B, Lin N, Madabusi LV, Muller KM, Pande N, Shang ZD, Yu N, Gutell RR (2002) The comparative RNA web (CRW) site: an online database of comparative sequence and structure information for ribosomal, intron, and other RNAs. BMC Bioinform 3:2

    Article  Google Scholar 

  • Carr TG, O’Neil K, Bailey CD (2006) Bootstrap hypothesis testing using BootHyp. http://biology-web.nmsu.edu/bailey/Boothyp.html

  • Crooks GE, Hon G, Chandonia J, Brenner SE (2004) WebLogo: a sequence logo generator. Genome Res 14:1188–1190

    Article  PubMed  CAS  Google Scholar 

  • Edwards EJ, Nyffeler R, Donoghue MJ (2005) Basal cactus phylogeny: implications of Pereskia (Cactaceae) paraphyly for the transition to the cactus life form. Am J Bot 92:1177–1188

    Article  Google Scholar 

  • Elder Jr JF, Turner BJ (1995) Concerted evolution of repetitive DNA sequences in eukaryotes. Q Rev Biol 70:297–320

    Article  PubMed  CAS  Google Scholar 

  • Felsenstein J (2005) PHYLIP (Phylogeny Inference Package) version 3.6, distributed by the author, Department of Genome Sciences. University of Washington, Seattle

  • Gardiner-Garden M, Sved JA, Frommer M (1992) DNA methylation in plant cells. J Mol Evol 34:219–230

    Article  CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Harpke D (2005) Non-concerted ITS evolution and analysis of functional and non-functional 5.8S rRNA genes in genus Mammillaria (Cactaceae). Diploma thesis, Martin-Luther-University, Halle

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

    Article  PubMed  CAS  Google Scholar 

  • Harpke D, Peterson A (2007) Quantitative PCR revealed a minority of ITS copies to be functional in Mammillaria (Cactaceae). Int J Plant Sci 168:1157–1160

    Article  CAS  Google Scholar 

  • Hartmann S, Nason JD, Bhattacharya D (2001) Extensive ribosomal DNA genic variation in the columnar cactus Lophocereus. J Mol Evol 53:124–134

    PubMed  CAS  Google Scholar 

  • Hershkovitz MA, Zimmer EA (1997) On the evolutionary origins of the cacti. Taxon 46:217–232

    Article  Google Scholar 

  • Hershkovitz MA, Zimmer EA, Hahn WJ (1999) Ribosomal DNA sequences and angiosperm systematics. In: Hollingsworth PM, Bateman RM, Cornall RJ (eds) Molecular systematics and plant evolution. Taylor & Francis, London, pp 268–326

    Google Scholar 

  • Hughes CE, Bailey CD, Harris SA (2002) Divergent and reticulate species relationships in Leucaena (Fabaceae) inferred from multiple data sources: insights into polyploid origins and nrDNA polymorphism. Am J Bot 89:1057–1073

    Article  CAS  Google Scholar 

  • Jobes DV, Thien LB (1997) A conserved motif in the 58S ribosomal RNA (rRNA) gene is a useful diagnostic marker for plant internal transcribed spacer (ITS) sequences. Plant Mol Biol Rep 15:326–334

    Article  CAS  Google Scholar 

  • Keller I, Chintauan-Marquier IC, Veltsos P, Nichols RA (2006) Ribosomal DNA in the grasshopper Podisma pedestris: escape from concerted evolution. Genetics 174:863–874

    Article  PubMed  CAS  Google Scholar 

  • Kim YD, Kim SH (1999) Phylogeny of Weigela and Diervilla (Caprifoliaceae) based on nuclear rDNA ITS sequences: biogeographic and taxonomic implications. J Plant Res 112:331–341

    Article  CAS  Google Scholar 

  • Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120

    Article  PubMed  CAS  Google Scholar 

  • Kishino H, Hasegawa M (1989) Evaluation of the maximum likelihood estimate of the evolutionary tree topologies from DNA sequence data, and the branching order in the Hominoidea. J Mol Evol 29:170–179

    Article  PubMed  CAS  Google Scholar 

  • Kita Y, Ito M (2000) Nuclear ribosomal ITS sequences and phylogeny in East Asian Aconitum subgenus Aconitum (Ranunculaceae), with special reference to extensive polymorphism in individual plants. Plant Syst Evol 225:1–13

    Article  CAS  Google Scholar 

  • Kluge AG, Farris JS (1969) Quantitative phyletics and evolution of Anurans. Syst Zool 18:1–32

    Article  Google Scholar 

  • Kumar S (1996) PHYLTEST: a program for testing phylogenetic hypothesis version 2.0. Institute of Molecular Evolutionary Genetics and Department of Biology, Pennsylvania State University

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

    Google Scholar 

  • Li J, Ledger J, Ward T, Del Tredici P (2004) Phylogenetics of Calycanthaceae based on molecular and morphological data, with special reference to divergent paralogues of the nrDNA ITS region. Harv Pap Bot 9:69–82

    Google Scholar 

  • Liò P, Goldman N (1998) Models of molecular evolution and phylogeny. Genome Res 8:1233–1224

    PubMed  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Márquez LM, Miller DJ, MacKenzie JB, Oppen MJH (2003) Pseudogenes contribute to the extreme diversity of nuclear ribosomal DNA in the hard coral Acropora. Mol Biol Evol 20:1077–1086

    Article  PubMed  Google Scholar 

  • Mathews DH, Sabina J, Zuker M, Turner DH (1999) Expanded sequence dependence of thermodynamic parameters improves prediction of RNA secondary structure. J Mol Biol 288:911–940

    Article  PubMed  CAS  Google Scholar 

  • Mayol M, Rosselò JA (2001) Why nuclear ribosomal DNA spacers (ITS) tell different stories in Quercus. Mol Phylogenet Evol 19:167–176

    Article  PubMed  CAS  Google Scholar 

  • Muir G, Fleming CC, Schloetterer C (2001) Three divergent rDNA clusters predate the species divergence in Quercus petraea (Matt) Liebl and Quercus robur L. Mol Biol Evol 18:112–119

    PubMed  CAS  Google Scholar 

  • Peterson A, John H, Koch E, Peterson J (2004) A molecular phylogeny of the genus Gagea (Liliaceae) in Germany inferred from non-coding chloroplast and nuclear DNA sequences. Plant Syst Evol 245:145–162

    Article  CAS  Google Scholar 

  • Razafimandimbison SG, Kellogg 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 

  • Ritz CM, Schmuths H, Wissemann V (2005) Evolution by reticulation: European dogroses originated by multiple hybridization across the genus Rosa. J Hered 96:4–14

    Article  PubMed  CAS  Google Scholar 

  • Ruggiero MV, Procaccini G (2004) The rDNA ITS region in the Lessepsian marine angiosperm Halophila stipulacea (Forssk.) Aschers. (Hydrocharitaceae): intragenomic variability and putative pseudogenic sequences. J Mol Evol 58:115–121

    Article  PubMed  Google Scholar 

  • Schnare MN, Damsberger SH, Gray MW, Gutell RR (1996) Comprehensive comparison of structural characteristics in eukaryotic cytoplasmic large subunit (23 S-like) ribosomal RNA. J Mol Biol 256:701–719

    Article  PubMed  CAS  Google Scholar 

  • Schneider TD, Stephens RM (1990) Sequence logos: a new way to display consensus sequences. Nucleic Acids Res 18:6097–6100

    Article  PubMed  CAS  Google Scholar 

  • Shaner MC, Blair IM, Schneider TD (1993) Sequence logos: a powerful, yet simple, tool. In: Mudge TN et al (eds) Proceedings of the 26th Annual Hawaii International Conference on System Sciences. Architecture and biotechnology computing, vol 1. IEEE Computer Society Press, Los Alamitos, pp 813–821

  • Small RL, Cronn RC, Wendel JF (2004) Use of nuclear genes for phylogeny reconstruction in plants. Aust Syst Bot 17:145–170

    Article  CAS  Google Scholar 

  • Suh YB, Thien LB, Zimmer EA (1992) Nucleotide sequences of the internal transcribed spacers and 58S rRNA gene in Canella winterana (Magnoliales; Canellaceae). Nucleic Acids Res 20:6101–6102

    Article  PubMed  CAS  Google Scholar 

  • Takezaki N, Razhetsky A, Nei M (1995) Phylogenetic test of the molecular clock and linearized trees. Mol Biol Evol 12:823–833

    PubMed  CAS  Google Scholar 

  • Wissemann V (2003) Hybridization and the evolution of the nrITS spacer region. In: Sharma AK, Sharma A (eds) Plant genome, biodiversity and evolution. Part A: phanerogams, vol. 1. Sci Publ Inc., Enfield, pp 57–71

    Google Scholar 

  • Wissemann V, Ritz CM (2005) The genus Rosa (Rosideae, Rosaceae) revisited: molecular analysis of nrITS-1 and atpB-rbsL intergenic spacer (IGS) versus conventional taxonomy. Bot J Linn Soc 147:275–290

    Article  Google Scholar 

  • Won H, Renner SS (2005) The internal transcribed spacer of nuclear ribosomal DNA in the gymnosperm Gnetum. Mol Phylogenet Evol 36:581–597

    Article  PubMed  CAS  Google Scholar 

  • Wuyts J, De Rijk P, Van de Peer Y, Winkelmans T, De Wachter R (2001) The European large subunit ribosomal RNA database. Nucleic Acids Res 29:175–177

    Article  PubMed  CAS  Google Scholar 

  • Yokota Y, Kawata T, Iida Y, Kato A, Tanifuji S (1989) Nucleotide sequences of the 58S rRNA gene and internal transcribed spacer regions in carrot and broad bean ribosomal DNA. J Mol Evol 29:294–301

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Biozentrum, Martin Luther University of Halle-Wittenberg, Weinbergweg 22, 06120, Halle/Saale, Germany

    Doerte Harpke & Angela Peterson

Authors
  1. Doerte Harpke
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Angela Peterson
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Angela Peterson.

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM (PDF 21 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Harpke, D., Peterson, A. Extensive 5.8S nrDNA polymorphism in Mammillaria (Cactaceae) with special reference to the identification of pseudogenic internal transcribed spacer regions. J Plant Res 121, 261–270 (2008). https://doi.org/10.1007/s10265-008-0156-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10265-008-0156-x

Keywords

Search

Navigation