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.
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
Andreasen K, Baldwin BG (2003) Nuclear ribosomal DNA sequence polymorphism and hybridization in checker mallows (Sidalcea, Malvaceae). Mol Phylogenet Evol 29:563–581
Bailey CD, Carr TG, Harris SA, Hughes CE (2003) Characterization of angiosperm nrDNA polymorphism, paralogy, and pseudogenes. Mol Phylogenet Evol 29:435–455
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
Blattner FR (2004) Phylogeny of Hordeum (Poaceae) as inferred by nuclear rDNA ITS sequences. Mol Phylogenet Evol 33:289–299
Buckler IV ES, Ippolito A, Holtsford TP (1997) The evolution of ribosomal DNA: divergent paralogues and phylogenetic implications. Genetics 145:821–832
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
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
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
Elder Jr JF, Turner BJ (1995) Concerted evolution of repetitive DNA sequences in eukaryotes. Q Rev Biol 70:297–320
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
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
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
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
Hartmann S, Nason JD, Bhattacharya D (2001) Extensive ribosomal DNA genic variation in the columnar cactus Lophocereus. J Mol Evol 53:124–134
Hershkovitz MA, Zimmer EA (1997) On the evolutionary origins of the cacti. Taxon 46:217–232
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
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
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
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
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
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
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
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
Kluge AG, Farris JS (1969) Quantitative phyletics and evolution of Anurans. Syst Zool 18:1–32
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
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
Liò P, Goldman N (1998) Models of molecular evolution and phylogeny. Genome Res 8:1233–1224
Liu JS, Schardl CL (1994) A conserved sequence in internal transcribed spacer 1 of plant nuclear rRNA genes. Plant Mol Biol 26:775–778
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
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
Mayol M, Rosselò JA (2001) Why nuclear ribosomal DNA spacers (ITS) tell different stories in Quercus. Mol Phylogenet Evol 19:167–176
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
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
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
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
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
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
Schneider TD, Stephens RM (1990) Sequence logos: a new way to display consensus sequences. Nucleic Acids Res 18:6097–6100
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
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
Takezaki N, Razhetsky A, Nei M (1995) Phylogenetic test of the molecular clock and linearized trees. Mol Biol Evol 12:823–833
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
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
Won H, Renner SS (2005) The internal transcribed spacer of nuclear ribosomal DNA in the gymnosperm Gnetum. Mol Phylogenet Evol 36:581–597
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
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
Zuker M (2003) Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res 31:3406–3415
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights 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
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10265-008-0156-x