Skip to main content
Log in

Nuclear ribosomal spacer regions in plant phylogenetics: problems and prospects

  • Published:
Molecular Biology Reports Aims and scope Submit manuscript

Abstract

The nuclear ribosomal locus coding for the large subunit is represented in tandem arrays in the plant genome. These consecutive gene blocks, consisting of several regions, are widely applied in plant phylogenetics. The regions coding for the subunits of the rRNA have the lowest rate of evolution. Also the spacer regions like the internal transcribed spacers (ITS) and external transcribed spacers (ETS) are widely utilized in phylogenetics. The fact, that these regions are present in many copies in the plant genome is an advantage for laboratory practice but might be problem for phylogenetic analysis. Beside routine usage, the rDNA regions provide the great potential to study complex evolutionary mechanisms, such as reticulate events or array duplications. The understanding of these processes is based on the observation that the multiple copies of rDNA regions are homogenized through concerted evolution. This phenomenon results to paralogous copies, which can be misleading when incorporated in phylogenetic analyses. The fact that non-functional copies or pseudogenes can coexist with ortholougues in a single individual certainly makes also the analysis difficult. This article summarizes the information about the structure and utility of the phylogenetically informative spacer regions of the rDNA, namely internal- and external transcribed spacer regions as well as the intergenic spacer (IGS).

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

Access this article

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

References

  1. Dixon MT, Hillis DM (1993) Ribosomal RNA secondary structure: compensatory mutations and implications for phylogenetic analysis. Mol Biol Evol 10(1):256–267

    PubMed  CAS  Google Scholar 

  2. Hillis DM, Dixon MT (1991) Ribosomal DNA: molecular evolution and phylogenetic inference. Q Rev Biol 66:411–453

    PubMed  CAS  Google Scholar 

  3. Lipscomb D, Farris JS, Källersjö M, Tehler A (1998) Support, ribosomal sequences and the phylogeny of the Eukaryotes. Cladistics 14(4):303–338

    Google Scholar 

  4. Caetano-Anollés G (2002) Tracing the evolution of RNA structures in ribosomes. Nucleic Acid Res 30:2575–2587

    PubMed  Google Scholar 

  5. Volkov RA, Medina FJ, Zentgraf U, Hemleben V (2004) Molecular cell biology: organization and molecular evolution of rDNA, nucleolar dominance, and nucleus structure. In: Esser K, Luttge Darmstadt U, Lüttge U, Beyschlag W (eds) Progress in botany. Springer, Berlin, pp 108–109

    Google Scholar 

  6. Wheeler WC, Honeycutt RL (1988) Paired sequence difference in ribosomal RNAs: evolutionary and phylogenetic implications. Mol Biol Evol 5:90–96

    PubMed  CAS  Google Scholar 

  7. 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

    Google Scholar 

  8. Maggini F, Marrocco R, Gelati TM, De Dominicis RI (1998) Length and nucleotide sequences of the internal spacers of nuclear ribosomal DNA in gymnosperms and pteridophytes. Plant Syst Evol 213(3–4):199–205

    Google Scholar 

  9. Liston A, Robinson WA, Oliphant JM, Alvarez-Buylla ER (1996) Length variation in the nuclear ribosomal DNA internal transcribed region of non-flowering seed plants. Syst Bot 21(2):109–120

    Google Scholar 

  10. Hadjiolova KV, Georgiev OI, Nosikov VV, Hadjiolov AA (1984) Localization and structure of endonuclease cleavage sites involved in the processing of the rat 32S precursor to ribosomal RNA. Biochem J 220:105–116

    PubMed  CAS  Google Scholar 

  11. Calonje M, Martin-Bravo S, Dobeš C, Gong W, Jordon-Thaden I, Kiefer C, Kiefer M, Paule J, Schmickl R, Koch MA (2008) Non-coding nuclear DNA markers in phylogenetic reconstruction. Plant Syst Evol. doi:10.1007/s00606-008-0031-1

    Google Scholar 

  12. Houseley J, Kotivic K, Hage AE, Tollervey D (2007) Trf4 targets ncRNAs from telomeric and rDNA spacer regions and functions in rDNA copy number control. EMBO J 26:4996–5006

    PubMed  CAS  Google Scholar 

  13. Baldridge GD, Dalton MW, Fallon AM (1992) Is higher-order structure conserved in eukaryotic ribosomal DNA intergenic spacers. J Mol Evol 35:514–523

    PubMed  CAS  Google Scholar 

  14. Mai JC, Coleman AW (1997) The internal transcribed spacer 2 exhibits a common secondary structure in green algae and flowering plants. J Mol Evol 44:258–271

    PubMed  CAS  Google Scholar 

  15. Hadjiolova KV, Normann A, Cavaillé J, Soupéne E, Mazan S, Hadjiolov AA, Bachellerie JP (1994) Processing of truncated mouse or human rRNA transcribed from ribosomal minigenes transfected into mouse cells. Mol Cell Biol 14:4044–4056

    PubMed  CAS  Google Scholar 

  16. Porter CH, Collins FH (1991) Species-diagnostic differences in the ribosomal DNA internal transcribed spacer from the sibling species Anopheles freeborni and Anopheles hermsi (Diptera:Culicidae). Am J Trop Med Hyg 45:271–279

    PubMed  CAS  Google Scholar 

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

    PubMed  Google Scholar 

  18. Vargas P, McAllister HA, Morton C, Jury SL, Wilkinson MJ (1998) Polyploid speciation in Hedera (Araliaceae): phylogenetic and biogeographic insights based on chromosome counts and ITS sequences. Plant Syst Evol 219:165–179

    Google Scholar 

  19. Vargas P, Morton C, Jury SL (1999) Biogeographic patterns in Mediterranean and Macaronesian species of Saxifraga (Saxifragaceae) inferred from phylogenetic analysis using ITS sequences. Am J Bot 86:724–734

    PubMed  CAS  Google Scholar 

  20. Baldwin BG (1993) Molecular phylogenetics of Calycadenia (Compositae) based on ITS sequences of nuclear ribosomal DNA: chromosomal and morphological evolution reexamined. Am J Bot 80:222–238

    CAS  Google Scholar 

  21. Yamaji H, Fukuda T, Yokoyama J, Pak J-H, Zhou C, Yang C, Kondo K, Morota T, Takeda S, Sasaki H, Maki M (2007) Reticulate evolution and phylogeography in Asarum sect. Asiasarum (Aristolochiaceae) documented in internal transcribed specer sequences (ITS) of nuclear ribosomal DNA. Mol Phylogenet Evol 44:863–884

    PubMed  CAS  Google Scholar 

  22. Takamatsu S, Hirata T, Sato Y (1998) Phylogenetic analysis and predicted secondary structures of the rDNA internal transcribed spacers of the powdery mildew fungi (Erysiphaceae). Mycoscience 39:441–453

    CAS  Google Scholar 

  23. Kiss L, Nakasone KK (1999) Ribosomal DNA internal transcribed spacer sequences do not support the species status of Ampelomyces quisqualis a hyperparasite of powdery mildew fungi. Curr Genet 33:362–367

    Google Scholar 

  24. Saenz GS, Taylor JW (1999) Phylogeny of the Erysiphales (powdery mildews) inferred from internal transcribed spacer ribosomal DNA sequences. Can J Bot 77(1):150–168

    CAS  Google Scholar 

  25. Lee SB, Taylor JW (1992) Phylogeny of five fungus-like protoctistan Phytophthora species, inferred from the internal transcribed spacers of ribosomal DNA. Mol Biol Evol 9(4):636–653

    PubMed  CAS  Google Scholar 

  26. Gardes M, Bruns TD (1993) ITS primers with enhanced specificity for basidiomycetes—application to the identification of mycorrhizae and rusts. Mol Ecol 3:113–118

    Google Scholar 

  27. Sikaroodi M, Lawrey JD, Hawksworth DL, Depriest PT (2001) The phylogenetic position of selected lichenicolous fungi: Hobsonia, Illosporium, and Marchandiomyces. Mycol Res 105(4):453–460

    CAS  Google Scholar 

  28. Stenroos S, Hyvönen J, Myllys L, Thell A, Ahti T (2002) Phylogeny of the genus Cladonia s.lat. (Cladoniaceae, Ascomycetes) inferred from molecular, morphological, and chemical data. Cladistics 18:237–278

    Google Scholar 

  29. Stenroos S, Stocker-Wörgötter E, Yoshimura I, Myllys L, Thell A, Hyvönen J (2003) Culture experiments and DNA sequence data confirm the identity of Lobaria photomorphs. Can J Bot 81(9):232–247

    CAS  Google Scholar 

  30. Wu Q-X, Mueller GM, Lutzoni FM, Huang Y-Q, Guo S-Y (2000) Phylogenetic and biogeographic relationships of eastern Asian and North American disjunct Suillus species (Fungi) as inferred from ITS sequences of nuclear ribosomal RNA ITS sequencies. Mol Phylogenet Evol 17:37–47

    PubMed  CAS  Google Scholar 

  31. Martín MP, LaGreaca S, Schmitt I, Lumbsch HT (2003) Molecular phylogeny of Diploschistes inferred from ITS sequence data. Lichenologist 35:27–32

    Google Scholar 

  32. Fritz GN, Conn J, Cockburn A, Seawright J (1994) Sequence analysis of the ribosomal DNA internal transcribed spacer 2 from populations of Anopheles nuneztovari (Diptera: Culucidae). Mol Biol Evol 11:406–416

    PubMed  CAS  Google Scholar 

  33. Nadler SA, Adams BJ, Lyons ET, DeLong RL, Melin SR (2000) Molecular and morphometric evidence for separate species of Uncinaria (Nematoda: Ancylostomatidae) in California sea lions and northern fur seals: hypothesis testing supplants verification. J Parasitol 86(5):1099–1106

    PubMed  CAS  Google Scholar 

  34. Arnheim N, Krystal M, Schnickel R, Wilson G, Ryder O, Zimmer E (1980) Molecular evidence for genetic exchanges among ribosomal genes on nonhomologous chromosomes in man and apes. Proc Natl Acad Sci USA 77(12):7323–7327

    PubMed  CAS  Google Scholar 

  35. Stothard JR, Hughes S, Rollinson D (1995) Variation within the internal transcribed spacer (ITS) of ribosomal DNA genes of intermediate snail hosts within the genus Bulinus (Gastropoda: Planorbidae). Acta Trop 61(1):19–29

    Google Scholar 

  36. Pleyte KA, Duncan SD, Phillips RB (1992) Evolutionary relationships of the salmonid fish genus Salvelinus inferred from DNA sequences of the fish internal transcribed spacer (ITS 1) of ribosomal DNA. Mol Phylogenet Evol 1(3):223–230

    PubMed  CAS  Google Scholar 

  37. van Oppen MJ, Mieog JC, Sanchez CA, Fabricius KE (2005) Diversity of algal endosymbionts (zooxanthellae) in octocorals: the roles of geography and host relationships. Mol Ecol 14:2403–2417

    PubMed  Google Scholar 

  38. Rocap G, Distel DL, Waterbury JB, Chisholm SW (2002) Resolution of Prochlorococcus and Synechococcus ecotypes by using 16S–23S ribosomal DNA internal transcribed spacer sequences. Appl Environ Microbiol 68(3):1180–1191

    PubMed  CAS  Google Scholar 

  39. Leclerc MC, Barrel V, Lecointre G, de Reviers B (1998) Low divergence in rDNA ITS sequences among five species of Fucus (Phaeophyceae) suggests a very recent radiation. J Mol Evol 46:115–120

    PubMed  CAS  Google Scholar 

  40. Miadlikowska J, McCune B, Lutzoni F (2002) Pseudocyphellaria perpetua, a new lichen from Western North America. Bryologist 105(1):1–10

    CAS  Google Scholar 

  41. Koskinen S, Hyvönen J (2004) Poganatum (Polytrichales, Briophyta) revisited. In: Goffinet B(Ed) Molecular systematics of Briophytes. Monographs in Systematic Botany 98:150–167

  42. Zhang Z, Kudo T, Nakajima Y, Wang Y (2001) Clarification of the relationship between the members of the family Thermomonosporaceae on the basis of the rDNS, 16S–23S rRNA internal transcribed spacer and 23S rDNA sequences and chemotaxonomic analysis. Int J Syst Evol Microbiol 51:373–383

    PubMed  CAS  Google Scholar 

  43. Leblond-Bourget N, Philippe H, Mangin I, Decaris B (1996) 16S rRNA and 16S to 23S internal transcribed spacer sequence analysis reveal inter- and intraspecific Bifidobacterium phylogeny. Int J Sys Bacteriol 46(1):102–111

    Article  CAS  Google Scholar 

  44. Brown MV, Fuhrman JA (2005) Marine bacterial microdiversity as revealed by internal transcribed spacer analysis. Aquat Microbiol Ecol 41(11):15–23

    Google Scholar 

  45. Chen F, Wang K, Kan J, Suzuki MT, Wommack KE (2006) Diverse and unique Picocyanobacteria in Chespeake Bay, revealed by 16S–23S rRNA internal transcribed spacer sequences. Appl Environ Microbiol 72(3):2239–2243

    PubMed  CAS  Google Scholar 

  46. Jan-Roblero J, Magos X, Fernández L, Hernández-Rodríguez C, Le Borgne S (2004) Phylogenetic analysis of bacterial populations in waters of the former Texoco Lake, Mexico. Can J Microbiol 50(12):1049–1059

    PubMed  CAS  Google Scholar 

  47. García-Martínez J, Bescós I, Rodríguez-Sala JJ, Rodríguez-Valera F (2001) RISSC: a novel database for ribosomal 16S–23S RNA genes spacer regions. Nucleic Acids Res 29(1):178–180

    PubMed  Google Scholar 

  48. Coleman AW (2003) ITS2 is a double-edged tool for eukaryote evolutionary comparisions. Trends Genet 19(7):370–375

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  50. Feliner NG, Rosselló JA (2007) Better the devil you know? Guidelines for insightful utilization of rDNA ITS in species-level evolutionary studies in plants. Mol Phylogenet Evol 44:911–919

    Google Scholar 

  51. Phillips RL, McMullen MD, Enomoto S, Rubenstein I (1988) Ribosomal DNA in maize. In: Gustafson JP, Appels R (eds) Chromosome structure and function; impact of new concepts. Plenum Press, New York, pp 201–214

    Google Scholar 

  52. Lapitan NLV (1992) Organization and evolution of higher plant nuclear genomes. Genome 35:171–181

    CAS  Google Scholar 

  53. Schrader O, Ahne R, Fuchs J, Schubert I (1997) Computer-aided karyotype analysis of Helianthus annuus after Giemsa banding and fluorescence in situ hybridization. Chromosome Res 5:451–456

    PubMed  CAS  Google Scholar 

  54. Fuchs J, Kühne M, Schubert I (1998) Assignment of linkage groups to pea chromosomes after karyotyping and gene mapping by fluorescent in situ hybridization. Chromosoma 107:272–276

    PubMed  CAS  Google Scholar 

  55. Sastri DC, Hilu K, Appels R, Lagudah ES, Playford J, Baum BR (1992) An overview of evolution in plant 5S DNA. Plant Syst Evol 183:169–181

    CAS  Google Scholar 

  56. Danna KJ, Workman R, Coryell V, Keim P (1996) 5S rRNA genes in tribe Phaseoleae: array size, number, and dynamics. Genome 39:445–455

    PubMed  CAS  Google Scholar 

  57. Pinkel D, Segraves R, Sudar D, Clark S, Poole I, Kowbel D, Collins C, Kuo W-L, Chen C, Zhai Y, Dairkee SH, Ljung B, Gray JW, Albertson DG (1998) High resolution analysis of DNA copy number variation using comparative genomic hybridization to microarrays. Nat Genet 20:207–211

    PubMed  CAS  Google Scholar 

  58. Rogers SO, Bendich AJ (1987) Ribosomal RNA genes in plants: variability in copy number and in the intergenic spacer. Plant Mol Biol 9(5):509–520

    CAS  Google Scholar 

  59. Patterson C (1987) Ortology and paralogy. In: Molecules and morphology in evolution: conflict or compromise? Cambridge University Press, London, pp 12

  60. Sandersomn J, Doyle JJ (1992) Reconstruction of organismal and gene phylogenies from data on multigene families: concerted evolution, homoplasy, and confidence. Syst Biol 41:4–17

    Google Scholar 

  61. Masterson J (1994) Stomatal size in fossil plants: evidence for polyploidy in majority of angiosperms. Science 264:421–423

    PubMed  CAS  Google Scholar 

  62. Liao D (1999) Concerted evolution: molecular mechanism and biological implications. Am J Hum Genet 64:24–30

    PubMed  CAS  Google Scholar 

  63. Dover G (1994) Concerted evolution, molecular drive and natural selection. Curr Biol 4:1165–1166

    PubMed  CAS  Google Scholar 

  64. Schlötterer C, Tautz D (1994) Chromosomal homogeneity of Drosophila ribosomal DNA arrays suggests intra chromosomal exchanges drive concerted evolution. Curr Biol 4:777–783

    PubMed  Google Scholar 

  65. Polanco C, Gonzalez AI, de la Fuente A, Dover GA (1998) Multigene family of ribosomal DNA in Drosophila melanogaster reveals contrasting patterns of homogenization for IGS and ITS spacer regions: a possible mechanism to resolve this paradox. Genetics 149:243–256

    PubMed  CAS  Google Scholar 

  66. Arnheim N (1983) Concerted evolution of multigene families. In: Nei M, Koehn RK (eds) Evolution of genes and proteins. Sinauer, Sunderland, pp 38–61

    Google Scholar 

  67. Soltis PS, Soltis DE (1991) Multiple origins of the allotetraploid Tragopogon mirus (Compositae): rDNA evidence. Syst Bot 16:407–413

    Google Scholar 

  68. Ritland CE, Ritland RK, Straus NA (1993) Variation in the ribosomal internal transcribed spacers (ITS1 and ITS2) among eight taxa of the Mimulus guttatus species complex. Mol Biol Evol 10:1273–1288

    PubMed  CAS  Google Scholar 

  69. 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

    PubMed  CAS  Google Scholar 

  70. Raucher JT, Doyle JJ, Brown HD (2002) Internal transcribed spacer repeat-specific primers and the analysis of hybridization in the Glycine tomentella (Leguminosae) polyploid complex. Mol Ecol 11:2691–2702

    Google Scholar 

  71. Zimmer EA, Jupe ER, Walbot V (1988) Ribosomal gene structure, variation and inheritance in maize and its ancestors. Genetics 120:1125–1136

    PubMed  CAS  Google Scholar 

  72. 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(3):338–350

    PubMed  CAS  Google Scholar 

  73. Wang QD, Zhang T, Wang JB (2007) Phylogenetic relationships and hybrid origin of Potamogeton species (Potamogetonaceae) distributed in China: insights from the nuclear ribosomal internal transcribed spacer sequences (ITS). Plant Syst Evol 267(1–4):65–78

    CAS  Google Scholar 

  74. Ainouche ML, Bayer RJ (1997) On the origins of the tetraploid Bromus species (section Bromus, Poaceae): insights from internal transcribed spacer sequences of nuclear ribosomal DNA. Genome 40(5):730–743

    PubMed  CAS  Google Scholar 

  75. Löhne C, Borsch T, Jacobs SWL, Hellquist CB, Wiersema JH (2008) Nuclear and plastid DNA sequences reveal complex reticulate patterns in Australian water-lilies (Nymphaea subgenus Anecphya, Nymphaeaceae). Aust Sys Bot 21:229–250

    Google Scholar 

  76. Fuertes Aguilar J, Rosselló JA, Nieto Feliner G (1999) Nuclear ribosomal DNA (nrDNA) concerted evolution in natural and artificial hybrids of Armeria (Plumbaginaceae). Mol Ecol 8(8):1341–1346

    PubMed  CAS  Google Scholar 

  77. Franzke A, Mummenhoff K (1999) Recen hybrid speciation in Cardamine (Brassicaceae)–conversion of nuclear ribosomal ITS sequences in statu nascendi. Theor Appl Genet 98(5):831–834

    CAS  Google Scholar 

  78. Hodkinson TR, Chase MW, Takahashi C (2002) The use of DNA sequencing (ITS and trnL-F), AFLP, and fluorescent in situ hybridization to study allopolyploid Miscanthus (Poaceae). Am J Bot 89:279–286

    CAS  Google Scholar 

  79. Whittall J, Liston A, Gisler S, Meinke RJ (2000) Detecting nucleotide additivity from direct sequences is a SNAP: an example from Sidalcea (Malvaceae). Plant Biol 2:211–217

    CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  81. Quijada A, Liston A, Robinson W, Alvarez Buylla E (1997) The ribosomal ITS region as a marker to detect hybridization in pines. Mol Ecol 6:995–996

    CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  83. Samuel R, Bachmair A, Jobst J, Ehrendorfer F (1998) ITS sequences from nuclear rDNA suggest phylogenetic relationships between Euro-Mediterranean, East Asiatic and north American taxa of Quercus (Fagaceae). Plant Syst Evol 211:129–139

    CAS  Google Scholar 

  84. Manos P, Doyle JJ, Nixon KC (1999) Phylogeny, biogeography, and processes of molecular differentiation in Quercus subgenus Quercus (Fagaceae). Mol Phylogenet Evol 12:333–349

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  86. Schultz J, Müller T, Achtziger M, Seibel PN, Dandekar T, Wolf M (2006) The internal transcribed spacer 2 database-a web based server for (not only) low level phylogenetic analyses. Nucleic Acids Res 34:704–707

    Google Scholar 

  87. Michot B, Joseph N, Mazan S, Bachellerie J (1999) Evolutionarily conserved structuresal features in the ITS2 of mammalian pre-RNAs and potential interactions with the snoRNA U8 detected by comparative analysis of new mouse sequences. Nucleic Acids Res 27:2271–2282

    PubMed  CAS  Google Scholar 

  88. Gonzales IL, Chambers C, Gorski JL, Stambolian D, Schmickel RD, Sylvester JE (1990) Sequence and structure correlation of human ribosomal transcribed spacers. J Mol Biol 212:27–35

    Google Scholar 

  89. Yeh LC, Lee JC (1990) Structural analysis of the internal transcribed spacer 2 of the prescursor ribosomal RNA from Saccharomyces cerevisiae. J Mol Biol 211:699–712

    PubMed  CAS  Google Scholar 

  90. van der Sande CAFM, Kwa M, van Nues RW, van Heerikhuizen H, Raue HA, Planta RJ (1992) Functional analysis of internal transcribed spacer 2 of Saccharomyces cerevisiae ribosomal DNA. J Mol Biol 223:899–910

    PubMed  Google Scholar 

  91. Van Nues RW, Rientjes JMJ, Morre SA, Mollee E, Planta RJ, Venema J, Raue HA (1995) Evolutionarily conserved structural elements are critical for processing of internal transcribed spacer 2 from Saccharomyces cerevisiae precursor ribosomal RNA. J Mol Biol 250:24–36

    PubMed  Google Scholar 

  92. Joseph N, Krauskopf E, Vera M, Michot B (1999) Ribosomal internal transcribed spacer 2 (ITS2) exhibits a common core of secondary structure in vertebrates and yeast. Nucleic Acids Res 27:4533–4540

    PubMed  CAS  Google Scholar 

  93. Cote CA, Greer CL, Peculis BA (2002) Dynamical conformational model for the role of the ITS2 in pre-RNA processing in yeast. RNA 8:786–797

    PubMed  CAS  Google Scholar 

  94. Chen CA, Chang CC, Wei NV, Chen CH, Lein YT, Lin HE, Dai CF, Wallace CC (2004) Secondary structure and phylogenetic utility of the ribosomal internal transcribed spacer 2 (ITS2) in scleractinian corals. Zool Stud 43:759–771

    CAS  Google Scholar 

  95. Gottschling M, Plötner J (2004) Secondary structure models of the nuclear internal transcribed spacer regions and 5.8S rRNA in Calciodinelloideae (Peridiniaceae) and other dinoagellates. Nucleic Acids Res 32:307–315

    PubMed  CAS  Google Scholar 

  96. Needleman SB, Wunsch CD (1970) A general method applicable to the search for similarities in the amino acid sequence of two proteins. J Mol Biol 48:443–453

    PubMed  CAS  Google Scholar 

  97. Schultz J, Maisel S, Gerlach D, Müller T, Wolf M (2005) A common core of secondary structure of the internal transcribed spacer 2 (ITS2) throughout the Eukaryota. RNA 11:361–364

    PubMed  CAS  Google Scholar 

  98. Wolf M, Friendrich J, Dandekar T, Müller T (2005) CBCAnalyzer: inferring phylogenies based on compensatory base changes in RNA secondary structures. In Silico Biol 5:291–294

    PubMed  CAS  Google Scholar 

  99. Müller T, Philippi N, Dandekar T, Schultz J, Wolf M (2007) Distinguishing species. RNA 13:1469–1472

    PubMed  Google Scholar 

  100. Kimura M (1985) The role of compensatory neutral mutation in molecular evolution. J Genet 64:7–19

    CAS  Google Scholar 

  101. Coleman AW, Vacquier VD (2002) Exploring the phylogenetic utility of ITS sequences for animals: a test case for abalone (Haliotis). J Mol Evol 54:246–257

    PubMed  CAS  Google Scholar 

  102. Aguilar C, Sánchez JA (2007) Phylogenetic hypotheses of gorgoniid octocorals according to ITS2 and their predicted RNA secondary structures. Mol Phylogenet Evol 43:774–786

    PubMed  CAS  Google Scholar 

  103. Sánchez JA, Lasker HR, Taylor DJ (2003) Phylogenetic analyses among octocorals (Cnidaria) according to mitochondrial and nuclear DNA sequences (lsu-rRNA 16S, and ssu-rRNA 18S) support two convergent clades of branching gorgonians. Mol Phylogenet Evol 29:31–42

    Google Scholar 

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

    PubMed  CAS  Google Scholar 

  105. Goertzen LR, Cannone JJ, Gutell RR, Jansen RK (2003) ITS secondary structure derived from comparative analysis: implications for sequence alignment and phylogeny of the Asteraceae. Mol Phylogenet Evol 29:216–234

    PubMed  CAS  Google Scholar 

  106. Van Nues RW, Rientejes JMJ, van der Sande CAFM, Zerp SF, Sluiter C, Venema J, Planta RJ, Raué HA (1994) Separate structural elements within internal transcribed spacer 1 of Saccharomyces cerevisiae precursor ribosomal RNA direct the formation of 17S and 26S rRNA. Nucleic Acids Res 22:912–919

    PubMed  Google Scholar 

  107. Schilthuizen M, Gittenberger E, Gultyaev AP (1995) Phylogenetic relationships inferred from the sequence and secondary structure of ITS1 rRNA in Albinaria and putative Isabellaria species (Gastropoda, Pulmonata, Clausiliidae). Mol Phylogenet Evol 4:457–462

    PubMed  CAS  Google Scholar 

  108. Coleman AW, Preparata RM, Mehrotra B, Mai JC (1998) Derivation of the secondary structure of the ITS-1 transcript in Volvocales and its taxonomic correlation. Protist 149:135–146

    Google Scholar 

  109. Kay KM, Whittall JB, Hodges SA (2006) A survey of nuclear ribosomal internal transcribed spacer substitution rates across angiosperms: an approximate molecular clock with life history effects. BMC Evol Biol 6:36

    PubMed  Google Scholar 

  110. Weider LJ, Elser JJ, Crease TJ, Mateos M, Cotner JB, Markow TA (2005) The functional significance of ribosomal (r) DNA variation: impacts on the evolutionary ecology of organisms. Annu Rev Ecol Evol Syst 36:219–242

    Google Scholar 

  111. Gorokhova E, Dowling TA, Crease T, Weider LJ, Elser JJ (2002) Functional and ecological significance of rDNA IGS variation in a clonal organism under divergent selection for production rate. Proc R Soc B 269:2373–2379

    PubMed  CAS  Google Scholar 

  112. Reeder RH (1984) Enhancers and ribosomal gene spacers. Cell 38:349–351

    PubMed  CAS  Google Scholar 

  113. Reeder RH (1990) rRNA synthesis in the nucleolus. Trends Genet 6:390–394

    PubMed  CAS  Google Scholar 

  114. Alvares LE, Brison O, Ruiz IR (1998) Identification of enchancer-like elements in the ribosomal intergenic spacer of Odontophrynus americanus 2n and 4n (Amphibia, Anura). Genetica 104:41–44

    PubMed  CAS  Google Scholar 

  115. Flavell RB (1993) Variation in structure and expression of ribosomal DNA loci in wheat. Genome 31:963–968

    Google Scholar 

  116. Paule MR, Lofquist AK (1996) Organization and expression of eukaryotic ribosomal RNA genes. In: Zimmerman RA, Dahlberg AE (eds) Ribosomal RNA: structure, evolution, processing, and function in protein biosynthesis. CRC Press, New York, pp 395–420

    Google Scholar 

  117. Fernnández M, Ruiz ML, Linares C, Fominaya A, Pérez de la Vega M (2005) 5S rDNA genome regions of Lens species. Genome 48:937–942

    Google Scholar 

  118. Bhatia S, Singh Negi M, Lakshmikumaran M (1996) Structural analysis of the rDNA intergenic spacer of Brassica nigra:evolutionary divergence of the spacers of the three diploid Brassica species. J Mol Evol 43:460–468

    PubMed  CAS  Google Scholar 

  119. Fernández M, Polanco C, Ruiz ML, Perez de la Vega M (2000) A comparative study of the structure of the rDNA intergenic spacer of Lens culinaris Medik., and other legume species. Genome 43:597–603

    PubMed  Google Scholar 

  120. McIntyre CL, Clarke BC, Appels R (1988) DNA sequence analyses of the ribosomal spacer regions in the Triticaceae. Plant Sys Evol 160:91–104

    CAS  Google Scholar 

  121. Perry KL, Palukaitis P (1990) Transcription of tomato ribosomal DNA and the organization of the intergenic spacer. Mol Gen Genet 221:102–112

    CAS  Google Scholar 

  122. Hemleben V, Ganal M, Grestner J, Schiebel K, Torres RA (1988) Organization and length heterogeneity of plant ribosomal RNA genes. In: Kahl G (ed) The architecture of eukaryotic gene. VHC, Weinheim, pp 371–384

    Google Scholar 

  123. Yakura K, Kato A, Tanifuji S (1983) Structural organization of ribosomal DNA in four Trillium species and Paris verticillata. Plant Cell Phys 24(7):1231–1240

    CAS  Google Scholar 

  124. Choumane W, Heizmann P (1988) Structure and variability of nuclear ribosomal genes in the genus Helianthus. Theor Appl Genet 76:481–489

    CAS  Google Scholar 

  125. Volkov R, Kostishin S, Ehrendorfer E, Schweizer D (1996) Molecular organization and evolution of the external transcribed rDNA spacer region in two diploid relatives of Nicotiana tabacum (Solanaceae). Plant Syst Evol 201:117–129

    CAS  Google Scholar 

  126. Volkov RA, Bachmair A, Panchuk II, Kostyshyn SS, Schweizer D (1999) 25S–18S rDNA intergenic spacer of Nicotiana sylvestris (Solanaceae): primary and secondary structure analysis. Plant Syst Evol 218:89–97

    CAS  Google Scholar 

  127. Volkov RA, Borisjuk NV, Panchuk BI, Schweizer D, Hemleben V (1999) Elimination and rearrangement of parental rDNA in the allotetraploid Nicotiana tabacum. Mol Biol Evol 16:311–320

    PubMed  CAS  Google Scholar 

  128. Maughan PJ, Kolano BA, Maluszynska J, Coles ND, Bonifacio A, Rojas J, Coleman CE, Stevens MR, Fairbanks DJ, Parkinson SE, Jellen EN (2006) Molecular and cytological characterization of ribosomal RNA genes in Chenopodium quinoa and Chenopodium berlandieri. Genome 49:825–839

    PubMed  CAS  Google Scholar 

  129. Da Rocha PS, Bertrand H (1995) Structure and comparative analysis of the rDNA intergenic spacer of Brassica rapa. Implications for the function and evolution of the Cruciferae spacer. Eur J Biochem 229:550–557

    PubMed  Google Scholar 

  130. King K, Torres RA, Zentgraf U, Hembleben V (1993) Molecular evolution of the intergeneric spacer in the nuclear ribosomal RNA genes of Cucurbitaceae. J Mol Evol 36:144–183

    PubMed  CAS  Google Scholar 

  131. Tautz D, Tautz C, Webb D, Dover GA (1987) Evolutionary divergence of promoters and spacers in the rDNA family of four Drosophila species. Implications for molecular coevolution in multigene families. J Mol Biol 195:525–542

    PubMed  CAS  Google Scholar 

  132. Ryu SH, Do YK, Hwang UW, Choe CP, Kim W (1999) Ribosomal DNA intergenic spacer of the swimming crab, Charybdis japonica. J Mol Evol 49:806–809

    PubMed  CAS  Google Scholar 

  133. Takaiwa F, Kikuchi S, Oono K (1990) The complete nucleotide sequence of the intergenic spacer between 25S and 17S rDNAs in rice. Plant Mol Biol 15:933–935

    PubMed  CAS  Google Scholar 

  134. Kato A, Yakura K, Tanifuji S (1984) Sequence analysis of Vicia faba repeated DNA, the FokI repeat element. Nucleic Acids Res 12:6415–6426

    PubMed  CAS  Google Scholar 

  135. Barker RF, Harberd NP, Jarvis MG, Flavell RB (1988) Structure and evolution of the intergenic region in a ribosomal DNA repeat unit of wheat. J Mol Biol 201:1–17

    PubMed  CAS  Google Scholar 

  136. Maggini F, Gelati MT, Spolverini M, Frediani M (2008) The intergenic spacer region of the rDNA in Olea europaea L. Tree Genet Genomes 4:293–298

    Google Scholar 

  137. Bauer N, Horvat T, Biruš I, Vičić V, Zoldoš V (2009) Nucleotide sequence structural organization and length heterogeneity of ribosomal DNA intergenic spacer in Quercus petraea (Matt.) Liebl. and Q. robur L. Mol Genet Genomics 281:207–221

    PubMed  CAS  Google Scholar 

  138. Dover GA, Tautz D (1986) Conservation and divergence in multigene families: alternatives to selection and drift. Philos Trans R Soc Lond B Biol Sci 312:275–289

    PubMed  CAS  Google Scholar 

  139. Ryu S, Do Y, Fitch DHA, Kim W, Mishra B (2009) Dropout alignment allows homology recognition and evolutionary analysis if rDNA intergenic spacers. J Mol Evol. doi:10.1007/s00239-008-9090-8

    Google Scholar 

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

    Google Scholar 

  141. Starr JR, Harris SA, Simpson DA (2003) Potential of the 5′ and 3′ ends of the intergenic spacer (IGS) of rDNA in the Cyperaceae: new sequences for lower-level phylogenies in sedges with an example from Uncinia Pers. Int J Plant Sci 164:213–227

    CAS  Google Scholar 

  142. Borisjuk N, Hemleben V (1993) Nucleotide sequence of the potato rDNA intergenic spacer. Plant Mol Biol 21:381–384

    PubMed  CAS  Google Scholar 

  143. Granneman S, Baserga SJ (2005) Crosstalk in gene expression: coupling and co-regulation of rDNA transcription, pre-ribosome assembley and pre-rRNA processing. Curr Op Cell Biol 17:281–286

    PubMed  CAS  Google Scholar 

  144. Azuma M, Toyama R, Laver E, Dawid IB (2006) Perturbation of rRNA synthesis in the bap28 mutation leads to apoptosis mediated by p53 in zebrafish central nervous system. J Biol Chem 281(19):13309–13316

    PubMed  CAS  Google Scholar 

  145. Baldwin BG, Markos S (1998) Phylogenetic utility of the external transcribed spacer (ETS) of 18S–26S rDNA: congruence of ETS and ITS trees of Calycadenia (Compositae). Mol Phylogenet Evol 10:449–463

    PubMed  CAS  Google Scholar 

  146. Linder CR, Goertzen LR, Vanden Heuvel B, Francisco-Ortega J, Jansen RK (2000) The complete external transcribed spacer of 18S–26S rDNA: amplification and phylogenetic utility at low taxonomic levels in Asteraceae and closely allied families. Mol Phylogenet Evol 14:285–303

    PubMed  CAS  Google Scholar 

  147. Chandler GT, Bayer RJ, Crisp MD (2001) A molecular phylogeny of the endemic Australian genus Gastrolobium (Fabaceae: Mirbelieae) and allied genera using chloroplast and nuclear markers. Am J Bot 88:1675–1687

    CAS  Google Scholar 

  148. Wright SD, Yong CG, Wichman SR, Dawson JW, Gardner RC (2001) Stepping stones to Hawaii: a trans-equatorial dispersal pathway for Metrosidos (Myrtaceae) inferred from rDNA (ITS + ETS). J Biogeogr 28:769–774

    Google Scholar 

  149. Tremousaygue D, Laudie M, Grellet F, Delseny M (1992) The Brassica oleracea rDNA spacer revisited. Plant Mol Biol 18:1013–1018

    PubMed  CAS  Google Scholar 

  150. Cordesse F, Cooke R, Tremousaygue D, Greellet F, Delseny M (1993) Fine structure and evolution of the rDNA intergenic spacer in rice and other cereals. J Mol Evol 36:369–379

    PubMed  CAS  Google Scholar 

  151. McMullen MD, Hunter B, Phillips RL, Rubenstein I (1986) The structure of the maize ribosomal DNA spacer region. Nucleic Acids Res 14:4953–4968

    PubMed  CAS  Google Scholar 

  152. Schiebel K, von Waldburg G, Gerstner J, Hemleben V (1989) Termination of transcription of ribosomal RNA genes of mung bean occurs within a 175 bp repetitive element of the spacer region. Mol Gen Genet 218:302–307

    PubMed  CAS  Google Scholar 

  153. Bena G, Jubier MF, Olivieri I, Lejeune B (1998) Ribosomal external and internal transcribed spacers: combined use in the phylogenetic analysis of Medicago (Leguminosae). J Mol Evol 46:299–306

    PubMed  CAS  Google Scholar 

  154. Jorgensen RA, Cluster PD (1988) Modes and tempos in the evolution of nuclear ribosomal DNA: new characters for evolutionary studies and new markers for genetic and population studies. Ann Missouri Bot Gard 75:1238–1247

    Google Scholar 

  155. Bena G (2001) Molecular phylogeny supports the morphologically based taxonomic transfer of the “medicagoid” Trigonella species to the genus Medicago L. Plant Syst Evol 229:217–236

    CAS  Google Scholar 

  156. Yamashiro T, Fukuda T, Yokoyama J, Maki M (2004) Molecular phylogeny of Vincetoxicum (Apocynaceae-Asclepladoideae) based on the nucleotide sequences of cpDNA and nrDNA. Mol Phylogenet Evol 31:689–700

    PubMed  CAS  Google Scholar 

  157. Roalson EH, Friar EA (2004) Phylogenetic relationships and biogeographic patterns in North American members of Carex section Acrocystis (Cyperaceae) using nrDNA ITS and ETS sequence data. Plant Syst Evol 243:175–187

    Google Scholar 

  158. Kay KM, Reeves PA, Olmstead RG, Schemske DW (2005) Rapid speciation and the evolution of hummingbird pollination in neotropical Costus subgenus Costus (Costaceae): evidence from nrDNA ITS and ETS sequences. Am J Bot 92:1899–1910

    CAS  Google Scholar 

  159. Hipp AL, Reznicek AA, Rothrock PE, Weber JA (2006) Phylogeny and classification of Carex section Ovales (Cyperaceae). Int J Plant Sci 167:1029–1048

    Google Scholar 

  160. Kim K-J, Mabry TJ (1991) Phylogenetic and evolutionary implications of nuclear ribosomal DNA variation in dwarf dandelions (Krigia, Lactuceae, Asteraceae). Plant Syst Evol 177:53–69

    CAS  Google Scholar 

  161. Vander Stappen J, Marant S, Volckaert G (2003) Molecular characterization and phylogenetic utility of the rDNA external transcribed spacer region in Stylosanthes (Fabaceae). Theor Appl Genet 107:291–298

    PubMed  CAS  Google Scholar 

  162. Vander Stappen J, De Laet J, Gama Lopez S, Van Campenhout S, Volckaert G (2002) Phylogenetic analysis of Stylosanthes (Fabaceae) based on the internal transcribed spacer region (ITS) of nuclear ribosomal DNA. Plant Syst Evol 234:27–51

    Google Scholar 

  163. Volkov RA, Kamarova NY, Panchuk II, Hemleben V (2003) Molecular evolution of rDNA external transcribed spacer and phylogeny of sect. Petota (genus Solanum). Mol Phylogenet Evol 29:187–202

    PubMed  CAS  Google Scholar 

  164. Kamarova NY, Grimm GW, Hemleben V, Volkov RA (2009) Molecular evolution of 35S rDNA and taxonomic status of Lycopersicon within Solanum sect. Petota. Plant Syst Evol. doi:10.1007/s00606-008-0091-2

    Google Scholar 

  165. Oh S-H, Potter D (2005) Molecular phylogenetic systematics and biogeography of tribe Neillieae (Rosaceae) using DNA sequences of cpDNA, rDNA, and LEAFY. Am J Bot 92(1):179–192

    CAS  Google Scholar 

  166. Markos S, Baldwin BG (2002) Structure, molecular evolution, and phylogenetic utility of the 5′ region of the external transcribed spacer of 18S–26S rDNA in Lessingia (Compositae, Asteraceae). Mol Phylogenet Evol 23:214–228

    PubMed  CAS  Google Scholar 

  167. Tucci GF, Simeone MC, Gregori C, Maggini F (1994) Intergenic spacers of rRNA genes in three species of the Cynareae (Asteraceae). Plant Syst Evol 190:187–193

    CAS  Google Scholar 

  168. Kluge AG (1989) A concern for evidence and phylogenetic hypothesis of relationships among Epicrates (Boidae, Serpentes). Syst Zool 38:7–25

    Google Scholar 

  169. Nixon KC, Carpenter JM (1996) On simultaneous analysis. Cladistics 12:221–241

    Google Scholar 

  170. Grant T, Kluge AG (2003) Data exploration in phylogenetic inference: scientific, heuristic, or neither. Cladistics 19:379–418

    Google Scholar 

  171. Varón A, Vinh LS, Bomash I, Wheeler WC (2009) POY 4.1.1. American Museum of Natural History. http://research.amnh.org/scicomp/projects/poy.php

  172. Wheeler WC, Cartwright P, Hayashi CY (1993) Arthropod phylogeny: combined approach. Cladistics 9:1–39

    Google Scholar 

  173. Huson DH, Steel M (2004) Phylogenetic trees based on gene content. Bioinformatics 20(13):2044–2049

    PubMed  CAS  Google Scholar 

  174. Huson DH, Kloepper TH (2005) Computing recombination networks from binary sequences. Bioinformatics 21(2):159–165

    Google Scholar 

  175. Huson DH, Bryant D (2006) Application of phylogenetic networks in evolutionary studies. Mol Biol Evol 23:254–267

    PubMed  CAS  Google Scholar 

  176. Bryant D, Moulton V (2004) NeighborNet: An agglomerative method for the construction of phylogenetic networks. Mol Biol Evol 21(2):255–265

    PubMed  CAS  Google Scholar 

  177. Than C, Ruths D, Nakhleh L (2008) PhyloNet: a software package for analyzing and reconstructing reticulate evolutionary relationships. BMC Bioinformatics 9:322

    PubMed  Google Scholar 

  178. Ruths D, Nakhleh L, Ram PT (2008) Rapidly exploring structural and dynamic properties of signaling networks using PathwayOracle. BMC Syst Biol 2:76

    PubMed  Google Scholar 

  179. Kanj I, Nakhleh L, Than C, Xia G (2008) Seeing the trees and their branches in the network is hard. Theor Comput Sci 401:153–164

    Google Scholar 

  180. Kanj I, Nakhleh L, Xia G (2008) The compatibility of binary characters on phylogenetic networks: complexity and parameterized algorithms. Algorithmica 51:99–128

    Google Scholar 

Download references

Acknowledgments

Thanks are due to Dr. János Taller for the editing of the manuscript and to three anonymous reviewers for the helpful advices and comments.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Péter Poczai.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Poczai, P., Hyvönen, J. Nuclear ribosomal spacer regions in plant phylogenetics: problems and prospects. Mol Biol Rep 37, 1897–1912 (2010). https://doi.org/10.1007/s11033-009-9630-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11033-009-9630-3

Keywords

Navigation