Molecular Biology Reports

, Volume 37, Issue 4, pp 1897–1912

Nuclear ribosomal spacer regions in plant phylogenetics: problems and prospects

Article

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).

Keywords

Internal transcribed spacer (ITS) External transcribed spacer (ETS) Intergenic spacer (IGS) Nuclear ribosomal DNA (rDNA) Phylogenetics 

References

  1. 1.
    Dixon MT, Hillis DM (1993) Ribosomal RNA secondary structure: compensatory mutations and implications for phylogenetic analysis. Mol Biol Evol 10(1):256–267PubMedGoogle Scholar
  2. 2.
    Hillis DM, Dixon MT (1991) Ribosomal DNA: molecular evolution and phylogenetic inference. Q Rev Biol 66:411–453PubMedGoogle Scholar
  3. 3.
    Lipscomb D, Farris JS, Källersjö M, Tehler A (1998) Support, ribosomal sequences and the phylogeny of the Eukaryotes. Cladistics 14(4):303–338Google Scholar
  4. 4.
    Caetano-Anollés G (2002) Tracing the evolution of RNA structures in ribosomes. Nucleic Acid Res 30:2575–2587PubMedGoogle Scholar
  5. 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 108–109Google Scholar
  6. 6.
    Wheeler WC, Honeycutt RL (1988) Paired sequence difference in ribosomal RNAs: evolutionary and phylogenetic implications. Mol Biol Evol 5:90–96PubMedGoogle Scholar
  7. 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 82:247–277Google Scholar
  8. 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):199–205Google Scholar
  9. 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):109–120Google Scholar
  10. 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 220:105–116PubMedGoogle Scholar
  11. 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. 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 26:4996–5006PubMedGoogle Scholar
  13. 13.
    Baldridge GD, Dalton MW, Fallon AM (1992) Is higher-order structure conserved in eukaryotic ribosomal DNA intergenic spacers. J Mol Evol 35:514–523PubMedGoogle Scholar
  14. 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 44:258–271PubMedGoogle Scholar
  15. 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 14:4044–4056PubMedGoogle Scholar
  16. 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 45:271–279PubMedGoogle Scholar
  17. 17.
    Álvarez I, Wendel JF (2003) Ribosomal ITS sequences and plant phylogenetic inference. Mol Phylogenet Evol 29:417–434PubMedGoogle Scholar
  18. 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 219:165–179Google Scholar
  19. 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 86:724–734PubMedGoogle Scholar
  20. 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 80:222–238Google Scholar
  21. 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 44:863–884PubMedGoogle Scholar
  22. 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 39:441–453Google Scholar
  23. 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 33:362–367Google Scholar
  24. 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):150–168Google Scholar
  25. 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):636–653PubMedGoogle Scholar
  26. 26.
    Gardes M, Bruns TD (1993) ITS primers with enhanced specificity for basidiomycetes—application to the identification of mycorrhizae and rusts. Mol Ecol 3:113–118Google Scholar
  27. 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):453–460Google Scholar
  28. 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 18:237–278Google Scholar
  29. 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):232–247Google Scholar
  30. 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 17:37–47PubMedGoogle Scholar
  31. 31.
    Martín MP, LaGreaca S, Schmitt I, Lumbsch HT (2003) Molecular phylogeny of Diploschistes inferred from ITS sequence data. Lichenologist 35:27–32Google Scholar
  32. 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 11:406–416PubMedGoogle Scholar
  33. 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):1099–1106PubMedGoogle Scholar
  34. 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):7323–7327PubMedGoogle Scholar
  35. 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):19–29Google Scholar
  36. 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):223–230PubMedGoogle Scholar
  37. 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 14:2403–2417PubMedGoogle Scholar
  38. 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):1180–1191PubMedGoogle Scholar
  39. 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 46:115–120PubMedGoogle Scholar
  40. 40.
    Miadlikowska J, McCune B, Lutzoni F (2002) Pseudocyphellaria perpetua, a new lichen from Western North America. Bryologist 105(1):1–10Google Scholar
  41. 41.
    Koskinen S, Hyvönen J (2004) Poganatum (Polytrichales, Briophyta) revisited. In: Goffinet B(Ed) Molecular systematics of Briophytes. Monographs in Systematic Botany 98:150–167Google Scholar
  42. 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 51:373–383PubMedGoogle Scholar
  43. 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):102–111CrossRefGoogle Scholar
  44. 44.
    Brown MV, Fuhrman JA (2005) Marine bacterial microdiversity as revealed by internal transcribed spacer analysis. Aquat Microbiol Ecol 41(11):15–23Google Scholar
  45. 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):2239–2243PubMedGoogle Scholar
  46. 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):1049–1059PubMedGoogle Scholar
  47. 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):178–180PubMedGoogle Scholar
  48. 48.
    Coleman AW (2003) ITS2 is a double-edged tool for eukaryote evolutionary comparisions. Trends Genet 19(7):370–375PubMedGoogle Scholar
  49. 49.
    Buckler ES, Ippolito A, Holtsford TP (1997) The evolution of ribosomal DNA: divergent paralogues and phylogenetic implications. Genetics 145:821–832PubMedGoogle Scholar
  50. 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 44:911–919Google Scholar
  51. 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 201–214Google Scholar
  52. 52.
    Lapitan NLV (1992) Organization and evolution of higher plant nuclear genomes. Genome 35:171–181Google Scholar
  53. 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 5:451–456PubMedGoogle Scholar
  54. 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 107:272–276PubMedGoogle Scholar
  55. 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 183:169–181Google Scholar
  56. 56.
    Danna KJ, Workman R, Coryell V, Keim P (1996) 5S rRNA genes in tribe Phaseoleae: array size, number, and dynamics. Genome 39:445–455PubMedGoogle Scholar
  57. 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 20:207–211PubMedGoogle Scholar
  58. 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):509–520Google Scholar
  59. 59.
    Patterson C (1987) Ortology and paralogy. In: Molecules and morphology in evolution: conflict or compromise? Cambridge University Press, London, pp 12Google Scholar
  60. 60.
    Sandersomn J, Doyle JJ (1992) Reconstruction of organismal and gene phylogenies from data on multigene families: concerted evolution, homoplasy, and confidence. Syst Biol 41:4–17Google Scholar
  61. 61.
    Masterson J (1994) Stomatal size in fossil plants: evidence for polyploidy in majority of angiosperms. Science 264:421–423PubMedGoogle Scholar
  62. 62.
    Liao D (1999) Concerted evolution: molecular mechanism and biological implications. Am J Hum Genet 64:24–30PubMedGoogle Scholar
  63. 63.
    Dover G (1994) Concerted evolution, molecular drive and natural selection. Curr Biol 4:1165–1166PubMedGoogle Scholar
  64. 64.
    Schlötterer C, Tautz D (1994) Chromosomal homogeneity of Drosophila ribosomal DNA arrays suggests intra chromosomal exchanges drive concerted evolution. Curr Biol 4:777–783PubMedGoogle Scholar
  65. 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 149:243–256PubMedGoogle Scholar
  66. 66.
    Arnheim N (1983) Concerted evolution of multigene families. In: Nei M, Koehn RK (eds) Evolution of genes and proteins. Sinauer, Sunderland, pp 38–61Google Scholar
  67. 67.
    Soltis PS, Soltis DE (1991) Multiple origins of the allotetraploid Tragopogon mirus (Compositae): rDNA evidence. Syst Bot 16:407–413Google Scholar
  68. 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 10:1273–1288PubMedGoogle Scholar
  69. 69.
    Wendel JF, Schnabel A, Seelanan T (1995) Bidirectional interlocus concerted evolution following allopolyploid speciation in cotton (Gossypium). Proc Natl Acad Sci USA 92:280–284PubMedGoogle Scholar
  70. 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 11:2691–2702Google Scholar
  71. 71.
    Zimmer EA, Jupe ER, Walbot V (1988) Ribosomal gene structure, variation and inheritance in maize and its ancestors. Genetics 120:1125–1136PubMedGoogle Scholar
  72. 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):338–350PubMedGoogle Scholar
  73. 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):65–78Google Scholar
  74. 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):730–743PubMedGoogle Scholar
  75. 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 21:229–250Google Scholar
  76. 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):1341–1346PubMedGoogle Scholar
  77. 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):831–834Google Scholar
  78. 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 89:279–286Google Scholar
  79. 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 2:211–217Google Scholar
  80. 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 92:6813–6817PubMedGoogle Scholar
  81. 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 6:995–996Google Scholar
  82. 82.
    Mayol M, Roselló JA (2001) Why nuclear ribosomal DNA spacers (ITS) tell different stories in Quercus? Mol Phylogenet Evol 19:167–176PubMedGoogle Scholar
  83. 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 211:129–139Google Scholar
  84. 84.
    Manos P, Doyle JJ, Nixon KC (1999) Phylogeny, biogeography, and processes of molecular differentiation in Quercus subgenus Quercus (Fagaceae). Mol Phylogenet Evol 12:333–349PubMedGoogle Scholar
  85. 85.
    Bailey CD, Carr TG, Harris SA, Hughes CE (2003) Characterization of angiosperm nrDNA polymorphism, paralogy, and pseudogenes. Mol Phylogenet Evol 29:435–455PubMedGoogle Scholar
  86. 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 34:704–707Google Scholar
  87. 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 27:2271–2282PubMedGoogle Scholar
  88. 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 212:27–35Google Scholar
  89. 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 211:699–712PubMedGoogle Scholar
  90. 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 223:899–910PubMedGoogle Scholar
  91. 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 250:24–36PubMedGoogle Scholar
  92. 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 27:4533–4540PubMedGoogle Scholar
  93. 93.
    Cote CA, Greer CL, Peculis BA (2002) Dynamical conformational model for the role of the ITS2 in pre-RNA processing in yeast. RNA 8:786–797PubMedGoogle Scholar
  94. 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 43:759–771Google Scholar
  95. 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 32:307–315PubMedGoogle Scholar
  96. 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 48:443–453PubMedGoogle Scholar
  97. 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 11:361–364PubMedGoogle Scholar
  98. 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 5:291–294PubMedGoogle Scholar
  99. 99.
    Müller T, Philippi N, Dandekar T, Schultz J, Wolf M (2007) Distinguishing species. RNA 13:1469–1472PubMedGoogle Scholar
  100. 100.
    Kimura M (1985) The role of compensatory neutral mutation in molecular evolution. J Genet 64:7–19Google Scholar
  101. 101.
    Coleman AW, Vacquier VD (2002) Exploring the phylogenetic utility of ITS sequences for animals: a test case for abalone (Haliotis). J Mol Evol 54:246–257PubMedGoogle Scholar
  102. 102.
    Aguilar C, Sánchez JA (2007) Phylogenetic hypotheses of gorgoniid octocorals according to ITS2 and their predicted RNA secondary structures. Mol Phylogenet Evol 43:774–786PubMedGoogle Scholar
  103. 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 29:31–42Google Scholar
  104. 104.
    Liu JS, Schardl CL (1994) A conserved sequence in internal transcribed spacer 1 of plant nuclear rRNA genes. Plant Mol Biol 26:775–778PubMedGoogle Scholar
  105. 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 29:216–234PubMedGoogle Scholar
  106. 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 22:912–919PubMedGoogle Scholar
  107. 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 4:457–462PubMedGoogle Scholar
  108. 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 149:135–146Google Scholar
  109. 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 6:36PubMedGoogle Scholar
  110. 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 36:219–242Google Scholar
  111. 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 269:2373–2379PubMedGoogle Scholar
  112. 112.
    Reeder RH (1984) Enhancers and ribosomal gene spacers. Cell 38:349–351PubMedGoogle Scholar
  113. 113.
    Reeder RH (1990) rRNA synthesis in the nucleolus. Trends Genet 6:390–394PubMedGoogle Scholar
  114. 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 104:41–44PubMedGoogle Scholar
  115. 115.
    Flavell RB (1993) Variation in structure and expression of ribosomal DNA loci in wheat. Genome 31:963–968Google Scholar
  116. 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 395–420Google Scholar
  117. 117.
    Fernnández M, Ruiz ML, Linares C, Fominaya A, Pérez de la Vega M (2005) 5S rDNA genome regions of Lens species. Genome 48:937–942Google Scholar
  118. 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 43:460–468PubMedGoogle Scholar
  119. 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 43:597–603PubMedGoogle Scholar
  120. 120.
    McIntyre CL, Clarke BC, Appels R (1988) DNA sequence analyses of the ribosomal spacer regions in the Triticaceae. Plant Sys Evol 160:91–104Google Scholar
  121. 121.
    Perry KL, Palukaitis P (1990) Transcription of tomato ribosomal DNA and the organization of the intergenic spacer. Mol Gen Genet 221:102–112Google Scholar
  122. 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 371–384Google Scholar
  123. 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):1231–1240Google Scholar
  124. 124.
    Choumane W, Heizmann P (1988) Structure and variability of nuclear ribosomal genes in the genus Helianthus. Theor Appl Genet 76:481–489Google Scholar
  125. 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 201:117–129Google Scholar
  126. 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 218:89–97Google Scholar
  127. 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 16:311–320PubMedGoogle Scholar
  128. 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 49:825–839PubMedGoogle Scholar
  129. 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 229:550–557PubMedGoogle Scholar
  130. 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 36:144–183PubMedGoogle Scholar
  131. 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 195:525–542PubMedGoogle Scholar
  132. 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 49:806–809PubMedGoogle Scholar
  133. 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 15:933–935PubMedGoogle Scholar
  134. 134.
    Kato A, Yakura K, Tanifuji S (1984) Sequence analysis of Vicia faba repeated DNA, the FokI repeat element. Nucleic Acids Res 12:6415–6426PubMedGoogle Scholar
  135. 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 201:1–17PubMedGoogle Scholar
  136. 136.
    Maggini F, Gelati MT, Spolverini M, Frediani M (2008) The intergenic spacer region of the rDNA in Olea europaea L. Tree Genet Genomes 4:293–298Google Scholar
  137. 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 281:207–221PubMedGoogle Scholar
  138. 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 312:275–289PubMedGoogle Scholar
  139. 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. 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 268–326Google Scholar
  141. 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 164:213–227Google Scholar
  142. 142.
    Borisjuk N, Hemleben V (1993) Nucleotide sequence of the potato rDNA intergenic spacer. Plant Mol Biol 21:381–384PubMedGoogle Scholar
  143. 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 17:281–286PubMedGoogle Scholar
  144. 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):13309–13316PubMedGoogle Scholar
  145. 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 10:449–463PubMedGoogle Scholar
  146. 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 14:285–303PubMedGoogle Scholar
  147. 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 88:1675–1687Google Scholar
  148. 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 28:769–774Google Scholar
  149. 149.
    Tremousaygue D, Laudie M, Grellet F, Delseny M (1992) The Brassica oleracea rDNA spacer revisited. Plant Mol Biol 18:1013–1018PubMedGoogle Scholar
  150. 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 36:369–379PubMedGoogle Scholar
  151. 151.
    McMullen MD, Hunter B, Phillips RL, Rubenstein I (1986) The structure of the maize ribosomal DNA spacer region. Nucleic Acids Res 14:4953–4968PubMedGoogle Scholar
  152. 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 218:302–307PubMedGoogle Scholar
  153. 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 46:299–306PubMedGoogle Scholar
  154. 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 75:1238–1247Google Scholar
  155. 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 229:217–236Google Scholar
  156. 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 31:689–700PubMedGoogle Scholar
  157. 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 243:175–187Google Scholar
  158. 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 92:1899–1910Google Scholar
  159. 159.
    Hipp AL, Reznicek AA, Rothrock PE, Weber JA (2006) Phylogeny and classification of Carex section Ovales (Cyperaceae). Int J Plant Sci 167:1029–1048Google Scholar
  160. 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 177:53–69Google Scholar
  161. 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 107:291–298PubMedGoogle Scholar
  162. 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 234:27–51Google Scholar
  163. 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 29:187–202PubMedGoogle Scholar
  164. 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. 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):179–192Google Scholar
  166. 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 23:214–228PubMedGoogle Scholar
  167. 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 190:187–193Google Scholar
  168. 168.
    Kluge AG (1989) A concern for evidence and phylogenetic hypothesis of relationships among Epicrates (Boidae, Serpentes). Syst Zool 38:7–25Google Scholar
  169. 169.
    Nixon KC, Carpenter JM (1996) On simultaneous analysis. Cladistics 12:221–241Google Scholar
  170. 170.
    Grant T, Kluge AG (2003) Data exploration in phylogenetic inference: scientific, heuristic, or neither. Cladistics 19:379–418Google Scholar
  171. 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. 172.
    Wheeler WC, Cartwright P, Hayashi CY (1993) Arthropod phylogeny: combined approach. Cladistics 9:1–39Google Scholar
  173. 173.
    Huson DH, Steel M (2004) Phylogenetic trees based on gene content. Bioinformatics 20(13):2044–2049PubMedGoogle Scholar
  174. 174.
    Huson DH, Kloepper TH (2005) Computing recombination networks from binary sequences. Bioinformatics 21(2):159–165Google Scholar
  175. 175.
    Huson DH, Bryant D (2006) Application of phylogenetic networks in evolutionary studies. Mol Biol Evol 23:254–267PubMedGoogle Scholar
  176. 176.
    Bryant D, Moulton V (2004) NeighborNet: An agglomerative method for the construction of phylogenetic networks. Mol Biol Evol 21(2):255–265PubMedGoogle Scholar
  177. 177.
    Than C, Ruths D, Nakhleh L (2008) PhyloNet: a software package for analyzing and reconstructing reticulate evolutionary relationships. BMC Bioinformatics 9:322PubMedGoogle Scholar
  178. 178.
    Ruths D, Nakhleh L, Ram PT (2008) Rapidly exploring structural and dynamic properties of signaling networks using PathwayOracle. BMC Syst Biol 2:76PubMedGoogle Scholar
  179. 179.
    Kanj I, Nakhleh L, Than C, Xia G (2008) Seeing the trees and their branches in the network is hard. Theor Comput Sci 401:153–164Google Scholar
  180. 180.
    Kanj I, Nakhleh L, Xia G (2008) The compatibility of binary characters on phylogenetic networks: complexity and parameterized algorithms. Algorithmica 51:99–128Google Scholar

Copyright information

© Springer Science+Business Media B.V. 2009

Authors and Affiliations

  1. 1.Department of Plant Sciences and Biotechnology, Georgikon FacultyUniversity of PannoniaKeszthelyHungary
  2. 2.Plant BiologyUniversity of HelsinkiHelsinkiFinland

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