Plant Molecular Biology

, Volume 9, Issue 5, pp 509–520 | Cite as

Ribosomal RNA genes in plants: variability in copy number and in the intergenic spacer

  • Scott O. Rogers
  • Arnold J. Bendich


Ribosomal RNA genes in plants are highly variable both in copy number and in intergenic spacer (IGS) length. This variability exists not only between distantly related species, but among members of the same genus and also among members of the same population of a single species. Analysis of inheritance indicates that copy number change is rapid, occurring even among somatic cells of individual plants, and that up to 90% or more of the gene copies are superfluous. Subrepetitive sequences within the IGS appear to be changing rapidly as well. They are not only variable in sequence from one species to the next, but can vary in number between neighboring gene repeats on the chromosome. In all species examined in detail they are located in the same region of the IGS and contain sequences that can be folded into stem-loop structures flanked by a pyrimidine-rich region. It has been suggested that these subrepeats function in transcriptional enhancement, termination or processing, or in recombination events generating the high multiplicity of ribosomal genes.

Key words

rDNA variability NTS intergenic spacer (IGS) 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. 1.
    Andronico F, DeLucchini S, Graziani F, NardiI, Batistoni R, Barsacchi-Pilone G: Molecular organization of ribosomal RNA genes clustered at variable chromosomal sites in Triturus vulgaris meridionalis (Amphibia, Urodela). J Mol Biol 186: 219–229 (1985).Google Scholar
  2. 2.
    Appels R, Dvořák J: The wheat ribosomal DNA spacer region: Its structure and variation in populations and among species. Theor Appl Genet 63: 337–348 (1982).Google Scholar
  3. 3.
    Appels R, Dvořák J: Relative rates of divergence of species and gene sequences within the rDNA region of species in the Triticeae: Implications for the maintenance of homogeneity of a repeated gene family. Theor Appl Genet 63: 361–365 (1982).Google Scholar
  4. 4.
    Appels R, Gerlach WL, Dennis ES, Swift H, Peacock WJ: Molecular and chromosomal organization of DNA sequences coding for the ribosomal RNAs in cereals. Chromosoma (Berl) 78: 293–311 (1980).Google Scholar
  5. 5.
    Appels R, Honeycutt RL: rDNA: Evolution over a billion years. In: DuttaSK (ed.) DNA Systematics, Vol II: Plants. CRC Press, Inc., Boca Raton, Florida (1986) pp. 81–135.Google Scholar
  6. 6.
    Appels R, MoranL B: The structure of DNA from the rye (Secale cereale) NOR R1 locus and its behaviour in wheat backgrounds. Can J Genet Cytol 28: 673–685 (1986).Google Scholar
  7. 7.
    Avanzi S, Maggini F, Innocenti M: Amplification of ribosomal cistrons during the maturation of metaxylem in the root of Allium cepa. Protoplasma 76: 197–210 (1973).Google Scholar
  8. 8.
    Baker SM, Platt T: Pol I transcription: Which comes first, the end or the beginning? Cell 47: 839–840 (1986).Google Scholar
  9. 9.
    Bassi P, Cionini PG, Cremonini R, Seghizzi P: Under-representation of nuclear DNA sequences in differentiating root cells of Vicia faba. Protoplasma 123: 70–77 (1984).Google Scholar
  10. 10.
    Bendich AJ: Plant mitochondrial DNA: Unusual variation on a common theme. In: Hohn B, Dennis ES (eds) Genetic Flux in Plants. Springer-Verlag, Vienna (1985) pp. 111–138.Google Scholar
  11. 11.
    Bendich AJ: Why do chloroplasts and mitochondria contain so many copies of their genome? BioEssays 6: 279–282 (1987).Google Scholar
  12. 12.
    Bendich AJ, Ward BL: On the evolution and functional significance of DNA sequence organization in vascular plants. In: LeaverCJ (ed.) Genome Organization and Expression in Plants. Plenum Press, New York (1980) pp. 17–30.Google Scholar
  13. 13.
    Buescher PJ, Phillips RL, Brambl R: Ribosomal RNA contents of maize genotypes with different ribosomal RNA gene numbers. Biochem Genet 22: 923–930 (1984).Google Scholar
  14. 14.
    Carmona MJ, DeDominicis RI, Salvi G, Maggini F: Ribosomal RNA genes in biotypes of Scilla peruviana (Liliaceae) Pl Syst Evol 146: 1–11 (1984).Google Scholar
  15. 15.
    Cullis CA: Molecular aspects of the environmental induction of heritable changes in flax. Heredity 38: 129–154 (1977).Google Scholar
  16. 16.
    Cullis CA: Quantitative variation of ribosomal RNA genes in flax genotrophs. Heredity 42: 237–246 (1979).Google Scholar
  17. 17.
    Cullis CA: Environmental induction of heritable changes in flax: Defined environments inducing changes in rDNA and peroxidase isozyme band pattern. Heredity 47: 87–94 (1981).Google Scholar
  18. 18.
    Cullis CA: Plant DNA variation and stress. In: Gustafson JP, Stebbins GL, Ayala FJ (eds) Genetics, Development, and Evolution. Plenum Publishing Co., New York (1986) pp. 143–155.Google Scholar
  19. 19.
    Cullis CA, Charlton L: The induction of ribosomal DNA changes in flax. Plant Sci Lett 20: 213–217 (1981).Google Scholar
  20. 20.
    Cullis CA, Davies DR: Ribosomal DNA amounts in Pisum sativum. Genetics 81: 485–492 (1975).Google Scholar
  21. 21.
    Delseny M, Cooke R, Penon P: Sequence heterogeneity in radish nuclear ribosomal RNA genes. Plant Sci Lett 30: 107–119 (1983).Google Scholar
  22. 22.
    DeWinter RFJ, Moss T: The ribosomal spacer in Xenopus laevis is transcribed as part of the primary ribosomal RNA. Nucleic Acids Res 14: 6041–6051 (1986).Google Scholar
  23. 23.
    Domoney C, Timmis JN: Ribosomal RNA gene redundancy in juvenile and mature ivy (Hedera helix). J Exptl Bot 31: 1093–1110 (1980).Google Scholar
  24. 24.
    Doyle JJ, Beachy RN: Ribosomal gene variation in soybean (Glycine) and its relatives. Theor Appl Genet 70: 369–376 (1985).Google Scholar
  25. 25.
    Dvořák J, Appels R: Chromosome and nucleotide sequence differentiation in genomes of polyploid Triticum species. Theor Appl Genet 63: 349–360 (1982).Google Scholar
  26. 26.
    Dvořák J, Appels R: Investigation of homologous crossing over and sister chromatid exchange in the wheat Nor-B2 locus coding for rRNA and Gli-B2 locus coding for gliadins. Genetics 113: 1037–1056 (1986).Google Scholar
  27. 27.
    Ellis THN, Davies DR, Castleton JA, Bedford ID: The organization and genetics of rDNA length variants in peas. Chromosoma (Berl) 91: 74–81 (1984).Google Scholar
  28. 28.
    Feingold J, Bellofatto V, Shapiro L, Amemiya K: Organization and nucleotide sequence of an rRNA and tRNA cluster from Caulobacter crescentus. J Bacteriol 163: 155–166 (1985).Google Scholar
  29. 29.
    Flavell RB: Repeated sequences and genome change. In: Hohn B, Dennis ES (eds) Genetic Flux in Plants. Springer-Verlag, Vienna/New York (1985) pp. 139–156.Google Scholar
  30. 30.
    Flavell RB: The structure and control of expression of ribosomal RNA genes. In: Miflin B (ed.) Oxford Surveys of Plant Molecular and Cell Biology. Oxford University Press, Oxford, England (1986) pp. 251–274.Google Scholar
  31. 31.
    Flavell RB, O'Dell M: The genetic control of nucleolus formation in wheat. Chromosoma (Berl) 71: 135–152 (1979).Google Scholar
  32. 32.
    Flavell RB, O'Dell M, Sharp P, Nevo E, Beiles A: Variation in the intergenic spacer of ribosomal DNA of wild wheat, Triticum dicoccoides, in Israel. Mol Biol Evol 3: 547–558 (1986).Google Scholar
  33. 33.
    Flavell RB, O'Dell M, Thompson WF, Vincentz M, Sardana R, Barker RF: The differential expression of ribosomal RNA genes. Phil Trans Royal Soc Lond, ser B 314: 385–397 (1986).Google Scholar
  34. 34.
    Fodor I, Beridze T: Structural organization of plant ribosomal DNA. Biochem International 1: 493–501 (1980).Google Scholar
  35. 35.
    Ganal M, Hemleben V: Comparison of the ribosomal RNA genes in four closely related Cucurbitaceae. Pl Syst Evol 154: 63–77 (1986).Google Scholar
  36. 36.
    Gerlach WL, Bedbrook JR: Cloning and characterization of ribosomal RNA genes from wheat and barley. Nucleic Acids Res 7: 1869–1885 (1979).Google Scholar
  37. 37.
    Gerstner J, Schiebel K, Frey M, Hemleben V: Different subrepeats in the ETS and “NTS” cause length heterogeneity of ribosomal DNA of Vigna radiata (mung bean). Plant Mol Biol (submitted).Google Scholar
  38. 38.
    Givens JF, Phillips RL: The nucleolus organizer region of maize (Zea mays L.): Ribosomal RNA gene distribution and nucleolar interactions. Chromosoma (Berl) 57: 103–117 (1976).Google Scholar
  39. 39.
    Goldsborough PB, Cullis CA: Characterization of the genes for ribosomal RNA in flax. NUcleic Acids Res 9: 1301–1309 (1981).Google Scholar
  40. 40.
    Grierson D, Hemleben V: Ribonucleic acid from the higher plant Matthiola incana: Molecular weight measurements and DNA RNA hybridisation studies. Biochim Biophys Acta 475: 424–436 (1977).Google Scholar
  41. 41.
    Grisvard J, Tuffet-Anghileri A: Variations in the satellite DNA content of Cucumis melo in relation to dedifferentiation and hormone concentration. Nucleic Acids Res 8: 2843–2858 (1980).Google Scholar
  42. 42.
    Harrington CA, Chikaraishi DM: Transcription of spacer sequences flanking the rat 45S ribosomal DNA gene. Mol Cell Biol 7: 314–325 (1987).Google Scholar
  43. 43.
    Hemleben V, Ganal M, Gerstner J, Schiebel K, Torres RA: Organization and length heterogeneity of plant ribosomal RNA genes. In: KahlG (ed.) The Architecture of Eukaryotic Genes. VHC, Weinheim (1986).Google Scholar
  44. 44.
    Henderson S, Sollner-Webb B: A transcriptional terminator is a novel element of the promoter of the mouse ribosomal RNA gene. Cell 47: 891–900 (1986).Google Scholar
  45. 45.
    Ingle J, Timmis JN, Sinclair J: The relationship between satellite DNA, ribosomal RNA gene redundancy, and genome size in plants. Plant Physiol 55: 496–501 (1975).Google Scholar
  46. 46.
    Jacqmard A, Kettmann R, Pryke JA, Thiry M, Sachs R: Ribosomal RNA genes and floral evocation in Sinapis. Ann Bot 47: 415–417 (1981).Google Scholar
  47. 47.
    Jorgensen RA, Cuellar RE, Thompson WF: Structure and variation in ribosomal RNA genes of pea: Characterization of a cloned rDNA repeat and chromosomal rDNA variants. Plant Mol Biol 8: 3–12 (1987).Google Scholar
  48. 48.
    Kafatos FC, Orr W, Delidakis: Developmentally regulated gene amplification. Trends in Genet 1: 301–306 (1985).Google Scholar
  49. 49.
    Kato A, Yakura K, Tanifuji S: Organization of ribosomal DNA in the carrot. Plant and Cell Physiol 23: 151–154 (1981).Google Scholar
  50. 50.
    Kato A, Yakura K, Tanifuji S: Repeated DNA sequences found in the large spacer of Vicia faba rDNA. Biochim Biophys Acta 825: 411–415 (1985).Google Scholar
  51. 51.
    Kavanagh TA, Timmis JN: Heterogeneity in cucumber ribosomal DNA. Theor Appl Genet 72: 337–345 (1986).Google Scholar
  52. 52.
    Knälmann M, Burger E-C: Cytologische Lokalisation von 5S und 18/25S RNA Genorten in Mitose-Chromosomen von Vicia faba. Chromosoma (Berl) 61: 177–192 (1977).Google Scholar
  53. 53.
    Labhart P, Reeder RH: Characterization of three sites of RNA 3′ end formation in the Xenopus ribosomal spacer. Cell 45: 431–433 (1986).Google Scholar
  54. 54.
    Lacandena JR, Cermeno MC, Orellana J, Santos JL: Evidence for wheat-rye nucleolar competition (amphiplasty) in triticale by silver staining procedure. Theor Appl Genet 67: 207–213 (1984).Google Scholar
  55. 55.
    Lamppa GK, Honda S, Bendich AJ: The relationship between ribosomal repeat length and genome size in Vicia. Chromosoma (Berl) 89: 1–7 (1984).Google Scholar
  56. 56.
    Lassner M, Dvořák J: Preferential homogenization between adjacent and alternate subrepeats in wheat rDNA. Nucleic Acids Res 14: 5499–5512 (1986).Google Scholar
  57. 57.
    Learn GH Jr, Schaal BA: Population subdivision for ribosomal DNA repeat variants in Clematis fremontii. Evolution 41: 433–438 (1987).Google Scholar
  58. 58.
    Lewin B (ed.) Gene Expression, Vol. 2. Eucaryotic Chromosomes. John Wiley and Sons, New York (1980) pp. 865–906.Google Scholar
  59. 59.
    Lima-de-Faria A, Pero R, Avanzi S, Durante M, Ståhle U, D'Amato F, Granström H: Relation between ribosomal RNA genes and the DNA satellites of Phaseolus coccineus. Hereditas 79: 5–20 (1975).Google Scholar
  60. 60.
    Lohmann K, Kraus K: Length polymorphism of rDNA indicates somatic alterations in the genome of Triturus vulgaris. Dev Biol 114: 534–536 (1986).Google Scholar
  61. 61.
    Long EO, Dawid IB: Repeated genes in eukaryotes. Ann Rev Biochem 49: 727–764 (1980).Google Scholar
  62. 62.
    Macgregor HC, Vlad M, Barnett L: An investigation of some problems concerning nucleolus organizers in salamanders. Chromosoma (Berl) 59: 283–299 (1977).Google Scholar
  63. 63.
    Maggini F, Barsanti P, Marazia T: Individual variation of the nucleolus organizer regions in Allium cepa and A. sativum. Chromosoma (Berl) 66: 173–183 (1978).Google Scholar
  64. 64.
    Maggini F, Carmona MJ: Sequence heterogeneity of the ribosomal DNA in Allium cepa (Liliaceae). Protoplasma 108: 163–171 (1981).Google Scholar
  65. 65.
    Maher EP, Fox DP: Multiplicity of ribosomal RNA genes in Vicia species with different nuclear contents. Nature New Biol 245: 170–172 (1973).Google Scholar
  66. 66.
    Martin PG, Shanks R: Does Vicia faba have multi-stranded chromosomes? Nature 211: 650–651 (1966).Google Scholar
  67. 67.
    Martini G, O'Dell M, Flavell RB: Partial inactivation of wheat nucleolus organisers by the nucleolus organiser chromosomes from Aegilops umbellulata. Chromosoma 84: 687–700 (1982).Google Scholar
  68. 68.
    McMullen MD, Hunter B, Phillips RL, Rubenstein I: The structure of the maize ribosomal DNA spacer region. Nucleic Acids Res 14: 4953–4968 (1986).Google Scholar
  69. 69.
    McStay B, Reeder RH: A termination site for Xenopus RNA polymerase I also acts as an element of an adjacent promoter. Cell 47: 913–920 (1986).Google Scholar
  70. 70.
    Nomura M, Gourse R, Baughman G: Regulation of the synthesis of ribosomes and ribosomal components. Ann Rev Biochem 53: 75–117 (1984).Google Scholar
  71. 71.
    Olmedilla A, Delcasso D, Delseny M, Cawet-Marc A-M: Variability in giant fennel (Ferula communis, Umbelliferae): Ribosomal RNA nuclear genes. Plant Syst Evol 150: 263–274 (1985).Google Scholar
  72. 72.
    Oono K, Sugiura M: Heterogeneity of the ribosomal RNA gene clusters in rice. Chromosoma 76: 85–89 (1980).Google Scholar
  73. 73.
    Polans NO, Weeden NF, Thompson WF: Distribution, inheritance and linkage relationship of ribosomal DNA spacer length variants in pea. Theor Appl Genet 72: 289–295 (1986).Google Scholar
  74. 74.
    Pruitt RE, Meyerowitz EM: Characterization of the genome of Arabidopsis thaliana. J Mol Biol 187: 169–183 (1986).Google Scholar
  75. 75.
    Rafalski JA, Weiwiorowski M, Soll D: Organization of ribosomal DNA in yellow lupine (Lupinus luteus) and sequence of the 5.8S RNA genes. FEBS Lett 152: 241–246 (1983).Google Scholar
  76. 76.
    Reeder RH: Enhancers and ribosomal gene spacers. Cell 38: 349–351 (1984).Google Scholar
  77. 77.
    Reeder RH: Mechanisms of nucleolar dominance in animals and plants. J Cell Biol 101: 2013–2016 (1985).Google Scholar
  78. 78.
    Riven CJ, Zimmer EA, Cullis CA, Walbot V, Huynh T, Davis RW: Evaluation of genomic variability at the nucleic acid level. Plant Mol Biol Rep 1: 9–16 (1983).Google Scholar
  79. 79.
    Riven CJ, Cullis CA, Walbot V: Evaluating quantitative variation in the genome of Zea mays. Genetics 113: 1009–1019 (1986).Google Scholar
  80. 80.
    Rogers SO, Bendich AJ: Heritability and variability in ribosomal RNA genes of Vicia faba. Genetics (in press).Google Scholar
  81. 81.
    Rogers SO, Bendich AJ: Recombination in E. coli between cloned ribosomal RNA intergenic spacers from V. faba: A model for the generation of ribosomal RNA gene heterogeneity in plants. Plant Science (in press).Google Scholar
  82. 82.
    Rogers SO, Honda S, Bendich AJ: Variation in the ribosomal RNA genes among individuals of Vicia faba. Plant Mol Biol 6: 339–345 (1986).Google Scholar
  83. 83.
    Saghai-Maroof MA, Soliman KM, Jorgensen RA, Allard RW: Ribosomal DNA spacer-length polymorphisms in barley: Mendelian inheritance, chromosomal location, and population dynamics. Proc Natl Acad Sci USA 81: 8014–8018 (1984).Google Scholar
  84. 84.
    Santos JL, Lacandena JR, Cermeno MC, Orellana J: Nucleolar organizer activity in wheat-barley chromosome addition lines. Heredity 52: 425–429 (1984).Google Scholar
  85. 85.
    Scheuermann W, Knälmann M: Localization of ribosomal cistrons in metaphase chromosomes of Vicia faba (L.). Exptl Cell Res 90: 463–465 (1975).Google Scholar
  86. 86.
    Schubert I, Bäumlein H, Wobus U: In situ hybridization of iodinated 5S and 18/25S RNA to Vicia faba metaphase chromosomes. Biol Zbl 97: 129–135 (1978).Google Scholar
  87. 87.
    Schubert I, Wobus U: In situ hybridization confirms jumping nucleolus organizing regions in Allium. Chromosoma (Berl) 92: 143–148 (1985).Google Scholar
  88. 88.
    Sears LMS, Lee-Chen S: Cytogenetic studies in Arabidopsis thaliana. Canad J Genet Cytol 12: 217–223 (1970).Google Scholar
  89. 89.
    Shermoen AW, Kiefer BI: Regulation in rDNA-deficient Drosophila melanogaster. Cell 4: 275–280 (1975).Google Scholar
  90. 90.
    Siegel A, Kolacz K: Heterogeneity of pumpkin ribosomal DNA. Plant Physiol 72: 166–171 (1983).Google Scholar
  91. 91.
    Sollner-Webb B, Tower J: Transcription of cloned eukaryotic ribosomal RNA genes. Ann Rev Biochem 55: 801–830 (1986).Google Scholar
  92. 92.
    Subrahmayam NC, Azad AA: Trisomic analysis of ribosomal RNA cistron multiplicity in barley (Hordeum vulgare L.). Chromosoma (Berl) 69: 255–264 (1978).Google Scholar
  93. 93.
    Systma KJ, Schaal BA: Phylogenetics of the Lisianthius skinneri (Gentianaceae) species complex in Panama utilizing DNA restriction fragment analysis. Evolution 39: 594–608 (1985).Google Scholar
  94. 94.
    Tartof KD: Redundant genes. Ann Rev Genet 9: 355–385 (1975).Google Scholar
  95. 95.
    Toloczyki C, Feix G: Occurrence of 9 homologous repeat units in the external spacer region of a nuclear maize rRNA gene unit. Nucleic Acids Res 14: 4969–4986 (1986).Google Scholar
  96. 96.
    Tucci GF, Maggini F: Ribosomal RNA genes in species of the Cynareae tribe (Compositae). I. Protoplasma 132: 76–84 (1986).Google Scholar
  97. 97.
    Vallejos CE, Tanksley SD, Bernatzky R: Localization in the tomato genome of DNA restriction fragments containing sequences homologous to the rRNA (45S), the major chlorophyll a/b binding polypeptide and the ribulose bisphosphate carboxylase genes. Genetics 112: 93–105 (1986).Google Scholar
  98. 98.
    Varsanyi-Breiner A, Gusella JF, Keys C, Houseman DE: The organization of a nuclear DNA sequence from a higher plant: Molecular cloning and characterization of soybean ribosomal DNA. Gene 7: 317–334 (1979).Google Scholar
  99. 99.
    VonKalm L, Vize PD, Smyth DR: An under-methylated region in the spacer of ribosomal RNA genes of Lilium henryi. Plant Mol Biol 6: 33–39 (1986).Google Scholar
  100. 100.
    Vogt VM, Braun R: Structure of ribosomal DNA in Physarum polycephalum. J Mol Biol 106: 567–587 (1976).Google Scholar
  101. 101.
    Vogt VM, Braun R: The replication of ribosomal DNA in Physarum polycephalum. Eur J Biochem 80: 557–587 (1977).Google Scholar
  102. 102.
    Walbot V: On the life strategies of plants and animals. Trends in Genet 1: 165–169 (1985).Google Scholar
  103. 103.
    Walbot V, Cullis CA: Rapid genomic changes in higher plants. Ann Rev Plant Physiol 36: 367–396 (1985).Google Scholar
  104. 104.
    Waldron J, Dunsmuir P, Bedbrook J: Characterization of the rDNA repeat units in the Mitchell Petunia genome. Plant Mol Biol 2: 57–65 (1983).Google Scholar
  105. 105.
    Wellauer PK, Reeder RH, Dawid IB, Brown DD: The arrangement of length heterogeneity in repeating units of amplified and chromosomal ribosomal DNA from Xenopus laevis. J Mol Biol 105: 487–505 (1976).Google Scholar
  106. 106.
    Williams SM, Strobeck C: Sister chromatid exchange and the evolution of rDNA spacer length. J Theor Biol 116: 625–636 (1985).Google Scholar
  107. 107.
    Yakura K, Kato A, Tanifuji S: Structural organization of ribosomal DNA in four Trillium species and Paris verticillata. Plant and Cell Physiol 24: 1231–1240 (1983).Google Scholar
  108. 108.
    Yakura K, Kato A, Tanifuji S: Length heterogeneity in the large spacer of Vicia faba rDNA is due to the differing number of 325 bp repetitive sequence elements. Molec Gen Genet 193: 400–405 (1984).Google Scholar
  109. 109.
    Yakura K, Tanifuji S: The organization of rRNA genes in Vicia faba. Plant and Cell Physiol 22: 1105–1111 (1981).Google Scholar
  110. 110.
    Yakura K, Tanifuji S: Molecular cloning and restriction analysis of EcoRI-fragments of Vicia faba rDNA. Plant and Cell Physiol 24: 1327–1330 (1983).Google Scholar

Copyright information

© Martinus Nijhoff Publishers 1987

Authors and Affiliations

  • Scott O. Rogers
    • 1
  • Arnold J. Bendich
    • 2
  1. 1.Department of BotanyUniversity of WashingtonSeattleUSA
  2. 2.Department of Botany and GeneticsUniversity of WashingtonSeattleUSA

Personalised recommendations