Summary
The intergenic spacer of a rice ribosomal RNA gene repeating unit has been completely sequenced. The spacer contains three imperfect, direct repeated regions of 264–253 bp, followed by a related but more highly divergent region. Detailed analysis of the sequence allows the presentation of an evolutionary scenario in which the 264–253-bp repeats are derived from an ancestral 150-bp sequence by deletion and amplification. Comparison of the rice sequence with those of maize, wheat, and rye shows that, despite considerable divergence from the ancestral sequence, several regions have been highly conserved, suggesting that they may play an important role in the structure and/or expression of the ribosomal genes.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Abbreviations
- IGS:
-
ribosomal gene intergenic spacer
- rDNA:
-
ribosomal DNA
- rRNA:
-
ribosomal RNA
References
Appels R, Moran LB, Gustafson JP (1986) 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
Barker RF, Harberd NP, Jarvis MG, Flavell RB (1988) Structure and evolution of the intergenic region of a ribosomal DNA repeat unit of wheat. J Mol Biol 201:1–17
Chen EY, Seeburg PH (1985) Supercoil sequencing: a fast and simple method for sequencing plasmid DNA. DNA 4:165–170
Cordesse F, Second G, Delseny M (1990) Ribosomal gene spacer length variability in cultivated and wild rice species. Theor Appl Genet 79:81–88
Cordesse F, Grellet F, Reddy AS, Delseny M (1992) Genome specificity of rDNA spacer fragments from Oryza sativa L. Theor Appl Genet 83:864–870
Delcasso-Tremousaygue D, Grellet F, Panabieres F, Ananiev ED, Delseny M (1988) Structural and transcriptional characterization of the external spacer of a ribosomal RNA nuclear gene from a higher plant. Eur J Biochem 172:767–776
Dover G (1986) Molecular drive in multigene families: how biological novelties arise, spread and are assimilated. Trends Genet 2:159–165
Dover G, Flavell RB (1984) Molecular coevolution: DNA divergence and the maintenance of function. Cell 38:622–633
Echeverria M, Tremousaygue D, Delseny M (1992) A nuclear protein fraction binding to dA/dT-rich sequences upstream from the radish rDNA promoter. Plant J 2:211–219
Flavell RB (1989) Variation in structure and expression of ribosomal DNA loci in wheat. Genome 31:963–968
Gerstner J, Schiebel K, von Waldburg G, Hemleben V (1988) Complex organization of the length heterogeous 5′external spacer of mung bean (Vigna radiata) ribosomal DNA. Genome 30:723–733
Grellet F, Delcasso-Tremousaygue D, Delseny M (1989) Isolation and characterization of an unusual repeated sequence from the ribosomal intergenic spacer of the crucifer Sisymbrium irio. Plant Mol Biol 12:695–706
Grellet F, Delcasso D, Panabieres F, Delseny M (1986) Organisation and evolution of a higher plant alphoid-like satellite DNA sequence. J Mol Biol 187:495–507
Gruendler P, Unfried I, Pointner R, Schweizer D (1989) Nucleotide sequence of the 25S–18S ribosomal gene spacer from Arabidopsis thaliana. Nucleic Acids Res 17:6395–6396
Hemleben V, Ganal M, Gerstner J, Schiebel K, Torres RA (1988) Organization and length heterogenicity of plant ribosomal RNA. In: Kahl G (ed) Genes in architecture of the eukaryotic gene, pp 371–383. VCH verlagsgellschaft, Weinkeim, Federal Republic of Germany
Higgins DG, Sharp PM (1989) Fast and sensitive multiple sequence alignments on a microcomputer. CABIOS 5:151–153
Kato A, Nakajima T, Yamashita J, Yamashita J, Tanifuji S (1990) The structure of the large spacer region of the rDNA in Vicia and Pisum sativum. Plant Mol Biol 14:983–993
Kelly RJ, Siegel A (1989) The Cucurbita maxima ribosomal DNA intergenic spacer has a complex structure. Gene 80:239–248
Lassner M, Dvorak J (1986) Preferential homogenization between adjacent and alternate subrepeats in wheat rDNA. Nucleic Acids Res 14:5499–5012
Lassner M, Anderson O, Dvorak J (1987) Hypervariation associated with a 12 nucleotide direct repeat and inferences on intergenomic homogenization of ribosomal RNA gene spacers based on the sequence of a clone from the wheat nor-d3 locus. Genome 29:770–777
McMullen MD, Hunter B, Philips RC, Rubenstein I (1986) The structure of the maize ribosomal DNA spacer region. Nucleic Acids Res 14:4953–4958
Maniatis T, Fritsch E, Sambrook J (1990) Molecular cloning: a laboratory manual. Cold Spring Harbor University Press, Cold Spring Harbor, NY
Marck C (1988) “DNA Strider”: a “C” program for the fast analysis of DNA and protein sequences on the Apple Macintosh family of computers. Nucleic Acids Res 16:1829–1836
Maxam AM, Gilbert W (1977) A new method for sequencing DNA. Proc Natl Acad Sci USA 74:560–564
Nandabalan K, Padayatty JD (1989) Initiation of transcription of rDNA in rice. Biochem Biophys Res Comm 160:1117–1123
Piller KJ, Baerson S, Polans NO, Kaufman LS (1990) Structural analysis of the short length ribosomal DNA variant from Pisum sativum L cv alaska. Nucleic Acids Res 18:3135–3145
Rathgeber J, Capesius I (1990) Nucleotide sequence of the intergenic spacer and the 18S ribosomal RNA gene from mustard (Sinapis alba). Nucleic Acids Res 18:1288–1288
Rogers JO, Bendich AJ (1987) Ribosomal RNA genes in plants: variability in copy number and in the intergenic spacer. Plant Mol Biol 9:509–520
Sanger F, Nicklens S, Coulson AR (1977) DNA sequencing with chain termination inhibitors. Proc Natl Acad Sci USA 74: 7463–7467
Sano Y, Sano T (1990) Variation of the intergenic spacer region of ribosomal DNA in cultivated and wild rice species. Genome 33:209–218
Schiebel K, Von Waldburg G, Gerstner J, Hemleben V (1989) Termination of transcription of ribosomal RNA genes of mung bean occurs within a 175 by repetitive element of the spacer region. Mol Gen Genet 218:302–307
Schmidt-Puchta W, Guenther I, Saenger HL (1989) Nucleotide sequence of the intergenic spacer (IGS) of the tomato ribosomal DNA. Plant Mol Biol 13:251–253
Sollner-Webb B, Tower J (1986) Transcription of cloned eukaryotic ribosomal RNA genes. Ann Rev Biochem 55:801–830
Staden R (1988) Methods to define and locate patterns of motifs in sequences. CABIOS 4:53–60
Taira T, Kato A, Tanifuji S (1988) Difference between two major size classes of carrot rDNA repeating units is due to reiteration of sequences of about 460 by in the large spacer. Mol Gen Genet 213:170–174
Takaiwa F, Oono K, Sugiura M (1984) The complete nucleotide sequence of a rice 17S rRNA gene. Nucleic Acids Res 12: 5369–5379
Takaiwa F, Ikuchi 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
Toloczyki C, Feix G (1986) Occurrence of nine homologous repeat units in the external spacer of a nuclear maize rRNA gene unit. Nucleic Acids Res 14:4969–4986
Tremousaygue D, Laudie M, Grellet F, Delseny M (1992) The Brassica oleracea rDNA spacer revisited. Plant Mol Biol 18: 1013–1018
Ueki M, Uchizawa E, Yakura K (1992) The nucleotide sequence of the rDNA intergenic spacer region in a wild species of the genus vicia, V angustifolia. Plant Mol Biol 18:175–178
Van't Hof J, Lamm SS (1991) Single stranded replication intermediates of ribosomal DNA replicons of pea. EMBO J 10: 1949–1953
Yanisch-Perron C, Viera J, Messing J (1985) Improved m13 phage cloning vectors and host strains: nucleotide sequences of the m13mp18 and puc19 vectors. Gene 33:103–119
Zentgraf U, Ganal M, Hemleben V (1990) Length heterogeneity of the rRNA precursor in cucumber (Cucumis sativus). Plant Mol Biol 15:465–474
Author information
Authors and Affiliations
Additional information
Offprint requests to: M. Delseny
Rights and permissions
About this article
Cite this article
Cordesse, F., Cooke, R., Tremousaygue, D. et al. Fine structure and evolution of the rDNA intergenic spacer in rice and other cereals. J Mol Evol 36, 369–379 (1993). https://doi.org/10.1007/BF00182184
Received:
Revised:
Issue Date:
DOI: https://doi.org/10.1007/BF00182184