Skip to main content
Log in

Role of transposable elements in the propagation of minisatellites in the rice genome

  • Original Paper
  • Published:
Molecular Genetics and Genomics Aims and scope Submit manuscript

Abstract

A survey of minisatellites (MSs) in 5.3 Mb of randomly selected rice DNA sequences from public databases was carried out to clarify the role of transposable elements (TEs) in the dispersal of MSs in the rice genome. The estimated frequency of MSs in this sample was one per 23.4 kb, and this frequency is approximately equivalent to that of Class I microsatellites in the rice genome. Of the MSs in the 5.3-Mb sequence sample, 82% were found to be present in multiple copies in the rice genome, and all of these were a part of TE sequences. In this study at least 61 TE groups were identified as MS carriers. It was also shown that the GC-rich MS pOs6.2H, which was previously reported to be one of the interspersed MSs in the rice genome, is a component of an En / Spm -like element. These results indicate that the majority of MSs in the rice genome are maintained in TEs, and amplified and dispersed as components of the TEs. The G+C content of the multi-locus MS sequences reflected that of the TE sequences containing those MSs, but no obvious bias towards the high G+C content of DNA was observed. Single locus MSs also did not show any obvious bias towards the high G+C content of DNA in the rice genome. In this respect, the MSs in the rice genome are quite different from those in the human genome: in the latter, the majority of MSs show an obvious bias towards the high G+C content of DNA.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2 A, B
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Amarger V, Gauguier D, Yerle M, Apiou F, Pinton P, Giraudeau F, Monfouilloux S, Lathrop M, Dutrillaux B, Buard J, Vergnaud G (1998) Analysis of distribution in the human, pig, and rat genomes points toward a general subtelomeric origin of minisatellite structures. Genomics 52:62–71

    Article  CAS  PubMed  Google Scholar 

  • Armour JAL, Wong Z, Wilson V, Royle NJ, Jeffreys AJ (1989) Sequences flanking the repeat arrays of human minisatellites: association with tandem and dispersed repeat elements. Nucleic Acids Res 17:4925–4935

    CAS  PubMed  Google Scholar 

  • Arumuganathan K, Earle ED (1991) Nuclear DNA content of some important plant species. Plant Mol Biol Rep 9:208–218

    CAS  Google Scholar 

  • Benson G (1999) Tandem Repeats Finder: a program to analyze DNA sequences. Nucleic Acids Res 27:573–580

    CAS  PubMed  Google Scholar 

  • Bois P, Jeffreys AJ (1999) Minisatellite instability and germline mutation. Cell Mol Life Sci 55:1636–1648

    CAS  PubMed  Google Scholar 

  • Broun P, Tanksley SD (1993) Characterization of tomato DNA clones with sequence similarity to human minisatellites 33.6 and 33.15. Plant Mol Biol 23:231–242

    CAS  PubMed  Google Scholar 

  • Bureau TE, Ronald PC, Wessler SR (1996) A computer-based systematic survey reveals the predominance of small inverted-repeat elements in wild-type rice genes. Proc Natl Acad Sci USA 93:8524–8529

    CAS  PubMed  Google Scholar 

  • Cheng C, Tsuchimoto S, Ohtsubo H, Ohtsubo E (2000) Tnr8, a foldback transposable element from rice. Genes Genet Syst 75:327–333

    Article  CAS  PubMed  Google Scholar 

  • Dallas JF (1988) Detection of DNA “fingerprints” of cultivated rice by hybridization with a human minisatellite DNA probe. Proc Natl Acad Sci USA 85:6831–6835

    CAS  PubMed  Google Scholar 

  • Eden FC (1985) Truncated repeated sequences generated by recombination in a specific region. Biochemistry 24:229–233

    CAS  PubMed  Google Scholar 

  • Feschotte C, Wessler SR (2002) Mariner -like transposases are widespread and diverse in flowering plants. Proc Natl Acad Sci USA 99:280–285

    Article  CAS  PubMed  Google Scholar 

  • Gierl A, Lutticke S, Saedler H (1988) Tnp A product encoded by the transposable element En-1 of Zea mays is a DNA binding protein. EMBO J 7:4045–4053

    CAS  Google Scholar 

  • Gustafson JP, Yano M (2000) Genetic mapping of hypervariable minisatellite sequences in rice ( Oryza sativa L.). Theor Appl Genet 100:447–453

    Article  CAS  Google Scholar 

  • Han C-G, Frank MJ, Ohtsubo H, Ohtsubo E (2000) New transposable elements identified as insertions in rice transposon Tnr1. Genes Genet Syst 75:69–77

    Article  CAS  PubMed  Google Scholar 

  • Hisatomi Y, Hanada K, Iida S (1997) The retrotransposon RTip1 is integrated into a novel type of minisatellite, MiniSip1 , in the genome of the common morning glory and carries another new type of minisatellite, MiniSip2. Theor Appl Genet 95: 1049–1056

    Article  CAS  Google Scholar 

  • Hoshino A, Inagaki Y, Iida S (1995) Structural analysis of Tpn1, a transposable element isolated from Japanese morning glory bearing variegated flowers. Mol Gen Genet 247:114–117

    CAS  PubMed  Google Scholar 

  • Inukai T, Sano Y (2002) Sequence rearrangement in the AT-rich minisatellite of the novel rice transposable element Basho. Genome 45:493–502

    Article  CAS  PubMed  Google Scholar 

  • Jarman AP, Wells RA (1989) Hypervariable minisatellites: recombinators or innocent bystanders? Trends Genet 5:367–371

    Article  CAS  PubMed  Google Scholar 

  • Jeffreys AJ, Wilson V, Thein SL (1985) Hypervariable ‘minisatellite’ regions in human DNA. Nature 314:67–73

    CAS  PubMed  Google Scholar 

  • Jiang N, Bao Z, Temnykh S, Cheng Z, Jiang J, Wing RA, McCouch SR, Wessler SR (2002) Dasheng: a recently amplified nonautonomous long terminal repeat element that is a major component of pericentromeric regions in rice. Genetics 161:1293–1305

    CAS  PubMed  Google Scholar 

  • Kapitonov VV, Jurka J (2001) Rolling-circle transposons in eukaryotes. Proc Natl Acad Sci USA 98:8714–8719

    Article  CAS  PubMed  Google Scholar 

  • Mariat D, Vergnaud G (1992) Detection of polymorphic loci in complex genomes with synthetic tandem repeats. Genomics 12:454–458

    CAS  PubMed  Google Scholar 

  • Martienssen RA, Baulcombe DC (1989) An unusual wheat insertion sequence ( WIS1) lies upstream of an α-amylase gene in hexaploid wheat, and carries a “minisatellite” array. Mol Gen Genet 217:401–410

    CAS  PubMed  Google Scholar 

  • Masson P, Surosky R, Kingsbury JA, Fedoroff NV (1987) Genetic and molecular analysis of the Spm -dependent a-m2 alleles of the maize a locus. Genetics 177:117–137

    Google Scholar 

  • Motohashi R, Ohtsubo E, Ohtsubo H (1996) Identification of Tnr3, a Suppressor-Mutator/Enhancer -like transposable element from rice. Mol Gen Genet 250:148–152

    Article  CAS  PubMed  Google Scholar 

  • Nagano H, Kunii M, Azuma T, Kishima Y, Sano Y (2002) Characterization of the repetitive sequences in a 200-kb region around the rice waxy locus: diversity of transposable elements and presence of veiled repetitive sequences. Genes Genet Syst 77:69–79

    Article  CAS  PubMed  Google Scholar 

  • Nakamura Y, Leppert M, O’Connell P, Wolff R, Holm T, Culver M, Martin C, Fujimoto E, Hoff M, Kumlin E, White R (1987) Variable number of tandem repeat (VNTR) markers for human gene mapping. Science 235:1616–1622

    CAS  PubMed  Google Scholar 

  • Noma K, Ohtsubo E (2000) Tnat1 and Tnat2 from Arabidopsis thaliana: novel transposable elements with tandem repeat sequences. DNA Res 7:1-7

    CAS  PubMed  Google Scholar 

  • Ohtsubo H, Ohtsubo E (1994) Involvement of transposition in dispersion of tandem repeat sequences (TrsA) in rice genomes. Mol Gen Genet 245:449–455

    CAS  PubMed  Google Scholar 

  • Song W-Y, Pi L-Y, Bureau TE, Ronald PC (1998) Identification and characterization of 14 transposon-like elements in the noncoding regions of members of the Xa21 family of disease resistance genes in rice. Mol Gen Genet 258:449–456

    CAS  PubMed  Google Scholar 

  • Tarchini R, Biddle P, Wineland R, Tingey S, Rafalski A (2000) The complete sequence of 340 kb of DNA around the rice Adh1-Adh2 region reveals interrupted colinearity with maize chromosome 4. Plant Cell 12:381–391

    CAS  PubMed  Google Scholar 

  • Temnykh S, DeClerck G, Lukashova A, Lipovich L, Cartinhour S, McCouch S (2001) Computational and experimental analysis of microsatellites in rice ( Oryza sativa L.): frequency, length variation, transposon associations, and genetic marker potential. Genome Res 11:1441–1452

    CAS  PubMed  Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    PubMed  Google Scholar 

  • Turcotte K, Srinivasan S, Bureau T (2001) Survey of transposable elements from rice genomic sequences. Plant J 25:169–179

    CAS  PubMed  Google Scholar 

  • Winberg BC, Zhou Z, Dallas JF, McIntyre CL, Gustafson JP (1993) Characterization of minisatellite sequences from Oryza sativa. Genome 36:978–983

    CAS  PubMed  Google Scholar 

  • Yoshida T, Obata N, Oosawa K (2000) Color-coding reveals tandem repeats in the Escherichia coli genome. J Mol Biol 298:343–349

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

I would like to thank two anonymous reviewers for suggesting improvements to the manuscript. This study was supported by grants from the Ministry of Education, Culture, Sports, Science and Technology, and the Hokuto Foundation for Bioscience, Japan

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to T. Inukai.

Additional information

Communicated by M.-A. Grandbastien

Electronic Supplementary Material

Rights and permissions

Reprints and permissions

About this article

Cite this article

Inukai, T. Role of transposable elements in the propagation of minisatellites in the rice genome. Mol Genet Genomics 271, 220–227 (2004). https://doi.org/10.1007/s00438-003-0973-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00438-003-0973-5

Keywords

Navigation