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Genetica

, Volume 100, Issue 1–3, pp 197–204 | Cite as

The chromosomal distributions of Ty1-copia group retrotransposable elements in higher plants and their implications for genome evolution

  • J.S. (Pat) Heslop-Harrison
  • Andrea Brandes
  • Shin Taketa
  • Thomas Schmidt
  • Alexander V. Vershinin
  • Elena G. Alkhimova
  • Anette Kamm
  • Robert L. Doudrick
  • Trude Schwarzacher
  • Andreas Katsiotis
  • Sybille Kubis
  • Amar Kumar
  • Steven R. Pearce
  • Andrew J. Flavell
  • Gill E. Harrison
Article

Abstract

Retrotransposons make up a major fraction – sometimes more than 40% – of all plant genomes investigated so far. We have isolated the reverse transcriptase domains of the Ty1-copia group elements from several species, ranging in genome size from some 100 Mbp to 23 000 Mbp, and determined the distribution patterns of these retrotransposons on metaphase chromosomes and within interphase nuclei by DNA:DNA in situ hybridization. With some exceptions, the reverse transcriptase domains were distributed over the length of the chromosomes. Exclusion from rDNA sites and some centromeres (e.g., slash pine, 23 000 Mbp, or barley, 5500 Mbp) is frequent, whereas many species exclude retrotransposons from other sites of heterochromatin (e.g., intercalary and centromeric sites in broad bean). In contrast, in the plant Arabidopsis thaliana, widely used for plant molecular genetic studies because of its small genome (c. 100 Mbp), the Ty1-copia group reverse transcriptase gene domains are concentrated in the centromeric regions, collocalizing with the 180 bp satellite sequence pAL1. Unlike the pAL1 sequence, however, the Ty1-copia signal is also detectable as weaker, diffuse hybridization along the lengths of the chromosomes. Possible mechanisms for evolution of the contrasting distributions are discussed. Understanding the physical distribution of retrotransposons and comparisons of the distribution between species is critical to understanding their evolution and the significance for generation of the new patterns of variability and in speciation.

in situ hybridization centromeres retrotransposons genome organization evolution sequence evolution Arabidopsis barley 

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References

  1. Bennett, M.D. & I.J. Leitch, 1995. Nuclear DNA amounts in angiosperms. Ann. Bot. 76: 113–176.CrossRefGoogle Scholar
  2. Bennett, M.D., J.B. Smith & J.S. Heslop-Harrison, 1982. Nuclear DNA amounts in angiosperms. Proc. R. Soc. Lond. B 216: 179–199.CrossRefGoogle Scholar
  3. Bennetzen, J.L., K. Schrick, P.S. Springer, W.E. Brown & P. San-Miguel, 1994. Active maize genes are unmodified and flanked by diverse classes of modified, highly repetitive DNA. Genome 37: 565–576.PubMedGoogle Scholar
  4. Bennetzen, J.L., P. SanMiguel, C-N. Liu, M. Chen, A. Tikhonov, A.C. Oliveira, Y-K. Jin & Z. Avramova, 1996, Microcollinearity and segmental duplication in the evolution of grass nuclear genomes, pp. 1–3 in Unifying Plant Genomes. 50th SEB Symposium, edited by Heslop-Harrison, Company of Biologists, Cambridge.Google Scholar
  5. Brandes, A., J.S. Heslop-Harrison, A. Kamm, S. Kubis, R.L. Doudrick & T. Schmidt, 1997a. Comparative analysis of the chromosomal and genomic organization of Ty1-copia-like retrotransposons in pteridophytes, gymnosperms and angiosperms. Plant Mol. Biol. 33: 11–21.PubMedCrossRefGoogle Scholar
  6. Brandes, A., H. Thompson, C. Dean & J.S. Heslop-Harrison, 1997b. Multiple repetitive DNAsequences in the paracentromeric regions of Arabidopsis thaliana L. Chromosome Res. 5: 238–246.PubMedCrossRefGoogle Scholar
  7. D'Amato, F., 1991. Nuclear changes in cultured plant cells. Caryologia 44: 217–224.Google Scholar
  8. Flavell, A.J., 1992. Tyl-copia group retrotransposons and the evolution of retroelements in the eukaryotes. Genetica 86: 203–214.PubMedCrossRefGoogle Scholar
  9. Flavell, A.J., E. Dunbar, R. Anderson, S.R. Pearce, R. Hartley & A. Kumar, 1992. Ty1-copia group retrotransposons are ubiquitous and heterogeneous in higher plants. Nucl. Acids Res. 20: 3639–3644.PubMedGoogle Scholar
  10. Flavell, A.J., S.R. Pearce & A. Kumar, 1994. Plant transposable elements and the genome. Curr. Op. Genet. Devel. 4: 838–844.CrossRefGoogle Scholar
  11. Flavell, R.B., 1986. Repetitive DNA and chromosome evolution in plants. Phil. Trans. R. Soc. Lond. B 312: 227–242.Google Scholar
  12. Heslop-Harrison, J.S., T. Schwarzacher, K. Anamthawat-Jónsson, A.R. Leitch, M. Shi & I.J. Leitch, 1991. In situ hybridization with automated chromosome denaturation. Technique 3: 109–115.Google Scholar
  13. Hirochika, H., K. Sugimoto, Y. Otsuki, H. Tsugawa & M. Kanda, 1996. Retrotransposons of rice involved in mutations induced by tissue culture. Proc Natl Acad Sci USA 93: 7783–7788.PubMedCrossRefGoogle Scholar
  14. Kamm, A., R.L. Doudrick, J.S. Heslop-Harrison & T. Schmidt, 1996. The genomic and physical organization of Ty1-copia-like sequences as a component of large genomes in Pinus elliottii var. elliottii and other gymnosperms. Proc. Natl. Acad. Sci. USA 93: 2708–2713.PubMedCrossRefGoogle Scholar
  15. Katsiotis, A., T. Schmidt & J.S. Heslop-Harrison, 1997. Chromosomal and genomic organization of Ty1-copia-like retrotransposon sequences in the genus Avena. Genome 39: 410–417.Google Scholar
  16. Kumar, A., 1996. The adventures of the Ty1-copia group of retro-transposons in plants. Trends Genet. 12: 41–43.PubMedCrossRefGoogle Scholar
  17. Lagercrantz, U. & D.J. Lydiate, 1995. RFLP mapping in Brassica nigra indicates differing recombination rates in male and female meiosis. Genome 38: 255–264.PubMedGoogle Scholar
  18. Maluszynska, J. & J.S. Heslop-Harrison, 1991. Localization of tandemly repeated DNA sequences in Arabidopsis thaliana. Plant J. 1: 159–166.CrossRefGoogle Scholar
  19. Manninen, I. & A.H. Schulman, 1993. BARE-1, a copia-like retroelement in barley (Hordeum vulgare L.). Plant Mol. Biol. 22: 829–846.PubMedCrossRefGoogle Scholar
  20. Martinez-Zapater, J.M., M.A. Estelle & C.R. Somerville, 1986. A highly repeated DNA sequence in Arabidopsis thaliana. Mol. Gen. Genet. 204: 417–423.CrossRefGoogle Scholar
  21. McClintock, B., 1984. The significance of responses of the genome to challenge. Science 226: 792–801.PubMedGoogle Scholar
  22. Mhiri, C., J-B. More, S. Vernhettes, J.M. Casacuberta, H. Lucas & M-A. Grandbastien, 1997. The promoter of the tobacco Tnt1 retrotransposon is induced by wounding and by abiotic stress. Plant Mol. Biol. 33: 1–10.CrossRefGoogle Scholar
  23. Murata, M., Y. Ogura & F. Motoyoshi, 1994. Centromeric repetitive sequences in Arabidopsis thaliana. Jap. J. Genet. 69: 361–370.CrossRefGoogle Scholar
  24. Parkin, I.A.P., A.G. Sharpe, D.J. Keith & D.J. Lydiate, 1995. Identification of the A and C genomes of amphidiploid Brassica napus (oilseed rape). Genome 38: 1122–1131.PubMedGoogle Scholar
  25. Pearce, S.R., G. Harrison, M. Wilkinson, D. Li, J.S. Heslop-Harrison, A.J. Flavell & A. Kumar, 1996a. The Ty1-copia group retrotransposons in Vici a species: copy number, sequence heterogeneity and chromosomal localisation. Mol. Gen. Genet. 250: 305–315.PubMedGoogle Scholar
  26. Pearce, S.R., U. Pich, G. Harrison, A.J. Flavell, J.S. Heslop-Harrison, I. Schubert & A. Kumar, 1996b. The Ty1-copia group retrotransposons of Allium cepa are distributed throughout the chromosomes but are enriched in the telomeric heterochromatin. Chromosome Res. 4: 357–364.PubMedCrossRefGoogle Scholar
  27. Pearce, S.R., G. Harrison, J.S. Heslop-Harrison, A.J. Flavell & A. Kumar, 1997. Characterisation and genomic organisation of Ty1-copia group retrotransposons in rye (Secale cereale). Genome, in press.Google Scholar
  28. Pearce, S.R., A. Kumar & A.J. Flavell, 1996c. Retrotransposon expression in potato. Plant Cell Reports 15: 949–953.CrossRefGoogle Scholar
  29. Pedersen, C. & I. Linde-Laursen, 1994. Chromosomal locations of four minor rDNA loci and a marker microsatellite sequence in barley. Chromosome Res. 2: 65–71.PubMedCrossRefGoogle Scholar
  30. Pélissier, T., S. Tutois, S. Tourmente, J.M. Deragon & G. Picard, 1996. DNAregions flanking the major Arabidopsis thaliana satellite are principally enriched in Athila retroelement sequences. Genetica 97: 141–151.PubMedCrossRefGoogle Scholar
  31. Pouteau, S., E. Huttner, M-A. Grandbastien & M. Caboche, 1991. Specific expression of the tobacco Tnt1 retrotransposon in protoplasts. EMBO J. 10: 1911–1918.PubMedGoogle Scholar
  32. Rees, H., 1986. The consequences of DNA change in chromosomes: Lathyrus and lathyrism. Proc. int. symposium sponsored by Inst. de. biocenotique experimentale des agrosystemes (IBEAS), edited by A.K. Kaul and D. Com. Paris, Third World.Google Scholar
  33. Rees, H. & R.N. Jones, 1972. The origin of the wide species variation in nuclear DNA content. Int. Rev. Cytol. 32: 53–91.PubMedCrossRefGoogle Scholar
  34. Richards, A.J., 1989. A comparison of within-plant karyological heterogeneity between agamospermous and sexual Taraxacum (Compositae) as assessed by the nucleolar organiser chromosome. Pl. Syst. Evol. 163: 177–185.CrossRefGoogle Scholar
  35. San Miguel, P., A. Tikhonov, Y-K. Jin, N. Motchoulskaia, D. Zakharov, A. Melake-Berhan, P.S. Springer, K.J. Edwards, M. Lee, Z. Avramova & J.L. Bennetzen, 1996. Nested retrotrans-posons in the intergenic regions of the maize genome. Science 274: 765–738.Google Scholar
  36. Schmidt, T. & J.S. Heslop-Harrison, 1994. Variability and evolution of highly repeated DNA sequences in the genus Beta. Genome 36: 1074–1079.Google Scholar
  37. Schmidt, T. & J.S. Heslop-Harrison, 1996. The physical and genomic organization of microsatellites in sugar beet. Proc. Natl. Acad. Sci. USA 93: 8761–8765.PubMedCrossRefGoogle Scholar
  38. Schmidt, T., S. Kubis & J.S. Heslop-Harrison, 1995. Analysis and chromosomal localization of retrotransposons in sugar beet (Beta vulgaris L.): LINEs and Ty1-copia-like elements as major components of the genome. Chromosome Res. 3: 335–345.PubMedCrossRefGoogle Scholar
  39. Schwarzacher, T., 1994. Mapping in plants: progress and prospects. Curr. Op. Genet. Devel. 4: 868–874.CrossRefGoogle Scholar
  40. Schwarzacher, T., A.R. Leitch & J.S. Heslop-Harrison, 1994, DNA:DNA in situ hybridization - methods for light microscopy, pp. 127–155 in Plant Cell Biology: A Practical Approach, edited by N. Harris & K.J. Oparka. Oxford University Press, Oxford.Google Scholar
  41. Seal, A.G., 1983, The distribution and consequences of changes in nuclear DNA content, pp. 225–232 in Kew Chromosome Conference II, edited by P.E. Brandham & M.D. Bennett. George Allen & Unwin, London.Google Scholar
  42. Sharpe, A.G., I.A.P. Parkin, D.J. Keith & D.J. Lydiate, 1995. Frequent nonreciprocal translocations in the amphidiploid genome of oilseed rape (Brassica napus). Genome 38: 1112–1121.PubMedGoogle Scholar
  43. Thompson, H., R. Schmidt, A. Brandes, J.S. Heslop-Harrison & C. Dean, 1996. A novel repetitive sequence associated with the centromeric regions of Arabidopsis thaliana chromosomes. Mol. Gen. Genet. 253: 247–252.PubMedCrossRefGoogle Scholar
  44. Tiersch, T.R. & S.S. Wachtel, 1991. On the evolution of genome size of birds. J. Heredity 82: 363–368.Google Scholar
  45. Waugh, R., K. McLean, A.J. Flavell, S.R. Pearce, A. Kumar, B.T. Thomas & W. Powell 1997. Genetic distribution of BARE-1 retro-transposable elements in the barley genome revealed by sequence-specific amplification polymorphism (S-SAP). Mol. Gen. Genet. 253: 687–694.PubMedCrossRefGoogle Scholar
  46. Wendel, J.F., A. Schnabel & T. Seelanan, 1995. Bidirectional interlocus concerted evolution following allopolyploid speciation in cotton (Gossypium). Proc Natl Acad Sci 92: 280–284.PubMedCrossRefGoogle Scholar
  47. Wessler, S.R., 1996. Plant retrotransposons: Turned on by stress. Current Biol. 6: 959–961.CrossRefGoogle Scholar

Copyright information

© Kluwer Academic Publishers 1997

Authors and Affiliations

  • J.S. (Pat) Heslop-Harrison
    • 1
  • Andrea Brandes
    • 1
  • Shin Taketa
    • 2
  • Thomas Schmidt
    • 1
  • Alexander V. Vershinin
    • 1
  • Elena G. Alkhimova
    • 1
    • 3
  • Anette Kamm
    • 1
  • Robert L. Doudrick
    • 4
  • Trude Schwarzacher
    • 1
  • Andreas Katsiotis
    • 5
  • Sybille Kubis
    • 6
    • 1
  • Amar Kumar
    • 7
  • Steven R. Pearce
    • 7
    • 8
  • Andrew J. Flavell
    • 8
  • Gill E. Harrison
    • 1
  1. 1.John Innes CentreNorwichUK
  2. 2.Research Institute for BioresourcesOkayama UniversityKurashiki OkayamaJapan
  3. 3.Laboratory of Cell Population Genetics, Institute of Molecular BiologyNational Academy of Sciences of UkraineKievUkraine
  4. 4.Usda Forest ServiceSouthern Institute of Forest Genetics, Harrison Experimental ForestSaucierUSA
  5. 5.Lab. of Molecular BiologyAgricultural University of Athens, Iera OdosAthensGreece
  6. 6.Norman Borlaug InstituteDe Montfort University Scraptoft CampusLeicesterUK
  7. 7.Scottish Crop Research InstituteInvergowerie DundeeScotland
  8. 8.Medical Sciences InstituteThe University DundeeScotland

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