Russian Journal of Genetics

, Volume 41, Issue 8, pp 890–896 | Cite as

Allopolyploidy in Wheat Induces Rapid and Heritable Alterations in DNA Methylation Patterns of Cellular Genes and Mobile Elements

  • Y. Z. Dong
  • Z. L. Liu
  • X. H. Shan
  • T. Qiu
  • M. Y. He
  • B. Liu
Plant Genetics

Abstract

Whereas accumulating recent evidences indicate that allopolyploid formation in plants is accompanied by rapid and non-Mendelian genomic changes, some other works showed genomic stasis in both nascent and natural allopolyploids. To further study the issue, we performed global DNA fingerprinting of a newly synthesized allohexaploid wheat and its natural counterpart, the common wheat, by AFLP analysis. It was found that ca. 20% bands showed deviation from parental additivity in both synthetic and natural common wheat. Sequence analysis indicates that a majority of the changed bands represent known-function genes and transposable elements. DNA gel blot analysis showed that the main type of changes in the amphiploid is epigenetic in nature, i.e., alteration in DNA methylation patterns. Two types of alterations in methylation, random and non-random, were detected, and both types were stably inherited. Possible causes and implications of the epigenetic changes in allopolyploid genome evolution and speciation are discussed.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

REFERENCES

  1. 1.
    Leitch, I.J. and Bennett, M.D., Polyploidy in Angiosperms, Trends Plant Sci., 1997, vol. 2, pp. 470–476.CrossRefGoogle Scholar
  2. 2.
    Wendel, J.F., Genome Evolution in Polyploids, Plant Mol. Biol., 2000, vol. 42, pp. 225–249.CrossRefPubMedGoogle Scholar
  3. 3.
    Liu, B. and Wendel, J.F., Non-Mendelian Phenomena in Allopolyploid Genome Evolution, Curr. Genomics, 2002, vol. 3, pp. 489–506.CrossRefGoogle Scholar
  4. 4.
    Comai, L., Tyagi, A.P., Winter, K., et al., Phenotypic Instability and Rapid Gene Silencing in Newly Formed Arabidopsis Allotetraploids, Plant Cell, 2000, vol. 12, pp. 1551–1567.CrossRefPubMedGoogle Scholar
  5. 5.
    Kashkush, K., Feldman, M., and Levy, A.A., Gene Loss, Silencing and Activation in a Newly Synthesized Wheat Allotetraploid, Genetics, 2002, vol. 160, pp. 1651–1659.PubMedGoogle Scholar
  6. 6.
    Adams, K.L., Cronn, R., Percifield, R., et al., Genes Duplicated by Polyploidy Show Unequal Contributions to the Transcriptome and Organ-Specific Reciprocal Silencing, Proc. Natl. Acad. Sci. USA, 2003, vol. 100, pp. 4649–4654.CrossRefPubMedGoogle Scholar
  7. 7.
    Feldman, M., Liu, B., Segal, G., et al., Rapid Elimination of Low-Copy DNA Sequences in Polyploid Wheat: A Possible Mechanism for Differentiation of Homoeologous Chromosomes, Genetics, 1997, vol. 147, pp. 1381–1387.PubMedGoogle Scholar
  8. 8.
    Liu, B., Vega, J.M., Segal, G., et al., Rapid Genomic Changes in Newly Synthesized Amphiploids of Triticum and Aegilops: Changes in Low-Copy Noncoding DNA Sequences, Genome, 1998, vol. 41, pp. 272–277.CrossRefGoogle Scholar
  9. 9.
    Ozkan, H., Levy, A.A., and Feldman, M., Allopolyploidy-Induced Rapid Genome Evolution in the Wheat (Aegilops-Triticum) Group, Plant Cell, 2001, vol. 13, pp. 1735–1747.CrossRefPubMedGoogle Scholar
  10. 10.
    Pestova, E.G., Goncharov, N.P., and Salina, E.A., Elimination of a Tandem Repeat of Telomeric Heterochromatin during the Evolution of Wheat, Theor. Appl. Genet., 1998, vol. 97, pp. 1380–1386.CrossRefGoogle Scholar
  11. 11.
    Pikaard, C.S., Genomic Change and Gene Silencing in Polyploids, Trends Genet., 2001, vol. 17, pp. 675–677.CrossRefPubMedGoogle Scholar
  12. 12.
    Rieseberg, L.H., Polyploid Evolution: Keeping the Peace at Genomic Reunions, Curr. Biol., 2001, vol. 11, pp. R925–R928.CrossRefPubMedGoogle Scholar
  13. 13.
    Cronn, R.C., Small, R.L., and Wendel, J.F., Duplicated Genes Evolve Independently after Polyploid Formation in Cotton, Proc. Natl. Acad. Sci. USA, 1999, vol. 96, pp. 14 406–14 411.CrossRefGoogle Scholar
  14. 14.
    Liu, B., Brubaker, C.L., et al., Polyploid Formation in Cotton Is Not Accompanied by Rapid Genomic Changes, Genome, 2001, vol. 44, pp. 321–330.CrossRefPubMedGoogle Scholar
  15. 15.
    Axelsson, T., Bowman, C.M., Sharpe, A.G., et al., Amphidiploid Brassica juncea Contains Conserved Progenitor Genomes, Genome, 2000, vol. 43, pp. 679–688.CrossRefPubMedGoogle Scholar
  16. 16.
    Baumel, A., Ainouche, M., Kalendar, R., et al., Retrotransposons and Genomic Stability in Populations of the Young Allopolyploid Species Spartina anglica C.E. Hubbard (Poaceae), Mol. Biol. Evol., 2002, vol. 19, pp. 1218–1227.PubMedGoogle Scholar
  17. 17.
    Shaked, H., Kashkush, K., Ozkan, H., et al., Sequence Elimination and Cytosine Methylation Are Rapid and Reproducible Responses of the Genome to Wide Hybridization and Allopolyploidy in Wheat, Plant Cell, 2001, vol. 13, pp. 1749–1759.CrossRefPubMedGoogle Scholar
  18. 18.
    Blair, M.W., Panaud, O., and McCouch, S.R., Inter-Simple Sequence Repeat (ISSR) Amplification for Analysis of Microsatellite Motif Frequency and Fingerprinting in Rice (Oryza sativa L.), Theor. Appl. Genet., 1999, vol. 98, pp. 780–792.CrossRefGoogle Scholar
  19. 19.
    Kidwell, K.K. and Osborn, T.C., Simple Plant DNA Isolation Procedures, Plant Genomes: Methods for Genetic and Physical Mapping, Beckman, J.S. and Osborn, T.C., Eds., Kluwer Academic, 1992, pp. 1–13.Google Scholar
  20. 20.
    Song, K., Lu, P., Tang, K., et al., Rapid Genome Change in Synthetic Polyploids of Brassica and Its Implications for Polyploid Evolution, Proc. Natl. Acad. Sci. USA, 1995, vol. 92, pp. 7719–7723.PubMedGoogle Scholar
  21. 21.
    Liu, B. and Wendel, J.F., Epigenetic Phenomena and the Evolution of Plant Allopolyploids, Mol. Phyl. Evol., 2003, vol. 29, pp. 365–379.CrossRefGoogle Scholar
  22. 22.
    Levy, A.A., Feldman, M., et al., The Impact of Polyploidy on Grass Genome Evolution, Plant Physiol., 2002, vol. 130, pp. 1587–1593.CrossRefPubMedGoogle Scholar
  23. 23.
    Wolffe, A.P. and Matzke, M.A., Epigenetics: Regulation through Repression, Science, 1999, vol. 286, pp. 481–486.Google Scholar
  24. 24.
    Lee, H.S. and Chen, Z.J., Protein-Coding Genes Are Epigenetically Regulated in Arabidopsis Polyploids, Proc. Natl. Acad. Sci. USA, 2001, vol. 98, pp. 6753–6758.CrossRefPubMedGoogle Scholar
  25. 25.
    He, P., Friebe, B.R., Gill, B.S., et al., Allopolyploidy Alters Gene Expression in the Highly Stable Hexaploid Wheat, Plant Mol. Biol., 2003, vol. 52, pp. 401–414.CrossRefPubMedGoogle Scholar
  26. 26.
    O’Neill, R.J.W., O’Neill, M.J., and Graves, J.A.M., Undermethylation Associated with Retroelement Activation and Mammalian Hybrid, Nature, 1998, vol. 393, pp. 68–72.CrossRefPubMedGoogle Scholar
  27. 27.
    Miura, A., Yonebayashi, S., Watanabe, K., et al., Mobilization of Transposons by a Mutation Abolishing Full DNA Methylation in Arabidopsis, Nature, 2001, vol. 411, pp. 212–214.CrossRefPubMedGoogle Scholar
  28. 28.
    Kashkush, K., Feldman, M., and Levy, A.A., Transcriptional Activation of Retrotransposons Alters the Expression of Adjacent Genes in Wheat, Nat. Genet., 2003, vol. 33, pp. 102–106.CrossRefPubMedGoogle Scholar
  29. 29.
    Schranz, M.E. and Osborn, T.C., Novel Flowering Time Variation in the Resynthesized Polyploid Brassica napus, J. Hered., 2000, vol. 91, pp. 242–246.CrossRefPubMedGoogle Scholar
  30. 30.
    Jiang, C., Wright, R., El-Zik, K., et al., Polyploid Formation Created Unique Avenues for Response to Selection in Gossypium (Cotton), Proc. Natl. Acad. Sci. USA, 1998, vol. 95, pp. 4419–4424PubMedGoogle Scholar

Copyright information

© MAIK “Nauka/Interperiodica” 2005

Authors and Affiliations

  • Y. Z. Dong
    • 1
    • 2
  • Z. L. Liu
    • 1
  • X. H. Shan
    • 1
  • T. Qiu
    • 1
  • M. Y. He
    • 1
  • B. Liu
    • 1
  1. 1.Laboratory of EpigeneticsNortheast Normal UniversityChangchunChina
  2. 2.Laboratory of Systematics and Evolutionary Botany Institute of BotanyChinese Academy of SciencesBeijingChina

Personalised recommendations