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Developmental changes in DNA methylation of pollen mother cells of David lily during meiotic prophase I

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Abstract

Epigenetic marks in the form of DNA methylation are involved in the development of germ cells and are important in the maintenance of fertility. However, the controlling system of the on-off switch for DNA methylation largely remains unclear. In this study, the extent of cytosine methylation during the meiotic prophase I in David lily is assessed using high pressure liquid chromatography to evaluate the DNA methylation rates. Comparing the degree of DNA methylation before, during, and after synizesis, both de novo methylation and demethylation occurred. Mainly the methylation level decreased by 21.3% (from 54.8 to 33.5%) during synizesis in the pollen mother cells. The developmental timing of genome-wide DNA methylation acquisition during pollen mother cell development is clarified in this paper. The relative amounts of 5-methyl-deoxycytidine of global methylation in leaf DNA in David lily were also higher than in other species reported.

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Abbreviations

PMCs:

pollen mother cells

References

  1. Yamagata K., Yamazaki T., Miki H., Ogonuki N., Inoue K., Ogura A., Baba T. 2007. Centromeric DNA hypomethylation as an epigenetic signature discriminates between germ and somatic cell lineages. Dev. Biol. 312, 419–426.

    Article  CAS  PubMed  Google Scholar 

  2. Oakes C.C., La Salle S., Smiraglia D.J., Robaire B., Trasler J.M. 2007. Developmental acquisition of genome-wide DNA methylation occurs prior to meiosis in male germ cells. Dev. Biol. 307, 368–379.

    Article  CAS  PubMed  Google Scholar 

  3. Kinoshita T., Miura A., Choi Y., Kinoshita Y., Cao X., Jacobsen S.E., Fischer R.L., Kakutani T. 2004. Oneway control of FWA imprinting in Arabidopsis endosperm by DNA methylation. Science. 303, 521–523.

    Article  CAS  PubMed  Google Scholar 

  4. Finnegan E.J., Peacock W.J., Dennis E. S. 2000. DNA methylation, a key regulator of plant development and other processes. Curr. Opin. Genet. Dev. 10, 217–223.

    Article  CAS  PubMed  Google Scholar 

  5. Vanyushin B.F. 2006. DNA methylation in plants. Curr. Top. Microbiol. Immunol. 301, 67–122.

    Article  CAS  PubMed  Google Scholar 

  6. Shilatifard A. 2006. Chromatin modifications by methylation and ubiquitination: Implications in the regulation of gene expression. Annu. Rev. Biochem. 75, 243–269.

    Article  CAS  PubMed  Google Scholar 

  7. Vasanthi D., Mishra R.K. 2008. Epigenetic regulation of genes during development: A conserved theme from flies to mammals. J. Genet. Genomics. 35, 413–429.

    Article  CAS  PubMed  Google Scholar 

  8. Li E. 2002. Chromatin modification and epigenetic reprogramming in mammalian development. Nature Rev. Genet. 3, 662–673.

    Article  CAS  PubMed  Google Scholar 

  9. Kimmins S., Sassone-Corsi P. 2005. Chromatin remodelling and epigenetic features of germ cells. Nature. 434, 583–589.

    Article  CAS  PubMed  Google Scholar 

  10. Klose R.J., Bird A. P. 2006. Genomic DNA methylation: The mark and its mediators. Trends. Biochem. Sci. 31, 89–97.

    Article  CAS  PubMed  Google Scholar 

  11. Both T.L., Sweatt J.D. 2009. Regulation of chromatin structure in memory formation. Curr. Opin. Neurobiol. 19, 336–342.

    Article  Google Scholar 

  12. Eden A., Gaudet F., Waghmare A., Jaenisch R. 2003. Chromosomal instability and tumors promoted by DNA hypomethylation. Science. 300, 455.

    Article  CAS  PubMed  Google Scholar 

  13. Gaudet F., Hodgson J.G., Eden A., Jackson-Grusby L., Dausman J., Gray J.W., Leonhardt H., Jaenisch R. 2003. Induction of tumors in mice by genomic hypomethylation. Science. 300, 489–492.

    Article  CAS  PubMed  Google Scholar 

  14. Fuks F., Burgers W.A., Brehm A., Hughes-Davies L., Kouzarides T. 2000. DNA methyltransferase Dnmt1 associates with histone deacetylase activity. Nature Genet. 24, 88–91.

    Article  CAS  PubMed  Google Scholar 

  15. Datta J., Ghoshal K., Sharma S.M., Tajima S., Jacob S.T. 2003. Biochemical fractionation reveals association of DNA methyltransferase (Dnmt) 3b with Dnmt 1 and that of Dnmt 3a with a histone H3 methyltransferase and Hdacl. J. Cell. Biochem. 88, 855–864.

    Article  CAS  PubMed  Google Scholar 

  16. Bourc’his D., Xu G.L., Lin C.S., Bollman B., Bestor T.H. 2001. Dnmt3L and the establishment of maternal genomic imprints. Science. 294, 2536–2539.

    Article  PubMed  Google Scholar 

  17. Hata K., Okano M., Lei H., Li E. 2002. Dnmt3L cooperates with the Dnmt3 family of de novo DNA methyltransferases to establish maternal imprints in mice. Development. 129, 1983–1993.

    CAS  PubMed  Google Scholar 

  18. Boateng K.A., Yang X., Dong F., Owen H.A., Makaroff C.A. 2008. SWI1 is required for meiotic chromosome remodeling events. Mol. Plant. 1, 620–633.

    Article  CAS  PubMed  Google Scholar 

  19. Richards E.J. 1997. DNA methylation and plant development. Trends. Genet. 13, 319–323.

    Article  CAS  PubMed  Google Scholar 

  20. Oakeley E.J., Podesta A., Jost J. P. 1997. Developmental changes in DNA methylation of the two tobacco pollen nuclei during maturation. Proc. Natl. Acad. Sci. USA. 94, 11721–11725.

    Article  CAS  PubMed  Google Scholar 

  21. Hotta Y., Hecht N. 1971. Methylation of Lilium DNA during the meiotic cycle. Biochim. Biophys. Acta. 238, 50–59.

    CAS  PubMed  Google Scholar 

  22. Ito M., Stern H. 1967. Studies of meiosis in vitro: 1. In vitro culture of meiotic cells. Dev. Biol. 16, 36–53.

    Article  CAS  PubMed  Google Scholar 

  23. Hotts Y., Ito M., Stern H. 1966. Synthesis of DNA during meiosis. Proc. Natl. Acad. Sci. USA. 56, 1184–1191.

    Article  Google Scholar 

  24. Oakeley E.J., Jost J. P. 1996. Nonsymmetrical cytosine methylation in tobacco pollen DNA. Plant. Mol. Biol. 31, 927–930.

    Article  CAS  PubMed  Google Scholar 

  25. Johnston J.W., Harding K., Bremner D.H., Souch G., Green J., Lynch P.T., Grout B., Benson E.E. 2005. HPLC analysis of plant DNA methylation: A study of critical methodological factors. Plant. Physiol. Biochem. 43, 844–853.

    Article  CAS  PubMed  Google Scholar 

  26. Baumel A., Ainouche M.L., Levasseur J.E. 2001. Molecular investigations in populations of Spartina anglica C.E. Hubbard (Poaceae) invading coastal Brittany (France). Mol. Ecol. 10, 1689–1701.

    Article  CAS  PubMed  Google Scholar 

  27. Demeulemeester M.A.C., van Stallen N., de Proft M.P. 1999. Degree of DNA methylation in chicory (Cichorium intybus L.): Influence of plant age and vernalisation. Plant. Sci. 142, 101–108.

    Article  CAS  Google Scholar 

  28. Wang X.Y., Guo G.Q., Nie X.W., Zheng G.C. 1998. Cytochemical localization of cellulase activity in pollen mother cells of David lily during meiotic prophase I and its relation to secondary formation of plasmodesmata. Protoplasma. 204, 128–138.

    Article  CAS  Google Scholar 

  29. Vanyushin B.F. 2005.Methylation of adenine residues in DNA of eucaryotes. Mol. Biol. (Mosk.). 39, 557–566.

    Google Scholar 

  30. Maatouk D.M., Kellam L.D., Mann M.R., Lei H., Li E., Bartolomei M.S., Resnick J.L. 2006. DNA methylation is a primary mechanism for silencing postmigratory primordial germ cell genes in both germ cell and somatic cell lineages. Development. 133, 3411–3341.

    Article  CAS  PubMed  Google Scholar 

  31. Ma H. 2005. Molecular genetic analyses of microsporogenesis and microgametogenesis in flowering plants. Annu. Rev. Plant. Biol. 56, 393–434.

    Article  CAS  PubMed  Google Scholar 

  32. Bestor T.H., Tycko B. 1996. Creation of genomic methylation patterns. Nature Genet. 12, 363–367.

    Article  CAS  PubMed  Google Scholar 

  33. Minard M.E., Jain A.K., Barton M.C. 2009. Analysis of epigenetic alterations to chromatin during development. Genesis. 47, 559–572.

    Article  CAS  PubMed  Google Scholar 

  34. Geyer C.B., Kiefer C.M., Yang T.P., McCarrey J.R. 2004. Ontogeny of a demethylation domain and its relationship to activation of tissue-specific transcription. Biol. Reprod. 71, 837–844.

    Article  CAS  PubMed  Google Scholar 

  35. Hotta Y., Stern H. 1971. Analysis of DNA synthesis during meiotic prophase in Lilium. J. Mol. Biol. 55, 337–355.

    Article  CAS  PubMed  Google Scholar 

  36. Montero L.M., Filipski J., Gil P., Capel J., Martínez-Zapater J.M., Salinas J. 1992. The distribution of 5-methylcytosine in the nuclear genome of plants. Nucleic Acids Res. 20, 3207–3210.

    Article  CAS  PubMed  Google Scholar 

  37. Morris F.M., Vasil I.K. 1989. DNA methylation and embryogenic competence in leaves and callus of Napiergrass (Pennisetum purpureum Schum.) Plant. Physiol. 90, 37–40.

    Article  Google Scholar 

  38. Wagner I., Capesius I. 1981. Determination of 5-methycytosine from plant DNA by high-performance liquid chromatography. Biochim. Biophys. Acta. 654, 52–56.

    CAS  PubMed  Google Scholar 

  39. Zhang X., Yazaki J., Sundaresan A., Cokus S., Chan S.W., Chen H., Henderson I.R., Shinn P., Pellegrini M., Jaeobsen S.E., Eeker J.R. 2006. Genomewide high-resolution mapping and functional analysis of DNA methylation in Cell. 126, 1189–1201.

    CAS  Google Scholar 

  40. Ma J., Devos K.M., Bennetzen J.L. 2004. Analyses of LTR-retrotransposon structures reveal recent and rapid genomic DNA loss in rice. Genome. Res. 14, 860–869.

    Article  CAS  PubMed  Google Scholar 

  41. Sabot F., Guyot R., Wicker T., Chantret N., Laubin B., Leroy P., Sourdille P., Bernard M. 2005. Updating of transposable element annotations from large wheat genomic sequences reveals diverse activities and gene associations. Mol. Genet. Genomics. 274, 119–130.

    Article  CAS  PubMed  Google Scholar 

  42. Ergle D.R., Katterman F.R.H. 1961. Deoxyribonucleic acid of cotton. Plant Physiol. 36, 811–815

    Article  CAS  PubMed  Google Scholar 

  43. Lengauer C. 2003. Cancer: An unstable liaison. Science. 300, 442–443.

    Article  CAS  PubMed  Google Scholar 

  44. Messeguer R., Ganal M.W., Steffens J.C., Tanksley S.D. 1991. Characterization of the level, target sites and inheritance of cytosine methylation in tomato nuclear DNA. Plant. Mol. Biol. 16, 753–770.

    Article  CAS  PubMed  Google Scholar 

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Correspondence to Guangqin Guo.

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Huang, J., Wang, H., Xie, X. et al. Developmental changes in DNA methylation of pollen mother cells of David lily during meiotic prophase I. Mol Biol 44, 754–759 (2010). https://doi.org/10.1134/S0026893310050110

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  • DOI: https://doi.org/10.1134/S0026893310050110

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