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Plant DNA methyltransferase genes: Multiplicity, expression, methylation patterns

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Abstract

Expression and methylation patterns of genes encoding DNA methyltransferases and their functionally related proteins were studied in organs of Arabidopsis thaliana plants. Genes coding for the major maintenance-type DNA methyltransferases, MET1 and CMT3, and the major de novo-type DNA methyltransferase, DRM2, are actively expressed in all organs. Similar constitutively active expression was observed for genes encoding their functionally related proteins, a histone H3K9 methyltransferase KYP and a catalytically non-active protein DRM3. Expression of the MET1 and CMT3 genes is significantly lower in developing endosperm compared with embryo. Vice versa, expression of the MET2a, MET2b, MET3, and CMT2 genes in endosperm is much more active compared with embryo. A special maintenance DNA methylation system seems to operate in endosperm. The DNMT2 and N6AMT genes encoding putative methyltransferases are constitutively expressed at low levels. CMT1 and DRM1 genes are expressed rather weakly in all investigated organs. Most of the studied genes have methylation patterns conforming to the “body-methylated gene” prototype. A peculiar feature of the MET family genes is methylation at all three possible site types (CG, CHG, and CHH). The most weakly expressed among genes of their respective families, CMT1 and DRM1, are practically unmethylated. The MET3 and N6AMT genes have unusual methylation patterns, promoter region, and most of the gene body devoid of any methylation, and the 3'-end proximal part of the gene body is highly methylated.

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Abbreviations

m5C:

5-methylcytosine

Nm6A:

N6-methyladenine

Nm4C:

N4-methylcytosine

Nm2G:

N2-methylguanine

RdDM:

RNA-directed DNA methylation

siRNA:

small interfering RNA

References

  1. Feng, S., and Jacobsen, S. E. (2011) Epigenetic modifications in plants: an evolutionary perspective, Curr. Opin. Plant Biol., 14, 179–186.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  2. Vanyushin, B. F., and Ashapkin, V. V. (2011) DNA methylation in higher plants: past, present and future, Biochim. Biophys. Acta, 1809, 360–368.

    Article  PubMed  CAS  Google Scholar 

  3. Cokus, S. J., Feng, S., Zhang, X., Chen, Z., Merriman, B., Haudenschild, C. D., Pradhan, S., Nelson, S. F., Pellegrini, M., and Jacobsen, S. E. (2008) Shotgun bisulfite sequencing of the Arabidopsis genome reveals DNA methylation patterning, Nature, 452, 215–219.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  4. Lister, R., O’Malley, R. C., Tonti-Filippini, J., Gregory, B. D., Berry, C. C., Millar, A. H., and Ecker, J. R. (2008) Highly integrated single-base resolution maps of the epigenome in Arabidopsis, Cell, 133, 523–536.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  5. Vanyushin, B. F., and Ashapkin, V. V. (2009) DNA Methylation in Plants, Nova Science Publishers Inc., N. Y.

    Google Scholar 

  6. Buryanov, Ya. I., and Shevchuk, T. V. (2005) DNA methyltransferases and structural-functional specificity of eukaryotic DNA modification, Biochemistry (Moscow), 70, 730–742.

    Article  CAS  Google Scholar 

  7. Goll, M. G., and Bestor, T. H. (2005) Eukaryotic cytosine methyltransferases, Annu. Rev. Biochem., 74, 481–514.

    Article  PubMed  CAS  Google Scholar 

  8. Pavlopoulou, A., and Kossida, S. (2007) Plant cytosine-5 DNA methyltransferases: structure, function, and molecular evolution, Genomics, 90, 530–541.

    PubMed  CAS  Google Scholar 

  9. Woo, H. R., Dittmer, T. A., and Richards, E. J. (2008) Three SRA-domain methylcytosine-binding proteins cooperate to maintain global CpG methylation and epigenetic silencing in Arabidopsis, PLoS Genet., 4, e1000156.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  10. Du, J., Zhong, X., Bernatavichute, Y. V., Stroud, H., Feng, S., Caro, E., Vashisht, A. A., Terragni, J., Chin, H. G., Tu, A., Hetzel, J., Wohlschlegel, J. A., Pradhan, S., Patel, D. J., and Jacobsen, S. E. (2012) Dual binding of chromomethylase domains to H3K9me2-containing nucleosomes directs DNA methylation in plants, Cell, 151, 167–180.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  11. Johnson, L. M., Bostick, M., Zhang, X., Kraft, E., Henderson, I., Callis, J., and Jacobsen, S. E. (2007) The SRA methylcytosine-binding domain links DNA and histone methylation, Curr. Biol., 17, 379–384.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  12. Cao, X., and Jacobsen, S. E. (2002) Role of the Arabidopsis DRM methyltransferases in de novo DNA methylation and gene silencing, Curr. Biol., 12, 1138–1144.

    Article  PubMed  CAS  Google Scholar 

  13. Cao, X., Aufsatz, W., Zilberman, D., Mette, M. F., Huang, M. S., Matzke, M., and Jacobsen, S. E. (2003) Role of the DRM and CMT3 methyltransferases in RNA-directed DNA methylation, Curr. Biol., 13, 2212–2217.

    Article  PubMed  CAS  Google Scholar 

  14. Johnson, L. M., Law, J. A., Khattar, A., Henderson, I. R., and Jacobsen, S. E. (2008) SRA-domain proteins required for DRM2-mediated de novo DNA methylation, PLoS Genet., 4, e1000280.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  15. Zhang, X., and Jacobsen, S. E. (2006) Genetic analyses of DNA methyltransferases in Arabidopsis thaliana, Cold Spring Harb. Symp. Quant. Biol., 71, 439–447.

    Article  PubMed  CAS  Google Scholar 

  16. Ashapkin, V. V., Kutueva, L. I., and Vanyushin, B. F. (2002) The gene for domains rearranged methyltransferase (DRM2) in Arabidopsis thaliana plants is methylated at both cytosine and adenine residues, FEBS Lett., 532, 367–372.

    Article  PubMed  CAS  Google Scholar 

  17. Perry, S. E., and Wang, H. (2003) Rapid isolation of Arabidopsis thaliana developing embryos, BioTechniques, 35, 278–282.

    PubMed  CAS  Google Scholar 

  18. Ashapkin, V. V., Linkova, N. S., Khavinson, V. Kh., and Vanyushin, B. F. (2015) Epigenetic mechanisms of peptidergic regulation of gene expression during aging of human cells, Biochemistry (Moscow), 80, 310–322.

    Article  CAS  Google Scholar 

  19. Suzuki, Y., Kawazu, T., and Koyama, H. (2004) RNA isolation from siliques, dry seeds, and other tissues of Arabidopsis thaliana, BioTechniques, 37, 542–544.

    PubMed  CAS  Google Scholar 

  20. Ashapkin, V. V., Kutueva, L. I., and Vanyushin, B. F. (2011) Is the cytosine DNA methyltransferase gene MET1 regulated by DNA methylation in Arabidopsis thaliana plants? Russ. J. Genet., 47, 279–288.

    Article  CAS  Google Scholar 

  21. Pagnussat, G. C., Yu, H.-J., Ngo, Q. A., Rajani, S., Mayalagu, S., Johnson, C. S., Capron, A., Xie, L.-F., Ye, D., and Sundaresan, V. (2005) Genetic and molecular identification of genes required for female gametophyte development and function in Arabidopsis, Development, 132, 603–614.

    Article  PubMed  CAS  Google Scholar 

  22. Makarevich, G., Villar, C. B. R., Erilova, A., and Koehler, C. (2008) Mechanism of PHERES1 imprinting in Arabidopsis, J. Cell Sci., 121, 906–912.

    Article  PubMed  CAS  Google Scholar 

  23. Hsieh, T.-F., Shin, J., Uzawa, R., Silva, P., Cohen, S., Bauer, M. J., Hashimoto, M., Kirkbride, R. C., Harada, J. J., Zilberman, D., and Fischer, R. L. (2011) Regulation of imprinted gene expression in Arabidopsis endosperm, Proc. Natl. Acad. Sci. USA, 108, 1755–1762.

    Article  PubMed Central  PubMed  Google Scholar 

  24. Jullien, P. E., Susaki, D., Yelagandula, R., Higashiyama, T., and Berger, F. (2012) DNA methylation dynamics during sexual reproduction in Arabidopsis thaliana, Curr. Biol., 22, 1825–1830.

    Article  PubMed  CAS  Google Scholar 

  25. Zemach, A., Kim, M. Y., Hsieh, P.-H., Coleman-Derr, D., Eshed-Williams, L., Thao, K., Harmer, S. L., and Zilberman, D. (2013) The Arabidopsis nucleosome remodeler DDM1 allows DNA methyltransferases to access H1containing heterochromatin, Cell, 153, 193–205.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  26. Stroud, H., Do, T., Du, J., Zhong, X., Feng, S., Johnson, L., Patel, D. J., and Jacobsen, S. E. (2014) Non-CG methylation patterns shape the epigenetic landscape in Arabidopsis, Nat. Struct. Mol. Biol., 21, 64–72.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  27. Henderson, I. R., Deleris, A., Wong, W., Zhong, X., Chin, H. G., Horwitz, G. A., Kelly, K. A., Pradhan, S., and Jacobsen, S. E. (2010) The de novo cytosine methyltransferase DRM2 requires intact UBA domains and a catalytically mutated paralog DRM3 during RNA-directed DNA methylation in Arabidopsis thaliana, PLoS Genet., 6, e1001182.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  28. Costa-Nunes, P., Kim, J. Y., Hong, E., and Pontes, O. (2014) The cytological and molecular role of domains rearranged methyltransferase3 in RNA-dependent DNA methylation of Arabidopsis thaliana, BMC Res. Notes, 7, 721.

    Article  PubMed Central  PubMed  Google Scholar 

  29. Zhong, X., Hale, C. J., Nguyen, M., Ausin, I., Groth, M., Hetzel, J., Vashisht, A. A., Henderson, I. R., Wohlschlegel, J. A., and Jacobsen, S. E. (2015) Domains rearranged methyltransferase3 controls DNA methylation and regulates RNA polymerase V transcript abundance in Arabidopsis, Proc. Natl. Acad. Sci. USA, 112, 911–916.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  30. Goll, M. G., Kirpekar, F., Maggert, K. A., Yoder, J. A., Hsieh, C. L., Zhang, X., Golic, K. G., Jacobsen, S. E., and Bestor, T. H. (2006) Methylation of tRNAAsp by the DNA methyltransferase homolog Dnmt2, Science, 311, 395–398.

    Article  PubMed  CAS  Google Scholar 

  31. Song, Y., Wu, K., Dhaubhadel, S., An, L., and Tian, L. (2010) Arabidopsis DNA methyltransferase AtDNMT2 associates with histone deacetylase AtHD2s activity, Biochem. Biophys. Res. Commun., 396, 187–192.

    Article  PubMed  CAS  Google Scholar 

  32. Shorning, B. Yu., and Vanyushin, B. F. (2001) Putative DNA-(amino)methyltransferases in eukaryotes, Biochemistry (Moscow), 66, 753–762.

    Article  CAS  Google Scholar 

  33. Chen, P., Jager, G., and Zheng, B. (2010) Transfer RNA modifications and genes for modifying enzymes in Arabidopsis thaliana, BMC Plant Biol., 10, 201.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  34. Greer, E. L., Blanco, M. A., Gu, L., Sendinc, E., Liu, J., Aristizabal-Corrales, D., Hsu, C.-H., Aravind, L., He, C., and Shi, Y. (2015) DNA methylation on N6-adenine in C. elegans, Cell, 161, 868–878.

    Article  PubMed  CAS  Google Scholar 

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Correspondence to V. V. Ashapkin.

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Published in Russian in Biokhimiya, 2016, Vol. 81, No. 2, pp. 238–250.

Originally published in Biochemistry (Moscow) On-Line Papers in Press, as Manuscript BM15-286, December 27, 2015.

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Ashapkin, V.V., Kutueva, L.I. & Vanyushin, B.F. Plant DNA methyltransferase genes: Multiplicity, expression, methylation patterns. Biochemistry Moscow 81, 141–151 (2016). https://doi.org/10.1134/S0006297916020085

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  • DOI: https://doi.org/10.1134/S0006297916020085

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