Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Epigenetic memory marks determine epiallele stability at loci targeted by de novo DNA methylation

Nature Plants volume 6, pages 661–674 (2020)Cite this article

Subjects

Abstract

It is generally assumed that DNA methylation changes at genomic regions targeted by the de novo RNA-directed DNA methylation (RdDM) pathway are unstable. Here, we show that RdDM targets in Arabidopsis can be classified into two groups on the basis of whether there is remethylation following the restoration of NRPD1 function in nrpd1 mutant plants—remethylable loci and non-remethylable loci. In contrast to the remethylable loci, the non-remethylable loci contain higher levels of the euchromatic marks of trimethylation at Lys 4 of histone H3 (H3K4me3), which interferes with the recruitment of the RdDM molecular machinery, and acetylation at Lys 18 of histone H3 (H3K18ac), which helps to recruit the DNA demethylase ROS1 to antagonize RdDM. Here, using targeted methylation erasure by CRISPR–dCas9–TET1, we demonstrate that methylated CG (mCG) and mCHG (where H represents A, C or T) are memory marks that are required for targeting the RdDM machinery to remethylable loci. Our results show that histone and DNA methylation marks are critical in determining the ability of RdDM target loci to form stable epialleles, and contribute to understanding the formation and transmission of epialleles.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: Transgenerational inheritance of DNA methylation changes at RdDM target loci.
Fig. 2: DNA methylation patterns of CDs and NDs in backcrosses.
Fig. 3: Genetic and epigenetic features of CDs and NDs.
Fig. 4: Increased H3K4me3 at specific NDs in the nrpd1 mutant prevents recruitment of the RdDM machinery.
Fig. 5: ROS1 antagonizes RdDM in the process of re-establishing DNA methylation at specific ND loci.
Fig. 6: The remaining mCG and mCHG act as memory marks for the recruitment of the RdDM machinery.
Fig. 7: The behaviour of NDs in other RdDM mutants and in long-term inheritance.

Similar content being viewed by others

Data availability

All high-throughput sequencing data reported in this paper are provided at the GEO (GSE140566). Source Data for Figs. 1–6 are provided with the paper.

References

  1. Zhang, H., Lang, Z. & Zhu, J.-K. Dynamics and function of DNA methylation in plants. Nat. Rev. Mol. Cell Biol. 19, 489–506 (2018).

    Article  CAS  PubMed  Google Scholar 

  2. Matzke, M. A., Kanno, T. & Matzke, A. J. RNA-directed DNA methylation: the evolution of a complex epigenetic pathway in flowering plants. Annu. Rev. Plant Biol. 66, 243–267 (2015).

    Article  CAS  PubMed  Google Scholar 

  3. Haag, J. R. et al. In vitro transcription activities of Pol IV, Pol V, and RDR2 reveal coupling of Pol IV and RDR2 for dsRNA synthesis in plant RNA silencing. Mol. Cell 48, 811–818 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Xie, Z. et al. Genetic and functional diversification of small RNA pathways in plants. PLoS Biol. 2, e104 (2004).

    Article  PubMed  PubMed Central  Google Scholar 

  5. Zilberman, D., Cao, X. & Jacobsen, S. E. ARGONAUTE4 control of locus-specific siRNA accumulation and DNA and histone methylation. Science 299, 716–719 (2003).

    Article  CAS  PubMed  Google Scholar 

  6. Gao, Z. et al. An RNA polymerase II-and AGO4-associated protein acts in RNA-directed DNA methylation. Nature 465, 106–109 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Zhong, X. et al. Molecular mechanism of action of plant DRM de novo DNA methyltransferases. Cell 157, 1050–1060 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Aufsatz, W., Mette, M. F., van der Winden, J., Matzke, M. & Matzke, A. J. HDA6, a putative histone deacetylase needed to enhance DNA methylation induced by double-stranded RNA. EMBO J. 21, 6832–6841 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Jackson, J. P. et al. Dimethylation of histone H3 lysine 9 is a critical mark for DNA methylation and gene silencing in Arabidopsis thaliana. Chromosoma 112, 308–315 (2004).

    Article  CAS  PubMed  Google Scholar 

  10. Ebbs, M. L. & Bender, J. Locus-specific control of DNA methylation by the Arabidopsis SUVH5 histone methyltransferase. Plant Cell 18, 1166–1176 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Jackson, J. P., Lindroth, A. M., Cao, X. & Jacobsen, S. E. Control of CpNpG DNA methylation by the KRYPTONITE histone H3 methyltransferase. Nature 416, 556–560 (2002).

    Article  CAS  PubMed  Google Scholar 

  12. Deleris, A. et al. Involvement of a Jumonji‐C domain‐containing histone demethylase in DRM2‐mediated maintenance of DNA methylation. EMBO Rep. 11, 950–955 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Searle, I. R., Pontes, O., Melnyk, C. W., Smith, L. M. & Baulcombe, D. C. JMJ14, a JmjC domain protein, is required for RNA silencing and cell-to-cell movement of an RNA silencing signal in Arabidopsis. Genes Dev. 24, 986–991 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Kim, J., Kim, J. H., Richards, E. J., Chung, K. M. & Woo, H. R. Arabidopsis VIM proteins regulate epigenetic silencing by modulating DNA methylation and histone modification in cooperation with MET1. Mol. Plant 7, 1470–1485 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Stroud, H. et al. Non-CG methylation patterns shape the epigenetic landscape in Arabidopsis. Nat. Struct. Mol. Biol. 21, 64–72 (2014).

    Article  CAS  PubMed  Google Scholar 

  16. Stroud, H., Greenberg, M. V., Feng, S., Bernatavichute, Y. V. & Jacobsen, S. E. Comprehensive analysis of silencing mutants reveals complex regulation of the Arabidopsis methylome. Cell 152, 352–364 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Du, J. et al. Dual binding of chromomethylase domains to H3K9me2-containing nucleosomes directs DNA methylation in plants. Cell 151, 167–180 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Zemach, A. et al. The Arabidopsis nucleosome remodeler DDM1 allows DNA methyltransferases to access H1-containing heterochromatin. Cell 153, 193–205 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Zhu, J.-K. Active DNA demethylation mediated by DNA glycosylases. Annu. Rev. Genet. 43, 143–166 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Gong, Z. et al. ROS1, a repressor of transcriptional gene silencing in Arabidopsis, encodes a DNA glycosylase/lyase. Cell 111, 803–814 (2002).

    Article  CAS  PubMed  Google Scholar 

  21. Gehring, M. et al. DEMETER DNA glycosylase establishes MEDEA polycomb gene self-imprinting by allele-specific demethylation. Cell 124, 495–506 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Ortega-Galisteo, A. P., Morales-Ruiz, T., Ariza, R. R. & Roldán-Arjona, T. Arabidopsis DEMETER-LIKE proteins DML2 and DML3 are required for appropriate distribution of DNA methylation marks. Plant Mol. Biol. 67, 671–681 (2008).

    Article  CAS  PubMed  Google Scholar 

  23. Lei, M. et al. Regulatory link between DNA methylation and active demethylation in Arabidopsis. Proc. Natl Acad. Sci. USA 112, 3553–3557 (2015).

    Article  CAS  PubMed  Google Scholar 

  24. Lang, Z. et al. The methyl-CpG-binding protein MBD7 facilitates active DNA demethylation to limit DNA hyper-methylation and transcriptional gene silencing. Mol. Cell 57, 971–983 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Duan, C. G. et al. A pair of transposon-derived proteins function in a histone acetyltransferase complex for active DNA demethylation. Cell Res. 27, 226–240 (2017).

    Article  CAS  PubMed  Google Scholar 

  26. Qian, W. et al. A histone acetyltransferase regulates active DNA demethylation in Arabidopsis. Science 336, 1445–1448 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Nie, W.-F. et al. Histone acetylation recruits the SWR1 complex to regulate active DNA demethylation in Arabidopsis. Proc. Natl Acad. Sci. USA 116, 16641–16650 (2019).

    Article  CAS  PubMed  Google Scholar 

  28. Tang, K., Lang, Z., Zhang, H. & Zhu, J.-K. The DNA demethylase ROS1 targets genomic regions with distinct chromatin modifications. Nat. Plants 2, 16169 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Jiang, C. et al. Environmentally responsive genome-wide accumulation of de novo Arabidopsis thaliana mutations and epimutations. Genome Res. 24, 1821–1829 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Zhang, H., Zhang, K. & Zhu, J.-K. A model for the aberrant DNA methylomes in aging cells and cancer cells. Biochem. Soc. Trans. 47, 997–1003 (2019).

    Article  CAS  PubMed  Google Scholar 

  31. Schmitz, R. J. et al. Transgenerational epigenetic instability is a source of novel methylation variants. Science 334, 369–373 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Zhang, Q. et al. Methylation interactions in Arabidopsis hybrids require RNA-directed DNA methylation and are influenced by genetic variation. Proc. Natl Acad. Sci. USA 113, E4248–E4256 (2016).

    Article  CAS  PubMed  Google Scholar 

  33. Hollick, J. B. Paramutation and related phenomena in diverse species. Nat. Rev. Genet 18, 5–23 (2017).

    Article  CAS  PubMed  Google Scholar 

  34. Vongs, A., Kakutani, T., Martienssen, R. A. & Richards, E. J. Arabidopsis thaliana DNA methylation mutants. Science 260, 1926–1928 (1993).

    Article  CAS  PubMed  Google Scholar 

  35. Saze, H., Mittelsten Scheid, O. & Paszkowski, J. Maintenance of CpG methylation is essential for epigenetic inheritance during plant gametogenesis. Nat. Genet. 34, 65–69 (2003).

    Article  CAS  PubMed  Google Scholar 

  36. Kankel, M. W. et al. Arabidopsis MET1 cytosine methyltransferase mutants. Genetics 163, 1109–1122 (2003).

    CAS  PubMed  PubMed Central  Google Scholar 

  37. Kakutani, T., Munakata, K., Richards, E. J. & Hirochika, H. Meiotically and mitotically stable inheritance of DNA hypomethylation induced by ddm1 mutation of Arabidopsis thaliana. Genetics 151, 831–838 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  38. Teixeira, F. K. et al. A role for RNAi in the selective correction of DNA methylation defects. Science 323, 1600–1604 (2009).

    Article  CAS  PubMed  Google Scholar 

  39. Blevins, T. et al. A two-step process for epigenetic inheritance in Arabidopsis. Mol. Cell 54, 30–42 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Catoni, M. et al. DNA sequence properties that predict susceptibility to epiallelic switching. EMBO J. 36, 617–628 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Law, J. A. et al. Polymerase IV occupancy at RNA-directed DNA methylation sites requires SHH1. Nature 498, 385–389 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Matzke, M. A. & Mosher, R. A. RNA-directed DNA methylation: an epigenetic pathway of increasing complexity. Nat. Rev. Genet. 15, 394–408 (2014).

    Article  CAS  PubMed  Google Scholar 

  43. Zhang, X., Bernatavichute, Y. V., Cokus, S., Pellegrini, M. & Jacobsen, S. E. Genome-wide analysis of mono-, di- and trimethylation of histone H3 lysine 4 in Arabidopsis thaliana. Genome Biol. 10, R62 (2009).

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  44. Gendrel, A. V., Lippman, Z., Yordan, C., Colot, V. & Martienssen, R. A. Dependence of heterochromatic histone H3 methylation patterns on the Arabidopsis gene DDM1. Science 297, 1871–1873 (2002).

    Article  CAS  PubMed  Google Scholar 

  45. Tariq, M. et al. Erasure of CpG methylation in Arabidopsis alters patterns of histone H3 methylation in heterochromatin. Proc. Natl Acad. Sci. USA 100, 8823–8827 (2003).

    Article  CAS  PubMed  Google Scholar 

  46. Barman, S. Construction and Senescence Phenotype Analysis of Double Mutants Encoding H3K4me3 Methyltransferases in Arabidopsis thaliana. MSc thesis, California State Univ. (2017).

  47. Chen, L.-Q. et al. ATX3, ATX4, and ATX5 encode putative H3K4 methyltransferases and are critical for plant development. Plant Physiol. 174, 1795–1806 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Saleh, A. et al. The highly similar Arabidopsis homologs of trithorax ATX1 and ATX2 encode proteins with divergent biochemical functions. Plant Cell 20, 568–579 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Guo, L., Yu, Y., Law, J. A. & Zhang, X. SET DOMAIN GROUP2 is the major histone H3 lysine 4 trimethyltransferase in Arabidopsis. Proc. Natl Acad. Sci. USA 107, 18557–18562 (2010).

    Article  CAS  PubMed  Google Scholar 

  50. Reinders, J. et al. Compromised stability of DNA methylation and transposon immobilization in mosaic Arabidopsis epigenomes. Genes Dev. 23, 939–950 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Mathieu, O., Reinders, J., Caikovski, M., Smathajitt, C. & Paszkowski, J. Transgenerational stability of the Arabidopsis epigenome is coordinated by CG methylation. Cell 130, 851–862 (2007).

    Article  CAS  PubMed  Google Scholar 

  52. Wu, X. & Zhang, Y. TET-mediated active DNA demethylation: mechanism, function and beyond. Nat. Rev. Genet. 18, 517–534 (2017).

    Article  CAS  PubMed  Google Scholar 

  53. Ji, L. et al. TET-mediated epimutagenesis of the Arabidopsis thaliana methylome. Nat. Commun. 9, 895 (2018).

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  54. Gallego-Bartolome, J. et al. Targeted DNA demethylation of the Arabidopsis genome using the human TET1 catalytic domain. Proc. Natl Acad. Sci. USA 115, E2125–E2134 (2018).

    Article  PubMed  CAS  Google Scholar 

  55. Jinek, M. et al. A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science 337, 816–821 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Becker, C. et al. Spontaneous epigenetic variation in the Arabidopsis thaliana methylome. Nature 480, 245–249 (2011).

    Article  CAS  PubMed  Google Scholar 

  57. Schmitz, R. J. et al. Patterns of population epigenomic diversity. Nature 495, 193–198 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Zhang, H. et al. DTF1 is a core component of RNA-directed DNA methylation and may assist in the recruitment of Pol IV. Proc. Natl Acad. Sci. USA 110, 8290–8295 (2013).

    Article  CAS  PubMed  Google Scholar 

  59. Stewart, K. R. et al. Dynamic changes in histone modifications precede de novo DNA methylation in oocytes. Genes Dev. 29, 2449–2462 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Morselli, M. et al. In vivo targeting of de novo DNA methylation by histone modifications in yeast and mouse. eLife 4, e06205 (2015).

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  61. Greenberg, M. V. et al. Interplay between active chromatin marks and RNA-directed DNA methylation in Arabidopsis thaliana. PLoS Genet. 9, e1003946 (2013).

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  62. Onodera, Y. et al. Plant nuclear RNA polymerase IV mediates siRNA and DNA methylation-dependent heterochromatin formation. Cell 120, 613–622 (2005).

    Article  CAS  PubMed  Google Scholar 

  63. Pontier, D. et al. Reinforcement of silencing at transposons and highly repeated sequences requires the concerted action of two distinct RNA polymerases IV in Arabidopsis. Genes Dev. 19, 2030–2040 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Berr, A. et al. Arabidopsis SET DOMAIN GROUP2 is required for H3K4 trimethylation and is crucial for both sporophyte and gametophyte development. Plant Cell 22, 3232–3248 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Pien, S. et al. ARABIDOPSIS TRITHORAX1 dynamically regulates FLOWERING LOCUS C activation via histone 3 lysine 4 trimethylation. Plant Cell 20, 580–588 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. He, X. J. et al. An effector of RNA-directed DNA methylation in Arabidopsis is an ARGONAUTE 4- and RNA-binding protein. Cell 137, 498–508 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Mao, Y. et al. Application of the CRISPR–Cas system for efficient genome engineering in plants. Mol. Plant 6, 2008–2011 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Zhang, Z. et al. A multiplex CRISPR/Cas9 platform for fast and efficient editing of multiple genes in Arabidopsis. Plant Cell Rep. 35, 1519–1533 (2016).

    Article  CAS  PubMed  Google Scholar 

  69. Clough, S. J. & Bent, A. F. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16, 735–743 (1998).

    Article  CAS  PubMed  Google Scholar 

  70. Rowland, L. J. & Nguyen, B. Use of polyethylene glycol for purification of DNA from leaf tissue of woody plants. Biotechniques 14, 734–736 (1993).

    CAS  PubMed  Google Scholar 

  71. Gruntman, E. et al. Kismeth: analyzer of plant methylation states through bisulfite sequencing. BMC Bioinform. 9, 371 (2008).

    Article  CAS  Google Scholar 

  72. Xi, Y. & Li, W. BSMAP: whole genome bisulfite sequence MAPping program. BMC Bioinform. 10, 232 (2009).

    Article  CAS  Google Scholar 

  73. Haynes, W. in Encyclopedia of Systems Biology (eds Dubitzky, W. et al.) 78–78 (Springer, 2013).

  74. Yang, D. L. et al. Dicer-independent RNA-directed DNA methylation in Arabidopsis. Cell Res. 26, 66–82 (2016).

    Article  CAS  PubMed  Google Scholar 

  75. Schultz, M. D., Schmitz, R. J. & Ecker, J. R. ‘Leveling’ the playing field for analyses of single-base resolution DNA methylomes. Trends Genet. 28, 583–585 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Langmead, B., Trapnell, C., Pop, M. & Salzberg, S. L. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 10, R25 (2009).

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  77. Saleh, A., Alvarez-Venegas, R. & Avramova, Z. An efficient chromatin immunoprecipitation (ChIP) protocol for studying histone modifications in Arabidopsis plants. Nat. Protoc. 3, 1018–1025 (2008).

    Article  CAS  PubMed  Google Scholar 

  78. Luo, C. et al. Integrative analysis of chromatin states in Arabidopsis identified potential regulatory mechanisms for natural antisense transcript production. Plant J. 73, 77–90 (2013).

    Article  CAS  PubMed  Google Scholar 

  79. Tian, T. et al. agriGO v2.0: a GO analysis toolkit for the agricultural community, 2017 update. Nucleic Acids Res. 45, W122–W129 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Bernatavichute, Y. V., Zhang, X., Cokus, S., Pellegrini, M. & Jacobsen, S. E. Genome-wide association of histone H3 lysine nine methylation with CHG DNA methylation in Arabidopsis thaliana. PLoS ONE 3, e3156 (2008).

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  81. Zheng, B. et al. Intergenic transcription by RNA polymerase II coordinates Pol IV and Pol V in siRNA-directed transcriptional gene silencing in Arabidopsis. Genes Dev. 23, 2850–2860 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We thank Q. Zhang for suggestions. This research was financially supported by the Chinese Academy of Sciences, including the CAS Strategic Priority Research Program, grant number XDB27040101 (to J.-K.Z.).

Author information

Authors and Affiliations

  1. Shanghai Center for Plant Stress Biology, Center for Excellence in Molecular Plant Sciences, Chinese Academy of Sciences, Shanghai, China

    Jingwen Li, Huan Huang, Guiping Zhang, Li He, Jia Pang, Rosa Lozano-Durán, Zhaobo Lang & Jian-Kang Zhu

  2. University of Chinese Academy of Sciences, Beijing, China

    Jingwen Li & Jia Pang

  3. State Key Laboratory of Crop Genetics and Germplasm Enhancement, Nanjing Agricultural University, Nanjing, China

    Dong-Lei Yang

  4. Department of Horticulture and Landscape Architecture, Purdue University, West Lafayette, IN, USA

    Jian-Kang Zhu

Authors
  1. Jingwen Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Dong-Lei Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Huan Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Guiping Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Li He
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Jia Pang
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Rosa Lozano-Durán
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Zhaobo Lang
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Jian-Kang Zhu
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

J.L., D.-L.Y. and J.-K.Z. designed the experiments. J.L., H.H., G.Z., J.P. and L.H. performed the experiments. J.L., R.L.-D., D.-L.Y., Z.L. and J.-K.Z. analysed the data and wrote the manuscript.

Corresponding author

Correspondence to Jian-Kang Zhu.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Peer review information Nature Plants thanks Tzung-Fu Hsieh, Jean Molinier and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Supplementary Information

Supplementary Figs. 1–10.

Reporting Summary

Supplementary Table 1

NRPD1-CD, NRPD1-ND, NRPE1-ND and RDR2-ND lists.

Supplementary Table 2

Primers used in this study.

Supplementary Table 3

Derepressed genes/TEs in the nrpd1-3 mutant.

Supplementary Table 4

CD/ND gene lists.

Supplementary Table 5

P values.

Supplementary Data

Source data for supplementary figures.

Source data

Source Data Fig. 1

Unprocessed gels.

Source Data Fig. 4

Unprocessed gels.

Source Data Fig. 4

Statistical source data.

Source Data Fig. 5

Unprocessed gels.

Source Data Fig. 5

Statistical source data.

Source Data Fig. 6

Unprocessed gels.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Li, J., Yang, DL., Huang, H. et al. Epigenetic memory marks determine epiallele stability at loci targeted by de novo DNA methylation. Nat. Plants 6, 661–674 (2020). https://doi.org/10.1038/s41477-020-0671-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41477-020-0671-x

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing