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.

Epigenome plasticity in plants

Abstract

Plant intra-individual and inter-individual variation can be determined by the epigenome, a set of covalent modifications of DNA and chromatin that can alter genome structure and activity without changes to the genome sequence. The epigenome of plant cells is plastic, that is, it can change in response to internal or external cues, such as during development or due to environmental changes, to create a memory of such events. Ongoing advances in technologies to read and write epigenomic patterns with increasing resolution, scale and precision are enabling the extent of plant epigenome variation to be more extensively characterized and functionally interrogated. In this Review, we discuss epigenome dynamics and variation within plants during development and in response to environmental changes, including stress, as well as between plants. We review known or potential functions of such plasticity and emphasize the importance of investigating the causality of epigenomic changes. Finally, we discuss emerging technologies that may underpin future research into plant epigenome plasticity.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Fig. 1: The landscape of DNA methylation in plants.
Fig. 2: Roles of DNA methylation in plant development.
Fig. 3: Epigenome plasticity in development in response to environmental cues.
Fig. 4: Models for epigenomic plasticity induced by stress.
Fig. 5: Epialleles are heritable changes in the epigenome that can confer a phenotype on the plant.
Fig. 6: Genome editing tools can be modified to edit the epigenome.

References

  1. 1.

    Henikoff, S. & Greally, J. M. Epigenetics, cellular memory and gene regulation. Curr. Biol. 26, R644–R648 (2016).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  2. 2.

    Lappalainen, T. & Greally, J. M. Associating cellular epigenetic models with human phenotypes. Nat. Rev. Genet. 18, 441–451 (2017).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  3. 3.

    Suzuki, M. M. & Bird, A. DNA methylation landscapes: provocative insights from epigenomics. Nat. Rev. Genet. 9, 465–476 (2008).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  4. 4.

    Niederhuth, C. E. et al. Widespread natural variation of DNA methylation within angiosperms. Genome Biol. 17, 194 (2016).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  5. 5.

    Deal, R. B. & Henikoff, S. A simple method for gene expression and chromatin profiling of individual cell types within a tissue. Dev. Cell 18, 1030–1040 (2010).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  6. 6.

    Lee, L. R., Wengier, D. L. & Bergmann, D. C. Cell-type-specific transcriptome and histone modification dynamics during cellular reprogramming in the Arabidopsis stomatal lineage. Proc. Natl Acad. Sci. USA 116, 21914–21924 (2019).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  7. 7.

    Song, Q.-X. et al. Genome-wide analysis of DNA methylation in soybean. Mol. Plant 6, 1961–1974 (2013).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  8. 8.

    Kawakatsu, T. et al. Unique cell-type-specific patterns of DNA methylation in the root meristem. Nat. Plants 2, 16058 (2016).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  9. 9.

    Niederhuth, C. E. & Schmitz, R. J. Covering your bases: inheritance of DNA methylation in plant genomes. Mol. Plant 7, 472–480 (2014).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  10. 10.

    Secco, D. et al. Stress induced gene expression drives transient DNA methylation changes at adjacent repetitive elements. eLife 4, e09343 (2015).

    PubMed Central  Article  Google Scholar 

  11. 11.

    Stroud, H. et al. Plants regenerated from tissue culture contain stable epigenome changes in rice. eLife 2, e00354 (2013).

    PubMed  PubMed Central  Article  Google Scholar 

  12. 12.

    Stelpflug, S. C., Eichten, S. R., Hermanson, P. J., Springer, N. M. & Kaeppler, S. M. Consistent and heritable alterations of DNA methylation are induced by tissue culture in maize. Genetics 198, 209–218 (2014).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  13. 13.

    Ong-Abdullah, M. et al. Loss of Karma transposon methylation underlies the mantled somaclonal variant of oil palm. Nature 525, 533–537 (2015). This work establishes that loss of DNA methylation of a Karma transposable element in oil palm plants with abnormal development that had been regenerated through tissue culture was preventing normal gene expression.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  14. 14.

    Han, Z. et al. Heritable epigenomic changes to the maize methylome resulting from tissue culture. Genetics 209, 983–995 (2018).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  15. 15.

    Wibowo, A. et al. Partial maintenance of organ-specific epigenetic marks during plant asexual reproduction leads to heritable phenotypic variation. Proc. Natl Acad. Sci. USA 115, E9145–E9152 (2018).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  16. 16.

    Gordon, S. P., Chickarmane, V. S., Ohno, C. & Meyerowitz, E. M. Multiple feedback loops through cytokinin signaling control stem cell number within the Arabidopsis shoot meristem. Proc. Natl Acad. Sci. USA 106, 16529–16534 (2009).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  17. 17.

    Xiao, J. et al. Cis and trans determinants of epigenetic silencing by Polycomb repressive complex 2 in Arabidopsis. Nat. Genet. 49, 1546–1552 (2017).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  18. 18.

    Costa, S. & Dean, C. Storing memories: the distinct phases of Polycomb-mediated silencing of Arabidopsis FLC. Biochem. Soc. Trans. 47, 1187–1196 (2019).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  19. 19.

    Petrella, R. et al. BPC transcription factors and a Polycomb group protein confine the expression of the ovule identity gene SEEDSTICK in Arabidopsis. Plant J. 102, 582–599 (2020).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  20. 20.

    Yamamuro, C. et al. Overproduction of stomatal lineage cells in Arabidopsis mutants defective in active DNA demethylation. Nat. Commun. 5, 4062 (2014).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  21. 21.

    Wang, Y., Xue, X., Zhu, J.-K. & Dong, J. Demethylation of ERECTA receptor genes by IBM1 histone demethylase affects stomatal development. Development 143, 4452–4461 (2016).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  22. 22.

    Gutzat, R. et al. Arabidopsis shoot stem cells display dynamic transcription and DNA methylation patterns. EMBO J. 39, e103667 (2020).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  23. 23.

    Higo, A. et al. DNA methylation is reconfigured at the onset of reproduction in rice shoot apical meristem. Nat. Commun. 11, 4079 (2020).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  24. 24.

    Zhou, M., Palanca, A. M. S. & Law, J. A. Locus-specific control of the de novo DNA methylation pathway in Arabidopsis by the CLASSY family. Nat. Genet. 50, 865–873 (2018).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  25. 25.

    Zhou, M. et al. The CLASSY family controls tissue-specific DNA methylation patterns in Arabidopsis. bioRxiv https://doi.org/10.1101/2021.01.23.427869 (2021). This paper identifies that most changes in the DNA methylomes of tissues examined in this study are the result of differences in RdDM levels, rather than other DNA methylation pathways. Expression of locus-specific CLSY chromatin remodellers explains many of the tissue-specific differences in DNA methylation levels.

    Article  PubMed  PubMed Central  Google Scholar 

  26. 26.

    Long, J. et al. Nurse cell-derived small RNAs define paternal epigenetic inheritance in Arabidopsis. Science 373, eabh0556 (2021).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  27. 27.

    Walker, J. et al. Sexual-lineage-specific DNA methylation regulates meiosis in Arabidopsis. Nat. Genet. 50, 130–137 (2018). This study identifies many DNA methylation changes in the male reproductive cells as genic targets of RdDM and finds that one change at a gene important for normal meiosis causes abnormal splicing in response to the gain in DNA methylation.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  28. 28.

    Jiang, H., Wang, F. F., Wu, Y. T., Zhou, X. & Huang, X. Y. Multipolar spindle 1 (MPS1), a novel coiled-coil protein of Arabidopsis thaliana, is required for meiotic spindle organization. Plant J. 59, 1001–1010 (2009).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  29. 29.

    Zhong, S. et al. Single-base resolution methylomes of tomato fruit development reveal epigenome modifications associated with ripening. Nat. Biotechnol. 31, 154–159 (2013).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  30. 30.

    Lang, Z. et al. Critical roles of DNA demethylation in the activation of ripening-induced genes and inhibition of ripening-repressed genes in tomato fruit. Proc. Natl Acad. Sci. USA 114, E4511–E4519 (2017). This study mutates the DNA demethylase encoding DML2 gene and shows that DML2 is vital for normal DNA demethylation during fruit ripening of tomatoes and identifies many possible targets of DNA demethylation that may be involved with this process.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  31. 31.

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

    CAS  PubMed  Article  Google Scholar 

  32. 32.

    Gall Trošelj, K., Novak Kujundzic, R. & Ugarkovic, D. Polycomb repressive complex’s evolutionary conserved function: the role of EZH2 status and cellular background. Clin. Epigenet. 8, 55 (2016).

    Article  CAS  Google Scholar 

  33. 33.

    Förderer, A., Zhou, Y. & Turck, F. The age of multiplexity: recruitment and interactions of Polycomb complexes in plants. Curr. Opin. Plant Biol. 29, 169–178 (2016).

    PubMed  Article  CAS  Google Scholar 

  34. 34.

    Chanvivattana, Y. et al. Interaction of Polycomb-group proteins controlling flowering in Arabidopsis. Development 131, 5263–5276 (2004).

    CAS  PubMed  Article  Google Scholar 

  35. 35.

    Ikeuchi, M. et al. PRC2 represses dedifferentiation of mature somatic cells in Arabidopsis. Nat. Plants 1, 15089 (2015).

    CAS  PubMed  Article  Google Scholar 

  36. 36.

    Makarevitch, I. et al. Genomic distribution of maize facultative heterochromatin marked by trimethylation of H3K27. Plant Cell 25, 780–793 (2013).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  37. 37.

    Eichten, S. R., Vaughn, M. W., Hermanson, P. J. & Springer, N. M. Variation in DNA methylation patterns is more common among maize inbreds than among tissues. Plant Genome 6, plantgenome2012.06.0009 (2013).

    Article  CAS  Google Scholar 

  38. 38.

    Mosquna, A. et al. Regulation of stem cell maintenance by the Polycomb protein FIE has been conserved during land plant evolution. Development 136, 2433–2444 (2009).

    CAS  PubMed  Article  Google Scholar 

  39. 39.

    Okano, Y. et al. A polycomb repressive complex 2 gene regulates apogamy and gives evolutionary insights into early land plant evolution. Proc. Natl Acad. Sci. USA 106, 16321–16326 (2009).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  40. 40.

    Satgé, C. et al. Reprogramming of DNA methylation is critical for nodule development in Medicago truncatula. Nat. Plants 2, 16166 (2016).

    PubMed  Article  CAS  Google Scholar 

  41. 41.

    Horvath, D. P., Anderson, J. V., Chao, W. S. & Foley, M. E. Knowing when to grow: signals regulating bud dormancy. Trends Plant Sci. 8, 534–540 (2003).

    CAS  PubMed  Article  Google Scholar 

  42. 42.

    Conde, D. et al. Chilling-responsive DEMETER-LIKE DNA demethylase mediates in poplar bud break. Plant Cell Environ. 40, 2236–2249 (2017).

    CAS  PubMed  Article  Google Scholar 

  43. 43.

    Zhang, Y. et al. Application of 5-azacytidine induces DNA hypomethylation and accelerates dormancy release in buds of tree peony. Plant Physiol. Biochem. 147, 91–100 (2020).

    CAS  PubMed  Article  Google Scholar 

  44. 44.

    de la Fuente, L., Conesa, A., Lloret, A., Badenes, M. L. & Ríos, G. Genome-wide changes in histone H3 lysine 27 trimethylation associated with bud dormancy release in peach. Tree Genet. Genomes 11, 45 (2015).

    Article  Google Scholar 

  45. 45.

    Crisp, P. A., Ganguly, D., Eichten, S. R., Borevitz, J. O. & Pogson, B. J. Reconsidering plant memory: intersections between stress recovery, RNA turnover, and epigenetics. Sci. Adv. 2, e1501340 (2016).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  46. 46.

    Sani, E., Herzyk, P., Perrella, G., Colot, V. & Amtmann, A. Hyperosmotic priming of Arabidopsis seedlings establishes a long-term somatic memory accompanied by specific changes of the epigenome. Genome Biol. 14, R59 (2013).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  47. 47.

    Wang, J. et al. A DNA methylation reader-chaperone regulator-transcription factor complex activates OsHKT1;5 expression during salinity stress. Plant Cell 32, 3535–3558 (2020).

    CAS  PubMed  Article  Google Scholar 

  48. 48.

    Crisp, P. A. et al. Rapid recovery gene downregulation during excess-light stress and recovery in Arabidopsis. Plant Cell 29, 1836–1863 (2017).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  49. 49.

    Ganguly, D. R., Crisp, P. A., Eichten, S. R. & Pogson, B. J. Maintenance of pre-existing DNA methylation states through recurring excess-light stress. Plant Cell Environ. 41, 1657–1672 (2018).

    CAS  PubMed  Article  Google Scholar 

  50. 50.

    Ganguly, D. R., Stone, B. A. B., Bowerman, A. F., Eichten, S. R. & Pogson, B. J. Excess light priming in Arabidopsis thaliana genotypes with altered DNA methylomes. G3 9, 3611–3621 (2019).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  51. 51.

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

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  52. 52.

    Wibowo, A. et al. Hyperosmotic stress memory in Arabidopsis is mediated by distinct epigenetically labile sites in the genome and is restricted in the male germline by DNA glycosylase activity. eLife 5, e13546 (2016).

    PubMed  PubMed Central  Article  Google Scholar 

  53. 53.

    Ganguly, D. R., Crisp, P. A., Eichten, S. R. & Pogson, B. J. The Arabidopsis DNA methylome is stable under transgenerational drought stress. Plant Physiol. 175, 1893–1912 (2017).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  54. 54.

    López, A., Ramírez, V., García-Andrade, J., Flors, V. & Vera, P. The RNA silencing enzyme RNA polymerase V is required for plant immunity. PLoS Genet. 7, e1002434 (2011).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  55. 55.

    Dowen, R. H. et al. Widespread dynamic DNA methylation in response to biotic stress. Proc. Natl Acad. Sci. USA 109, E2183–91 (2012).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  56. 56.

    Yu, A. et al. Dynamics and biological relevance of DNA demethylation in Arabidopsis antibacterial defense. Proc. Natl Acad. Sci. USA 110, 2389–2394 (2013).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  57. 57.

    Martinez, G., Castellano, M., Tortosa, M., Pallas, V. & Gomez, G. A pathogenic non-coding RNA induces changes in dynamic DNA methylation of ribosomal RNA genes in host plants. Nucleic Acids Res. 42, 1553–1562 (2014).

    CAS  PubMed  Article  Google Scholar 

  58. 58.

    Le, T.-N. et al. DNA demethylases target promoter transposable elements to positively regulate stress responsive genes in Arabidopsis. Genome Biol. 15, 458 (2014).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  59. 59.

    Rambani, A. et al. The methylome of soybean roots during the compatible interaction with the soybean Cyst nematode. Plant Physiol. 168, 1364–1377 (2015).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  60. 60.

    López Sánchez, A., Stassen, J. H. M., Furci, L., Smith, L. M. & Ton, J. The role of DNA (de)methylation in immune responsiveness of Arabidopsis. Plant J. 88, 361–374 (2016).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  61. 61.

    Hewezi, T. et al. Cyst nematode parasitism induces dynamic changes in the root epigenome. Plant Physiol. 174, 405–420 (2017).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  62. 62.

    Slaughter, A. et al. Descendants of primed Arabidopsis plants exhibit resistance to biotic stress. Plant Physiol. 158, 835–843 (2012).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  63. 63.

    Liu, S. et al. Role of H1 and DNA methylation in selective regulation of transposable elements during heat stress. N. Phytol. 229, 2238–2250 (2021).

    CAS  Article  Google Scholar 

  64. 64.

    Ito, H. et al. An siRNA pathway prevents transgenerational retrotransposition in plants subjected to stress. Nature 472, 115–119 (2011).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  65. 65.

    Cavrak, V. V. et al. How a retrotransposon exploits the plant’s heat stress response for its activation. PLoS Genet. 10, e1004115 (2014).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  66. 66.

    Stuart, T. et al. Population scale mapping of transposable element diversity reveals links to gene regulation and epigenomic variation. eLife 5, e20777 (2016).

    PubMed  PubMed Central  Article  Google Scholar 

  67. 67.

    Quadrana, L. et al. The Arabidopsis thaliana mobilome and its impact at the species level. eLife 5, e15716 (2016).

    PubMed  PubMed Central  Article  Google Scholar 

  68. 68.

    Choi, J. Y. & Purugganan, M. D. Evolutionary epigenomics of retrotransposon-mediated methylation spreading in rice. Mol. Biol. Evol. 35, 365–382 (2018).

    CAS  PubMed  Article  Google Scholar 

  69. 69.

    Noshay, J. M. et al. Monitoring the interplay between transposable element families and DNA methylation in maize. PLoS Genet. 15, e1008291 (2019).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  70. 70.

    Luna, E., Bruce, T. J. A., Roberts, M. R., Flors, V. & Ton, J. Next-generation systemic acquired resistance. Plant Physiol. 158, 844–853 (2012).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  71. 71.

    Cubas, P., Vincent, C. & Coen, E. An epigenetic mutation responsible for natural variation in floral symmetry. Nature 401, 157–161 (1999).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  72. 72.

    Luff, B., Pawlowski, L. & Bender, J. An inverted repeat triggers cytosine methylation of identical sequences in Arabidopsis. Mol. Cell 3, 505–511 (1999).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  73. 73.

    Durand, S., Bouché, N., Perez Strand, E., Loudet, O. & Camilleri, C. Rapid establishment of genetic incompatibility through natural epigenetic variation. Curr. Biol. 22, 326–331 (2012).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  74. 74.

    Manning, K. et al. A naturally occurring epigenetic mutation in a gene encoding an SBP-box transcription factor inhibits tomato fruit ripening. Nat. Genet. 38, 948–952 (2006).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  75. 75.

    Chen, W. et al. Requirement of CHROMOMETHYLASE3 for somatic inheritance of the spontaneous tomato epimutation Colourless non-ripening. Sci. Rep. 5, 9192 (2015). This work identifies CMT3 as the most significant DNA methyltransferase for the maintenance of the highly stable cnr epiallele in tomatoes, supporting studies that suggested CMT3-related proteins are important for acquisition of novel epialleles.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  76. 76.

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

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  77. 77.

    Kawakatsu, T. et al. Epigenomic diversity in a global collection of Arabidopsis thaliana accessions. Cell 166, 492–505 (2016).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  78. 78.

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

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  79. 79.

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

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  80. 80.

    van der Graaf, A. et al. Rate, spectrum, and evolutionary dynamics of spontaneous epimutations. Proc. Natl Acad. Sci. USA 112, 6676–6681 (2015).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  81. 81.

    Hofmeister, B. T. et al. A genome assembly and the somatic genetic and epigenetic mutation rate in a wild long-lived perennial Populus trichocarpa. Genome Biol. 21, 259 (2020).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  82. 82.

    Zhang, Y., Wendte, J. M., Ji, L. & Schmitz, R. J. Natural variation in DNA methylation homeostasis and the emergence of epialleles. Proc. Natl Acad. Sci. USA 117, 874–4884 (2020). This work finds that genes with CG DNA methylation in some natural populations of Arabidopsis could either lack DNA methylation in others or have transposable element-like methylation patterns associated with silencing, suggesting that natural epialleles result from mis-targeting of silencing machinery to active genes.

    Google Scholar 

  83. 83.

    Zilberman, D. An evolutionary case for functional gene body methylation in plants and animals. Genome Biol. 18, 87 (2017).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  84. 84.

    Bewick, A. J. et al. On the origin and evolutionary consequences of gene body DNA methylation. Proc. Natl Acad. Sci. USA 113, 9111–9116 (2016).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  85. 85.

    Wendte, J. M. et al. Epimutations are associated with CHROMOMETHYLASE 3-induced de novo DNA methylation. eLife 8, e47891 (2019).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  86. 86.

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

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  87. 87.

    Jaligot, E., Rival, A., Beulé, T., Dussert, S. & Verdeil, J.-L. Somaclonal variation in oil palm (Elaeis guineensis Jacq.): the DNA methylation hypothesis. Plant Cell Rep. 19, 684–690 (2000).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  88. 88.

    Mgbeze, G. C. & Iserhienrhien, A. Somaclonal variation associated with oil palm (Elaeis guineensis Jacq.) clonal propagation: a review. Afr. J. Biotechnol. 13, 989–997 (2014).

    Article  CAS  Google Scholar 

  89. 89.

    Johannes, F. et al. Assessing the impact of transgenerational epigenetic variation on complex traits. PLoS Genet. 5, e1000530 (2009).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  90. 90.

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

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  91. 91.

    Soppe, W. J. et al. The late flowering phenotype of fwa mutants is caused by gain-of-function epigenetic alleles of a homeodomain gene. Mol. Cell 6, 791–802 (2000).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  92. 92.

    Furci, L. et al. Identification and characterisation of hypomethylated DNA loci controlling quantitative resistance in Arabidopsis. eLife 8, e40655 (2019).

    PubMed  PubMed Central  Article  Google Scholar 

  93. 93.

    Zhang, Y.-Y., Latzel, V., Fischer, M. & Bossdorf, O. Understanding the evolutionary potential of epigenetic variation: a comparison of heritable phenotypic variation in epiRILs, RILs, and natural ecotypes of Arabidopsis thaliana. Heredity 121, 257–265 (2018).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  94. 94.

    Hollwey, E., Watson, M. & Meyer, P. Expression of the C-terminal domain of mammalian TET3 DNA dioxygenase in Arabidopsis thaliana induces heritable methylation changes at rDNA loci. Adv. Biosci. Biotechnol. 7, 243 (2016).

    CAS  Article  Google Scholar 

  95. 95.

    Hollwey, E., Out, S., Watson, M. R. & Heidmann, I. TET3-mediated demethylation in tomato activates expression of a CETS gene that stimulates vegetative growth. Plant Direct 1, e00022 (2017).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  96. 96.

    Zhang, T.-Q., Xu, Z.-G., Shang, G.-D. & Wang, J.-W. A single-cell RNA sequencing profiles the developmental landscape of Arabidopsis root. Mol. Plant 12, 648–660 (2019).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  97. 97.

    Denyer, T. et al. Spatiotemporal developmental trajectories in the Arabidopsis root revealed using high-throughput single-cell RNA sequencing. Dev. Cell 48, 840–852.e5 (2019).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  98. 98.

    Zhang, T.-Q., Chen, Y. & Wang, J.-W. A single-cell analysis of the Arabidopsis vegetative shoot apex. Dev. Cell 56, 1056–1074.e8 (2021).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  99. 99.

    Farmer, A., Thibivilliers, S., Ryu, K. H., Schiefelbein, J. & Libault, M. Single-nucleus RNA and ATAC sequencing reveals the impact of chromatin accessibility on gene expression in Arabidopsis roots at the single-cell level. Mol. Plant 14, 372–383 (2021).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  100. 100.

    Zhao, Y. & Garcia, B. A. Comprehensive catalog of currently documented histone modifications. Cold Spring Harb. Perspect. Biol. 7, a025064 (2015).

    PubMed  PubMed Central  Article  Google Scholar 

  101. 101.

    Mulqueen, R. M. et al. Highly scalable generation of DNA methylation profiles in single cells. Nat. Biotechnol. 36, 428–431 (2018).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  102. 102.

    Kaya-Okur, H. S. et al. CUT&Tag for efficient epigenomic profiling of small samples and single cells. Nat. Commun. 10, 1930 (2019).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  103. 103.

    Ku, W. L. et al. Single-cell chromatin immunocleavage sequencing (scChIC-seq) to profile histone modification. Nat. Methods 16, 323–325 (2019).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  104. 104.

    Bartlett, D. A., Dileep, V., Henikoff, S. & Gilbert, D. M. High throughput genome-wide single cell protein:DNA binding site mapping by targeted insertion of promoters (TIP-seq). bioRxiv https://doi.org/10.1101/2021.03.17.435909 (2021).

    Article  Google Scholar 

  105. 105.

    Amabile, A. et al. Inheritable silencing of endogenous genes by hit-and-run targeted epigenetic editing. Cell 167, 219–232.e14 (2016).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  106. 106.

    Stepper, P. et al. Efficient targeted DNA methylation with chimeric dCas9–Dnmt3a–Dnmt3L methyltransferase. Nucleic Acids Res. 45, 1703–1713 (2017).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  107. 107.

    Galonska, C. et al. Genome-wide tracking of dCas9-methyltransferase footprints. Nat. Commun. 9, 597 (2018).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  108. 108.

    Pflueger, C. et al. A modular dCas9–SunTag DNMT3A epigenome editing system overcomes pervasive off-target activity of direct fusion dCas9–DNMT3A constructs. Genome Res. 28, 1193–1206 (2018).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  109. 109.

    Ford, E. E. et al. Frequent lack of repressive capacity of promoter DNA methylation identified through genome-wide epigenomic manipulation. bioRxiv https://doi.org/10.1101/170506 (2017).

    Article  Google Scholar 

  110. 110.

    Johnson, L. M. et al. SRA- and SET-domain-containing proteins link RNA polymerase V occupancy to DNA methylation. Nature 507, 124 (2014).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  111. 111.

    Gallego-Bartolomé, 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).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  112. 112.

    Papikian, A., Liu, W., Gallego-Bartolomé, J. & Jacobsen, S. E. Site-specific manipulation of Arabidopsis loci using CRISPR–Cas9 SunTag systems. Nat. Commun. 10, 729 (2019).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  113. 113.

    Gallego-Bartolomé, J. et al. Co-targeting RNA polymerases IV and V promotes efficient de novo DNA methylation in Arabidopsis. Cell 176, 1068–1082.e19 (2019).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  114. 114.

    Bewick, A. J. & Schmitz, R. J. Gene body DNA methylation in plants. Curr. Opin. Plant Biol. 36, 103–110 (2017).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  115. 115.

    Kenchanmane Raju, S. K., Ritter, E. J. & Niederhuth, C. E. Establishment, maintenance, and biological roles of non-CG methylation in plants. Essays Biochem. 63, 743–755 (2019).

    PubMed  PubMed Central  Article  Google Scholar 

  116. 116.

    Cao, X. et al. Conserved plant genes with similarity to mammalian de novo DNA methyltransferases. Proc. Natl Acad. Sci. USA 97, 4979–4984 (2000).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  117. 117.

    Finnegan, E. J. & Dennis, E. S. Isolation and identification by sequence homology of a putative cytosine methyltransferase from Arabidopsis thaliana. Nucleic Acids Res. 21, 2383–2388 (1993).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  118. 118.

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

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  119. 119.

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

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  120. 120.

    Watson, M., Hawkes, E. & Meyer, P. Transmission of epi-alleles with MET1-dependent dense methylation in Arabidopsis thaliana. PLoS ONE 9, e105338 (2014).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  121. 121.

    Papa, C. M., Springer, N. M., Muszynski, M. G., Meeley, R. & Kaeppler, S. M. Maize chromomethylase Zea methyltransferase2 is required for CpNpG methylation. Plant Cell 13, 1919–1928 (2001).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  122. 122.

    Lindroth, A. M. et al. Requirement of CHROMOMETHYLASE3 for maintenance of CpXpG methylation. Science 292, 2077–2080 (2001).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  123. 123.

    Johnson, L., Cao, X. & Jacobsen, S. Interplay between two epigenetic marks. DNA methylation and histone H3 lysine 9 methylation. Curr. Biol. 12, 1360–1367 (2002).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  124. 124.

    Johnson, L. M. et al. The SRA methyl-cytosine-binding domain links DNA and histone methylation. Curr. Biol. 17, 379–384 (2007).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  125. 125.

    Du, J. et al. Mechanism of DNA methylation-directed histone methylation by KRYPTONITE. Mol. Cell 55, 495–504 (2014).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  126. 126.

    Li, X. et al. Mechanistic insights into plant SUVH family H3K9 methyltransferases and their binding to context-biased non-CG DNA methylation. Proc. Natl Acad. Sci. USA 115, E8793–E8802 (2018).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  127. 127.

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

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  128. 128.

    Li, Q. et al. Genetic perturbation of the maize methylome. Plant Cell 26, 4602–4616 (2014).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  129. 129.

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

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  130. 130.

    Swiezewski, S., Liu, F., Magusin, A. & Dean, C. Cold-induced silencing by long antisense transcripts of an Arabidopsis Polycomb target. Nature 462, 799–802 (2009).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  131. 131.

    Rosa, S., Duncan, S. & Dean, C. Mutually exclusive sense–antisense transcription at FLC facilitates environmentally induced gene repression. Nat. Commun. 7, 13031 (2016).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  132. 132.

    Fang, X. et al. The 3′ processing of antisense RNAs physically links to chromatin-based transcriptional control. Proc. Natl Acad. Sci. USA 117, 5316–15321 (2020). This work highlights the importance of interactions between 3′ end RNA processing and chromatin modifications in the creation of a stable epigenetic state.

    Google Scholar 

  133. 133.

    Yang, H., Howard, M. & Dean, C. Antagonistic roles for H3K36me3 and H3K27me3 in the cold-induced epigenetic switch at Arabidopsis FLC. Curr. Biol. 24, 1793–1797 (2014).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  134. 134.

    Angel, A., Song, J., Dean, C. & Howard, M. A Polycomb-based switch underlying quantitative epigenetic memory. Nature 476, 105–108 (2011).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  135. 135.

    Finnegan, E. J. & Dennis, E. S. Vernalization-induced trimethylation of histone H3 lysine 27 at FLC is not maintained in mitotically quiescent cells. Curr. Biol. 17, 1978–1983 (2007).

    CAS  PubMed  Article  Google Scholar 

  136. 136.

    Yang, H. et al. Distinct phases of Polycomb silencing to hold epigenetic memory of cold in Arabidopsis. Science 357, 1142–1145 (2017).

    CAS  PubMed  Article  Google Scholar 

  137. 137.

    Jiang, D. & Berger, F. DNA replication-coupled histone modification maintains Polycomb gene silencing in plants. Science 357, 1146–1149 (2017). This work reveals the mechanism of inheritance of PcG repression of genes with H3K27me3 marks in plants via the histone variant H3.1, demonstrating how this mark is epigenetic.

    CAS  PubMed  Article  Google Scholar 

  138. 138.

    Escobar, T. M., Loyola, A. & Reinberg, D. Parental nucleosome segregation and the inheritance of cellular identity. Nat. Rev. Genet. 22, 379–392 (2021).

    CAS  PubMed  Article  Google Scholar 

  139. 139.

    Annunziato, A. T. Assembling chromatin: the long and winding road. Biochim. Biophys. Acta 1819, 196–210 (2013).

    PubMed  Article  CAS  Google Scholar 

  140. 140.

    Loyola, A. et al. The HP1α–CAF1–SetDB1-containing complex provides H3K9me1 for Suv39-mediated K9me3 in pericentric heterochromatin. EMBO Rep. 10, 769–775 (2009).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  141. 141.

    Rowbotham, S. P. et al. Maintenance of silent chromatin through replication requires SWI/SNF-like chromatin remodeler SMARCAD1. Mol. Cell 42, 285–296 (2011).

    CAS  PubMed  Article  Google Scholar 

  142. 142.

    Jang, S. M. et al. KAP1 facilitates reinstatement of heterochromatin after DNA replication. Nucleic Acids Res. 46, 8788–8802 (2018).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  143. 143.

    Benoit, M. et al. Replication-coupled histone H3.1 deposition determines nucleosome composition and heterochromatin dynamics during Arabidopsis seedling development. N. Phytol. 221, 385–398 (2019).

    CAS  Article  Google Scholar 

  144. 144.

    Borg, M. et al. Targeted reprogramming of H3K27me3 resets epigenetic memory in plant paternal chromatin. Nat. Cell Biol. 22, 621–629 (2020).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

Download references

Acknowledgements

The authors thank B. Kidd and A. de Mendoza for critical feedback on this manuscript, and M. Oliva and D. Lam for insightful discussions.

Author information

Affiliations

Authors

Contributions

The authors contributed equally to all aspects of the article.

Corresponding author

Correspondence to Ryan Lister.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Peer review information

Nature Reviews Genetics thanks S. Jacobsen, 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.

Glossary

Memory

A recording of past events or actions that is ‘stored’ at the epigenetic level.

Epimutation

The process of generating a heritable phenotypic change without change in the genome sequence, which creates an epiallele.

DNA methylation

Covalent addition of a methyl group to the fifth carbon of cytosine bases in DNA.

Histone post-translational modifications

(Histone PTMs). Covalent modification of the tails of histone proteins, around which DNA is wrapped, that can affect gene expression and DNA accessibility.

Transposable elements

Selfish genetic elements that can expand in copy number within a genome, often at a fitness cost to the host.

Epialleles

Heritable phenotypic changes that are not the result of a change in the genome sequence, often encoded by stable changes in DNA methylation or histone post-translational modifications (PTMs).

Epigenome

The map of epigenetic marks decorating the genome, which can be informative about how epigenetic information can produce a particular phenotype.

RNA-directed DNA methylation

(RdDM). A molecular pathway in plants, in which small RNAs target de novo DNA methylation and silence the locus.

Transdifferentiation

The process of a differentiated cell adopting the cell type identity of another cell type without going through a dedifferentiation process.

Biotic

A term to denote a living factor that can influence plant growth, such as a bacterial pathogen.

Abiotic

A term to denote a non-living factor that can have an impact on plant growth, such as salt or heat.

Epigenetic recombinant inbred lines

(epiRILs). Plants derived from a cross of genetically identical plants, except for one parent harbouring a mutation that disrupts a certain epigenetic mark. Over subsequent generations, the lines become homozygous for the normal or disrupted epigenetic states at particular genomic regions, with each line harbouring normal or altered modification states at different regions in the genome.

Epigenome-wide association study

A study design that aims to link the presence or absence of an epigenetic mark, such as DNA methylation, at different genomic positions, with a phenotypic trait.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Lloyd, J.P.B., Lister, R. Epigenome plasticity in plants. Nat Rev Genet (2021). https://doi.org/10.1038/s41576-021-00407-y

Download citation

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