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.

  • Review Article
  • Published:

RNA-directed DNA methylation: an epigenetic pathway of increasing complexity

A Corrigendum to this article was published on 18 July 2014

This article has been updated

Key Points

  • RNA-directed DNA methylation (RdDM) is prevalent in flowering plants and induces transcriptional silencing at repetitive DNA, including all types of transposons.

  • During RdDM, RNA polymerase IV (Pol IV) initiates production of 24-nucleotide small interfering RNAs (siRNAs) that direct transcriptionally repressive DNA methylation to homologous Pol V-transcribed loci. Pol IV and Pol V are recruited to genomic regions that contain transcriptionally repressive epigenetic marks, thereby reinforcing and maintaining the silent state.

  • Recent research has uncovered variations on the canonical RdDM pathway, including the involvement of RNA-DEPENDENT RNA POLYMERASE 6 (RDR6) and NEEDED FOR RDR2-INDEPENDENT DNA METHYLATION (NERD), which might allow 'young' (that is, recently acquired) transposons to come under the control of RdDM.

  • In additional to transposon control, RdDM might help hosts to respond to biotic or abiotic challenges, or to faithfully transmit DNA methylation patterns to their offspring. RdDM might also affect germ cell specification and parent-specific gene expression.

  • There is increasing evidence that siRNAs are used to communicate epigenetic states between homologous sequences within a nucleus or indeed between nuclei.

Abstract

RNA-directed DNA methylation (RdDM) is the major small RNA-mediated epigenetic pathway in plants. RdDM requires a specialized transcriptional machinery that comprises two plant-specific RNA polymerases — Pol IV and Pol V — and a growing number of accessory proteins, the functions of which in the RdDM mechanism are only partially understood. Recent work has revealed variations in the canonical RdDM pathway and identified factors that recruit Pol IV and Pol V to specific target sequences. RdDM, which transcriptionally represses a subset of transposons and genes, is implicated in pathogen defence, stress responses and reproduction, as well as in interallelic and intercellular communication.

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

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

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

Figure 1: Canonical RdDM pathway.
Figure 2: Non-canonical Pol II–RDR6-dependent RdDM pathway.
Figure 3: Release of RdDM during stress.
Figure 4: Biological processes involving siRNAs and RdDM components.

Similar content being viewed by others

Change history

  • 18 July 2014

    In this article, on page 394 and in the footnote of Table 1 (page 397) the sequence contexts of DNA methylation were incorrectly defined. For CHG and CHH sequences, H represents A, C or T (not A, T or G as originally written). The article has been corrected online. The authors and editors apologize for these errors.

References

  1. Castel, S. E. & Martienssen, R. A. RNA interference in the nucleus: roles for small RNAs in transcription, epigenetics and beyond. Nature Rev. Genet. 14, 100–112 (2013).

    Article  CAS  PubMed  Google Scholar 

  2. Luteijn, M. J. & Ketting, R. F. PIWI-interacting RNAs: from generation to transgenerational epigenetics. Nature Rev. Genet. 14, 523–534 (2013).

    Article  CAS  PubMed  Google Scholar 

  3. Jones, A. L., Thomas, C. L. & Maule, A. J. De novo methylation and co-suppression induced by a cytoplasmically replicating plant RNA virus. EMBO J. 17, 6385–6393 (1998).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Wassenegger, M., Heimes, S., Riedel, L. & Sanger, H. L. RNA-directed de novo methylation of genomic sequences in plants. Cell 76, 567–576 (1994).

    Article  CAS  PubMed  Google Scholar 

  5. Eun, C. et al. Use of forward genetic screens to identify genes required for RNA-directed DNA methylation in Arabidopsis thaliana. Cold Spring Harb. Symp. Quant. Biol. 77, 195–204 (2012).

    Article  CAS  PubMed  Google Scholar 

  6. Mette, M. F., Aufsatz, W., van der Winden, J., Matzke, M. A. & Matzke, A. J. M. Transcriptional silencing and promoter methylation triggered by double-stranded RNA. EMBO J. 19, 5194–5201 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Chan, S. W. et al. RNA silencing genes control de novo DNA methylation. Science 303, 1336 (2004).

    Article  CAS  PubMed  Google Scholar 

  8. Haag, J. R. & Pikaard, C. S. Multisubunit RNA polymerases IV and V: purveyors of non-coding RNA for plant gene silencing. Nature Rev. Mol. Cell Biol. 12, 483–492 (2011).

    Article  CAS  Google Scholar 

  9. Yamanaka, S. et al. RNAi triggered by specialized machinery silences developmental genes and retrotransposons. Nature 493, 557–560 (2013).

    Article  CAS  PubMed  Google Scholar 

  10. 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). This methylome analysis of 86 A. thaliana gene silencing mutants provides a resource for epigenetics researchers.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Mosher, R. A., Schwach, F., Studholme, D. & Baulcombe, D. C. PolIVb influences RNA-directed DNA-methylation independently of its role in siRNA biogenesis. Proc. Natl Acad. Sci. USA 105, 3145–3150 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Zhang, X., Henderson, I. R., Lu, C., Green, P. J. & Jacobsen, S. E. Role of RNA polymerase IV in plant small RNA metabolism. Proc. Natl Acad. Sci. USA 104, 4536–4541 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Law, J. A. et al. Polymerase IV occupancy at RNA-directed DNA methylation sites requires SHH1. Nature 498, 385–389 (2013). Using ChIP–seq, this study identifies 928 high-confidence Pol IV peaks. The Pol IV-interacting protein SHH1 is shown to interact with H3K9me and recruit Pol IV to chromatin at 44% of Pol IV target sites.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. 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  PubMed Central  Google Scholar 

  16. 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 

  17. Law, J. A., Vashisht, A. A., Wohlschlegel, J. A. & Jacobsen, S. E. SHH1, a homeodomain protein required for DNA methylation, as well as RDR2, RDM4, and chromatin remodeling factors, associate with RNA polymerase IV. PLoS Genet. 7, e1002195 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Smith, L. M. et al. An SNF2 protein associated with nuclear RNA silencing and the spread of a silencing signal between cells in Arabidopsis. Plant Cell 19, 1507–1521 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Ji, L. J. & Chen, X. M. Regulation of small RNA stability: methylation and beyond. Cell Res. 22, 624–636 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Eun, C. et al. AGO6 functions in RNA-mediated transcriptional gene silencing in shoot and root meristems in Arabidopsis thaliana. PLoS ONE 6, e25730 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Havecker, E. R. et al. The Arabidopsis RNA- directed DNA methylation Argonautes functionally diverge based on their expression and interaction with target loci. Plant Cell 22, 321–334 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Olmedo-Monfil, V. et al. Control of female gamete formation by a small RNA pathway in Arabidopsis. Nature 464, 628–632 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Wierzbicki, A. T., Haag, J. R. & Pikaard, C. S. Noncoding transcription by RNA polymerase Pol IVb/Pol V mediates transcriptional silencing of overlapping and adjacent genes. Cell 135, 635–648 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Zhong, X. et al. DDR complex facilitates global association of RNA polymerase V to promoters and evolutionarily young transposons. Nature Struct. Mol. Biol. 19, 870–875 (2012).

    Article  CAS  Google Scholar 

  25. Wierzbicki, A. T. et al. Spatial and functional relationships among Pol V-associated loci, Pol IV-dependent siRNAs, and cytosine methylation in the Arabidopsis epigenome. Genes Dev. 26, 1825–1836 (2012). Using ChIP–seq, this study identifies 1,157 high-confidence Pol V peaks that are distributed throughout the genome. Most of these peaks are associated with 24-nucleotide siRNAs and CHH methylation, but a consensus sequence for Pol V binding could not be discerned.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Lee, T. F. et al. RNA polymerase V-dependent small RNAs in Arabidopsis originate from small, intergenic loci including most SINE repeats. Epigenetics 7, 781–795 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Zemach, A. et al. The Arabidopsis nucleosome remodeler DDM1 allows DNA methyltransferases to access H1-containing heterochromatin. Cell 153, 193–205 (2013). This paper shows that most transposons in A. thaliana are silenced by DDM1 and RdDM pathways that act preferentially in highly heterochromatic and more euchromatic regions, respectively. CMT2 is identified as a CHH methyltransferase that functions independently of siRNAs in heterochromatin.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Zheng, Q. et al. RNA polymerase V targets transcriptional silencing components to promoters of protein-coding genes. Plant J. 73, 179–189 (2013).

    Article  CAS  PubMed  Google Scholar 

  29. Schoft, V. K. et al. Induction of RNA-directed DNA methylation upon decondensation of constitutive heterochromatin. EMBO Rep. 10, 1015–1021 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  32. Kuhlmann, M. & Mette, M. F. Developmentally non-redundant SET domain proteins SUVH2 and SUVH9 are required for transcriptional gene silencing in Arabidopsis thaliana. Plant Mol. Biol. 79, 623–633 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Johnson, L. M. et al. SRA- and SET-domain-containing proteins link RNA polymerase V occupancy to DNA methylation. Nature 507, 124–128 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Liu, Z. W. et al. The SET domain proteins SUVH2 and SUVH9 are required for Pol V occupancy at RNA-directed DNA methylation loci. PLoS Genet. 10, e1003948 (2014). References 33 and 34 show that Pol V is recruited to methylated DNA at some loci by methyl DNA-binding proteins SUVH2 and SUVH9.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  35. Law, J. A. et al. A protein complex required for polymerase V transcripts and RNA-directed DNA methylation in Arabidopsis. Curr. Biol. 20, 951–956 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Wierzbicki, A. T., Ream, T. S., Haag, J. R. & Pikaard, C. S. RNA polymerase V transcription guides ARGONAUTE4 to chromatin. Nature Genet. 41, 630–634 (2009).

    Article  CAS  PubMed  Google Scholar 

  37. Gao, Z. H. 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 

  38. Huang, L. F. et al. An atypical RNA polymerase involved in RNA silencing shares small subunits with RNA polymerase II. Nature Struct. Mol. Biol. 16, 91–93 (2009).

    Article  CAS  Google Scholar 

  39. Bies-Etheve, N. et al. RNA-directed DNA methylation requires an AGO4-interacting member of the SPT5 elongation factor family. EMBO Rep. 10, 649–654 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. 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 

  41. Ausin, I. et al. INVOLVED IN DE NOVO 2-containing complex involved in RNA-directed DNA methylation in Arabidopsis. Proc. Natl Acad. Sci. USA 109, 8374–8381 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Lorkovic, Z. J., Naumann, U., Matzke, A. J. & Matzke, M. Involvement of a GHKL ATPase in RNA-directed DNA methylation in Arabidopsis thaliana. Curr. Biol. 22, 933–938 (2012).

    Article  CAS  PubMed  Google Scholar 

  43. Zhang, C. J. et al. IDN2 and its paralogs form a complex required for RNA-directed DNA methylation. PLoS Genet. 8, e1002693 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Xie, M., Ren, G., Costa-Nunes, P., Pontes, O. & Yu, B. A subgroup of SGS3-like proteins act redundantly in RNA-directed DNA methylation. Nucleic Acids Res. 40, 4422–4431 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Finke, A., Kuhlmann, M. & Mette, M. F. IDN2 has a role downstream of siRNA formation in RNA-directed DNA methylation. Epigenetics 7, 950–960 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Zhu, Y., Rowley, M. J., Bohmdorfer, G. & Wierzbicki, A. T. A. SWI/SNF chromatin-remodeling complex acts in noncoding RNA-mediated transcriptional silencing. Mol. Cell 49, 298–309 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. 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  PubMed Central  CAS  Google Scholar 

  48. Enke, R. A., Dong, Z. & Bender, J. Small RNAs prevent transcription-coupled loss of histone H3 lysine 9 methylation in Arabidopsis thaliana. PLoS Genet. 7, e1002350 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Liu, X. et al. HDA6 directly interacts with DNA methyltransferase MET1 and maintains transposable element silencing in Arabidopsis. Plant Physiol. 158, 119–129 (2012).

    Article  CAS  PubMed  Google Scholar 

  50. To, T. K. et al. Arabidopsis HDA6 regulates locus-directed heterochromatin silencing in cooperation with MET1. PLoS Genet. 7, e1002055 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. 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 

  52. 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 

  53. 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  PubMed Central  CAS  Google Scholar 

  54. Sridhar, V. V. et al. Control of DNA methylation and heterochromatic silencing by histone H2B deubiquitination. Nature 447, 735–738 (2007).

    Article  CAS  PubMed  Google Scholar 

  55. Brabbs, T. R. et al. The stochastic silencing phenotype of Arabidopsis morc6 mutants reveals a role in efficient RNA-directed DNA methylation. Plant J. 75, 836–846 (2013).

    Article  CAS  PubMed  Google Scholar 

  56. Moissiard, G. et al. MORC family ATPases required for heterochromatin condensation and gene silencing. Science 336, 1448–1451 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  58. 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 

  59. Jones, L., Ratcliff, F. & Baulcombe, D. C. RNA-directed transcriptional gene silencing in plants can be inherited independently of the RNA trigger and requires Met1 for maintenance. Curr. Biol. 11, 747–757 (2001).

    Article  CAS  PubMed  Google Scholar 

  60. 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 

  61. Law, J. A. & Jacobsen, S. E. Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nature Rev. Genet. 11, 204–220 (2010).

    Article  CAS  PubMed  Google Scholar 

  62. Huettel, B. et al. Endogenous targets of RNA-directed DNA methylation and Pol IV in Arabidopsis. EMBO J. 25, 2828–2836 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Zhang, H. & Zhu, J. K. Active DNA demethylation in plants and animals. Cold Spring Harb. Symp. Quant. Biol. 77, 161–173 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Li, X. et al. Antisilencing role of the RNA-directed DNA methylation pathway and a histone acetyltransferase in Arabidopsis. Proc. Natl Acad. Sci. USA 109, 11425–11430 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Wu, L. et al. DNA methylation mediated by a microRNA pathway. Mol. Cell 38, 465–475 (2010).

    Article  CAS  PubMed  Google Scholar 

  66. Khraiwesh, B. et al. Transcriptional control of gene expression by microRNAs. Cell 140, 111–122 (2010).

    Article  CAS  PubMed  Google Scholar 

  67. Wu, L., Mao, L. & Qi, Y. Roles of Dicer-like and Argonaute proteins in TAS-derived small interfering RNA-triggered DNA methylation. Plant Physiol. 160, 990–999 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Nuthikattu, S. et al. The initiation of epigenetic silencing of active transposable elements is triggered by RDR6 and 21–22 nucleotide small interfering RNAs. Plant Physiol. 162, 116–131 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Mari-Ordonez, A. et al. Reconstructing de novo silencing of an active plant retrotransposon. Nature Genet. 45, 1029–1039 (2013). This study follows a newly activated retrotransposon through many generations. Initially silenced through PTGS, saturation of DCL2 and DCL4 activity leads to 24-nucleotide siRNA production by DCL3 and initiates canonical RdDM.

    Article  CAS  PubMed  Google Scholar 

  70. Pontier, D. et al. NERD, a plant-specific GW protein, defines an additional RNAi-dependent chromatin-based pathway in Arabidopsis. Mol. Cell 48, 121–132 (2012). This paper identifies NERD as an AGO hook protein and, together with reference 68, defines more fully the non-canonical RDR6-dependent RdDM pathway that is independent of Pol IV and that relies instead on Pol II.

    Article  CAS  PubMed  Google Scholar 

  71. 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 

  72. You, W., Lorkovic, Z. J., Matzke, A. J. & Matzke, M. Interplay among RNA polymerases II, IV and V in RNA-directed DNA methylation at a low copy transgene locus in Arabidopsis thaliana. Plant Mol. Biol. 82, 85–96 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Perez-Hormaeche, J. et al. Invasion of the Arabidopsis genome by the tobacco retrotransposon Tnt1 is controlled by reversible transcriptional gene silencing. Plant Physiol. 147, 1264–1278 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Ito, H. et al. An siRNA pathway prevents transgenerational retrotransposition in plants subjected to stress. Nature 472, 115–119 (2011). This study shows that heat stress triggers transcription of the ONSEN retrotransposon, but such transposition is only possible in some RdDM mutant backgrounds. Insertion of ONSEN near genes can confer heat-responsive transcription.

    Article  CAS  PubMed  Google Scholar 

  75. Ruiz-Ferrer, V. & Voinnet, O. Roles of plant small RNAs in biotic stress responses. Annu. Rev. Plant Biol. 60, 485–510 (2009).

    Article  CAS  PubMed  Google Scholar 

  76. Buchmann, R. C., Asad, S., Wolf, J. N., Mohannath, G. & Bisaro, D. M. Geminivirus AL2 and L2 proteins suppress transcriptional gene silencing and cause genome-wide reductions in cytosine methylation. J. Virol. 83, 5005–5013 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Yang, L. P. et al. C2-mediated decrease in DNA methylation, accumulation of siRNAs, and increase in expression for genes involved in defense pathways in plants infected with beet severe curly top virus. Plant J. 73, 910–917 (2013).

    Article  CAS  PubMed  Google Scholar 

  78. Zhang, Z. et al. BSCTV C2 attenuates the degradation of SAMDC1 to suppress DNA methylation-mediated gene silencing in Arabidopsis. Plant Cell 23, 273–288 (2011).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  79. Romanel, E. et al. Global alteration of microRNAs and transposon-derived small RNAs in cotton (Gossypium hirsutum) during Cotton leafroll dwarf polerovirus (CLRDV) infection. Plant Mol. Biol. 80, 443–460 (2012).

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Dowen, R. H. et al. Widespread dynamic DNA methylation in response to biotic stress. Proc. Natl Acad. Sci. USA 109, E2183–E2191 (2012). This genome-wide analysis of DNA methylation during pathogen infection reveals transposon- associated demethylation that affects expression of neighbouring genes.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Gohlke, J. et al. DNA methylation mediated control of gene expression is critical for development of crown gall tumors. PLoS Genet. 9, e1003267 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Ou, X. et al. Transgenerational inheritance of modified DNA methylation patterns and enhanced tolerance induced by heavy metal stress in rice (Oryza sativa L.). PLoS ONE 7, e41143 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Tricker, P. J., Gibbings, J. G., Rodriguez Lopez, C. M., Hadley, P. & Wilkinson, M. J. Low relative humidity triggers RNA-directed de novo DNA methylation and suppression of genes controlling stomatal development. J. Exp. Bot. 63, 3799–3813 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Popova, O. V., Dinh, H. Q., Aufsatz, W. & Jonak, C. The RdDM pathway is required for basal heat tolerance in Arabidopsis. Mol. Plant 6, 396–410 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Yao, Y., Bilichak, A., Golubov, A., Blevins, T. & Kovalchuk, I. Differential sensitivity of Arabidopsis siRNA biogenesis mutants to genotoxic stress. Plant Cell Rep. 29, 1401–1410 (2010).

    Article  CAS  PubMed  Google Scholar 

  89. Verhoeven, K. J., Jansen, J. J., van Dijk, P. J. & Biere, A. Stress-induced DNA methylation changes and their heritability in asexual dandelions. New Phytol. 185, 1108–1118 (2010).

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  92. Suter, L. & Widmer, A. Environmental heat and salt stress induce transgenerational phenotypic changes in Arabidopsis thaliana. PLoS ONE 8, e60364 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Luna, E. & Ton, J. The epigenetic machinery controlling transgenerational systemic acquired resistance. Plant Signal. Behav. 7, 615–618 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Calarco, J. P. et al. Reprogramming of DNA methylation in pollen guides epigenetic inheritance via small RNA. Cell 151, 194–205 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  96. Singh, M. et al. Production of viable gametes without meiosis in maize deficient for an ARGONAUTE protein. Plant Cell 23, 443–458 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  97. Garcia-Aguilar, M., Michaud, C., Leblanc, O. & Grimanelli, D. Inactivation of a DNA methylation pathway in maize reproductive organs results in apomixis-like phenotypes. Plant Cell 22, 3249–3267 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  98. Garnier, O., Laoueille-Duprat, S. & Spillane, C. Genomic imprinting in plants. Epigenetics 3, 14–20 (2008).

    Article  PubMed  Google Scholar 

  99. Gehring, M., Bubb, K. L. & Henikoff, S. Extensive demethylation of repetitive elements during seed development underlies gene imprinting. Science 324, 1447–1451 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  100. Mosher, R. A. et al. Uniparental expression of PolIV-dependent siRNAs in developing endosperm of Arabidopsis. Nature 460, 283–286 (2009).

    Article  CAS  PubMed  Google Scholar 

  101. Rodrigues, J. A. et al. Imprinted expression of genes and small RNA is associated with localized hypomethylation of the maternal genome in rice endosperm. Proc. Natl Acad. Sci. USA 110, 7934–7939 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. Hsieh, T. F. et al. Genome-wide demethylation of Arabidopsis endosperm. Science 324, 1451–1454 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  103. Ibarra, C. A. et al. Active DNA demethylation in plant companion cells reinforces transposon methylation in gametes. Science 337, 1360–1364 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  104. Mosher, R. A. & Melnyk, C. W. siRNAs and DNA methylation: seedy epigenetics. Trends Plant Sci. 15, 204–210 (2010).

    Article  CAS  PubMed  Google Scholar 

  105. Mosher, R. A. et al. An atypical epigenetic mechanism affects uniparental expression of Pol IV-dependent siRNAs. PLoS ONE 6, e25756 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  106. Vu, T. M. et al. RNA-directed DNA methylation regulates parental genomic imprinting at several loci in Arabidopsis. Development 140, 2953–2960 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  107. Mosher, R. A. Maternal control of Pol IV-dependent siRNAs in Arabidopsis endosperm. New Phytol. 186, 358–364 (2010).

    Article  CAS  PubMed  Google Scholar 

  108. Erhard, K. F. Jr & Hollick, J. B. Paramutation: a process for acquiring trans-generational regulatory states. Curr. Opin. Plant Biol. 14, 210–216 (2011).

    Article  CAS  PubMed  Google Scholar 

  109. Arteaga-Vazquez, M. et al. RNA-mediated trans-communication can establish paramutation at the b1 locus in maize. Proc. Natl Acad. Sci. USA 107, 12986–12991 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  110. Slotkin, R. K. et al. Epigenetic reprogramming and small RNA silencing of transposable elements in pollen. Cell 136, 461–472 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  111. Dunoyer, P. et al. An endogenous, systemic RNAi pathway in plants. EMBO J. 29, 1699–1712 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  112. Molnar, A. et al. Small silencing RNAs in plants are mobile and direct epigenetic modification in recipient cells. Science 328, 872–875 (2010).

    Article  CAS  PubMed  Google Scholar 

  113. Melnyk, C. W., Molnar, A., Bassett, A. & Baulcombe, D. C. Mobile 24 nt small RNAs direct transcriptional gene silencing in the root meristems of Arabidopsis thaliana. Curr. Biol. 21, 1678–1683 (2011).

    Article  CAS  PubMed  Google Scholar 

  114. Groszmann, M. et al. Changes in 24-nt siRNA levels in Arabidopsis hybrids suggest an epigenetic contribution to hybrid vigor. Proc. Natl Acad. Sci. USA 108, 2617–2622 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  115. Li, Y., Varala, K., Moose, S. P. & Hudson, M. E. The inheritance pattern of 24 nt siRNA clusters in Arabidopsis hybrids is influenced by proximity to transposable elements. PLoS ONE 7, e47043 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  116. He, G. et al. Global epigenetic and transcriptional trends among two rice subspecies and their reciprocal hybrids. Plant Cell 22, 17–33 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  117. Barber, W. T. et al. Repeat associated small RNAs vary among parents and following hybridization in maize. Proc. Natl Acad. Sci. USA 109, 10444–10449 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  118. Greaves, I. K. et al. Trans chromosomal methylation in Arabidopsis hybrids. Proc. Natl Acad. Sci. USA 109, 3570–3575 (2012). This paper analyses DNA methylation in Arabidopsis intraspecific hybrids and reveals interactions between chromosomes that result in non-additive methylation. This methylation can alter gene expression and potentially contributes to heterosis.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  119. Shen, H. et al. Genome-wide analysis of DNA methylation and gene expression changes in two Arabidopsis ecotypes and their reciprocal hybrids. Plant Cell 24, 875–892 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  120. Chodavarapu, R. K. et al. Transcriptome and methylome interactions in rice hybrids. Proc. Natl Acad. Sci. USA 109, 12040–12045 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  121. Ha, M. et al. Small RNAs serve as a genetic buffer against genomic shock in Arabidopsis interspecific hybrids and allopolyploids. Proc. Natl Acad. Sci. USA 106, 17835–17840 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  122. Kenan-Eichler, M. et al. Wheat hybridization and polyploidization results in deregulation of small RNAs. Genetics 188, 263–272 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  123. Josefsson, C., Dilkes, B. & Comai, L. Parent-dependent loss of gene silencing during interspecies hybridization. Curr. Biol. 16, 1322–1328 (2006).

    Article  CAS  PubMed  Google Scholar 

  124. Kashkush, K., Feldman, M. & Levy, A. A. Transcriptional activation of retrotransposons alters the expression of adjacent genes in wheat. Nature Genet. 33, 102–106 (2003).

    Article  CAS  PubMed  Google Scholar 

  125. Shivaprasad, P. V., Dunn, R. M., Santos, B. A., Bassett, A. & Baulcombe, D. C. Extraordinary transgressive phenotypes of hybrid tomato are influenced by epigenetics and small silencing RNAs. EMBO J. 31, 257–266 (2012).

    Article  CAS  PubMed  Google Scholar 

  126. Henderson, I. R. et al. Dissecting Arabidopsis thaliana DICER function in small RNA processing, gene silencing and DNA methylation patterning. Nature Genet. 38, 721–725 (2006).

    Article  CAS  PubMed  Google Scholar 

  127. Kozieradzka-Kiszkurno, M. & Plachno, B. J. Are there symplastic connections between the endosperm and embryo in some angiosperms?—a lesson from the Crassulaceae family. Protoplasma 249, 1081–1089 (2012).

    Article  CAS  PubMed  Google Scholar 

  128. Huang, Y., Kendall, T. & Mosher, R. Pol IV-Dependent siRNA production is reduced in Brassica rapa. Biology 2, 1210–1223 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  129. Tucker, S. L., Reece, J., Ream, T. S. & Pikaard, C. S. Evolutionary history of plant multisubunit RNA polymerases IV and V: subunit origins via genome-wide and segmental gene duplications, retrotransposition, and lineage-specific subfunctionalization. Cold Spring Harb. Symp. Quant. Biol. 75, 285–297 (2010). This bioinformatic analysis of transcriptomes across the plant kingdom reveals stepwise evolution of Pol IV- and Pol V-specific subunits.

    Article  CAS  PubMed  Google Scholar 

  130. Ream, T. S. et al. Subunit compositions of the RNA-silencing enzymes Pol IV and Pol V reveal their origins as specialized forms of RNA polymerase II. Mol. Cell 33, 192–203 (2009).

    Article  CAS  PubMed  Google Scholar 

  131. Landick, R. Functional divergence in the growing family of RNA polymerases. Structure 17, 323–325 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  132. Bellaoui, M. & Gruissem, W. Altered expression of the Arabidopsis ortholog of DCL affects normal plant development. Planta 219, 819–826 (2004).

    Article  CAS  PubMed  Google Scholar 

  133. Li, C. F. et al. An ARGONAUTE4-containing nuclear processing center colocalized with Cajal bodies in Arabidopsis thaliana. Cell 126, 93–106 (2006).

    Article  CAS  PubMed  Google Scholar 

  134. Tan, E. H., Blevins, T., Ream, T. S. & Pikaard, C. S. Functional consequences of subunit diversity in RNA polymerases II and V. Cell Rep. 1, 208–214 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  135. Lahmy, S. et al. PolV(PolIVb) function in RNA-directed DNA methylation requires the conserved active site and an additional plant-specific subunit. Proc. Natl Acad. Sci. USA 106, 941–946 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  136. Czeko, E., Seizl, M., Augsberger, C., Mielke, T. & Cramer, P. Iwr1 directs RNA polymerase II nuclear import. Mol. Cell 42, 261–266 (2011).

    Article  CAS  PubMed  Google Scholar 

  137. He, X. J. et al. A conserved transcriptional regulator is required for RNA-directed DNA methylation and plant development. Genes Dev. 23, 2717–2722 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  138. Kanno, T. et al. RNA-directed DNA methylation and plant development require an IWR1-type transcription factor. EMBO Rep. 11, 65–71 (2010).

    Article  CAS  PubMed  Google Scholar 

  139. Luo, J. & Hall, B. D. A multistep process gave rise to RNA polymerase IV of land plants. J. Mol. Evol. 64, 101–112 (2007).

    Article  CAS  PubMed  Google Scholar 

  140. Dolgosheina, E. V. et al. Conifers have a unique small RNA silencing signature. RNA 14, 1508–1515 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  141. Morin, R. D. et al. Comparative analysis of the small RNA transcriptomes of Pinus contorta and Oryza sativa. Genome Res. 18, 571–584 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  142. Nystedt, B. et al. The Norway spruce genome sequence and conifer genome evolution. Nature 497, 579–584 (2013).

    Article  CAS  PubMed  Google Scholar 

  143. Zhang, J. et al. Dynamic expression of small RNA populations in larch (Larix leptolepis). Planta 237, 89–101 (2013).

    Article  CAS  PubMed  Google Scholar 

  144. Wan, L. C. et al. Identification and characterization of small non-coding RNAs from Chinese fir by high throughput sequencing. BMC Plant Biol. 12, 146 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  145. Molnar, A., Schwach, F., Studholme, D. J., Thuenemann, E. C. & Baulcombe, D. C. miRNAs control gene expression in the single-cell alga Chlamydomonas reinhardtii. Nature 447, 1126–U1115 (2007).

    Article  CAS  PubMed  Google Scholar 

  146. Axtell, M. J., Snyder, J. A. & Bartel, D. P. Common functions for diverse small RNAs of land plants. Plant Cell 19, 1750–1769 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  147. Cho, S. H. et al. Physcomitrella patens DCL3 is required for 22–24 nt siRNA accumulation, suppression of retrotransposon-derived transcripts, and normal development. PLoS Genet. 4, e1000314 (2008).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  148. Pikaard, C. S., Haag, J. R., Pontes, O. M., Blevins, T. & Cocklin, R. A transcription fork model for Pol IV and Pol V-dependent RNA-directed DNA methylation. Cold Spring Harb. Symp. Quant. Biol. 77, 205–212 (2012).

    Article  CAS  PubMed  Google Scholar 

  149. Panda, K. & Slotkin, R. K. Proposed mechanism for the initiation of transposable element silencing by the RDR6-directed DNA methylation pathway. Plant Signal. Behav. 8, e25206 (2013).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  150. Herr, A. J., Jensen, M. B., Dalmay, T. & Baulcombe, D. RNA polymerase IV directs silencing of endogenous DNA. Science 308, 118–120 (2005).

    Article  CAS  PubMed  Google Scholar 

  151. 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 

  152. 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 

  153. Kanno, T. et al. Atypical RNA polymerase subunits required for RNA-directed DNA methylation. Nature Genet. 37, 761–765 (2005).

    Article  CAS  PubMed  Google Scholar 

  154. He, X. J. et al. NRPD4, a protein related to the RPB4 subunit of RNA polymerase II, is a component of RNA polymerases IV and V and is required for RNA-directed DNA methylation. Genes Dev. 23, 318–330 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  155. Daxinger, L. et al. A stepwise pathway for biogenesis of 24-nt secondary siRNAs and spreading of DNA methylation. EMBO J. 28, 48–57 (2009).

    Article  CAS  PubMed  Google Scholar 

  156. Greenberg, M. V. et al. Identification of genes required for de novo DNA methylation in Arabidopsis. Epigenetics 6, 344–354 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  157. Kanno, T. et al. Involvement of putative SNF2 chromatin remodeling protein DRD1 in RNA-directed DNA methylation. Curr. Biol. 14, 801–805 (2004).

    Article  CAS  PubMed  Google Scholar 

  158. Ausin, I., Mockler, T. C., Chory, J. & Jacobsen, S. E. IDN1 and IDN2 are required for de novo DNA methylation in Arabidopsis thaliana. Nature Struct. Mol. Biol. 16, 1325–1327 (2009).

    Article  CAS  Google Scholar 

  159. Kanno, T. et al. A structural-maintenance-of-chromosomes hinge domain-containing protein is required for RNA-directed DNA methylation. Nature Genet. 40, 670–675 (2008).

    Article  CAS  PubMed  Google Scholar 

  160. Naumann, U. et al. Genetic evidence that DNA methyltransferase DRM2 has a direct catalytic role in RNA-directed DNA methylation in Arabidopsis thaliana. Genetics 187, 977–979 (2011).

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

M.A.M. thanks Academia Sinica for financial support and C. Ying for editorial assistance. R.A.M. is supported by the US National Science Foundation under grant MCB-1243608. The authors apologize to colleagues whose publications are not cited owing to space limitations.

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Marjori A. Matzke or Rebecca A. Mosher.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Related links

PowerPoint slides

Glossary

Dicer

(DCR). A ribonuclease III enzyme that cleaves double-stranded RNA precursors into small RNAs of 20–30 nucleotides. In plants, homologues of Dicer are referred to as DICER-LIKE (DCL). Of the four DCL enzymes in Arabidopsis thaliana, DCL3 produces 24-nucleotide small interfering RNAs (siRNAs) that act in the canonical RNA-directed DNA methylation pathway.

Argonaute

(AGO). A family of effector proteins of RNA interference that bind to small interfering RNAs (siRNAs) through their PAZ (PIWI–AGO–ZWILLE) and MID (middle) domains and, in some cases, slice RNA through their PIWI domain. Of the ten AGOs in Arabidopsis thaliana, AGO4, AGO6 and AGO9 act in canonical RNA-directed DNA methylation and/or transcriptional gene silencing.

Transposons

Invasive genetic elements that move within a genome and that are sometimes associated with replicative movement which produces many copies. Transposons include retrotransposons, DNA transposons and helitrons.

de novo methylation

Methylation of a previously unmodified DNA sequence. Small interfering RNAs (siRNAs) in the RNA-directed DNA methylation pathway are well-known triggers of sequence-specific de novo methylation of cytosines in all sequence contexts.

Silencing effector complex

A multiprotein complex that elicits RNA interference and related small RNA-mediated gene silencing pathways. It is composed of an Argonaute protein (which binds to the small RNA guide) and, in the case of RNA-directed DNA methylation, cofactors that aid in directing DNA methylation to the small RNA-targeted region of the genome.

Pericentromeric

Pertaining to the region surrounding the centromere, which is the chromosomal region where two sister chromatids are joined.

RNA-dependent RNA polymerase

(RDR). A cellular enzyme that copies single-stranded RNAs to produce double-stranded RNA precursors, which are processed by Dicer-like proteins to generate small interfering RNAs (siRNAs). Of the six RDRs in Arabidopsis thaliana, RDR2 is associated with the canonical RdDM pathway.

Structural maintenance of chromosomes

(SMC). A large family of ATPases that can manipulate chromosome-sized molecules and that contribute to higher-order chromatin structure and dynamics.

Symmetrical methylation

Cytosine methylation at CG:GC and CHG:GHC nucleotide groups in both DNA strands. As a result of complementary base pairing, CG and CHG are base-paired to GC and GHC, respectively, on the opposite DNA strand and hence considered symmetrical.

Maintenance methylation

The preservation of pre-existing methylation at symmetrical CG and CHG sites after DNA replication by the DNA methyltransferases MET1 and CMT3, which recognize hemimethylated substrates (that is, those methylated on one strand but not the other).

MicroRNAs

(miRNAs). Small non-coding RNAs (~21–23 nucleotides) that silence gene expression by mRNA degradation or translational repression through complementarity with the target transcripts.

Trans-acting siRNAs

(tasiRNAs). A class of small interfering RNAs (siRNAs) that silences gene expression in land plants by targeting complementary mRNAs for cleavage. Their biogenesis depends on microRNA (miRNA)-mediated cleavage of longer TAS RNA precursors that are further acted on by RNA-DEPENDENT RNA POLYMERASE 6 (RDR6) and DICER-LIKE 4 (DCL4). The miRNA-triggered initiation followed by DCL4 cleavage results in a phased pattern of accumulation, in which small RNAs are in an exact head-to-tail arrangement. tasiRNAs are one category of 'phased' siRNA (phasiRNA).

Retrotransposition

The process of mobilizing a retrotransposon. It involves transcription, processing of the RNA, translation, reverse transcription of the transposon RNA and integration of the reverse-transcribed DNA into a new genomic location.

Epialleles

Alleles that differ in transcriptional level from other genetically identical alleles, frequently owing to DNA methylation. Some epialleles are faithfully transmitted to the progeny.

Lamarckian inheritance

The hypothesis that an organism can pass on traits acquired during its lifetime to its progeny.

Gametophytes

The multicellular structure formed through mitosis from a single haploid spore. Male and female gametophytes contain sperm and egg cells, respectively.

Diplosporous apomixis

A process of reproduction whereby failure of meiosis produces an unreduced female gametophyte. An embryo then develops from the diploid egg cell and forms a clone of the maternal plant.

Heterochronic

Pertaining to an evolutionary change in the timing of a developmental process so that a character or process occurs earlier or later in ontogeny, or grows at a different rate.

Genomic imprinting

A phenomenon whereby differential epigenetic marks on maternally and paternally derived alleles result in uniparental gene expression.

Paramutation

A process whereby a transcriptionally silent allele confers meiotically heritable silencing on an active sister allele.

Hybridization

Crossing of two different plant varieties to combine valuable traits from each variety.

Vegetative cell

A haploid cell in the male gametophyte (that is, the pollen grain) that assists fertilization but that does not directly contribute to the zygote.

Endosperm

A tissue in the seed that supports the growth of the embryo. Endosperm is produced after fertilization of the diploid (2N) central cell by a haploid (1N) sperm cell, which creates a maternal:paternal genome ratio of 2:1.

Meristems

Regions of undifferentiated cells at the shoot or root apex that is responsible for cell division and organogenesis. All aerial tissues, including the germ line, arise from the shoot meristem, and all root tissues arise from the root meristem.

Additive gene expression

Gene expression in a hybrid that is the average of the expression levels in the two parental lines.

Interspecific hybrids

Crosses between two closely related but distinct species.

Hybrid vigour

Increase in fitness associated with crosses between distinct inbred strains.

Introgression lines

Lines into which defined DNA segments have been introduced from a different line through backcrossing.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Matzke, M., Mosher, R. RNA-directed DNA methylation: an epigenetic pathway of increasing complexity. Nat Rev Genet 15, 394–408 (2014). https://doi.org/10.1038/nrg3683

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nrg3683

This article is cited by

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