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Epigenetic inheritance in plants

Abstract

The function of plant genomes depends on chromatin marks such as the methylation of DNA and the post-translational modification of histones. Techniques for studying model plants such as Arabidopsis thaliana have enabled researchers to begin to uncover the pathways that establish and maintain chromatin modifications, and genomic studies are allowing the mapping of modifications such as DNA methylation on a genome-wide scale. Small RNAs seem to be important in determining the distribution of chromatin modifications, and RNA might also underlie the complex epigenetic interactions that occur between homologous sequences. Plants use these epigenetic silencing mechanisms extensively to control development and parent-of-origin imprinted gene expression.

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Figure 1: The epigenetic 'landscape' of A. thaliana.
Figure 2: RNA-directed DNA methylation.
Figure 3: Trans-epiallele interactions at b1 and FWA.
Figure 4: PcG-protein-mediated silencing throughout the A. thaliana life cycle.

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References

  1. Gregory, T. R. The C-value enigma in plants and animals: a review of parallels and an appeal for partnership. Ann. Bot. (Lond.) 95, 133–146 (2005).

    Article  CAS  Google Scholar 

  2. Hall, I. M. & Grewal, S. I. in RNAi: A Guide to Gene Silencing (ed. Hannon, G. J.) 205–232 (Cold Spring Harbor Laboratory Press, Woodbury, 2003).

    Google Scholar 

  3. Bernstein, B. E., Meissner, A. & Lander, E. S. The mammalian epigenome. Cell 128, 669–681 (2007).

    Article  CAS  Google Scholar 

  4. Bernard, P. et al. Requirement of heterochromatin for cohesion at centromeres. Science 294, 2539–2542 (2001).

    Article  ADS  CAS  Google Scholar 

  5. Bejerano, G. et al. A distal enhancer and an ultraconserved exon are derived from a novel retroposon. Nature 441, 87–90 (2006).

    Article  ADS  CAS  Google Scholar 

  6. Liu, J., He, Y., Amasino, R. & Chen, X. siRNAs targeting an intronic transposon in the regulation of natural flowering behavior in Arabidopsis. Genes Dev. 18, 2873–2878 (2004).

    Article  CAS  Google Scholar 

  7. Comfort, N. C. From controlling elements to transposons: Barbara McClintock and the Nobel Prize. Trends Biochem. Sci. 26, 454–457 (2001).

    Article  CAS  Google Scholar 

  8. Chandler, V. L. & Stam, M. Chromatin conversations: mechanisms and implications of paramutation. Nature Rev. Genet. 5, 532–544 (2004).

    Article  CAS  Google Scholar 

  9. Hamilton, A. J. & Baulcombe, D. C. A species of small antisense RNA in posttranscriptional gene silencing in plants. Science 286, 950–952 (1999).

    Article  CAS  Google Scholar 

  10. 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  Google Scholar 

  11. Zhang, X. et al. Genome-wide high-resolution mapping and functional analysis of DNA methylation in Arabidopsis. Cell 126, 1189–1201 (2006).

    Article  CAS  Google Scholar 

  12. Zilberman, D., Gehring, M., Tran, R. K., Ballinger, T. & Henikoff, S. Genome-wide analysis of Arabidopsis thaliana DNA methylation uncovers an interdependence between methylation and transcription. Nature Genet. 39, 61–69 (2007).

    Article  CAS  Google Scholar 

  13. nalysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408, 796–815 (2000).

  14. Fransz, P. F. et al. High-resolution physical mapping in Arabidopsis thaliana and tomato by fluorescence in situ hybridization to extended DNA fibres. Plant J. 9, 421–430 (1996).

    Article  CAS  Google Scholar 

  15. Lippman, Z. et al. Role of transposable elements in heterochromatin and epigenetic control. Nature 430, 471–476 (2004).

    Article  ADS  CAS  Google Scholar 

  16. Volpe, T. A. et al. Regulation of heterochromatic silencing and histone H3 lysine-9 methylation by RNAi. Science 297, 1833–1837 (2002).

    Article  ADS  CAS  Google Scholar 

  17. Aufsatz, W., Mette, M. F., van der Winden, J., Matzke, A. J. & Matzke, M. RNA-directed DNA methylation in Arabidopsis. Proc. Natl Acad. Sci. USA 99 (suppl. 4), 16499–16506 (2002).

    Article  ADS  CAS  Google Scholar 

  18. Mochizuki, K., Fine, N. A., Fujisawa, T. & Gorovsky, M. A. Analysis of a piwi-related gene implicates small RNAs in genome rearrangement in Tetrahymena. Cell 110, 689–699 (2002).

    Article  CAS  Google Scholar 

  19. Matzke, M., Matzke, A. J. & Kooter, J. M. RNA: guiding gene silencing. Science 293, 1080–1083 (2001).

    Article  CAS  Google Scholar 

  20. Lu, C. et al. Elucidation of the small RNA component of the transcriptome. Science 309, 1567–1569 (2005).

    Article  ADS  CAS  Google Scholar 

  21. Cao, X. et al. Role of the DRM and CMT3 methyltransferases in RNA-directed DNA methylation. Curr. Biol. 13, 2212–2217 (2003).

    Article  CAS  Google Scholar 

  22. 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).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  24. Zilberman, D. et al. Role of Arabidopsis ARGONAUTE4 in RNA-directed DNA methylation triggered by inverted repeats. Curr. Biol. 14, 1214–1220 (2004).

    Article  CAS  Google Scholar 

  25. 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  Google Scholar 

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

    Article  Google Scholar 

  27. Chan, S. W. et al. RNAi, DRD1, and histone methylation actively target developmentally important non-CG DNA methylation in Arabidopsis. PLoS Genet. 2, e83 (2006).

    Article  Google Scholar 

  28. 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  Google Scholar 

  29. Pontes, O. et al. The Arabidopsis chromatin-modifying nuclear siRNA pathway involves a nucleolar RNA processing center. Cell 126, 79–92 (2006).

    Article  CAS  Google Scholar 

  30. Qi, Y. et al. Distinct catalytic and non-catalytic roles of ARGONAUTE4 in RNA-directed DNA methylation. Nature 443, 1008–1012 (2006).

    Article  ADS  Google Scholar 

  31. 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  ADS  CAS  Google Scholar 

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

    Article  ADS  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  35. 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  Google Scholar 

  36. 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  Google Scholar 

  37. Cao, X. & Jacobsen, S. E. Locus-specific control of asymmetric and CpNpG methylation by the DRM and CMT3 methyltransferase genes. Proc. Natl Acad. Sci. USA 99 (suppl. 4), 16491–16498 (2002).

    Article  ADS  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  Google Scholar 

  41. 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  ADS  CAS  Google Scholar 

  42. Malagnac, F., Bartee, L. & Bender, J. An Arabidopsis SET domain protein required for maintenance but not establishment of DNA methylation. EMBO J. 21, 6842–6852 (2002).

    Article  CAS  Google Scholar 

  43. Jacobsen, S. E. & Meyerowitz, E. M. Hypermethylated SUPERMAN epigenetic alleles in Arabidopsis. Science 277, 1100–1103 (1997).

    Article  CAS  Google Scholar 

  44. Herman, H. et al. Trans allele methylation and paramutation-like effects in mice. Nature Genet. 34, 199–202 (2003).

    Article  CAS  Google Scholar 

  45. Stam, M. et al. The regulatory regions required for B′ paramutation and expression are located far upstream of the maize b1 transcribed sequences. Genetics 162, 917–930 (2002).

    CAS  PubMed  PubMed Central  Google Scholar 

  46. Stam, M., Belele, C., Dorweiler, J. E. & Chandler, V. L. Differential chromatin structure within a tandem array 100 kb upstream of the maize b1 locus is associated with paramutation. Genes Dev. 16, 1906–1918 (2002).

    Article  CAS  Google Scholar 

  47. Alleman, M. et al. An RNA-dependent RNA polymerase is required for paramutation in maize. Nature 442, 295–298 (2006).

    Article  ADS  CAS  Google Scholar 

  48. Woodhouse, M. R., Freeling, M. & Lisch, D. Initiation, establishment, and maintenance of heritable MuDR transposon silencing in maize are mediated by distinct factors. PLoS Biol. 4, e339 (2006).

    Article  Google Scholar 

  49. Chan, S. W.-L., Zhang, X., Bernatavichute, Y. V. & Jacobsen, S. E. Two-step recruitment of RNA-directed DNA methylation to tandem repeats. PLoS Biol. 4, e363 (2006).

    Article  Google Scholar 

  50. Lisch, D., Carey, C. C., Dorweiler, J. E. & Chandler, V. L. A mutation that prevents paramutation in maize also reverses Mutator transposon methylation and silencing. Proc. Natl Acad. Sci. USA 99, 6130–6135 (2002).

    Article  ADS  CAS  Google Scholar 

  51. 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).

    Article  CAS  Google Scholar 

  52. Gehring, M., Choi, Y. & Fischer, R. L. Imprinting and seed development. Plant Cell 16, S203–S213 (2004).

    Article  CAS  Google Scholar 

  53. Kinoshita, T. et al. One-way control of FWA imprinting in Arabidopsis endosperm by DNA methylation. Science 303, 521–523 (2004).

    Article  ADS  CAS  Google Scholar 

  54. Choi, Y. et al. DEMETER, a DNA glycosylase domain protein, is required for endosperm gene imprinting and seed viability in Arabidopsis. Cell 110, 33–42 (2002).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  56. Morales-Ruiz, T. et al. DEMETER and REPRESSOR OF SILENCING 1 encode 5-methylcytosine DNA glycosylases. Proc. Natl Acad. Sci.USA 103, 6853–6858 (2006).

    Article  ADS  CAS  Google Scholar 

  57. Jullien, P. E., Kinoshita, T., Ohad, N. & Berger, F. Maintenance of DNA methylation during the Arabidopsis life cycle is essential for parental imprinting. Plant Cell 18, 1360–1372 (2006).

    Article  CAS  Google Scholar 

  58. Kinoshita, Y. et al. Control of FWA gene silencing in Arabidopsis thaliana by SINE-related direct repeats. Plant J. 49, 38–45 (2007).

    Article  CAS  Google Scholar 

  59. 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  Google Scholar 

  60. Agius, F., Kapoor, A. & Zhu, J. K. Role of the Arabidopsis DNA glycosylase/lyase ROS1 in active DNA demethylation. Proc. Natl Acad. Sci. USA 103, 11796–11801 (2006).

    Article  ADS  CAS  Google Scholar 

  61. Barreto, G. et al. Gadd45a promotes epigenetic gene activation by repair-mediated DNA demethylation. Nature 445, 671–675 (2007).

    Article  CAS  Google Scholar 

  62. Jost, J. P., Siegmann, M., Sun, L. & Leung, R. Mechanisms of DNA demethylation in chicken embryos. Purification and properties of a 5-methylcytosine-DNA glycosylase. J. Biol. Chem. 270, 9734–9739 (1995).

    Article  CAS  Google Scholar 

  63. Danilevskaya, O. N. et al. Duplicated fie genes in maize: expression pattern and imprinting suggest distinct functions. Plant Cell 15, 425–438 (2003).

    Article  CAS  Google Scholar 

  64. Gutierrez-Marcos, J. F. et al. Epigenetic asymmetry of imprinted genes in plant gametes. Nature Genet. 38, 876–878 (2006).

    Article  CAS  Google Scholar 

  65. Shiba, H. et al. Dominance relationships between self-incompatibility alleles controlled by DNA methylation. Nature Genet. 38, 297–299 (2006).

    Article  CAS  Google Scholar 

  66. Kohler, C. & Grossniklaus, U. Epigenetic inheritance of expression states in plant development: the role of Polycomb group proteins. Curr. Opin. Cell Biol. 14, 773–779 (2002).

    Article  CAS  Google Scholar 

  67. Kinoshita, T., Yadegari, R., Harada, J. J., Goldberg, R. B. & Fischer, R. L. Imprinting of the MEDEA polycomb gene in the Arabidopsis endosperm. Plant Cell 11, 1945–1952 (1999).

    Article  CAS  Google Scholar 

  68. Baroux, C., Gagliardini, V., Page, D. R. & Grossniklaus, U. Dynamic regulatory interactions of Polycomb group genes: MEDEA autoregulation is required for imprinted gene expression in Arabidopsis. Genes Dev. 20, 1081–1086 (2006).

    Article  CAS  Google Scholar 

  69. Jullien, P. E., Katz, A., Oliva, M., Ohad, N. & Berger, F. Polycomb group complexes self-regulate imprinting of the Polycomb group gene MEDEA in Arabidopsis. Curr. Biol. 16, 486–492 (2006).

    Article  CAS  Google Scholar 

  70. Mager, J., Montgomery, N. D., de Villena, F. P. & Magnuson, T. Genome imprinting regulated by the mouse Polycomb group protein Eed. Nature Genet. 33, 502–507 (2003).

    Article  CAS  Google Scholar 

  71. Bastow, R. et al. Vernalization requires epigenetic silencing of FLC by histone methylation. Nature 427, 164–167 (2004).

    Article  ADS  CAS  Google Scholar 

  72. Gendall, A. R., Levy, Y. Y., Wilson, A. & Dean, C. The VERNALIZATION 2 gene mediates the epigenetic regulation of vernalization in Arabidopsis. Cell 107, 525–535 (2001).

    Article  CAS  Google Scholar 

  73. Sung, S. & Amasino, R. M. Vernalization in Arabidopsis thaliana is mediated by the PHD finger protein VIN3. Nature 427, 159–164 (2004).

    Article  ADS  CAS  Google Scholar 

  74. Sung, S., Schmitz, R. J. & Amasino, R. M. A PHD finger protein involved in both the vernalization and photoperiod pathways in Arabidopsis. Genes Dev. 20, 3244–3248 (2006).

    Article  CAS  Google Scholar 

  75. Mylne, J. S. et al. LHP1, the Arabidopsis homologue of HETEROCHROMATIN PROTEIN1, is required for epigenetic silencing of FLC. Proc. Natl Acad. Sci. USA 103, 5012–5017 (2006).

    Article  ADS  CAS  Google Scholar 

  76. Sung, S. et al. Epigenetic maintenance of the vernalized state in Arabidopsis thaliana requires LIKE HETEROCHROMATIN PROTEIN 1. Nature Genet. 38, 706–710 (2006).

    Article  CAS  Google Scholar 

  77. Levy, Y. Y., Mesnage, S., Mylne, J. S., Gendall, A. R. & Dean, C. Multiple roles of Arabidopsis VRN1 in vernalization and flowering time control. Science 297, 243–246 (2002).

    Article  ADS  CAS  Google Scholar 

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Acknowledgements

We thank S. Chan, C. Fei Li, K. Niakan, M. Ong and all members of the Jacobsen laboratory for useful comments and discussion. We apologize to colleagues whose research we did not have space to discuss. I.R.H. was supported by a long-term fellowship from the European Molecular Biology Organization, a Special Fellow grant from The Leukemia & Lymphoma Society, and a grant from the National Institutes of Health. S.E.J is an investigator of the Howard Hughes Medical Institute.

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Correspondence should be addressed to S.E.J. (jacobsen@ucla.edu).

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Henderson, I., Jacobsen, S. Epigenetic inheritance in plants. Nature 447, 418–424 (2007). https://doi.org/10.1038/nature05917

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