siRNA-mediated DNA methylation and H3K9 dimethylation in plants

Protein and Cell

Volumn 4, Issue 9, 2013, Pages 656-663

  Xu, Chi ^a   Tian, Jing ^a   Mo, Beixin ^a  

^a SHENZHEN UNIVERSITY   (China)

Author keywords

argonaute; DNA methylation; epigenetic; heterochromatic siRNA; histone methylation

Indexed keywords

HISTONE; PLANT PROTEIN; SMALL INTERFERING RNA;

ARABIDOPSIS; BIOSYNTHESIS; DNA METHYLATION; GENE SILENCING; GENETIC EPIGENESIS; GENETICS; METABOLISM; METHYLATION; PLANT;

ARABIDOPSIS; DNA METHYLATION; EPIGENESIS, GENETIC; GENE SILENCING; HISTONES; METHYLATION; PLANT PROTEINS; PLANTS; RNA, SMALL INTERFERING;

EID: 84892897533     PISSN: 1674800X     EISSN: 16748018     Source Type: Journal    
DOI: 10.1007/s13238-013-3052-7     Document Type: Review

References (79)

1. Alleman, M., Sidorenko, L., McGinnis, K., Seshadri, V., Dorweiler, J. E., White, J., Sikkink, K., and Chandler, V. L. (2006). An RNA-dependent RNA polymerase is required for paramutation in maize. Nature 442, 295-298.
2. Barreto, G., Schafer, A., Marhold, J., Stach, D., Swaminathan, S. K., Handa, V., Doderlein, G., Maltry, N., Wu, W., Lyko, F., et al. (2007). Gadd45a promotes epigenetic gene activation by repair-mediated DNA demethylation. Nature 445, 671-675.
3. Barth, T. K., and Imhof, A. (2010). Fast signals and slow marks: the dynamics of histone modifications. Trends Biochem Sci 35, 618-626.
4. Berger, S. L. (2007). The complex language of chromatin regulation during transcription. Nature 447, 407-412.
5. Bernatavichute, Y. V., Zhang, X., Cokus, S., Pellegrini, M., and Jacobsen, S. E. (2008). Genome-wide association of histone H3 lysine nine methylation with CHG DNA methylation in Arabidopsis thaliana. PLoS One 3, e3156.
6. Bernstein, B. E., Meissner, A., and Lander, E. S. (2007). The mammalian epigenome. Cell 128, 669-681.
7. Bird, A. P. (1986). CpG-rich islands and the function of DNA methylation. Nature 321, 209-213.
8. Buhler, M., Haas, W., Gygi, S. P., and Moazed, D. (2007). RNAidependent and -independent RNA turnover mechanisms contribute to heterochromatic gene silencing. Cell 129, 707-721.
9. Cao, X., and Jacobsen, S. E. (2002a). Locus-specific control of asymmetric and CpNpG methylation by the DRM and CMT3 methyltransferase genes. Proc Natl Acad Sci U S A 99 Suppl 4, 16491-16498.
10. Cao, X., and Jacobsen, S. E. (2002b). Role of the arabidopsis DRM methyltransferases in de novo DNA methylation and gene silencing. Curr Biol 12, 1138-1144.
11. Cartagena, J. A., Matsunaga, S., Seki, M., Kurihara, D., Yokoyama, M., Shinozaki, K., Fujimoto, S., Azumi, Y., Uchiyama, S., and Fukui, K. (2008). The Arabidopsis SDG4 contributes to the regulation of pollen tube growth by methylation of histone H3 lysines 4 and 36 in mature pollen. Dev Biol 315, 355-368.
12. Chan, S. W., Zhang, X., Bernatavichute, Y. V., and Jacobsen, S. E. (2006). Two-step recruitment of RNA-directed DNA methylation to tandem repeats. PLoS Biol 4, e363.
13. Chan, S. W., Zilberman, D., Xie, Z., Johansen, L. K., Carrington, J. C., and Jacobsen, S. E. (2004). RNA silencing genes control de novo DNA methylation. Science 303, 1336.
14. Cokus, S. J., Feng, S., Zhang, X., Chen, Z., Merriman, B., Haudenschild, C. D., Pradhan, S., Nelson, S. F., Pellegrini, M., and Jacobsen, S. E. (2008). Shotgun bisulphite sequencing of the Arabidopsis genome reveals DNA methylation patterning. Nature 452, 215-219.
15. Du, J., Zhong, X., Bernatavichute, Y. V., Stroud, H., Feng, S., Caro, E., Vashisht, A. A., Terragni, J., Chin, H. G., Tu, A., et al. (2012). Dual binding of chromomethylase domains to H3K9me2-containing nucleosomes directs DNA methylation in plants. Cell 151, 167-180.
16. Ebbs, M. L., Bartee, L., and Bender, J. (2005). H3 lysine 9 methylation is maintained on a transcribed inverted repeat by combined action of SUVH6 and SUVH4 methyltransferases. Mol Cell Biol 25, 10507-10515.
17. Ebbs, M. L., and Bender, J. (2006). Locus-specific control of DNA methylation by the Arabidopsis SUVH5 histone methyltransferase. Plant Cell 18, 1166-1176.
18. Erhard, K. F., Jr., Stonaker, J. L., Parkinson, S. E., Lim, J. P., Hale, C. J., and Hollick, J. B. (2009). RNA polymerase IV functions in paramutation in Zea mays. Science 323, 1201-1205.
19. Espada, J., and Esteller, M. (2010). DNA methylation and the functional organization of the nuclear compartment. Semin Cell Dev Biol 21, 238-246.
20. Fan, D., Dai, Y., Wang, X., Wang, Z., He, H., Yang, H., Cao, Y., Deng, X. W., and Ma, L. (2012). IBM1, a JmjC domain-containing histone demethylase, is involved in the regulation of RNA-directed DNA methylation through the epigenetic control of RDR2 and DCL3 expression in Arabidopsis. Nucleic Acids Res 40, 8905-8916.
21. Finke, A., Kuhlmann, M., and Mette, M. F. (2012). IDN2 has a role downstream of siRNA formation in RNA-directed DNA methylation. Epigenetics 7, 950-960.
22. Gao, Z., Liu, H. L., Daxinger, L., Pontes, O., He, X., Qian, W., Lin, H., Xie, M., Lorkovic, Z. J., Zhang, S., et al. (2010). An RNA polymerase II- and AGO4-associated protein acts in RNA-directed DNA methylation. Nature 465, 106-109.
23. Grossniklaus, U., Vielle-Calzada, J. P., Hoeppner, M. A., and Gagliano, W. B. (1998). Maternal control of embryogenesis by MEDEA, a polycomb group gene in Arabidopsis. Science 280, 446-450.
24. Havecker, E. R., Wallbridge, L. M., Hardcastle, T. J., Bush, M. S., Kelly, K. A., Dunn, R. M., Schwach, F., Doonan, J. H., and Baulcombe, D. C. (2010). The Arabidopsis RNA-directed DNA methylation argonautes functionally diverge based on their expression and interaction with target loci. Plant Cell 22, 321-334.
25. Henderson, I. R., and Jacobsen, S. E. (2008). Tandem repeats upstream of the Arabidopsis endogene SDC recruit non-CG DNA methylation and initiate siRNA spreading. Genes Dev 22, 1597-1606.
26. Herr, A. J., Jensen, M. B., Dalmay, T., and Baulcombe, D. C. (2005). RNA polymerase IV directs silencing of endogenous DNA. Science 308, 118-120.
27. Inagaki, S., and Kakutani, T. (2010). Control of genic DNA methylation in Arabidopsis. J Plant Res 123, 299-302.
28. Inagaki, S., Miura-Kamio, A., Nakamura, Y., Lu, F., Cui, X., Cao, X., Kimura, H., Saze, H., and Kakutani, T. (2010). Autocatalytic differentiation of epigenetic modifications within the Arabidopsis genome. EMBO J 29, 3496-3506.
29. Jackson, J. P., Lindroth, A. M., Cao, X., and Jacobsen, S. E. (2002). Control of CpNpG DNA methylation by the KRYPTONITE histone H3 methyltransferase. Nature 416, 556-560.
30. Jacob, Y., Feng, S., LeBlanc, C. A., Bernatavichute, Y. V., Stroud, H., Cokus, S., Johnson, L. M., Pellegrini, M., Jacobsen, S. E., and Michaels, S. D. (2009). ATXR5 and ATXR6 are H3K27 monomethyltransferases required for chromatin structure and gene silencing. Nat Struct Mol Biol 16, 763-768.
31. Jia, Y., Lisch, D. R., Ohtsu, K., Scanlon, M. J., Nettleton, D., and Schnable, P. S. (2009). Loss of RNA-dependent RNA polymerase 2 (RDR2) function causes widespread and unexpected changes in the expression of transposons, genes, and 24-nt small RNAs. PLoS Genet 5, e1000737.
32. Johnson, L. M., Bostick, M., Zhang, X., Kraft, E., Henderson, I., Callis, J., and Jacobsen, S. E. (2007). The SRA methyl-cytosine-binding domain links DNA and histone methylation. Curr Biol 17, 379-384.
33. Kanno, T., Aufsatz, W., Jaligot, E., Mette, M. F., Matzke, M., and Matzke, A. J. (2005). A SNF2-like protein facilitates dynamic control of DNA methylation. EMBO Rep 6, 649-655.
34. Kanno, T., Bucher, E., Daxinger, L., Huettel, B., Bohmdorfer, G., Gregor, W., Kreil, D. P., Matzke, M., and Matzke, A. J. (2008). A structural-maintenance-of-chromosomes hinge domain-containing protein is required for RNA-directed DNA methylation. Nat Genet 40, 670-675.
35. Kanno, T., Bucher, E., Daxinger, L., Huettel, B., Kreil, D. P., Breinig, F., Lind, M., Schmitt, M. J., Simon, S. A., Gurazada, S. G., et al. (2010). RNA-directed DNA methylation and plant development require an IWR1-type transcription factor. EMBO Rep 11, 65-71.
36. Kasschau, K. D., Fahlgren, N., Chapman, E. J., Sullivan, C. M., Cumbie, J. S., Givan, S. A., and Carrington, J. C. (2007). Genome-wide profiling and analysis of Arabidopsis siRNAs. PLoS Biol 5, e57.
37. Lachner, M., and Jenuwein, T. (2002). The many faces of histone lysine methylation. Curr Opin Cell Biol 14, 286-298.
38. Lachner, M., O'Sullivan, R. J., and Jenuwein, T. (2003). An epigenetic road map for histone lysine methylation. J Cell Sci 116, 2117-2124.
39. Law, J. A., Du, J., Hale, C. J., Feng, S., Krajewski, K., Palanca, A. M., Strahl, B. D., Patel, D. J., and Jacobsen, S. E. (2013). Polymerase IV occupancy at RNA-directed DNA methylation sites requires SHH1. Nature 498, 385-389.
40. Law, J. A., and Jacobsen, S. E. (2010). Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nat Rev Genet 11, 204-220.
41. Lee, T. F., Gurazada, S. G., Zhai, J., Li, S., Simon, S. A., Matzke, M. A., Chen, X., and Meyers, B. C. (2012). RNA polymerase V-dependent small RNAs in Arabidopsis originate from small, intergenic loci including most SINE repeats. Epigenetics 7, 781-795.
42. Li, K. K., Luo, C., Wang, D., Jiang, H., and Zheng, Y. G. (2010). Chemical and biochemical approaches in the study of histone methylation and demethylation. Med Res Rev 32, 815-867.
43. Lindroth, A. M., Shultis, D., Jasencakova, Z., Fuchs, J., Johnson, L., Schubert, D., Patnaik, D., Pradhan, S., Goodrich, J., Schubert, I., et al. (2004). Dual histone H3 methylation marks at lysines 9 and 27 required for interaction with CHROMOMETHYLASE3. EMBO J 23, 4286-4296.
44. Lippman, Z., Gendrel, A. V., Black, M., Vaughn, M. W., Dedhia, N., Mc-Combie, W. R., Lavine, K., Mittal, V., May, B., Kasschau, K. D., et al. (2004). Role of transposable elements in heterochromatin and epigenetic control. Nature 430, 471-476.
45. Liu, C., Lu, F., Cui, X., and Cao, X. (2010). Histone methylation in higher plants. Ann Rev Plant Biol 61, 395-420.
46. Liu, J., He, Y., Amasino, R., and Chen, X. (2004). siRNAs targeting an intronic transposon in the regulation of natural flowering behavior in Arabidopsis. Genes Dev 18, 2873-2878.
47. Lorkovic, Z. J., Naumann, U., Matzke, A. J., and Matzke, M. (2012). Involvement of a GHKL ATPase in RNA-directed DNA methylation in Arabidopsis thaliana. Curr Biol 22, 933-938.
48. Lu, C., Tej, S. S., Luo, S., Haudenschild, C. D., Meyers, B. C., and Green, P. J. (2005). Elucidation of the small RNA component of the transcriptome. Science 309, 1567-1569.
49. Luger, K., Mader, A. W., Richmond, R. K., Sargent, D. F., and Richmond, T. J. (1997). Crystal structure of the nucleosome core particle at 2. 8 A resolution. Nature 389, 251-260.
50. Matzke, M., Kanno, T., Daxinger, L., Huettel, B., and Matzke, A. J. (2009). RNA-mediated chromatin-based silencing in plants. Curr Opin Cell Biol 21, 367-376.
51. Miura, A., Nakamura, M., Inagaki, S., Kobayashi, A., Saze, H., and Kakutani, T. (2009). An Arabidopsis jmjC domain protein protects transcribed genes from DNA methylation at CHG sites. EMBO J 28, 1078-1086.
52. Mosher, R. A., Schwach, F., Studholme, D., and Baulcombe, D. C. (2008). PolIVb influences RNA-directed DNA methylation independently of its role in siRNA biogenesis. Proc Natl Acad Sci U S A 105, 3145-3150.
53. Onodera, Y., Haag, J. R., Ream, T., Costa Nunes, P., Pontes, O., and Pikaard, C. S. (2005). Plant nuclear RNA polymerase IV mediates siRNA and DNA methylation-dependent heterochromatin formation. Cell 120, 613-622.
54. Pontier, D., Yahubyan, G., Vega, D., Bulski, A., Saez-Vasquez, J., Hakimi, M. A., Lerbs-Mache, S., Colot, V., and Lagrange, T. (2005). 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.
55. Qi, Y., He, X., Wang, X. J., Kohany, O., Jurka, J., and Hannon, G. J. (2006). Distinct catalytic and non-catalytic roles of ARGONAUTE4 in RNA-directed DNA methylation. Nature 443, 1008-1012.
56. Qian, W., Miki, D., Zhang, H., Liu, Y., Zhang, X., Tang, K., Kan, Y., La, H., Li, X., Li, S., et al. (2012). A histone acetyltransferase regulates active DNA demethylation in Arabidopsis. Science 336, 1445-1448.
57. Saleh, A., Alvarez-Venegas, R., Yilmaz, M., Le, O., Hou, G., Sadder, M., Al-Abdallat, A., Xia, Y., Lu, G., Ladunga, I., et al. (2008). The highly similar Arabidopsis homologs of trithorax ATX1 and ATX2 encode proteins with divergent biochemical functions. Plant Cell 20, 568-579.
58. Saze, H., and Kakutani, T. (2011). Differentiation of epigenetic modifications between transposons and genes. Curr Opin Plant Biol 14, 81-87.
59. Saze, H., Mittelsten Scheid, O., and Paszkowski, J. (2003). Maintenance of CpG methylation is essential for epigenetic inheritance during plant gametogenesis. Nat Genet 34, 65-69.
60. Saze, H., Shiraishi, A., Miura, A., and Kakutani, T. (2008). Control of genic DNA methylation by a jmjC domain-containing protein in Arabidopsis thaliana. Science 319, 462-465.
61. Sidorenko, L., Dorweiler, J. E., Cigan, A. M., Arteaga-Vazquez, M., Vyas, M., Kermicle, J., Jurcin, D., Brzeski, J., Cai, Y., and Chandler, V. L. (2009). A dominant mutation in mediator of paramutation2, one of three second-largest subunits of a plant-specific RNA polymerase, disrupts multiple siRNA silencing processes. PLoS Genet 5, e1000725.
62. Soppe, W. J., Jacobsen, S. E., Alonso-Blanco, C., Jackson, J. P., Kakutani, T., Koornneef, M., and Peeters, A. J. (2000). The late flowering phenotype of fwa mutants is caused by gain-of-function epigenetic alleles of a homeodomain gene. Mol Cell 6, 791-802.
63. Takuno, S., and Gaut, B. S. (2012). Body-methylated genes in Arabidopsis thaliana are functionally important and evolve slowly. Mol Biol Evol 29, 219-227.
64. Tran, R. K., Henikoff, J. G., Zilberman, D., Ditt, R. F., Jacobsen, S. E., and Henikoff, S. (2005). DNA methylation profiling identifies CG methylation clusters in Arabidopsis genes. Curr Biol 15, 154-159.
65. Turck, F., Roudier, F., Farrona, S., Martin-Magniette, M. L., Guillaume, E., Buisine, N., Gagnot, S., Martienssen, R. A., Coupland, G., and Colot, V. (2007). Arabidopsis TFL2/LHP1 specifically associates with genes marked by trimethylation of histone H3 lysine 27. PLoS Genet 3, e86.
66. Wang, Z., Zang, C., Rosenfeld, J. A., Schones, D. E., Barski, A., Cuddapah, S., Cui, K., Roh, T. Y., Peng, W., Zhang, M. Q., et al. (2008). Combinatorial patterns of histone acetylations and methylations in the human genome. Nat Genet 40, 897-903.
67. Wierzbicki, A. T., Cocklin, R., Mayampurath, A., Lister, R., Rowley, M. J., Gregory, B. D., Ecker, J. R., Tang, H., and Pikaard, C. S. (2012). 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.
68. Wierzbicki, A. T., Haag, J. R., and Pikaard, C. S. (2008). Noncoding transcription by RNA polymerase Pol IVb/Pol V mediates transcriptional silencing of overlapping and adjacent genes. Cell 135, 635-648.
69. Wierzbicki, A. T., Ream, T. S., Haag, J. R., and Pikaard, C. S. (2009). RNA polymerase V transcription guides ARGONAUTE4 to chromatin. Nat Genet 41, 630-634.
70. Xie, Z., Johansen, L. K., Gustafson, A. M., Kasschau, K. D., Lellis, A. D., Zilberman, D., Jacobsen, S. E., and Carrington, J. C. (2004). Genetic and functional diversification of small RNA pathways in plants. PLoS Biol 2, e104.
71. Ye, R., Wang, W., Iki, T., Liu, C., Wu, Y., Ishikawa, M., Zhou, X., and Qi, Y. (2012). Cytoplasmic assembly and selective nuclear import of Arabidopsis Argonaute4/siRNA complexes. Mol Cell 46, 859-870.
72. Zaratiegui, M., Irvine, D. V., and Martienssen, R. A. (2007). Noncoding RNAs and gene silencing. Cell 128, 763-776.
73. Zhang, C. J., Ning, Y. Q., Zhang, S. W., Chen, Q., Shao, C. R., Guo, Y. W., Zhou, J. X., Li, L., Chen, S., and He, X. J. (2012). IDN2 and its paralogs form a complex required for RNA-directed DNA methylation. PLoS Genet 8, e1002693.
74. Zhang, H., Ma, Z. Y., Zeng, L., Tanaka, K., Zhang, C. J., Ma, J., Bai, G., Wang, P., Zhang, S. W., Liu, Z. W., et al. (2013). DTF1 is a core component of RNA-directed DNA methylation and may assist in the recruitment of Pol IV. Proc Natl Acad Sci U S A 110, 8290-8295.
75. Zhang, X., Henderson, I. R., Lu, C., Green, P. J., and Jacobsen, S. E. (2007). Role of RNA polymerase IV in plant small RNA metabolism. Proc Natl Acad Sci U S A 104, 4536-4541.
76. Zhang, X., Yazaki, J., Sundaresan, A., Cokus, S., Chan, S. W., Chen, H., Henderson, I. R., Shinn, P., Pellegrini, M., Jacobsen, S. E., et al. (2006). Genome-wide high-resolution mapping and functional analysis of DNA methylation in arabidopsis. Cell 126, 1189-1201.
77. Zheng, B., Wang, Z., Li, S., Yu, B., Liu, J. Y., and Chen, X. (2009). 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.
78. Zilberman, D., Cao, X., and Jacobsen, S. E. (2003). ARGONAUTE4 control of locus-specific siRNA accumulation and DNA and histone methylation. Science 299, 716-719.
79. Zilberman, D., and Henikoff, S. (2007). Genome-wide analysis of DNA methylation patterns. Development 134, 3959-3965.