Identification and characterization of an Epi-allele of FIE1 reveals a regulatory linkage between two epigenetic marks in riceW OA

Plant Cell

Volumn 24, Issue 11, 2012, Pages 4407-4421

  Zhang, Liguo ^a   Cheng, Zhijun ^a   Qin, Ruizhen ^b   Qiu, Yang ^b   Wang, Jiu Lin ^b   Cui, Xiekui ^c   Gu, Lianfeng ^c   Zhang, Xin ^b   Guo, Xiuping ^b   Wang, Dan ^b   Jiang, Ling ^a   Wu, Chuan yin ^b   Wang, Haiyang ^b   Cao, Xiaofeng ^c   Wan, Jianmin ^a,b  

^a NANJING AGRICULTURAL UNIVERSITY   (China)

^b INSTITUTE OF PLANT PROTECTION   (China)

^c INSTITUTE OF GENETICS AND DEVELOPMENTAL BIOLOGY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ORYZA SATIVA;

EID: 84871882077     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.112.102269     Document Type: Article

References (69)

1. Bartee, L., Malagnac, F., and Bender, J. (2001). Arabidopsis cmt3 chromomethylase mutations block non-CG methylation and silencing of an endogenous gene. Genes Dev. 15: 1753-1758.
2. 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.
3. Cao, R., and Zhang, Y. (2004). The functions of E(Z)/EZH2-mediated meth-ylation of lysine 27 in histone H3. Curr. Opin. Genet. Dev. 14: 155-164.
4. Cao, X., Aufsatz, W., Zilberman, D., Mette, M.F., Huang, M.S., Matzke, M., and Jacobsen, S.E. (2003). Role of the DRM and CMT3 methyltransferases in RNA-directed DNA methylation. Curr. Biol. 13: 2212-2217.
5. Cao, X., and Jacobsen, S.E. (2002). Role of the Arabidopsis DRM methyltransferases in de novo DNA methylation and gene silencing. Curr. Biol. 12: 1138-1144.
6. Chanvivattana, Y., Bishopp, A., Schubert, D., Stock, C., Moon, Y. H., Sung, Z.R., and Goodrich, J. (2004). Interaction of Polycomb-group proteins controlling flowering in Arabidopsis. Development 131: 5263-5276.
7. Chaudhury, A.M., Ming, L., Miller, C., Craig, S., Dennis, E.S., and Peacock, W.J. (1997). Fertilization-independent seed development in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 94: 4223-4228.
8. Cheng, Z., Buell, C.R., Wing, R.A., Gu, M., and Jiang, J. (2001). Toward a cytological characterization of the rice genome. Genome Res. 11: 2133-2141.
9. 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.
10. Cubas, P., Vincent, C., and Coen, E. (1999). An epigenetic mutation responsible for natural variation in floral symmetry. Nature 401: 157-161.
11. Danilevskaya, O.N., Hermon, P., Hantke, S., Muszynski, M.G., Kollipara, K., and Ananiev, E.V. (2003). Duplicated fie genes in maize: expression pattern and imprinting suggest distinct functions. Plant Cell 15: 425-438.
12. Ding, Y., Wang, X., Su, L., Zhai, J., Cao, S., Zhang, D., Liu, C., Bi, Y., Qian, Q., Cheng, Z., Chu, C., and Cao, X. (2007). SDG714, a his-tone H3K9 methyltransferase, is involved in Tos17 DNA methylation and transposition in rice. Plant Cell 19: 9-22.
13. Ehrlich, M., Gama-Sosa, M.A., Huang, L.H., Midgett, R.M., Kuo, K.C., McCune, R.A., and Gehrke, C. (1982). Amount and distribution of 5-methylcytosine in human DNA from different types of tissues of cells. Nucleic Acids Res. 10: 2709-2721.
14. Fischle, W., Wang, Y., and Allis, C.D. (2003). Histone and chromatin cross-talk. Curr. Opin. Cell Biol. 15: 172-183.
15. Frei, E., Baumgartner, S., Edström, J.E., and Noll, M. (1985). Cloning of the extra sex combs gene of Drosophila and its identification by P-element-mediated gene transfer. EMBO J. 4: 979-987.
16. Gong, Z., Morales-Ruiz, T., Ariza, R.R., Roldán-Arjona, T., David, L., and Zhu, J.K. (2002). ROS1, a repressor of transcriptional gene silencing in Arabidopsis, encodes a DNA glycosylase/lyase. Cell 111: 803-814.
17. Gruntman, E., Qi, Y., Slotkin, R.K., Roeder, T., Martienssen, R.A., and Sachidanandam, R. (2008). Kismeth: analyzer of plant methylation states through bisulfite sequencing. BMC Bioinformatics 9: 371.
18. Hiei, Y., and Komari, T. (2008). Agrobacterium-mediated transformation of rice using immature embryos or calli induced from mature seed. Nat. Protoc. 3: 824-834.
19. 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.
20. 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.
21. Jacobsen, S.E., and Meyerowitz, E.M. (1997). Hypermethylated SUPERMAN epigenetic alleles in Arabidopsis. Science 277: 1100-1103.
22. Kapazoglou, A., Tondelli, A., Papaefthimiou, D., Ampatzidou, H., Francia, E., Stanca, M.A., Bladenopoulos, K., and Tsaftaris, A.S. (2010). Epigenetic chromatin modifiers in barley: IV. The study of barley polycomb group (PcG) genes during seed development and in response to external ABA. BMC Plant Biol. 10: 73.
23. Katz, A., Oliva, M., Mosquna, A., Hakim, O., and Ohad, N. (2004). FIE and CURLY LEAF polycomb proteins interact in the regulation of homeobox gene expression during sporophyte development. Plant J. 37: 707-719.
24. Kinoshita, T., Yadegari, R., Harada, J.J., Goldberg, R.B., and Fischer, R.L. (1999). Imprinting of the MEDEA polycomb gene in the Arabidopsis endosperm. Plant Cell 11: 1945-1952.
25. Kinoshita, T., Miura, A., Choi, Y., Kinoshita, Y., Cao, X., Jacobsen, S.E., Fischer, R.L., and Kakutani, T. (2004). One-way control of FWA imprinting in Arabidopsis endosperm by DNA methylation. Science 303: 521-523.
26. Kiyosue, T., Ohad, N., Yadegari, R., Hannon, M., Dinneny, J., Wells, D., Katz, A., Margossian, L., Harada, J.J., Goldberg, R.B., and Fischer, R.L. (1999). Control of fertilization-independent endosperm development by the MEDEA polycomb gene in Arabidopsis. Proc. Natl. Acad. Sci. USA 96: 4186-4191.
27. Köhler, C., and Villar, C.B. (2008). Programming of gene expression by Polycomb group proteins. Trends Cell Biol. 18: 236-243.
28. La, H., Ding, B., Mishra, G.P., Zhou, B., Yang, H., Bellizzi, Mdel.R., Chen, S., Meyers, B.C., Peng, Z., Zhu, J.K., and Wang, G.L. (2011). A 5-methylcytosine DNA glycosylase/lyase demethylates the retrotransposon Tos17 and promotes its transposition in rice. Proc. Natl. Acad. Sci. USA 108: 15498-15503.
29. Langmead, B., Trapnell, C., Pop, M., and Salzberg, S.L. (2009). Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 10: R25.
30. 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.
31. Li, X., et al. (2008). High-resolution mapping of epigenetic modifications of the rice genome uncovers interplay between DNA methylation, histone methylation, and gene expression. Plant Cell 20: 259-276.
32. Lindroth, A.M., Cao, X., Jackson, J.P., Zilberman, D., McCallum, C. M., Henikoff, S., and Jacobsen, S.E. (2001). Requirement of CHROMOMETHYLASE3 for maintenance of CpXpG methylation. Science 292: 2077-2080.
33. Liu, C., Lu, F., Cui, X., and Cao, X. (2010). Histone methylation in higher plants. Annu. Rev. Plant Biol. 61: 395-420.
34. Lu, F., Cui, X., Zhang, S., Jenuwein, T., and Cao, X. (2011). Arabi-dopsis REF6 is a histone H3 lysine 27 demethylase. Nat. Genet. 43: 715-719.
35. Luo, M., Bilodeau, P., Dennis, E.S., Peacock, W.J., and Chaudhury, A. (2000). Expression and parent-of-origin effects for FIS2, MEA, and FIE in the endosperm and embryo of developing Arabidopsis seeds. Proc. Natl. Acad. Sci. USA 97: 10637-10642.
36. Luo, M., Bilodeau, P., Koltunow, A., Dennis, E.S., Peacock, W.J., and Chaudhury, A.M. (1999). Genes controlling fertilization-independent seed development in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 96: 296-301.
37. Luo, M., Platten, D., Chaudhury, A., Peacock, W.J., and Dennis, E.S. (2009). Expression, imprinting, and evolution of rice homologs of the polycomb group genes. Mol. Plant 2: 711-723.
38. Malagnac, F., Bartee, L., and Bender, J. (2002). An Arabidopsis SET domain protein required for maintenance but not establishment of DNA methylation. EMBO J. 21: 6842-6852.
39. Manning, K., Tör, M., Poole, M., Hong, Y., Thompson, A.J., King, G.J., Giovannoni, J.J., and Seymour, G.B. (2006). A naturally occurring epigenetic mutation in a gene encoding an SBP-box transcription factor inhibits tomato fruit ripening. Nat. Genet. 38: 948-952.
40. Martienssen, R.A., and Colot, V. (2001). DNA methylation and epi-genetic inheritance in plants and filamentous fungi. Science 293: 1070-1074.
41. Messing, J., and Bennetzen, J.L. (2008). Grass genome structure and evolution. Genome Dyn. 4: 41-56.
42. Miki, D., and Shimamoto, K. (2008). De novo DNA methylation induced by siRNA targeted to endogenous transcribed sequences is gene-specific and OsMet1-independent in rice. Plant J. 56: 539-549.
43. Miura, K., Agetsuma, M., Kitano, H., Yoshimura, A., Matsuoka, M., Jacobsen, S.E., and Ashikari, M. (2009b). A metastable DWARF1 epigenetic mutant affecting plant stature in rice. Proc. Natl. Acad. Sci. USA 106: 11218-11223.
44. Miura, A., Nakamura, M., Inagaki, S., Kobayashi, A., Saze, H., and Kakutani, T. (2009a). An Arabidopsis jmjC domain protein protects transcribed genes from DNA methylation at CHG sites. EMBO J. 28: 1078-1086.
45. Moritoh, S., Eun, C.H., Ono, A., Asao, H., Okano, Y., Yamaguchi, K., Shimatani, Z., Koizumi, A., and Terada, R. (2012). Targeted disruption of an orthologue of DOMAINS REARRANGED METHYLASE 2, OsDRM2, impairs the growth of rice plants by abnormal DNA methylation. Plant J. 71: 85-98.
46. Nagaki, K., Cheng, Z., Ouyang, S., Talbert, P.B., Kim, M., Jones, K.M., Henikoff, S., Buell, C.R., and Jiang, J. (2004). Sequencing of a rice centromere uncovers active genes. Nat. Genet. 36: 138-145.
47. Nicol, J.W., Helt, G.A., Blanchard, S.G., JrRaja, A., and Loraine, A.E. (2009). The Integrated Genome Browser: Free software for distribution and exploration of genome-scale datasets. Bio-informatics 25: 2730-2731.
48. Ohad, N., Margossian, L., Hsu, Y.C., Williams, C., Repetti, P., and Fischer, R.L. (1996). A mutation that allows endosperm development without fertilization. Proc. Natl. Acad. Sci. USA 93: 5319-5324.
49. Ohad, N., Yadegari, R., Margossian, L., Hannon, M., Michaeli, D., Harada, J.J., Goldberg, R.B., and Fischer, R.L. (1999). Mutations in FIE, a WD polycomb group gene, allow endosperm development without fertilization. Plant Cell 11: 407-416.
50. Pien, S., and Grossniklaus, U. (2007). Polycomb group and tritho-rax group proteins in Arabidopsis. Biochim. Biophys. Acta 1769: 375-382.
51. Qin, R., Cheng, Z., and Guo, X. (2005). The establishment of mutant pool using anther culture of autotetrapolyploid rice. Acta Agronomica Sinica. 31: 392-394.
52. Rodrigues, J.C., Luo, M., Berger, F., and Koltunow, A.M. (2010). Polycomb group gene function in sexual and asexual seed development in angiosperms. Sex. Plant Reprod. 23: 123-133.
53. 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.
54. Schwartz, Y.B., Kahn, T.G., Nix, D.A., Li, X.Y., Bourgon, R., Biggin, M., and Pirrotta, V. (2006). Genome-wide analysis of Polycomb targets in Drosophila melanogaster. Nat. Genet. 38: 700-705.
55. 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.
56. Spillane, C., Schmid, K.J., Laoueillé-Duprat, S., Pien, S., Escobar-Restrepo, J.M., Baroux, C., Gagliardini, V., Page, D.R., Wolfe, K.H., and Grossniklaus, U. (2007). Positive darwinian selection at the imprinted MEDEA locus in plants. Nature 448: 349-352.
57. Springer, N.M., Danilevskaya, O.N., Hermon, P., Helentjaris, T.G., Phillips, R.L., Kaeppler, H.F., and Kaeppler, S.M. (2002). Sequence relationships, conserved domains, and expression patterns for maize homologs of the polycomb group genes E(z), esc, and E(Pc). Plant Physiol. 128: 1332-1345.
58. Struhl, G. (1981). A gene product required for correct initiation of segmental determination in Drosophila. Nature 293: 36-41.
59. Teerawanichpan, P., Chandrasekharan, M.B., Jiang, Y., Narangajavana, J., and Hall, T.C. (2004). Characterization of two rice DNA methyl-transferase genes and RNAi-mediated reactivation of a silenced trans-gene in rice callus. Planta 218: 337-349.
60. Tolhuis, B., de Wit, E., Muijrers, I., Teunissen, H., Talhout, W., van Steensel, B., and van Lohuizen, M. (2006). Genome-wide profiling of PRC1 and PRC2 Polycomb chromatin binding in Drosophila melanogaster. Nat. Genet. 38: 694-699.
61. Tusher, V.G., Tibshirani, R., and Chu, G. (2001). Significance analysis of microarrays applied to the ionizing radiation response. Proc. Natl. Acad. Sci. USA 98: 5116-5121.
62. Wang, X., Shi, X., Hao, B., Ge, S., and Luo, J. (2005). Duplication and DNA segmental loss in the rice genome: Implications for diploid-ization. New Phytol. 165: 937-946.
63. Weinhofer, I., Hehenberger, E., Roszak, P., Hennig, L., and Köhler, C. (2010). H3K27me3 profiling of the endosperm implies exclusion of polycomb group protein targeting by DNA methylation. PLoS Genet. 6: e1001152.
64. Xu, H., Wei, C.L., Lin, F., and Sung, W.K. (2008). An HMM approach to genome-wide identification of differential histone modification sites from ChIP-seq data. Bioinformatics 24: 2344-2349.
65. Yadegari, R., Kinoshita, T., Lotan, O., Cohen, G., Katz, A., Choi, Y., Katz, A., Nakashima, K., Harada, J.J., Goldberg, R.B., Fischer, R.L., and Ohad, N. (2000). Mutations in the FIE and MEA genes that encode interacting polycomb proteins cause parent-of-origin effects on seed development by distinct mechanisms. Plant Cell 12: 2367-2382.
66. Yan, H., and Jiang, J. (2007). Rice as a model for centromere and heterochromatin research. Chromosome Res. 15: 77-84.
67. Zhang, X., Clarenz, O., Cokus, S., Bernatavichute, Y.V., Pellegrini, M., Goodrich, J., and Jacobsen, S.E. (2007). Whole-genome analysis of histone H3 lysine 27 trimethylation in Arabidopsis. PLoS Biol. 5: e129.
68. Zhang, X., Yazaki, J., Sundaresan, A., Cokus, S., Chan, S.W., Chen, H., Henderson, I.R., Shinn, P., Pellegrini, M., Jacobsen, S.E., and Ecker, J.R. (2006). Genome-wide high-resolution mapping and functional analysis of DNA methylation in Arabidopsis. Cell 126: 1189-1201.
69. Zhang, Y., Liu, T., Meyer, C.A., Eeckhoute, J., Johnson, D.S., Bernstein, B.E., Nusbaum, C., Myers, R.M., Brown, M., Li, W., and Liu, X.S. (2008). Model-based analysis of ChIP-Seq (MACS). Genome Biol. 9: R137.