Jumonji C domain protein JMJ705-mediated removal of histone H3 lysine 27 trimethylation is involved in defense-related gene activation in rice

Plant Cell

Volumn 25, Issue 11, 2013, Pages 4725-4736

  Li, Tiantian ^a   Chen, Xiangsong ^a   Zhong, Xiaochao ^a   Zhao, Yu ^a   Liu, Xiaoyun ^a   Zhou, Shaoli ^a   Cheng, Saifeng ^a   Zhou, Dao Xiu ^a,b  

^a HUAZHONG AGRICULTURAL UNIVERSITY   (China)

^b INSTITUT D'OPTIQUE GRADUATE SCHOOL   (France)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE; HISTONE DEMETHYLASE; LYSINE;

ARTICLE; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; METHYLATION; MICROBIOLOGY; PATHOGENICITY; RICE; TRANSGENIC PLANT; XANTHOMONAS;

GENE EXPRESSION REGULATION, PLANT; HISTONES; JUMONJI DOMAIN-CONTAINING HISTONE DEMETHYLASES; LYSINE; METHYLATION; ORYZA SATIVA; PLANTS, GENETICALLY MODIFIED; XANTHOMONAS;

EID: 84891524616     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.113.118802     Document Type: Article

References (54)

1. Alvarez-Venegas, R., Abdallat, A.A., Guo, M., Alfano, J.R., and Avramova, Z. (2007). Epigenetic control of a transcription factor at the cross section of two antagonistic pathways. Epigenetics 2: 106-113.
2. Alvarez-Venegas, R., and Avramova, Z. (2005). Methylation patterns of histone H3 Lys 4, Lys 9 and Lys 27 in transcriptionally active and inactive Arabidopsis genes and in atx1 mutants. Nucleic Acids Res. 33: 5199-5207.
3. Berger, S.L. (2007). The complex language of chromatin regulation during transcription. Nature 447: 407-412.
4. Berr, A., McCallum, E.J., Alioua, A., Heintz, D., Heitz, T., and Shen, W.H. (2010). Arabidopsis histone methyltransferase SET DOMAIN GROUP8 mediates induction of the jasmonate/ethylene pathway genes in plant defense response to necrotrophic fungi. Plant Physiol. 154: 1403-1414.
5. Berr, A., Ménard, R., Heitz, T., and Shen, W.H. (2012). Chromatin modification and remodelling: A regulatory landscape for the control of Arabidopsis defence responses upon pathogen attack. Cell. Microbiol. 14: 829-839.
6. Berr, A., Shafiq, S., and Shen, W.H. (2011). Histone modifications in transcriptional activation during plant development. Biochim. Biophys. Acta 1809: 567-576.
7. Bonasio, R., Tu, S., and Reinberg, D. (2010). Molecular signals of epigenetic states. Science 330: 612-616.
8. Chen, H., Wang, S., and Zhang, Q. (2002). New gene for bacterial blight resistance in rice located on chromosome 12 identified from minghui 63, an elite restorer line. Phytopathology 92: 750-754.
9. Chen, Q., Chen, X., Wang, Q., Zhang, F., Lou, Z., Zhang, Q., and Zhou, D.X. (2013). Structural basis of a histone H3 lysine 4 demethylase required for stem elongation in rice. PLoS Genet. 9: e1003239.
10. Chittoor, J.M., Leach, J.E., and White, F.F. (1997). Differential induction of a peroxidase gene family during infection of rice by Xanthomonas oryzae pv. oryzae. Mol. Plant Microbe Interact. 10: 861-871.
11. Choi, S.M., Song, H.R., Han, S.K., Han, M., Kim, C.Y., Park, J., Lee, Y.H., Jeon, J.S., Noh, Y.S., and Noh, B. (2012). HDA19 is required for the repression of salicylic acid biosynthesis and salicylic acidmediated defense responses in Arabidopsis. Plant J. 71: 135-146.
12. Cui, X., Jin, P., Cui, X., Gu, L., Lu, Z., Xue, Y., Wei, L., Qi, J., Song, X., Luo, M., An, G., and Cao, X. (2013). Control of transposon activity by a histone H3K4 demethylase in rice. Proc. Natl. Acad. Sci. USA 110: 1953-1958.
13. Deleris, A., Greenberg, M.V., Ausin, I., Law, R.W., Moissiard, G., Schubert, D., and Jacobsen, S.E. (2010). Involvement of a Jumonji-C domain-containing histone demethylase in DRM2-mediated maintenance of DNA methylation. EMBO Rep. 11: 950-955.
14. Ding, B., Bellizzi, del M.R., Ning, Y., Meyers, B.C., and Wang, G.L. (2012). HDT701, a histone H4 deacetylase, negatively regulates plant innate immunity by modulating histone H4 acetylation of defense-related genes in rice. Plant Cell 24: 3783-3794.
15. Ding, Y., Avramova, Z., and Fromm, M. (2011). The Arabidopsis trithoraxlike factor ATX1 functions in dehydration stress responses via ABAdependent and ABA-independent pathways. Plant J. 66: 735-744.
16. He, G., et al. (2010). Global epigenetic and transcriptional trends among two rice subspecies and their reciprocal hybrids. Plant Cell 22: 17-33.
17. Hu, Y., Liu, D., Zhong, X., Zhang, C., Zhang, Q., and Zhou, D.X. (2012). CHD3 protein recognizes and regulates methylated histone H3 lysines 4 and 27 over a subset of targets in the rice genome. Proc. Natl. Acad. Sci. USA 109: 5773-5778.
18. Huang, L., Sun, Q., Qin, F., Li, C., Zhao, Y., and Zhou, D.X. (2007). Downregulation of a SILENT INFORMATION REGULATOR2-related histone deacetylase gene, OsSRT1, induces DNA fragmentation and cell death in rice. Plant Physiol. 144: 1508-1519.
19. Jaskiewicz, M., Conrath, U., and Peterhänsel, C. (2011). Chromatin modification acts as a memory for systemic acquired resistance in the plant stress response. EMBO Rep. 12: 50-55.
20. Kim, D.H., Zografos, B.R., and Sung, S. (2010). Vernalization-mediated VIN3 induction overcomes the LIKE-HETEROCHROMATIN PROTEIN1/ H3K27me3 Removal in Disease Resistance 4735 POLYCOMB REPRESSION COMPLEX2-mediated epigenetic repression. Plant Physiol. 154: 949-957.
21. Kim, J.M., To, T.K., Ishida, J., Morosawa, T., Kawashima, M., Matsui, A., Toyoda, T., Kimura, H., Shinozaki, K., and Seki, M. (2008a). Alterations of lysine modifications on the histone H3 N-tail under drought stress conditions in Arabidopsis thaliana. Plant Cell Physiol. 49: 1580-1588.
22. Kim, K.C., Lai, Z., Fan, B., and Chen, Z. (2008b). Arabidopsis WRKY38 and WRKY62 transcription factors interact with histone deacetylase 19 in basal defense. Plant Cell 20: 2357-2371.
23. Kwon, C.S., Lee, D., Choi, G., and Chung, W.I. (2009). Histone occupancy-dependent and-independent removal of H3K27 trimethylation at cold-responsive genes in Arabidopsis. Plant J. 60: 112-121.
24. Lee, M.W., Qi, M., and Yang, Y. (2001). A novel jasmonic acidinducible rice myb gene associates with fungal infection and host cell death. Mol. Plant Microbe Interact. 14: 527-535.
25. 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.
26. Liu, C., Lu, F., Cui, X., and Cao, X. (2010). Histone methylation in higher plants. Annu. Rev. Plant Biol. 61: 395-420.
27. Lorrain, S., Vailleau, F., Balagué, C., and Roby, D. (2003). Lesion mimic mutants: Keys for deciphering cell death and defense pathways in plants? Trends Plant Sci. 8: 263-271.
28. Lu, F., Cui, X., Zhang, S., Jenuwein, T., and Cao, X. (2011). Arabidopsis REF6 is a histone H3 lysine 27 demethylase. Nat. Genet. 43: 715-719.
29. Lu, F., Cui, X., Zhang, S., Liu, C., and Cao, X. (2010). JMJ14 is an H3K4 demethylase regulating flowering time in Arabidopsis. Cell Res. 20: 387-390.
30. Mosammaparast, N., and Shi, Y. (2010). Reversal of histone methylation: Biochemical and molecular mechanisms of histone demethylases. Annu. Rev. Biochem. 79: 155-179.
31. Mosher, R.A., Durrant, W.E., Wang, D., Song, J., and Dong, X. (2006). A comprehensive structure-function analysis of Arabidopsis SNI1 defines essential regions and transcriptional repressor activity. Plant Cell 18: 1750-1765.
32. Muramoto, T., Müller, I., Thomas, G., Melvin, A., and Chubb, J.R. (2010). Methylation of H3K4 is required for inheritance of active transcriptional states. Curr. Biol. 20: 397-406.
33. Noh, B., Lee, S.H., Kim, H.J., Yi, G., Shin, E.A., Lee, M., Jung, K.J., Doyle, M.R., Amasino, R.M., and Noh, Y.S. (2004). Divergent roles of a pair of homologous jumonji/zinc-finger-class transcription factor proteins in the regulation of Arabidopsis flowering time. Plant Cell 16: 2601-2613.
34. Pien, S., and Grossniklaus, U. (2007). Polycomb group and trithorax group proteins in Arabidopsis. Biochim. Biophys. Acta 1769: 375-382.
35. Roudier, F., et al. (2011). Integrative epigenomic mapping defines four main chromatin states in Arabidopsis. EMBO J. 30: 1928-1938.
36. Searle, I.R., Pontes, O., Melnyk, C.W., Smith, L.M., and Baulcombe, D.C. (2010). 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.
37. Shi, X., et al. (2006). ING2 PHD domain links histone H3 lysine 4 methylation to active gene repression. Nature 442: 96-99.
38. Shi, Y., Lan, F., Matson, C., Mulligan, P., Whetstine, J.R., Cole, P.A., Casero, R.A., and Shi, Y. (2004). Histone demethylation mediated by the nuclear amine oxidase homolog LSD1. Cell 119: 941-953.
39. Shin, S., and Janknecht, R. (2007). Diversity within the JMJD2 histone demethylase family. Biochem. Biophys. Res. Commun. 353: 973-977.
40. Sun, B., Xu, Y., Ng, K.H., and Ito, T. (2009). A timing mechanism for stem cell maintenance and differentiation in the Arabidopsis floral meristem. Genes Dev. 23: 1791-1804.
41. Sun, Q., and Zhou, D.X. (2008). Rice jmjC domain-containing gene JMJ706 encodes H3K9 demethylase required for floral organ development. Proc. Natl. Acad. Sci. USA 105: 13679-13684.
42. Tian, L., Fong, M.P., Wang, J.J., Wei, N.E., Jiang, H., Doerge, R.W., and Chen, Z.J. (2005). Reversible histone acetylation and deacetylation mediate genome-wide, promoter-dependent and locus-specific changes in gene expression during plant development. Genetics 169: 337-345.
43. Tsukada, Y., Fang, J., Erdjument-Bromage, H., Warren, M.E., Borchers, C.H., Tempst, P., and Zhang, Y. (2006). Histone demethylation by a family of JmjC domain-containing proteins. Nature 439: 811-816.
44. 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 genesmarked by trimethylation of histone H3 lysine 27. PLoS Genet. 3: e86.
45. van Dijk, K., Ding, Y., Malkaram, S., Riethoven, J.J., Liu, R., Yang, J., Laczko, P., Chen, H., Xia, Y., Ladunga, I., Avramova, Z., and Fromm, M. (2010). Dynamic changes in genome-wide histone H3 lysine 4 methylation patterns in response to dehydration stress in Arabidopsis thaliana. BMC Plant Biol. 10: 238.
46. van Loon, L.C., Rep, M., and Pieterse, C.M. (2006). Significance of inducible defense-related proteins in infected plants. Annu. Rev. Phytopathol. 44: 135-162.
47. Vermeulen, M., Mulder, K.W., Denissov, S., Pijnappel, W.W., van Schaik, F.M., Varier, R.A., Baltissen, M.P., Stunnenberg, H.G., Mann, M., and Timmers, H.T. (2007). Selective anchoring of TFIID to nucleosomes by trimethylation of histone H3 lysine 4. Cell 131: 58-69.
48. Whetstine, J.R., Nottke, A., Lan, F., Huarte, M., Smolikov, S., Chen, Z., Spooner, E., Li, E., Zhang, G., Colaiacovo, M., and Shi, Y. (2006). Reversal of histone lysine trimethylation by the JMJD2 family of histone demethylases. Cell 125: 467-481.
49. Wu, K., Zhang, L., Zhou, C., Yu, C.W., and Chaikam, V. (2008). HDA6 is required for jasmonate response, senescence and flowering in Arabidopsis. J. Exp. Bot. 59: 225-234.
50. Yang, H., et al. (2012a). A companion cell-dominant and developmentally regulated H3K4 demethylase controls flowering time in Arabidopsis via the repression of FLC expression. PLoS Genet. 8: e1002664.
51. Yang, H., Mo, H., Fan, D., Cao, Y., Cui, S., and Ma, L. (2012b). Overexpression of a histone H3K4 demethylase, JMJ15, accelerates flowering time in Arabidopsis. Plant Cell Rep. 31: 1297-1308.
52. 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.
53. Zheng, B., and Chen, X. (2011). Dynamics of histone H3 lysine 27 trimethylation in plant development. Curr. Opin. Plant Biol. 14: 123-129.
54. Zhou, C., Zhang, L., Duan, J., Miki, B., and Wu, K. (2005). HISTONE DEACETYLASE19 is involved in jasmonic acid and ethylene signaling of pathogen response in Arabidopsis. Plant Cell 17: 1196-1204.