Histone lysine methyltransferase SDG8 is involved in brassinosteroid- regulated gene expression in Arabidopsis thaliana

Molecular Plant

Volumn 7, Issue 8, 2014, Pages 1303-1315

  Wang, Xiaolei ^a,b   Chen, Jiani ^b   Xie, Zhouli ^b   Liu, Sanzhen ^b,c   Nolan, Trevor ^b   Ye, Huaxun ^b,d   Zhang, Mingcai ^a   Guo, Hongqing ^b   Schnable, Patrick S ^b,e   Li, Zhaohu ^a   Yin, Yanhai ^b  

^a CHINA AGRICULTURAL UNIVERSITY   (China)

^b IOWA STATE UNIVERSITY   (United States)

^c KANSAS STATE UNIVERSITY   (United States)

^d Pioneer Dupont   (United States)

^e Data2Bio LLC   (United States)

Author keywords

Brassinosteroid; gene regulation; histone modifications

Indexed keywords

ARABIDOPSIS PROTEIN; BES1 PROTEIN, ARABIDOPSIS; BRASSINOSTEROID; HISTONE; HISTONE LYSINE METHYLTRANSFERASE; IWS1 PROTEIN, ARABIDOPSIS; LAZ2 PROTEIN, ARABIDOPSIS; LYSINE; NUCLEAR PROTEIN; TRANSCRIPTION FACTOR;

ARABIDOPSIS; CHEMISTRY; CYTOLOGY; DEFICIENCY; GENE EXPRESSION REGULATION; GENE INACTIVATION; GENETICS; GENOMICS; METABOLISM; METHYLATION; MUTATION; PHENOTYPE; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; BRASSINOSTEROIDS; GENE EXPRESSION REGULATION, PLANT; GENE KNOCKOUT TECHNIQUES; GENOMICS; HISTONE-LYSINE N-METHYLTRANSFERASE; HISTONES; LYSINE; METHYLATION; MUTATION; NUCLEAR PROTEINS; PHENOTYPE; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS;

EID: 84906251511     PISSN: 16742052     EISSN: 17529867     Source Type: Journal    
DOI: 10.1093/mp/ssu056     Document Type: Article

References (85)

1. Alonso, J.M., et al. (2003). Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science. 301, 653-657.
2. Asami, T., and Yoshida, S. (1999). Brassinosteroid biosynthesis inhibitors. Trends Plant Sci. 4, 348-353.
3. Benjamini, Y., and Hochberg, Y. (1995). Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. Roy. Statist. Soc. Ser. B. 57, 289-300.
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. Bullard, J.H., Purdom, E., Hansen, K.D., and Dudoit, S. (2010). Evaluation of statistical methods for normalization and differential expression in mRNA-Seq experiments. BMC Bioinformatics. 11, 94.
6. Cazzonelli, C.I., Roberts, A.C., Carmody, M.E., and Pogson, B.J. (2009). Regulation of carotenoid composition and shoot branching in Arabidopsis by a chromatin modifying histone methyltransferase, SDG8. Plant Cell. 21, 39-53.
7. Cazzonelli, C.I., Roberts, A.C., Carmody, M.E., and Pogson, B.J. (2010). Transcriptional control of SET DOMAIN GROUP 8 and CAROTENOID ISOMERASE during Arabidopsis development. Mol. Plant. 3, 174-191.
8. Choe, S., Schmitz, R.J., Fujioka, S., Takatsuto, S., Lee, M.O., Yoshida, S., Feldmann, K.A., and Tax, F.E. (2002). Arabidopsis brassinosteroid- insensitive dwarf12 mutants are semidominant and defective in a glycogen synthase kinase 3beta-like kinase. Plant Physiol. 130, 1506-1515.
9. Clouse, S.D. (2011). Brassinosteroid signal transduction: from receptor kinase activation to transcriptional networks regulating plant development. Plant Cell. 23, 1219-1230.
10. Darley, C.P., Forrester, A.M., and McQueen-Mason, S.J. (2001). The molecular basis of plant cell wall extension. Plant Mol. Biol. 47, 179-195.
11. Di Rubbo, S., Irani, N.G., and Russinova, E. (2011). PP2A phosphatases: the 'on-off' regulatory switches of brassinosteroid signaling. Sci. Signal. 4, pe25.
12. Divi, U.K., and Krishna, P. (2009). Brassinosteroid: a biotechnological target for enhancing crop yield and stress tolerance. N. Biotechnol. 26, 131-136.
13. Dong, G., and Li, J. (2013). MicroRNAs profiling reveals a potential link between the SDG8 methyltransferase and brassinosteroid- regulated gene expression in Arabidopsis. J. Data Mining Genomics Proteomics. 4, e110.
14. Dong, G., Ma, D.P., and Li, J. (2008). The histone methyltransferase SDG8 regulates shoot branching in Arabidopsis. Biochem. Biophys. Res. Commun. 373, 659-664.
15. Fischbeck, J.A., Kraemer, S.M., and Stargell, L.A. (2002). SPN1, a conserved gene identified by suppression of a postrecruitmentdefective yeast TATA-binding protein mutant. Genetics. 162, 1605-1616.
16. Gou, X., Yin, H., He, K., Du, J., Yi, J., Xu, S., Lin, H., Clouse, S.D., and Li, J. (2012). Genetic evidence for an indispensable role of somatic embryogenesis receptor kinases in brassinosteroid signaling. PLoS Genet. 8, e1002452.
17. Grini, P.E., Thorstensen, T., Alm, V., Vizcay-Barrena, G., Windju, S.S., Jorstad, T.S., Wilson, Z.A., and Aalen, R.B. (2009). The ASH1 HOMOLOG 2 (ASHH2) histone H3 methyltransferase is required for ovule and anther development in Arabidopsis. PLoS One. 4, e7817.
18. Guo, H., Li, L., Aluru, M., Aluru, S., and Yin, Y. (2013). Mechanisms and networks for brassinosteroid regulated gene expression. Curr. Opin. Plant Biol. 16, 545-553.
19. Hao, J., Yin, Y., and Fei, S.Z. (2013). Brassinosteroid signaling network: implications on yield and stress tolerance. Plant Cell Rep. 32, 1017-1030.
20. He, F., et al. (2010). Structural insight into the zinc finger CW domain as a histone modification reader. Structure. 18, 1127-1139.
21. He, J.X., Gendron, J.M., Yang, Y., Li, J., and Wang, Z.Y. (2005). BZR1 is a transcriptional repressor with dual roles in brassinosteroid homeostasis and growth responses. Science. 307, 1634-1638.
22. He, J.X., Gendron, J.M., Yang, Y., Li, J., and Wang, Z.Y. (2002). The GSK3-like kinase BIN2 phosphorylates and destabilizes BZR1, a positive regulator of the brassinosteroid signaling pathway in Arabidopsis. Proc. Natl Acad. Sci. U S A. 99, 10185-10190.
23. Hoppmann, V., Thorstensen, T., Kristiansen, P.E., Veiseth, S.V., Rahman, M.A., Finne, K., Aalen, R.B., and Aasland, R. (2011). The CW domain, a new histone recognition module in chromatin proteins. EMBO J. 30, 1939-1952.
24. Hothorn, M., Belkhadir, Y., Dreux, M., Dabi, T., Noel, J.P., Wilson, I.A., and Chory, J. (2011). Structural basis of steroid hormone perception by the receptor kinase BRI1. Nature. 474, 467-471.
25. Jaillais, Y., Hothorn, M., Belkhadir, Y., Dabi, T., Nimchuk, Z.L., Meyerowitz, E.M., and Chory, J. (2011). Tyrosine phosphorylation controls brassinosteroid receptor activation by triggering membrane release of its kinase inhibitor. Genes Dev. 25, 232-237.
26. Jenuwein, T., and Allis, C.D. (2001). Translating the histone code. Science. 293, 1074-1080.
27. Kim, S.Y., He, Y., Jacob, Y., Noh, Y.S., Michaels, S., and Amasino, R. (2005). Establishment of the vernalization-responsive, winter- annual habit in Arabidopsis requires a putative histone H3 methyl transferase. Plant Cell. 17, 3301-3310.
28. Kim, T.W., and Wang, Z.Y. (2010). Brassinosteroid signal transduction from receptor kinases to transcription factors. Annu. Rev. Plant Biol. 61, 681-704.
29. Kim, T.W., Guan, S., Burlingame, A.L., and Wang, Z.Y. (2011). The CDG1 kinase mediates brassinosteroid signal transduction from BRI1 receptor kinase to BSU1 phosphatase and GSK3-like kinase BIN2. Mol. Cell. 43, 561-571.
30. Kim, T.W., Guan, S., Sun, Y., Deng, Z., Tang, W., Shang, J.X., Burlingame, A.L., and Wang, Z.Y. (2009). Brassinosteroid signal transduction from cell-surface receptor kinases to nuclear transcription factors. Nat. Cell Biol. 11, 1254-1260.
31. Klose, R.J., and Zhang, Y. (2007). Regulation of histone methylation by demethylimination and demethylation. Nat. Rev. Mol. Cell Biol. 8, 307-318.
32. Krogan, N.J., Kim, M., Ahn, S.H., Zhong, G., Kobor, M.S., Cagney, G., Emili, A., Shilatifard, A., Buratowski, S., and Greenblatt, J.F. (2002). RNA polymerase II elongation factors of Saccharomyces cerevisiae: a targeted proteomics approach. Mol. Cell Biol. 22, 6979-6992.
33. Li, B., Carey, M., and Workman, J.L. (2007a). The role of chromatin during transcription. Cell. 128, 707-719.
34. Li, B., Gogol, M., Carey, M., Lee, D., Seidel, C., and Workman, J.L. (2007b). Combined action of PHD and chromo domains directs the Rpd3S HDAC to transcribed chromatin. Science. 316, 1050-1054.
35. Li, J. (2010). Regulation of the nuclear activities of brassinosteroid signaling. Curr. Opin. Plant Biol. 13, 540-547.
36. Li, J., and Chory, J. (1997). A putative leucine-rich repeat receptor kinase involved in brassinosteroid signal transduction. Cell. 90, 929-938.
37. Li, J., and Nam, K.H. (2002). Regulation of brassinosteroid signaling by a GSK3/SHAGGY-like kinase. Science. 295, 1299-1301.
38. Li, J., Wen, J., Lease, K.A., Doke, J.T., Tax, F.E., and Walker, J.C. (2002). BAK1, an Arabidopsis LRR receptor-like protein kinase, interacts with BRI1 and modulates brassinosteroid signaling. Cell. 110, 213-222.
39. Li, L., Ye, H., Guo, H., and Yin, Y. (2010). Arabidopsis IWS1 interacts with transcription factor BES1 and is involved in plant steroid hormone brassinosteroid regulated gene expression. Proc. Natl Acad. Sci. U S A. 107, 3918-3923.
40. Lindstrom, D.L., Squazzo, S.L., Muster, N., Burckin, T.A., Wachter, K.C., Emigh, C.A., McCleery, J.A., Yates, J.R., 3rd, and Hartzog, G.A. (2003). Dual roles for Spt5 in pre-mRNA processing and transcription elongation revealed by identification of Spt5- associated proteins. Mol. Cell Biol. 23, 1368-1378.
41. Ling, Y., Smith, A.J., and Morgan, G.T. (2006). A sequence motif conserved in diverse nuclear proteins identifies a protein interaction domain utilised for nuclear targeting by human TFIIS. Nucleic Acids Res. 34, 2219-2229.
42. 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.
43. Mayer, A., Lidschreiber, M., Siebert, M., Leike, K., Soding, J., and Cramer, P. (2010). Uniform transitions of the general RNA polymerase II transcription complex. Nat. Struct. Mol. Biol. 17, 1272-1278.
44. Mora-Garcia, S., Vert, G., Yin, Y., Cano-Delgado, A., Cheong, H., and Chory, J. (2004). Nuclear protein phosphatases with Kelchrepeat domains modulate the response to brassinosteroids in Arabidopsis. Genes Dev. 18, 448-460.
45. Nam, K.H., and Li, J. (2002). BRI1/BAK1, a receptor kinase pair mediating brassinosteroid signaling. Cell. 110, 203-212.
46. Nettleton, D., Hwang, J.T.G., Caldo, R.A., and Wise, R.P. (2006). Estimating the number of true null hypotheses from a histogram of p-values. J. Agricultural, Biological, and Environmental Statistics. 11, 337-356.
47. 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.
48. Oh, M.H., Wang, X., Clouse, S.D., and Huber, S.C. (2012). Deactivation of the Arabidopsis BRASSINOSTEROID INSENSITIVE 1 (BRI1) receptor kinase by autophosphorylation within the glycine- rich loop. Proc. Natl Acad. Sci. U S A. 109, 327-332.
49. Oh, M.H., Wang, X., Kota, U., Goshe, M.B., Clouse, S.D., and Huber, S.C. (2009). Tyrosine phosphorylation of the BRI1 receptor kinase emerges as a component of brassinosteroid signaling in Arabidopsis. Proc. Natl Acad. Sci. U S A. 106, 658-663.
50. Palma, K., Thorgrimsen, S., Malinovsky, F.G., Fiil, B.K., Nielsen, H.B., Brodersen, P., Hofius, D., Petersen, M., and Mundy, J. (2010). Autoimmunity in Arabidopsis acd11 is mediated by epigenetic regulation of an immune receptor. PLoS Pathog. 6, e1001137.
51. Perez-Perez, J.M., Ponce, M.R., and Micol, J.L. (2002). The UCU1 Arabidopsis gene encodes a SHAGGY/GSK3-like kinase required for cell expansion along the proximodistal axis. Dev. Biol. 242, 161-173.
52. Pokholok, D.K., et al. (2005). Genome-wide map of nucleosome acetylation and methylation in yeast. Cell. 122, 517-527.
53. Roudier, F., et al. (2011). Integrative epigenomic mapping defines four main chromatin states in Arabidopsis. EMBO J. 30, 1928-1938.
54. Russinova, E., et al. (2004). Heterodimerization and endocytosis of Arabidopsis brassinosteroid receptors BRI1 and AtSERK3 (BAK1). Plant Cell. 16, 3216-3229.
55. Ryu, H., Cho, H., Kim, K., and Hwang, I. (2010a). Phosphorylation dependent nucleocytoplasmic shuttling of BES1 is a key regulatory event in brassinosteroid signaling. Mol. Cells. 29, 283-290.
56. Ryu, H., Kim, K., Cho, H., and Hwang, I. (2010b). Predominant actions of cytosolic BSU1 and nuclear BIN2 regulate subcellular localization of BES1 in brassinosteroid signaling. Mol. Cells. 29, 291-296.
57. Shafiq, S., Berr, A., and Shen, W.H. (2014). Combinatorial functions of diverse histone methylations in Arabidopsis thaliana flowering time regulation. New Phytol. 201, 312-322.
58. She, J., Han, Z., Kim, T.W., Wang, J., Cheng, W., Chang, J., Shi, S., Yang, M., Wang, Z.Y., and Chai, J. (2011). Structural insight into brassinosteroid perception by BRI1. Nature. 474, 472-476.
59. Sui, P., Jin, J., Ye, S., Mu, C., Gao, J., Feng, H., Shen, W.H., Yu, Y., and Dong, A. (2012). H3K36 methylation is critical for brassinosteroid- regulated plant growth and development in rice. Plant J. 70, 340-347.
60. Sui, P., Shi, J., Gao, X., Shen, W.H., and Dong, A. (2013). H3K36 methylation is involved in promoting rice flowering. Mol. Plant. 6, 975-977.
61. Sun, Y., et al. (2010). Integration of brassinosteroid signal transduction with the transcription network for plant growth regulation in Arabidopsis. Dev. Cell. 19, 765-777.
62. Tang, W., Kim, T.W., Oses-Prieto, J.A., Sun, Y., Deng, Z., Zhu, S., Wang, R., Burlingame, A.L., and Wang, Z.Y. (2008). BSKs mediate signal transduction from the receptor kinase BRI1 in Arabidopsis. Science. 321, 557-560.
63. Tang, W., et al. (2011). PP2A activates brassinosteroid-responsive gene expression and plant growth by dephosphorylating BZR1. Nat. Cell Biol. 13, 124-131.
64. Tang, X., et al. (2012). Synergistic repression of the embryonic programme by SET DOMAIN GROUP 8 and EMBRYONIC FLOWER 2 in Arabidopsis seedlings. J. Exp. Bot . 63, 1391-1404.
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. Voinnet, O., Rivas, S., Mestre, P., and Baulcombe, D. (2003). An enhanced transient expression system in plants based on suppression of gene silencing by the p19 protein of tomato bushy stunt virus. Plant J. 33, 949-956.
67. Wang, H., Yang, C., Zhang, C., Wang, N., Lu, D., Wang, J., Zhang, S., Wang, Z.X., Ma, H., and Wang, X. (2011). Dual role of BKI1 and 14-3-3 s in brassinosteroid signaling to link receptor with transcription factors. Dev. Cell. 21, 825-834.
68. Wang, X., and Chory, J. (2006). Brassinosteroids regulate dissociation of BKI1, a negative regulator of BRI1 signaling, from the plasma membrane. Science. 313, 1118-1122.
69. Wang, X., Goshe, M.B., Soderblom, E.J., Phinney, B.S., Kuchar, J.A., Li, J., Asami, T., Yoshida, S., Huber, S.C., and Clouse, S.D. (2005). Identification and functional analysis of in vivo phosphorylation sites of the Arabidopsis BRASSINOSTEROID-INSENSITIVE1 receptor kinase. Plant Cell. 17, 1685-1703.
70. Wang, X., Kota, U., He, K., Blackburn, K., Li, J., Goshe, M.B., Huber, S.C., and Clouse, S.D. (2008). Sequential transphosphorylationof the BRI1/BAK1 receptor kinase complex impacts early events in brassinosteroid signaling. Dev. Cell. 15, 220-235.
71. Wu, G., Wang, X., Li, X., Kamiya, Y., Otegui, M.S., and Chory, J. (2011). Methylation of a phosphatase specifies dephosphorylation and degradation of activated brassinosteroid receptors. Sci. Signal. 4, ra29.
72. Wu, T.D., and Nacu, S. (2010). Fast and SNP-tolerant detection of complex variants and splicing in short reads. Bioinformatics. 26, 873-881.
73. Xu, L., Zhao, Z., Dong, A., Soubigou-Taconnat, L., Renou, J.P., Steinmetz, A., and Shen, W.H. (2008). Di- and tri- but not monomethylation on histone H3 lysine 36 marks active transcription of genes involved in flowering time regulation and other processes in Arabidopsis thaliana. Mol. Cell Biol. 28, 1348-1360.
74. Yang, C.J., Zhang, C., Lu, Y.N., Jin, J.Q., and Wang, X.L. (2011). The mechanisms of brassinosteroids' action: from signal transduction to plant development. Mol. Plant. 4, 588-600.
75. Yin, Y., Vafeados, D., Tao, Y., Yoshida, S., Asami, T., and Chory, J. (2005). A new class of transcription factors mediates brassinosteroid- regulated gene expression in Arabidopsis. Cell. 120, 249-259.
76. Yin, Y., Wang, Z.Y., Mora-Garcia, S., Li, J., Yoshida, S., Asami, T., and Chory, J. (2002). BES1 accumulates in the nucleus in response to brassinosteroids to regulate gene expression and promote stem elongation. Cell. 109, 181-191.
77. Yoh, S.M., Cho, H., Pickle, L., Evans, R.M., and Jones, K.A. (2007). The Spt6 SH2 domain binds Ser2-P RNAPII to direct Iws1-dependent mRNA splicing and export. Genes Dev. 21, 160-174.
78. Yoh, S.M., Lucas, J.S., and Jones, K.A. (2008). The Iws1:Spt6:CTD complex controls cotranscriptional mRNA biosynthesis and HYPB/Setd2- mediated histone H3K36 methylation. Genes Dev. 22, 3422-3434.
79. Yu, X., Li, L., Guo, M., Chory, J., and Yin, Y. (2008). Modulation of brassinosteroid-regulated gene expression by Jumonji domaincontaining proteins ELF6 and REF6 in Arabidopsis. Proc. Natl Acad. Sci. U S A. 105, 7618-7623.
80. Yu, X., Li, L., Zola, J., Aluru, M., Ye, H., Foudree, A., Guo, H., Anderson, S., Aluru, S., Liu, P., Rodermel, S., and Yin, Y. (2011). A brassinosteroid transcriptional network revealed by genomewide identification of BESI target genes in Arabidopsis thaliana. Plant J. 65, 634-646.
81. Zhang, L., Fletcher, A.G., Cheung, V., Winston, F., and Stargell, L.A. (2008). Spn1 regulates the recruitment of Spt6 and the Swi/Snf complex during transcriptional activation by RNA polymerase II. Mol. Cell Biol. 28, 1393-1403.
82. Zhang, X., Germann, S., Blus, B.J., Khorasanizadeh, S., Gaudin, V., and Jacobsen, S.E. (2007). The Arabidopsis LHP1 protein colocalizes with histone H3 Lys27 trimethylation. Nat. Struct. Mol. Biol. 14, 869-871.
83. Zhao, J., Peng, P., Schmitz, R.J., Decker, A.D., Tax, F.E., and Li, J. (2002). Two putative BIN2 substrates are nuclear components of brassinosteroid signaling. Plant Physiol. 130, 1221-1229.
84. Zhao, Z., Yu, Y., Meyer, D., Wu, C., and Shen, W.H. (2005). Prevention of early flowering by expression of FLOWERING LOCUS C requires methylation of histone H3 K36. Nat. Cell Biol. 7, 1256-1260.
85. Zhu, J.Y., Sae-Seaw, J., and Wang, Z.Y. (2013). Brassinosteroid signalling. Development. 140, 1615-1620.