Abstract
Histone modifications are known to play important roles in plant development through epigenetic regulation of gene expression. How these modifications regulate downstream targets in response to various environmental cues and developmental stimuli is still largely unknown. Here, we provide evidence that Arabidopsis histone H3K4 methyltransferase SET DOMAIN GROUP2 (SDG2) is required for full activation of hormone responsive genes upon hormone treatment. The pleiotropic phenotypes of sdg2 were closely related to those of auxin deficient mutants and RNA analysis revealed that expression of early hormone responsive genes was significantly reduced in sdg2-5. By ChIP analyses we found that H3K4 tri-methylations on chromatin region of hormone responsive genes such as SAUR27, KIN1 and GASA6 were enriched in WT upon hormone treatments whereas these enrichments were largely abolished in sdg2-5. After hormone treatment, chromatin regions of responsive genes that accumulated H3K4me3 in WT overlapped with those displaying decreased H3K4me3 levels in sdg2-5. Histone H3K4 di-methylation levels on tested genes were increased rather than decreased in sdg2-5, suggesting that SDG2 mediates transition of H3K4me2 to H3K4me3. Taken together, we conclude that the SDG2 activity is required to regulate the expression of hormone responsive genes via histone H3K4 tri-methylation.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Alvarez-Venegas R, Abdallat AA, Guo M, Alfano JR, Avramova Avramova Z (2007) Epigenetic control of a transcription factor at the cross section of two antagonistic pathways. Epigenetics 2:106–113
Alvarez-Venegas R, Avramova Z (2001) Two Arabidopsis homologs of the animal trithorax genes, a new structural domain is a signature feature of the trithorax gene family. Gene 271:215–221
Alvarez-Venegas R, Avramova Z (2002) SET-domain proteins of the Su(var) 3–9, E(z) and trithorax families. Gene 285:25–37
Alvarez-Venegas R, 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
Alvarez-Venegas R, Pien S, Sadder M, Witmer X, Grossniklaus U, Avramova Z (2003) ATX-1, an Arabidopsis Homolog of Trithorax, Activates Flower Homeotic Genes. Curr Biol 13:627–637
Anzola JM, Sieberer T, Ortbauer M, Butt H, Korbei B, Weinhofer I, Müllner AE, Luschnig C (2010) Putative Arabidopsis Transcriptional Adaptor Protein PROPORZ1. is required to modulate histone acetylation in response to auxin. Proc Natl Acad Sci USA 107:10308–10313
Bannister AJ, Schneider R, Kouzarides T (2002) Histone Methylation, Dynamic or Static? Cell 109:801–806
Baumbusch LO, Thorstensen T, Krauss V, Fischer A, Naumann K, Assalkhou R, Schulz I, Reuter G, Aalen RB (2001) The Arabidopsis thaliana genome contains at least 29 active genes encoding SET domain proteins that can be assigned to four evolutionarily conserved classes. Nucleic Acids Res 29:4319–4333
Barski A, Cuddapah S, Cui K, Roh TY, Schones DE, Wang Z, Wei G, Chepelev I, Zhao K (2007) High-resolution profiling of histone methylations in the human genome. Cell 129:823–837
Berr A, Xu., Gao J, Cognat V, Steinmetz A, Dong A, Shen W-H (2009) SET DOMAIN GROUP25 encodes a histone methyltransferase and is involved in FLOWERING LOCUS C activation and repression of flowering. Plant Physiol 151:1476–1485
Berr A, McCallum EJ, Ménard R, Meyer D, Fuchs J, Dong A, Shen W-H (2010) Arabidopsis SET DOMAIN GROUP2 is required for H3K4 tri-methylation and is crucial for both sporophyte and gametophyte development. Plant Cell 22:3232–3248
Cecchetti V, Altamura MM, Falasca G, Costantino P, Cardarelli M (2008) Auxin regulates arabidopsis anther dehiscence, pollen maturation, and filament elongation. Plant Cell 20:1760–1774
Celenza JL, Quiel JA, Smolen GA, Merrikh H, Silvestro AR, Normanly J, Bender J (2005) The Arabidopsis ATR1 Myb transcription factor controls indolic glucosinolate homeostasis. Plant Physiol 137:253–262
Chen LT, Luo M, Wang YY, Wu K (2010) Involvement of Arabidopsis histone deacetylase HDA6 in ABA and salt stress response. J Exp Bot 61:3345–3353
Cheng Y, Dai X, Zhao Y (2006) Auxin biosynthesis by the YUCCA flavin monooxygenases controls the formation of floral organs and vascular tissues in Arabidopsis. Genes Dev 20:1790–1799
Cheng Y, Dai X, Zhao Y (2007) Auxin synthesized by the YUCCA flavin monooxygenases is essential for embryogenesis and leaf formation in arabidopsis. Plant Cell 19:2430–2439
Chinnusamy V, Gong Z, Zhu JK (2008) Abscisic acid-mediated epigenetic processes in plant development and stress responses. J Int Plant Biol 50:1187–1195
Cohen R, Schocken J, Kaldis A, Vlachonasios KE, Hark AT, McCain ER (2009) The histone acetyltransferase GCN5 affects the inflorescence meristem and stamen development in Arabidopsis. Planta 230:1207–1221
Dreijerink KM, Mulder KW, Winkler GS, Hoppener JW, Lips CJ, Timmers HT (2006) Menin links estrogen receptor activation to histone H3K4 tri-methylation. Cancer Res 66:4929–4935.
Guo L, Yu Y, Law JA, Zhang X (2010) SET DOMAIN GROUP2 is the major histone H3 lysie 4 tri-methyltransferase in Arabidopsis. Proc Nat Acad Sci USA 107:18557–18562
Jang IC, Chung PJ, Hemmes H, Jung C, Chua NH (2011) Rapid and reversible light-mediated chromatin modifications of Arabidopsis phytochrome A locus. Plant Cell 23:459–470
He Y, Amasino RM (2005) Role of chromatin modification in floweringtime control. Trends Plant Sci 10:30–35
Jenuwein T, Allis CD (2001) Translating the histone code. Science 293:1074–1080.
Jullien PE, Katz A, Oliva M, Ohad N, Berger F (2006) Polycomb group complexes self-regulate imprinting of the Polycomb group gene MEDEA in Arabidopsis. Curr Biol 16:486–492
Kim J-M, To TK, Ishida J, Morosawa T, Kawashima M, Matsui A, Toyoda T, Kimura H, Shinozaki K, Seki M (2008) Alterations of lysine modifications on the histone h3 n-tail under drought stress conditions in Arabidopsis thaliana. Plant Cell Physiol 49:1580–1588
Kohler, C, Makarevich, G (2006) Epigenetic mechanisms governing seed development in plants. EMBO Rep 7:223–1227
Krichevsky A, Zaltsman A, Kozlovsky SV, Tian GW, Citovsky V (2009) Regulation of root elongation by histone acetylation in Arabidopsis. J Mol Biol 385:45–50
Lafos M, Kroll P, Hohenstatt ML, Thorpe FL, Clarenz O, Schubert D (2011) Dynamic regulation of H3K27 tri-methylation during Arabidopsis differentiation. PLoS Genet 7:e1002040
Locatelli S, Piatti P, Motto M, Rossi V (2009) Chromatin and DNA modifications in the Opaque2-mediated regulation of gene transcription during maize endosperm development. Plant Cell 21:1410–1427
Mikkelsen TS, Ku M, Jaffe DB, Issac B, Lieberman E, Giannoukos G, Alvarez P, Brockman W, Kim TK, Koche RP, Lee W, Mendenhall E, O’Donovan A, Presser A, Russ C, Xie X, Meissner A, Wernig M, Jaenisch R, Nusbaum C, Lander ES, Bernstein BE (2007) Genome-wide maps of chromatin state in pluripotent and lineage-committed cells. Nature 448:553–560
Nemhauser JL, Hong F, Chory J (2006) Different plant hormones regulate similar processes through largely non-overlapping transcriptional responses. Cell 126:467–475
Pien S, Fleury D, Mylne JS, Crevillen P, Inzé D, Avramova Z, Dean C, Grossniklaus U (2008) ARABIDOPSIS TRITHORAX1 dynamically regulates FLOWERING LOCUS C activation via histone 3 lysine 4 tri-methylation. Plant Cell 20:580–588
Pontvianne F, Blevins T, Pikaard CS (2010) Arabidopsis histone lysine methyltransferases. Adv Bot Res 53:1–22
Shilatifard A (2008) Molecular implementation and physiological roles for histone H3 lysine 4 methylation. Curr Opi Cell Biol 20:341–348
Sims Iii RJ, Nishioka K, Reinberg D (2003) Histone lysine methylation, a signature for chromatin function. Trends Genet 19:629–639
Song CP, Agarwal M, Ohta M, Guo Y, Halfter U, Wang P, Zhu JK (2005) Role of an Arabidopsis AP2/EREBP-type transcriptional repressor in abscisic acid and drought stress responses. Plant Cell 17:2384–2396
Springer NM, Napoli CA, Selinger DA, Pandey R, Cone KC, Chandler VL, Kaeppler HF, Kaeppler SM (2003) Comparative analysis of set domain proteins in maize and arabidopsis reveals multiple duplications preceding the divergence of monocots and dicots. Plant Physiol 132:907–925
Sridha S, Wu K (2006) Identification of AtHD2C as a novel regulator of abscisic acid responses in Arabidopsis. Plant J 46:124–133
Strahl BD, Allis CD (2000) The language of covalent histone modifications. Nature 403:41–45
Sun B, Xu Y, Ng KH, Ito T (2009) A timing mechanism for stem cell maintenance and differentiation in the Arabidopsis floral meristem. Genes Dev 23:1791–1804
Sung S, Amasino RM (2004) Vernalization in Arabidopsis thaliana is mediated by the PHD finger protein VIN3. Nature 427:159–164
Tamada Y, Yun JY, Woo SC, Amasino RM (2009) ARABIDOPSIS TRITHORAX-RELATED7 is required for methylation of lysine 4 of histone H3 and for transcriptional activation of FLOWERING LOCUS C. Plant Cell 21:3257–3269
Tan X, Calderon-Villalobos LIA, Sharon M, Zheng C, Robinson CV, Estelle M, Zheng N (2007) Mechanism of auxin perception by the TIR1 ubiquitin ligase. Nature 446:640–645
Tanaka M, Kikuchi A, Kamada H (2008) The Arabidopsis histone deacetylases HDA6 and HDA19 contribute to the repression of embryonic properties after germination. Plant Physiol 146:149–161
To TK, Nakaminami K, Kim JM, Morosawa T, Ishida J, Tanaka M, Yokoyama S, Shinozaki K, Seki M (2011) Arabidopsis HDA6 is required for freezing tolerance. Biochem Biophys Res Comm 406:414–419
Tsuji H, Saika H, Tsutsumi N, Hirai A, Nakazono M (2006) Dynamic and reversible changes in histone H3-Lys4 methylation and H3 acetylation occurring at submergence-inducible genes in rice. Plant Cell Physiol 47:995–1003
Wu K, Zhang L, Zhou C, Yu CW, Chaikam V (2008) HDA6 is required for jasmonate response, senescence and flowering in Arabidopsis. J Exp Bot 59:225–234
Yin H, Zhang X, Liu J, Wang Y, He J, Yang T, Hong X, Yang Q, Gong Z (2009) Epigenetic regulation, somatic homologous recombination, and abscisic acid signaling are influenced by DNA polymerase mutation in Arabidopsis. Plant Cell 21:386–402
Yu X, Li L, Guo M, Chory J, Yin Y (2008) Modulation of brassinosteroidregulated gene expression by Jumonji domain-containing proteins ELF6 and REF6 in Arabidopsis. Proc Nat Acad Sci USA 105:7618–7623
Yun J-Y, Tamada Y, Kang YE, Amasino RM (2012) ARABIDOPSIS TRITHORAX-RELATED3/SET DOMAIN GROUP2 is Required for the Winter-Annual Habit of Arabidopsis thaliana. Plant Cell Physiol 53:834–846
Zhang X, Bernatavichute Y, Cokus S, Pellegrini M, Jacobsen S (2009) Genome-wide analysis of mono-, di- and tri-methylation of histone H3 lysine 4 in Arabidopsis thaliana. Genome Biol 10:R62
Zhao Y, Hull AK, Gupta NR, Goss KA, Alonso J, Ecker JR, Normanly J, Chory J, Celenza JL (2002) Trp-dependent auxin biosynthesis in Arabidopsis, involvement of cytochrome P450s CYP79B2 and CYP79B3. Genes Dev 16:3100–3112
Zhou C, Zhang L, Duan J, Miki B, Wu K (2005) HISTONE DEACETYLASE19 is involved in jasmonic acid and ethylene signaling of pathogen response in Arabidopsis. Plant Cell 17:1196–1204
Zhu J, Jeong JC, Zhu Y, Sokolchik I, Miyazaki S, Zhu J-K, Hasegawa PM, Bohnert HJ, Shi H, Yun D-J, Bressan RA (2008) Involvement of Arabidopsis HOS15 in histone deacetylation and cold tolerance. Proc Nat Acad Sci USA 105:4945–4950
Author information
Authors and Affiliations
Corresponding author
Additional information
These authors contributed equally in this work.
Electronic supplementary material
Electronic supplementary material
Rights and permissions
About this article
Cite this article
Kim, S., Lee, J., Yang, JY. et al. Arabidopsis histone methyltransferase SET DOMAIN GROUP2 is required for regulation of various hormone responsive genes. J. Plant Biol. 56, 39–48 (2013). https://doi.org/10.1007/s12374-012-0320-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12374-012-0320-7