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Circadian expression profiles of chromatin remodeling factor genes in Arabidopsis

Abstract

The circadian clock is a biological time keeper mechanism that regulates biological rhythms to a period of approximately 24 h. The circadian clock enables organisms to anticipate environmental cycles and coordinates internal cellular physiology with external environmental cues. In plants, correct matching of the clock with the environment confers fitness advantages to plant survival and reproduction. Therefore, circadian clock components are regulated at multiple layers to fine-tune the circadian oscillation. Epigenetic regulation provides an additional layer of circadian control. However, little is known about which chromatin remodeling factors are responsible for circadian control. In this work, we analyzed circadian expression of 109 chromatin remodeling factor genes and identified 17 genes that display circadian oscillation. In addition, we also found that a candidate interacts with a core clock component, supporting that clock activity is regulated in part by chromatin modification. As an initial attempt to elucidate the relationship between chromatin modification and circadian oscillation, we identified novel regulatory candidates that provide a platform for future investigations of chromatin regulation of the circadian clock.

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Abbreviations

HAT:

Histone acetyltransferase

HDAC:

Histone deacetylase

HDM:

Histone demethylase

HKMT:

Histone lysine methyltransferase

HMT:

Histone methyltransferase

HRMT:

Histone arginine methyltransferase

JMJ:

Jumonji C domain-containing protein

LSD:

Lysine demethylase

References

  • Agius F, Kapoor A, Zhu JK (2006) Role of the Arabidopsis DNA glycosylase/lyase ROS1 in active DNA demethylation. Proc Natl Acad Sci USA 103:11796–11801

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Alabadí D, Oyama T, Yanovsky MJ, Harmon FG, Más P, Kay SA (2001) Reciprocal regulation between TOC1 and LHY/CCA1 within the Arabidopsis circadian clock. Science 293:880–883

    PubMed  Article  Google Scholar 

  • Baroux C, Spillane C, Grossniklaus U (2002) Evolutionary origins of the endosperm in flowering plants. Genome Biol 3:reviews1026

  • Baudry A, Ito S, Song YH, Strait AA, Kiba T, Lu S, Henriques R, Pruneda-Paz JL, Chua NH, Tobin EM, Kay SA, Imaizumi T (2010) F-box proteins FKF1 and LKP2 act in concert with ZEITLUPE to control Arabidopsis clock progression. Plant Cell 22:606–622

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Berger F, Gaudin V (2003) Chromatin dynamics and Arabidopsis development. Chromosome Res 11:277–304

    CAS  PubMed  Article  Google Scholar 

  • Bowers EM, Yan G, Mukherjee C, Orry A, Wang L, Holbert MA, Crump NT, Hazzalin CA, Liszczak G, Yuan H, Larocca C, Saldanha SA, Abagyan R, Sun Y, Meyers DJ, Marmorstein R, Mahadevan LC, Alani RM, Cole PA (2010) Virtual ligand screening of the p300/CBP histone acetyltransferase: identification of a selective small molecule inhibitor. Chem Biol 7:471–482

    Article  Google Scholar 

  • Carré IA, Kim JY (2002) MYB transcription factors in the Arabidopsis circadian clock. J Exp Bot 53:1551–1557

    PubMed  Article  Google Scholar 

  • Cedar H, Bergman Y (2009) Linking DNA methylation and histone modification: patterns and paradigms. Nat Rev Genet 10:295–304

    CAS  PubMed  Article  Google Scholar 

  • Chaudhury AM, Berger F (2001) Maternal control of seed development. Semin Cell Dev Biol 12:381–386

    CAS  PubMed  Article  Google Scholar 

  • Chen ZJ, Tian L (2007) Roles of dynamic and reversible histone acetylation in plant development and polyploidy. Biochim Biophys Acta 1769:295–307

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Chen X, Hu Y, Zhou DX (2011) Epigenetic gene regulation by plant Jumonji group of histone demethylase. Biochim Biophys Acta 1809:421–426

    CAS  PubMed  Article  Google Scholar 

  • Chinnusamy V, Zhu JK (2009) Epigenetic regulation of stress responses in plants. Curr Opin Plant Biol 12:133–139

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Chow BY, Helfer A, Nusinow DA, Kay SA (2012) ELF3 recruitment to the PRR9 promoter requires other evening complex members in the Arabidopsis circadian clock. Plant Signal Behav 7:170–173

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Covington MF, Maloof JN, Straume M, Kay SA, Harmer SL (2008) Global transcriptome analysis reveals circadian regulation of key pathways in plant growth and development. Genome Biol 9:R130

    PubMed Central  PubMed  Article  Google Scholar 

  • Dodd AN, Salathia N, Hall A, Kévei E, Tóth R, Nagy F, Hibberd JM, Millar AJ, Webb AA (2005) Plant circadian clocks increase photosynthesis, growth, survival, and competitive advantage. Science 309:630–633

    CAS  PubMed  Article  Google Scholar 

  • Earley K, Lawrence RJ, Pontes O, Reuther R, Enciso AJ, Silva M, Neves N, Gross M, Viegas W, Pikaard CS (2006) Erasure of histone acetylation by Arabidopsis HDA6 mediates large-scale gene silencing in nucleolar dominance. Genes Dev 20:1283–1293

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Earley KW, Shook MS, Brower-Toland B, Hicks L, Pikaard CS (2007) In vitro specificities of Arabidopsis co-activator histone acetyltransferases: implications for histone hyperacetylation in gene activation. Plant J 52:615–626

    CAS  PubMed  Article  Google Scholar 

  • Farinas B, Mas P (2011) Functional implication of the MYB transcription factor RVE8/LCL5 in the circadian control of histone acetylation. Plant J 66:318–329

    CAS  PubMed  Article  Google Scholar 

  • Filichkin SA, Mockler TC (2012) Unproductive alternative splicing and nonsense mRNAs: a widespread phenomenon among plant circadian clock genes. Biol Direct 7:20

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Filichkin SA, Priest HD, Givan SA, Shen R, Bryant DW, Fox SE, Wong WK, Mockler TC (2010) Genome-wide mapping of alternative splicing in Arabidopsis thaliana. Genome Res 20:45–58

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Fu YL, Zhang GB, Lv XF, Guan Y, Yi HY, Gong JM (2013) Arabidopsis histone methylase CAU1/PRMT5/SKB1 acts as an epigenetic suppressor of the calcium signaling gene CAS to mediate stomatal closure in response to extracellular calcium. Plant Cell 25:2878–2891

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Fujiwara S, Oda A, Yoshida R, Niinuma K, Miyata K, Tomozoe Y, Tajima T, Nakagawa M, Hayashi K, Coupland G, Mizoguchi T (2008) Circadian clock proteins LHY and CCA1 regulate SVP protein accumulation to control flowering in Arabidopsis. Plant Cell 20:2960–2971

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Furner IJ, Matzke M (2011) Methylation and demethylation of the Arabidopsis genome. Curr Opin Plant Biol 14:137–141

    CAS  PubMed  Article  Google Scholar 

  • Gao Y, Yang S, Yuan L, Cui Y, Wu K (2012) Comparative analysis of SWIRM domain-containing proteins in plants. Comp Funct Genomics 2012:310402

    PubMed Central  PubMed  Article  Google Scholar 

  • Grimaldi B, Nakahata Y, Kaluzova M, Masubuchi S, Sassone-Corsi P (2009) Chromatin remodeling, metabolism and circadian clocks: the interplay of CLOCK and SIRT1. Int J Biochem Cell Biol 41:81–86

    CAS  PubMed  Article  Google Scholar 

  • Haydon MJ, Mielczarek O, Robertson FC, Hubbard KE, Webb AA (2013) Photosynthetic entrainment of the Arabidopsis thaliana circadian clock. Nature 502:689–692

    CAS  PubMed  Article  Google Scholar 

  • Hemmes H, Henriques R, Jang IC, Kim S, Chua NH (2012) Circadian clock regulates dynamic chromatin modifications associated with Arabidopsis CCA1/LHY and TOC1 transcriptional rhythms. Plant Cell Physiol 53:2016–2029

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Henderson IR, Jacobsen SE (2008) Tandem repeats upstream of the Arabidopsis endogene SDC recruit non-CG DNA methylation and initiate siRNA spreading. Genes Dev 22:1597–1606

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Henriques R, Mas P (2013) Chromatin remodeling and alternative splicing: pre- and post-transcriptional regulation of the Arabidopsis circadian clock. Semin Cell Dev Biol 24:399–406

    CAS  PubMed  Article  Google Scholar 

  • Herrero E, Kolmos E, Bujdoso N, Yuan Y, Wang M, Berns MC, Uhlworm H, Coupland G, Saini R, Jaskolski M, Webb A, Gonçalves J, Davis SJ (2012) EARLY FLOWERING4 recruitment of EARLY FLOWERING3 in the nucleus sustains the Arabidopsis circadian clock. Plant Cell 24:428–443

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Hollender C, Liu Z (2008) Histone deacetylase genes in Arabidopsis development. J Integr Plant Biol 875–885

  • Hsu PY, Harmer SL (2012) Circadian phase has profound effects on differential expression analysis. PLoS One 7:e49853

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Huang W, Pérez-García P, Pokhilko A, Millar AJ, Antoshechkin I, Riechmann JL, Mas P (2012) Mapping the core of the Arabidopsis circadian clock defines the network structure of the oscillator. Science 336:75–79

    CAS  PubMed  Article  Google Scholar 

  • Ito S, Song YH, Imaizumi T (2012) LOV domain-containing F-box proteins: light-dependent protein degradation modules in Arabidopsis. Mol Plant 5:573–582

    PubMed  Article  Google Scholar 

  • James AB, Syed NH, Bordage S, Marshall J, Nimmo GA, Jenkins GI, Herzyk P, Brown JW, Nimmo HG (2012) Alternative splicing mediates responses of the Arabidopsis circadian clock to temperature changes. Plant Cell 24:961–981

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Jarillo JA, Piñeiro M, Cubas P, Martínez-Zapater JM (2009) Chromatin remodeling in plant development. Int J Dev Biol 53:1581–1596

    CAS  PubMed  Article  Google Scholar 

  • Jones MA, Covington MF, DiTacchio L, Vollmers C, Panda S, Harmer SL (2010) Jumonji domain protein JMJD5 functions in both the plant and human circadian systems. Proc Natl Acad Sci USA 107:21623–21628

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Kato M, Miura A, Bender J, Jacobsen SE, Kakutani T (2003) Role of CG and non-CG methylation in immobilization of transposons in Arabidopsis. Curr Biol 13:421–426

    CAS  PubMed  Article  Google Scholar 

  • Kiba T, Henriques R, Sakakibara H, Chua NH (2007) Targeted degradation of PSEUDO-RESPONSE REGULATOR5 by an SCFZTL complex regulates clock function and photomorphogenesis in Arabidopsis thaliana. Plant Cell 19:2516–2530

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Kim WY, Geng R, Somers DE (2003) Circadian phase-specific degradation of the F-box protein ZTL is mediated by the proteasome. Proc Natl Acad Sci USA 100:4933–4938

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Ko JH, Mitina I, Tamada Y, Hyun Y, Choi Y, Amasino RM, Noh B, Noh YS (2010) Growth habit determination by the balance of histone methylation activities in Arabidopsis. EMBO J 29:3208–3215

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Kusakina J, Dodd AN (2012) Phosphorylation in the plant circadian system. Trends Plant Sci 17:575–583

    CAS  PubMed  Article  Google Scholar 

  • Lau OS, Huang X, Charron JB, Lee JH, Li G, Deng XW (2011) Interaction of Arabidopsis DET1 with CCA1 and LHY in mediating transcriptional repression in the plant circadian clock. Mol Cell 43:703–712

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Lu SX, Knowles SM, Webb CJ, Celaya RB, Cha C, Siu JP, Tobin EM (2011) The Jumonji C domain-containing protein JMJ30 regulates period length in the Arabidopsis circadian clock. Plant Physiol 55:906–915

    Article  Google Scholar 

  • Lu SX, Webb CJ, Knowles SM, Kim SH, Wang Z, Tobin EM (2012) CCA1 and ELF3 interact in the control of hypocotyl length and flowering time in Arabidopsis. Plant Physiol 158:1079–1088

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Malapeira J, Khaitova LC, Mas P (2012) Ordered changes in histone modifications at the core of the Arabidopsis circadian clock. Proc Natl Acad Sci USA 109:21540–21545

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Más P (2008) Circadian clock function in Arabidopsis thaliana: time beyond transcription. Trends Cell Biol 18:273–281

    PubMed  Article  Google Scholar 

  • Más P, Kim WY, Somers DE, Kay SA (2003) Targeted degradation of TOC1 by ZTL modulates circadian function in Arabidopsis thaliana. Nature 426:567–570

    PubMed  Article  Google Scholar 

  • Meyer P (2000) Transcriptional transgene silencing and chromatin components. Plant Mol Biol 43:221–234

    CAS  PubMed  Article  Google Scholar 

  • Mizuno T, Yamashino T (2008) Comparative transcriptome of diurnally oscillating genes and hormone-responsive genes in Arabidopsis thaliana: insight into circadian clock-controlled daily responses to common ambient stresses in plants. Plant Cell Physiol 49:481–487

    CAS  PubMed  Article  Google Scholar 

  • Morales-Ruiz T, Ortega-Galisteo AP, Ponferrada-Marín MI, Martínez-Macías MI, Ariza RR, Roldán-Arjona T (2006) DEMETER and REPRESSOR OF SILENCING 1 encode 5-methylcytosine DNA glycosylases. Proc Natl Acad Sci USA 103:6853–6858

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Nagel DH, Kay SA (2012) Complexity in the wiring and regulation of plant circadian networks. Curr Biol 22:R648–R657

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Nakahata Y, Kaluzova M, Grimaldi B, Sahar S, Hirayama J, Chen D, Guarente LP, Sassone-Corsi P (2008) The NAD+-dependent deacetylase SIRT1 modulates CLOCK-mediated chromatin remodeling and circadian control. Cell 134:329–340

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Nakahata Y, Sahar S, Astarita G, Kaluzova M, Sassone-Corsi P (2009) Circadian control of the NAD+ salvage pathway by CLOCK-SIRT1. Science 324:654–657

    CAS  PubMed  Article  Google Scholar 

  • Nakamichi N, Kita M, Ito S, Yamashino T, Mizuno T (2005) PSEUDO-RESPONSE REGULATORS, PRR9, PRR7 and PRR5, together play essential roles close to the circadian clock of Arabidopsis thaliana. Plant Cell Physiol 46:686–698

    CAS  PubMed  Article  Google Scholar 

  • Nakamichi N, Kiba T, Henriques R, Mizuno T, Chua NH, Sakakibara H (2010) PSEUDO-RESPONSE REGULATORS 9, 7, and 5 are transcriptional repressors in the Arabidopsis circadian clock. Plant Cell 22:594–605

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Ng HH, Bird A (2000) Histone deacetylases: silencers for hire. Trends Biochem Sci 25:121–126

    CAS  PubMed  Article  Google Scholar 

  • Niu L, Lu F, Pei Y, Liu C, Cao X (2007) Regulation of flowering time by the protein arginine methyltransferase AtPRMT10. EMBO Rep 8:1190–1195

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Nusinow DA, Helfer A, Hamilton EE, King JJ, Imaizumi T, Schultz TF, Farré EM, Kay SA (2011) The ELF4-ELF3-LUX complex links the circadian clock to diurnal control of hypocotyl growth. Nature 475:398–402

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Pandey R, Müller A, Napoli CA, Selinger DA, Pikaard CS, Richards EJ, Bender J, Mount DW, Jorgensen RA (2002) Analysis of histone acetyltransferase and histone deacetylase families of Arabidopsis thaliana suggests functional diversification of chromatin modification among multicellular eukaryotes. Nucleic Acids Res 30:5036–5055

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Park BS, Eo HJ, Jang IC, Kang HG, Song JT, Seo HS (2010) Ubiquitination of LHY by SINAT5 regulates flowering time and is inhibited by DET1. Biochem Biophys Res Commun 398:242–246

    CAS  PubMed  Article  Google Scholar 

  • Penterman J, Zilberman D, Huh JH, Ballinger T, Henikoff S, Fischer RL (2007) DNA demethylation in the Arabidopsis genome. Proc Natl Acad Sci USA 104:6752–6757

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Perales M, Más P (2007) A functional link between rhythmic changes in chromatin structure and the Arabidopsis biological clock. Plant Cell 19:2111–2123

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Perez-Santángelo S, Schlaen RG, Yanovsky MJ (2013) Genomic analysis reveals novel connections between alternative splicing and circadian regulatory networks. Brief Funct Genomics 12:13–24

    PubMed  Article  Google Scholar 

  • Pfluger J, Wagner D (2007) Histone modifications and dynamic regulation of genome accessibility in plants. Curr Opin Plant Biol 10:645–652

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Pokhilko A, Mas P, Millar AJ (2013) Modelling the widespread effects of TOC1 signalling on the plant circadian clock and its outputs. BMC Syst Biol 7:23

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Pontvianne F, Blevins T, Pikaard CS (2010) Arabidopsis histone lysine methyltransferases. Adv Bot Res 53:1–22

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Ruotolo R, Tosi F, Vernarecci S, Ballario P, Mai A, Filetici P, Ottonello S (2010) Chemogenomic profiling of the cellular effects associated with histone H3 acetylation impairment by a quinoline-derived compound. Genomics 96:272–280

    CAS  PubMed  Article  Google Scholar 

  • Salomé PA, McClung CR (2004) The Arabidopsis thaliana clock. J Biol Rhythms 19:425–435

    PubMed  Article  Google Scholar 

  • Salomé PA, Weigel D, McClung CR (2010) The role of the Arabidopsis morning loop components CCA1, LHY, PRR7, and PRR9 in temperature compensation. Plant Cell 22:3650–3661

    PubMed Central  PubMed  Article  Google Scholar 

  • Sanchez SE, Petrillo E, Beckwith EJ, Zhang X, Rugnone ML, Hernando CE, Cuevas JC, Godoy Herz MA, Depetris-Chauvin A, Simpson CG, Brown JW, Cerdán PD, Borevitz JO, Mas P, Ceriani MF, Kornblihtt AR, Yanovsky MJ (2010) A methyl transferase links the circadian clock to the regulation of alternative splicing. Nature 468:112–116

    CAS  PubMed  Article  Google Scholar 

  • Seo PJ, Park MJ, Lim MH, Kim SG, Lee M, Baldwin IT, Park CM (2012) A self-regulatory circuit of CIRCADIAN CLOCK-ASSOCIATED1 underlies the circadian clock regulation of temperature responses in Arabidopsis. Plant Cell 24:2427–2442

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Song HR, Carré IA (2005) DET1 regulates the proteasomal degradation of LHY, a component of the Arabidopsis circadian clock. Plant Mol Biol 57:761–771

    CAS  PubMed  Article  Google Scholar 

  • Song HR, Noh YS (2012) Rhythmic oscillation of histone acetylation and methylation at the Arabidopsis central clock loci. Mol Cells 34:279–287

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Spedaletti V, Polticelli F, Capodaglio V, Schininà ME, Stano P, Federico R, Tavladoraki P (2008) Characterization of a lysine-specific histone demethylase from Arabidopsis thaliana. Biochemistry 47:4936–4947

    CAS  PubMed  Article  Google Scholar 

  • Stratmann T, Más P (2008) Chromatin, photoperiod and the Arabidopsis circadian clock: a question of time. Semin Cell Dev Biol 19:554–559

    CAS  PubMed  Article  Google Scholar 

  • Thorstensen T, Grini PE, Aalen RB (2011) SET domain proteins in plant development. Biochim Biophys Acta 1809:407–420

    CAS  PubMed  Article  Google Scholar 

  • Troncoso-Ponce MA, Mas P (2012) Newly described components and regulatory mechanisms of circadian clock function in Arabidopsis thaliana. Mol Plant 5:545–553

    PubMed  Article  Google Scholar 

  • Wang L, Kim J, Somers DE (2013) Transcriptional corepressor TOPLESS complexes with pseudoresponse regulator proteins and histone deacetylases to regulate circadian transcription. Proc Natl Acad Sci USA 110:761–766

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Xu CR, Liu C, Wang YL, Li LC, Chen WQ, Xu ZH, Bai SN (2005) Histone acetylation affects expression of cellular patterning genes in the Arabidopsis root epidermis. Proc Natl Acad Sci USA 102:14469–14474

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Xydous M, Sekeri-Pataryas KE, Prombona A, Sourlingas TG (2012) Nicotinamide treatment reduces the levels of histone H3K4 trimethylation in the promoter of the mper1 circadian clock gene and blocks the ability of dexamethasone to induce the acute response. Biochim Biophys Acta 1819:877–884

    CAS  PubMed  Article  Google Scholar 

  • Yao X, Feng H, Yu Y, Dong A, Shen WH (2013) SDG2-mediated H3K4 methylation is required for proper Arabidopsis root growth and development. PLoS One 8:e56537

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Yoo SK, Hong SM, Lee JS, Ahn JH (2011) A genetic screen for leaf movement mutants identifies a potential role for AGAMOUS-LIKE 6 (AGL6) in circadian-clock control. Mol Cells 31:281–287

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Yu JW, Rubio V, Lee NY, Bai S, Lee SY, Kim SS, Liu L, Zhang Y, Irigoyen ML, Sullivan JA, Zhang Y, Lee I, Xie Q, Paek NC, Deng XW (2008) COP1 and ELF3 control circadian function and photoperiodic flowering by regulating GI stability. Mol Cell 32:617–630

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Zhang C, Xie Q, Anderson RG, Ng G, Seitz NC, Peterson T, McClung CR, McDowell JM, Kong D, Kwak JM, Lu H (2013) Crosstalk between the circadian clock and innate immunity in Arabidopsis. PLoS Pathog 9:e1003370

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Zografos BR, Sung S (2012) Vernalization-mediated chromatin changes. J Exp Bot 63:4343–4348

    CAS  PubMed  Article  Google Scholar 

  • Zubko E, Gentry M, Kunova A, Meyer P (2012) De novo DNA methylation activity of methyltransferase 1 (MET1) partially restores body methylation in Arabidopsis thaliana. Plant J 71:1029–1037

    CAS  PubMed  Article  Google Scholar 

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Acknowledgments

This research was supported by the Basic Science Research Program (NRF-2013R1A1A1004831) and Global Research Laboratory Program (2012K1A1A2055546) through the National Research Foundation of Korea (NRF) funded by the Ministry of Education. H.G.L., K.L., and K.J. were supported by the BK21 Plus program in the Department of Bioactive Material Sciences.

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Correspondence to Pil Joon Seo.

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Lee, H.G., Lee, K., Jang, K. et al. Circadian expression profiles of chromatin remodeling factor genes in Arabidopsis . J Plant Res 128, 187–199 (2015). https://doi.org/10.1007/s10265-014-0665-8

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Keywords

  • Arabidopsis
  • Chromatin remodeling
  • Circadian clock
  • DNA methylation
  • Histone modification