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Overexpression of a histone H3K4 demethylase, JMJ15, accelerates flowering time in Arabidopsis

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Abstract

The methylation of histone 3 lysine 4 (H3K4) is essential for gene activation. Flowering Locus C (FLC), an important flowering repressor, quantitatively regulates flowering time in Arabidopsis and its expression level is coincident with H3K4 trimethylation (H3K4me3) dynamics. The methylation state of FLC chromatin is determined by the balance between methylation and demethylation, which is mediated by histone methyltransferases and demethylases, respectively. However, little is known about the role of histone demethylase(s) in FLC regulation. Here, we characterized the biochemical activity and biological function of a novel JmjC domain-containing H3K4 demethylase, JMJ15, in Arabidopsis. JMJ15, which is a member of the H3K4 demethylase JARID1 family, displayed H3K4me3 demethylase activity both in vitro and in vivo. The mutation of JMJ15 did not produce an obvious phenotype; however, overexpression JMJ15 resulted in an obvious early flowering phenotype, which was associated with the repression of FLC level and reduction in H3K4me3 at the FLC locus, resulting in increased FT expression. Our results suggest that JMJ15 is a novel H3K4 demethylase, involved in the control of flowering time by demethylating H3K4me3 at FLC chromatin when it was overexpressed in Arabidopsis.

Key message Overexpression of a histone H3K4 demethylase, JMJ15, represses FLC expression by decreasing its chromatin H3K4me3 level, thereby controlling flowering time in Arabidopsis.

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References

  • Angel A, Song J, Dean C, Howard M (2011) A Polycomb-based switch underlying quantitative epigenetic memory. Nature 476(7358):105–108

    Article  PubMed  CAS  Google Scholar 

  • Bastow R, Mylne JS, Lister C, Lippman Z, Martienssen RA, Dean C (2004) Vernalization requires epigenetic silencing of FLC by histone methylation. Nature 427(6970):164–167

    Article  PubMed  CAS  Google Scholar 

  • 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(21):4319–4333

    Article  PubMed  CAS  Google Scholar 

  • Bowler C, Benvenuto G, Laflamme P, Molino D, Probst AV, Tariq M, Paszkowski J (2004) Chromatin techniques for plant cells. Plant J 39(5):776–789

    Article  PubMed  CAS  Google Scholar 

  • Briggs SD, Bryk M, Strahl BD, Cheung WL, Davie JK, Dent SY, Winston F, Allis CD (2001) Histone H3 lysine 4 methylation is mediated by Set1 and required for cell growth and rDNA silencing in Saccharomyces cerevisiae. Genes Dev 15(24):3286–3295

    Article  PubMed  CAS  Google Scholar 

  • Cao Y, Dai Y, Cui S, Ma L (2008) Histone H2B monoubiquitination in the chromatin of FLOWERING LOCUS C regulates flowering time in Arabidopsis. Plant Cell 20(10):2586–2602

    Article  PubMed  CAS  Google Scholar 

  • Chanvivattana Y, Bishopp A, Schubert D, Stock C, Moon YH, Sung ZR, Goodrich J (2004) Interaction of Polycomb-group proteins controlling flowering in Arabidopsis. Development 131(21):5263–5276

    Article  PubMed  CAS  Google Scholar 

  • Chen Z, Zang J, Whetstine J, Hong X, Davrazou F, Kutateladze TG, Simpson M, Mao Q, Pan CH, Dai S, Hagman J, Hansen K, Shi Y, Zhang G (2006) Structural insights into histone demethylation by JMJD2 family members. Cell 125(4):691–702

    Article  PubMed  CAS  Google Scholar 

  • Christensen J, Agger K, Cloos PA, Pasini D, Rose S, Sennels L, Rappsilber J, Hansen KH, Salcini AE, Helin K (2007) RBP2 belongs to a family of demethylases, specific for tri-and dimethylated lysine 4 on histone 3. Cell 128(6):1063–1076

    Article  PubMed  CAS  Google Scholar 

  • Clarke JH, Dean C (1994) Mapping FRI, a locus controlling flowering time and vernalization response in Arabidopsis thaliana. Mol Gen Genet 242(1):81–89

    PubMed  CAS  Google Scholar 

  • Cloos PA, Christensen J, Agger K, Maiolica A, Rappsilber J, Antal T, Hansen KH, Helin K (2006) The putative oncogene GASC1 demethylates tri- and dimethylated lysine 9 on histone H3. Nature 442(7100):307–311

    Article  PubMed  CAS  Google Scholar 

  • Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16(6):735–743

    Article  PubMed  CAS  Google Scholar 

  • De Lucia F, Crevillen P, Jones AM, Greb T, Dean C (2008) A PHD-polycomb repressive complex 2 triggers the epigenetic silencing of FLC during vernalization. Proc Natl Acad Sci USA 105(44):16831–16836

    Article  PubMed  Google Scholar 

  • Deleris A, Greenberg MV, Ausin I, Law RW, Moissiard G, Schubert D, Jacobsen SE (2010) Involvement of a Jumonji-C domain-containing histone demethylase in DRM2-mediated maintenance of DNA methylation. EMBO Rep 11(12):950–955

    Article  PubMed  CAS  Google Scholar 

  • Eissenberg JC, Lee MG, Schneider J, Ilvarsonn A, Shiekhattar R, Shilatifard A (2007) The trithorax-group gene in Drosophila little imaginal discs encodes a trimethylated histone H3 Lys4 demethylase. Nat Struct Mol Biol 14(4):344–346

    Article  PubMed  CAS  Google Scholar 

  • Geraldo N, Baurle I, Kidou S, Hu X, Dean C (2009) FRIGIDA delays flowering in Arabidopsis via a cotranscriptional mechanism involving direct interaction with the nuclear cap-binding complex. Plant Physiol 150(3):1611–1618

    Article  PubMed  CAS  Google Scholar 

  • He Y, Amasino RM (2005) Role of chromatin modification in flowering-time control. Trends Plant Sci 10(1):30–35

    Article  PubMed  CAS  Google Scholar 

  • He Y, Michaels SD, Amasino RM (2003) Regulation of flowering time by histone acetylation in Arabidopsis. Science 302(5651):1751–1754

    Article  PubMed  CAS  Google Scholar 

  • He Y, Doyle MR, Amasino RM (2004) PAF1-complex-mediated histone methylation of FLOWERING LOCUS C chromatin is required for the vernalization-responsive, winter-annual habit in Arabidopsis. Genes Dev 18(22):2774–2784

    Article  PubMed  CAS  Google Scholar 

  • Iwase S, Lan F, Bayliss P, de la Torre-Ubieta L, Huarte M, Qi HH, Whetstine JR, Bonni A, Roberts TM, Shi Y (2007) The X-linked mental retardation gene SMCX/JARID1C defines a family of histone H3 lysine 4 demethylases. Cell 128(6):1077–1088

    Article  PubMed  CAS  Google Scholar 

  • Jeong JH, Song HR, Ko JH, Jeong YM, Kwon YE, Seol JH, Amasino RM, Noh B, Noh YS (2009) Repression of FLOWERING LOCUS T chromatin by functionally redundant histone H3 lysine 4 demethylases in Arabidopsis. PLoS ONE 4(11):e8033

    Article  PubMed  Google Scholar 

  • Jiang D, Yang W, He Y, Amasino RM (2007) Arabidopsis relatives of the human lysine-specific Demethylase1 repress the expression of FWA and FLOWERING LOCUS C and thus promote the floral transition. Plant Cell 19(10):2975–2987

    Article  PubMed  CAS  Google Scholar 

  • Jiang D, Wang Y, He Y (2008) Repression of FLOWERING LOCUS C and FLOWERING LOCUS T by the Arabidopsis Polycomb repressive complex 2 components. PLoS ONE 3(10):e3404

    Article  PubMed  Google Scholar 

  • Johanson U, West J, Lister C, Michaels S, Amasino R, Dean C (2000) Molecular analysis of FRIGIDA, a major determinant of natural variation in Arabidopsis flowering time. Science 290(5490):344–347

    Article  PubMed  CAS  Google Scholar 

  • Kim DH, Doyle MR, Sung S, Amasino RM (2009) Vernalization: winter and the timing of flowering in plants. Annu Rev Cell Dev Biol 25:277–299

    Article  PubMed  CAS  Google Scholar 

  • Klose RJ, Zhang Y (2007) Regulation of histone methylation by demethylimination and demethylation. Nat Rev Mol Cell Biol 8(4):307–318

    Article  PubMed  CAS  Google Scholar 

  • Klose RJ, Kallin EM, Zhang Y (2006) JmjC-domain-containing proteins and histone demethylation. Nat Rev Genet 7(9):715–727

    Article  PubMed  CAS  Google Scholar 

  • Klose RJ, Yan Q, Tothova Z, Yamane K, Erdjument-Bromage H, Tempst P, Gilliland DG, Zhang Y, Kaelin WG Jr (2007) The retinoblastoma binding protein RBP2 is an H3K4 demethylase. Cell 128(5):889–900

    Article  PubMed  CAS  Google Scholar 

  • Kouzarides T (2007) Chromatin modifications and their function. Cell 128(4):693–705

    Article  PubMed  CAS  Google Scholar 

  • Lempe J, Balasubramanian S, Sureshkumar S, Singh A, Schmid M, Weigel D (2005) Diversity of flowering responses in wild Arabidopsis thaliana strains. PLoS Genet 1(1):109–118

    Article  PubMed  CAS  Google Scholar 

  • Li B, Carey M, Workman JL (2007) The role of chromatin during transcription. Cell 128(4):707–719

    Article  PubMed  CAS  Google Scholar 

  • Li F, Huarte M, Zaratiegui M, Vaughn MW, Shi Y, Martienssen R, Cande WZ (2008) Lid2 is required for coordinating H3K4 and H3K9 methylation of heterochromatin and euchromatin. Cell 135(2):272–283

    Article  PubMed  CAS  Google Scholar 

  • Li W, Liu H, Cheng ZJ, Su YH, Han HN, Zhang Y, Zhang XS (2011) DNA methylation and histone modifications regulate De Novo shoot regeneration in Arabidopsis by modulating WUSCHEL expression and auxin signaling. PLoS Genet 7(8):e1002243

    Article  PubMed  CAS  Google Scholar 

  • Liu F, Quesada V, Crevillen P, Baurle I, Swiezewski S, Dean C (2007) The Arabidopsis RNA-binding protein FCA requires a lysine-specific demethylase 1 homolog to downregulate FLC. Mol Cell 28(3):398–407

    Article  PubMed  Google Scholar 

  • Liu C, Lu F, Cui X, Cao X (2010) Histone methylation in higher plants. Annu Rev Plant Biol 61:395–420

    Article  PubMed  CAS  Google Scholar 

  • Lu F, Li G, Cui X, Liu C, Wang XJ, Cao X (2008) Comparative analysis of JmjC domain-containing proteins reveals the potential histone demethylases in Arabidopsis and rice. J Integr Plant Biol 50(7):886–896

    Article  PubMed  CAS  Google Scholar 

  • Lu F, Cui X, Zhang S, Liu C, Cao X (2010a) JMJ14 is an H3K4 demethylase regulating flowering time in Arabidopsis. Cell Res 20(3):387–390

    Article  PubMed  Google Scholar 

  • Lu SX, Knowles SM, Webb CJ, Celaya RB, Cha C, Siu JP, Tobin EM (2010b) The JmjC domain-containing protein JMJ30 regulates period length in the Arabidopsis circadian clock. Plant Physiol 155(2):906–915

    Article  PubMed  Google Scholar 

  • Lu F, Cui X, Zhang S, Jenuwein T, Cao X (2011) Arabidopsis REF6 is a histone H3 lysine 27 demethylase. Nat Genet 43(7):715–719

    Article  PubMed  CAS  Google Scholar 

  • Michaels SD, Amasino RM (1999) FLOWERING LOCUS C encodes a novel MADS domain protein that acts as a repressor of flowering. Plant Cell 11(5):949–956

    PubMed  CAS  Google Scholar 

  • Miura A, Nakamura M, Inagaki S, Kobayashi A, Saze H, Kakutani T (2009) An Arabidopsis jmjC domain protein protects transcribed genes from DNA methylation at CHG sites. EMBO J 28(8):1078–1086

    Article  PubMed  CAS  Google Scholar 

  • Mosammaparast N, Shi Y (2010) Reversal of histone methylation: biochemical and molecular mechanisms of histone demethylases. Annu Rev Biochem 79:155–179

    Article  PubMed  CAS  Google Scholar 

  • Mylne J, Greb T, Lister C, Dean C (2004) Epigenetic regulation in the control of flowering. Cold Spring Harb Symp Quant Biol 69:457–464

    Article  PubMed  CAS  Google Scholar 

  • Noh B, Lee SH, Kim HJ, Yi G, Shin EA, Lee M, Jung KJ, Doyle MR, Amasino RM, Noh YS (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(10):2601–2613

    Article  PubMed  CAS  Google Scholar 

  • Pagnussat GC, Yu HJ, Ngo QA, Rajani S, Mayalagu S, Johnson CS, Capron A, Xie LF, Ye D, Sundaresan V (2005) Genetic and molecular identification of genes required for female gametophyte development and function in Arabidopsis. Development 132(3):603–614

    Article  PubMed  CAS  Google Scholar 

  • Pien S, Fleury D, Mylne JS, Crevillen P, Inze D, Avramova Z, Dean C, Grossniklaus U (2008) ARABIDOPSIS TRITHORAX1 dynamically regulates FLOWERING LOCUS C activation via histone 3 lysine 4 trimethylation. Plant Cell 20(3):580–588

    Article  PubMed  CAS  Google Scholar 

  • Reyes JC (2006) Chromatin modifiers that control plant development. Curr Opin Plant Biol 9(1):21–27

    Article  PubMed  CAS  Google Scholar 

  • Saleh A, Alvarez-Venegas R, Avramova Z (2008) An efficient chromatin immunoprecipitation (ChIP) protocol for studying histone modifications in Arabidopsis plants. Nat Protoc 3(6):1018–1025

    Article  PubMed  CAS  Google Scholar 

  • Saze H, Shiraishi A, Miura A, Kakutani T (2008) Control of genic DNA methylation by a jmjC domain-containing protein in Arabidopsis thaliana. Science 319(5862):462–465

    Article  PubMed  CAS  Google Scholar 

  • Searle IR, Pontes O, Melnyk CW, Smith LM, Baulcombe DC (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(10):986–991

    Article  PubMed  CAS  Google Scholar 

  • Secombe J, Li L, Carlos L, Eisenman RN (2007) The Trithorax group protein Lid is a trimethyl histone H3K4 demethylase required for dMyc-induced cell growth. Genes Dev 21(5):537–551

    Article  PubMed  CAS  Google Scholar 

  • Sheldon CC, Hills MJ, Lister C, Dean C, Dennis ES, Peacock WJ (2008) Resetting of FLOWERING LOCUS C expression after epigenetic repression by vernalization. Proc Natl Acad Sci USA 105(6):2214–2219

    Article  PubMed  CAS  Google Scholar 

  • Shi Y, Lan F, Matson C, Mulligan P, Whetstine JR, Cole PA, Casero RA (2004) Histone demethylation mediated by the nuclear amine oxidase homolog LSD1. Cell 119(7):941–953

    Article  PubMed  CAS  Google Scholar 

  • Shindo C, Lister C, Crevillen P, Nordborg M, Dean C (2006) Variation in the epigenetic silencing of FLC contributes to natural variation in Arabidopsis vernalization response. Genes Dev 20(22):3079–3083

    Article  PubMed  CAS  Google Scholar 

  • Sun Q, Zhou DX (2008) Rice jmjC domain-containing gene JMJ706 encodes H3K9 demethylase required for floral organ development. Proc Natl Acad Sci USA 105(36):13679–13684

    Article  PubMed  CAS  Google Scholar 

  • Sung S, Amasino RM (2004) Vernalization in Arabidopsis thaliana is mediated by the PHD finger protein VIN3. Nature 427(6970):159–164

    Article  PubMed  CAS  Google Scholar 

  • Sung S, Amasino RM (2005) Remembering winter: toward a molecular understanding of vernalization. Annu Rev Plant Biol 56:491–508

    Article  PubMed  CAS  Google Scholar 

  • Sung S, He Y, Eshoo TW, Tamada Y, Johnson L, Nakahigashi K, Goto K, Jacobsen SE, Amasino RM (2006) Epigenetic maintenance of the vernalized state in Arabidopsis thaliana requires LIKE HETEROCHROMATIN PROTEIN 1. Nat Genet 38(6):706–710

    Article  PubMed  CAS  Google Scholar 

  • 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(10):3257–3269

    Article  PubMed  CAS  Google Scholar 

  • Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24(8):1596–1599

    Article  PubMed  CAS  Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22(22):4673–4680

    Article  PubMed  CAS  Google Scholar 

  • Wang H, Cao R, Xia L, Erdjument-Bromage H, Borchers C, Tempst P, Zhang Y (2001) Purification and functional characterization of a histone H3-lysine 4-specific methyltransferase. Mol Cell 8(6):1207–1217

    Article  PubMed  CAS  Google Scholar 

  • Whetstine JR, Nottke A, Lan F, Huarte M, Smolikov S, Chen Z, Spooner E, Li E, Zhang G, Colaiacovo M, Shi Y (2006) Reversal of histone lysine trimethylation by the JMJD2 family of histone demethylases. Cell 125(3):467–481

    Article  PubMed  CAS  Google Scholar 

  • Yang W, Jiang D, Jiang J, He Y (2010) A plant-specific histone H3 lysine 4 demethylase represses the floral transition in Arabidopsis. Plant J 62(4):663–673

    Article  PubMed  CAS  Google Scholar 

  • Yu X, Li L, Guo M, Chory J, Yin Y (2008) Modulation of brassinosteroid-regulated gene expression by Jumonji domain-containing proteins ELF6 and REF6 in Arabidopsis. Proc Natl Acad Sci USA 105(21):7618–7623

    Article  PubMed  CAS  Google Scholar 

  • Zhang X, Germann S, Blus BJ, Khorasanizadeh S, Gaudin V, Jacobsen SE (2007) The Arabidopsis LHP1 protein colocalizes with histone H3 Lys27 trimethylation. Nat Struct Mol Biol 14(9):869–871

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

We thank Dr. Jessica Habashi for critical reading of the manuscript, and the ABRC for the T-DNA insertion line. This work was supported by grants from the National Basic Research Program of China (973 Program) (2012CB910900 and 2012CB114200), and Hebei Province key laboratory program.

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Correspondence to Ligeng Ma.

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Communicatòed by K. Chong.

H. Yang and H. Mo contributed equally to this work.

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Yang, H., Mo, H., Fan, D. et al. Overexpression of a histone H3K4 demethylase, JMJ15, accelerates flowering time in Arabidopsis . Plant Cell Rep 31, 1297–1308 (2012). https://doi.org/10.1007/s00299-012-1249-5

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