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Evolution and conservation of JmjC domain proteins in the green lineage

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Abstract

Histone modification regulates plant development events by epigenetically silencing or activating gene expression, and histone methylation is regulated by histone lysine methyltransferases (KMTs) and histone lysine demethylases (KDMs). The JmjC domain proteins, an important KDM family, erase methyl marks (CH3-) from histones and play key roles in maintaining homeostasis of histone methylation in vivo. Here, we analyzed 169 JmjC domain proteins from whole genomes of plants ranging from green alga to higher plants together with 36 from two animals (fruit fly and human). The plant JmjC domain proteins were divided into seven groups. Group-I KDM4/JHDM3 and Group-V JMJD6 were found in all the plant species and the other groups were detected mainly in vascular or seed plants. Group-I KDM4/JHDM3 was potentially associated with demethylation of H3K9me2/3, H3K27me2/3, and H3K36me1/2/3, Group-II KDM5A with H3K4me1/2/3, Group-III KDM5B with H3K4me1/2/3 and H3K9me1/2/3, Group-V JMJD6 with H3R2, H4R3, and hydroxylation of H4, and Group-VII KDM3/JHDM2 with H3K9me1/2/3. Group-IV/Group-VI JmjC domain-only A/B proteins were involved in hydroxylation and demethylation of unknown substrate sites. The binding sites for the cofactors Fe(II) and α-ketoglutarate in the JmjC domains also were analyzed. In the α-ketoglutarate binding sites, Thr/Phe/Ser and Lys were conserved and in the Fe(II) binding sites, two His and Glu/Asp were conserved. The results show that JmjC domain proteins are a conserved family in which domain organization and cofactor binding sites have been modified in some species. Our results provide insights into KDM evolution and lay a foundation for functional characterization of KDMs.

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References

  • Allis CD, Berger SL, Cote J, Dent S, Jenuwien T, Kouzarides T, Pillus L, Reinberg D, Shi Y, Shiekhattar R, Shilatifard A, Workman J, Zhang Y (2007) New nomenclature for chromatin-modifying enzymes. Cell 131(4):633–636

    Article  PubMed  CAS  Google Scholar 

  • Audonnet L (2014) Caractérisation fonctionnelle de JMJ24, une déméthylase d’histone de la famille JUMONJI, chez Arabidopsis thaliana (D). Université Paris Sud

  • Ay N, Janack B, Humbeck K (2014) Epigenetic control of plant senescence and linked processes. J Exp Bot 65(14):3875–3887

    Article  PubMed  Google Scholar 

  • Bachi A, Braun IC, Rodrigues JP, Panté N, Ribbeck K, von Kobbe C, Kutay U, Wilm M, Görlich D, Carmo-Fonseca M, Izaurralde E (2000) The C-terminal domain of TAP interacts with the nuclear pore complex and promotes export of specific CTE-bearing RNA substrates. RNA 6(1):136–158

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Banerjee T, Chakravarti D (2011) A peek into the complex realm of histone phosphorylation. Mol Cell Biol 31(24):4858–4873

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Bannister AJ, Kouzarides T (2011) Regulation of chromatin by histone modifications. Cell Res 21(3):381–395

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Benevolenskaya EV (2007) Histone H3K4 demethylases are essential in development and differentiation. Biochem Cell Biol 85(4):435–443

    Article  PubMed  CAS  Google Scholar 

  • Binda O (2013) On your histone mark, SET, methylate. Epigenetics 8(5):457–463

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Bustin M, Trieschmann L, Postnikov YV (1995) The HMG-14/-17 chromosomal protein family: architectural elements that enhance transcription from chromatin templates. Semin Cell Biol 6(4):247–255

    Article  PubMed  CAS  Google Scholar 

  • Chang B, Chen Y, Zhao Y, Bruick RK (2007) JMJD6 is a histone arginine demethylase. Science 318(5849):444–447

    Article  PubMed  CAS  Google Scholar 

  • Chen YW, Allen MD, Veprintsev DB, Löwe J, Bycroft M (2004) The structure of the AXH domain of spinocerebellar ataxin-1. J Biol Chem 279(5):3758–3765

    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 

  • Chen X, Hu Y, Zhou DX (2011) Epigenetic gene regulation by plant Jumonji group of histone demethylase. Biochim Biophys Acta 1809(8):421–426

    Article  PubMed  CAS  Google Scholar 

  • Chen S, Ma J, Wu F, Xiong LJ, Ma H, Xu W, Lv R, Li X, Villen J, Gygi SP, Liu XS, Shi Y (2012) The histone H3 Lys 27 demethylase JMJD3 regulates gene expression by impacting transcriptional elongation. Genes Dev 26(12):1364–1375

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Chen Q, Chen X, Wang Q, Zhang F, Lou Z, Zhang Q, Zhou DX (2013) Structural basis of a histone H3 lysine 4 demethylase required for stem elongation in rice. PLoS Genet 9(1):e1003239

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Cho JN, Ryu JY, Jeong YM, Park J, Song JJ, Amasino RM, Noh B, Noh YS (2012) Control of seed germination by light-induced histone arginine demethylation activity. Dev Cell 22(4):736–748

    Article  PubMed  CAS  Google Scholar 

  • Cox R, Mason-Gamer RJ, Jackson CL, Segev N (2004) Phylogenetic analysis of Sec7-domain-containing Arf nucleotide exchangers. Mol Biol Cell 15(4):1487–1505

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Craig KL, Tyers M (1999) The F-box: a new motif for ubiquitin dependent proteolysis in cell cycle regulation and signal transduction. Prog Biophys Mol Biol 72(3):299–328

    Article  PubMed  CAS  Google Scholar 

  • de Chiara C, Giannini C, Adinolfi S, de Boer J, Guida S, Ramos A, Jodice C, Kioussis D, Pastore A (2003) The AXH module: an independently folded domain common to ataxin-1 and HBP1. FEBS Lett 551(1–3):107–112

    Article  PubMed  CAS  Google Scholar 

  • Del Rizzo PA, Krishnan S, Trievel RC (2012) Crystal structure and functional analysis of JMJD5 indicate an alternate specificity and function. Mol Cell Biol 32(19):4044–4052

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Dupont C, Armant DR, Brenner CA (2009) Epigenetics: definition, mechanisms and clinical perspective. Semin Reprod Med 27(5):351–357

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Erickson D (2012) Role of histone demethylases in pathogen defense. Syracuse University Honors Program Capstone Projects. p140

  • Fan D, Dai Y, Wang X, Wang Z, He H, Yang H, Cao Y, Deng XW, Ma L (2012) IBM1, a JmjC domain-containing histone demethylase, is involved in the regulation of RNA-directed DNA methylation through the epigenetic control of RDR2 and DCL3 expression in Arabidopsis. Nucleic Acids Res 40(18):8905–8916

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Feng T, Yamamoto A, Wilkins SE, Sokolova E, Yates LA, Münzel M, Singh P, Hopkinson RJ, Fischer R, Cockman ME, Shelley J, Trudgian DC, Schödel J, McCullagh JS, Ge W, Kessler BM, Gilbert RJ, Frolova LY, Alkalaeva E, Ratcliffe PJ, Schofield CJ, Coleman ML (2014) Optimal translational termination requires C4 lysyl hydroxylation of eRF1. Mol Cell 53(4):645–654

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • García-Alai MM, Allen MD, Joerger AC, Bycroft M (2010) The structure of the FYR domain of transforming growth factor beta regulator 1. Protein Sci 19(7):1432–1438

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Gelato KA, Fischle W (2008) Role of histone modifications in defining chromatin structure and function. Biol Chem 389(4):353–363

    Article  PubMed  CAS  Google Scholar 

  • Hahn P, Wegener I, Burrells A, Böse J, Wolf A, Erck C, Butler D, Schofield CJ, Böttger A, Lengeling A (2010) Analysis of Jmjd6 cellular localization and testing for its involvement in histone demethylation. PLoS One 5(10):e13769

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Han G, Li J, Wang Y, Li X, Mao H, Liu Y, Chen CD (2012) The hydroxylation activity of Jmjd6 is required for its homo-oligomerization. J Cell Biochem 113(5):1663–1670

    PubMed  CAS  Google Scholar 

  • Holec S, Berger F (2012) Polycomb group complexes mediate developmental transitions in plants. Plant Physiol 158(1):35–43

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Hong MJ, Kim DY, Lee TG, Jeon WB, Seo YW (2010) Functional characterization of pectin methylesterase inhibitor (PMEI) in wheat. Genes Genet Syst 85(2):97–106

    Article  PubMed  CAS  Google Scholar 

  • Hou H, Yu H (2010) Structural insights into histone lysine demethylation. Curr Opin Struct Biol 20(6):739–748

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Huang F, Chandrasekharan MB, Chen YC, Bhaskara S, Hiebert SW, Sun ZW (2010) The JmjN domain of Jhd2 is important for its protein stability, and the plant homeodomain (PHD) finger mediates its chromatin association independent of H3K4 methylation. J Biol Chem 285(32):24548–24561

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Huang Y, Liu C, Shen WH, Ruan Y (2011) Phylogenetic analysis and classification of the Brassica rapa SET-domain protein family. BMC Plant Biol 11:175

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Ishimura A, Minehata K, Terashima M, Kondoh G, Hara T, Suzuki T (2012) Jmjd5, an H3K36me2 histone demethylase, modulates embryonic cell proliferation through the regulation of Cdkn1a expression. Development 139(4):749–759

    Article  PubMed  CAS  Google Scholar 

  • Jain M, Nijhawan A, Arora R, Agarwal P, Ray S, Sharma P, Kapoor S, Tyagi AK, Khurana JP (2007) F-box proteins in rice. Genome-wide analysis, classification, temporal and spatial gene expression during panicle and seed development, and regulation by light and abiotic stress. Plant Physiol 143(4):1467–1483

    Article  PubMed  CAS  PubMed Central  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  PubMed Central  CAS  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  PubMed Central  Google Scholar 

  • Joazeiro CA, Weissman AM (2000) RING finger proteins: mediators of ubiquitin ligase activity. Cell 102(5):549–552

    Article  PubMed  CAS  Google Scholar 

  • Jones MA, Harmer S (2011) JMJD5 Functions in concert with TOC1 in the Arabidopsis circadian system. Plant Signal Behav 6(3):445–448

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Jones B, Su H, Bhat A, Lei H, Bajko J, Hevi S, Baltus GA, Kadam S, Zhai H, Valdez R, Gonzalo S, Zhang Y, Li E, Chen T (2008) The histone H3K79 methyltransferase Dot1L is essential for mammalian development and heterochromatin structure. PLoS Genet 4(9):e1000190

    Article  PubMed  PubMed Central  CAS  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. PNAS 107(50):21623–21628

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Kalkhoven E, Teunissen H, Houweling A, Verrijzer CP, Zantema A (2002) The PHD type zinc finger is an integral part of the CBP acetyltransferase domain. Mol Cell Biol 22(7):1961–1970

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Kim S, Zhang Z, Upchurch S, Isern N, Chen Y (2004) Structure and DNA-binding sites of the SWI1 AT-rich interaction domain (ARID) suggest determinants for sequence-specific DNA recognition. J Biol Chem 279(16):16670–16676

    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 

  • Klosterman SJ, Hadwiger LA (2002) Plant HMG proteins bearing the AT-hook motif. Plant Sci 162(6):855–866

    Article  CAS  Google Scholar 

  • Klug A (1999) Zinc finger peptides for the regulation of gene expression. J Mol Biol 293(2):215–218

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Kuroki S, Matoba S, Akiyoshi M, Matsumura Y, Miyachi H, Mise N, Abe K, Ogura A, Wilhelm D, Koopman P, Nozaki M, Kanai Y, Shinkai Y, Tachibana M (2013) Epigenetic regulation of mouse sex determination by the histone demethylase Jmjd1a. Science 341(6150):1106–1109

    Article  PubMed  CAS  Google Scholar 

  • Lan F, Nottke AC, Shi Y (2008) Mechanisms involved in the regulation of histone lysine demethylases. Curr Opin Cell Biol 20:316–325

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Legge GB, Martinez-Yamout MA, Hambly DM, Trinh T, Lee BM, Dyson HJ, Wright PE (2004) ZZ domain of CBP: an unusual zinc finger fold in a protein interaction module. J Mol Biol 343(4):1081–1093

    Article  PubMed  CAS  Google Scholar 

  • Lennartsson A, Ekwall K (2009) Histone modification patterns and epigenetic codes. Biochim Biophys Acta 1790(9):863–868

    Article  PubMed  CAS  Google Scholar 

  • Li Y, Qiu L, Huang L, Cao J (2012) BcJMJ30, the gene encoding jmjC domain-containing histone demethylase is associated with pollen development and fertilization in Brassica campestris ssp. chinensis. Plant Mol Biol Rep 30(3):529–538

    Article  CAS  Google Scholar 

  • Li T, Chen X, Zhong X, Zhao Y, Liu X, Zhou S, Cheng S, Zhou DX (2013) Jumonji C domain protein JMJ705-mediated removal of histone H3 lysine 27 trimethylation is involved in defense-related gene activation in rice. Plant Cell 25(11):4725–4736

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Liang Y, Vogel JL, Arbuckle JH, Rai G, Jadhav A, Simeonov A, Maloney DJ, Kristie TM (2013) Targeting the JMJD2 histone demethylases to epigenetically control herpesvirus infection and reactivation from latency. Sci Transl Med 5(167):167ra5

    Article  PubMed  CAS  Google Scholar 

  • Loh YH, Zhang W, Chen X, George J, Ng HH (2007) Jmjd1a and Jmjd2c histone H3 Lys 9 demethylases regulate self-renewal in embryonic stem cells. Genes Dev 21(20):2545–2557

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Lorick KL, Jensen JP, Fang S, Ong AM, Hatakeyama S, Weissman AM (1999) RING fingers mediate ubiquitin-conjugating enzyme (E2)-dependent ubiquitination. PNAS 96(20):11364–11369

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Lu J, Matunis MJ (2013) A mediator methylation mystery: JMJD1C demethylates MDC1 to regulate DNA repair. Nat Struct Mol Biol 20(12):1346–1348

    Article  PubMed  CAS  PubMed Central  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 (2010) JMJ14 is an H3K4 demethylase regulating flowering time in Arabidopsis. Cell Res 20:387–390

    Article  PubMed  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Lu SX, Knowles SM, Webb CJ, Celaya RB, Cha C, Siu JP, Tobin EM (2011b) The Jumonji C domain-containing protein JMJ30 regulates period length in the Arabidopsis circadian clock. Plant Physiol 155(2):906–915

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Lu J, Marjon KD, Mold C, Du Clos TW, Sun PD (2013) Pentraxins and Fc receptors. Immunol Rev 250(1):230–238

    Article  CAS  Google Scholar 

  • Luo M, Hung FY, Yang S, Liu X, Wu K (2014) Histone lysine demethylases and their functions in plants. Plant Mol Biol Rep 32(2):558–565

    Article  CAS  Google Scholar 

  • Maris C, Dominguez C, Allain FH (2005) The RNA recognition motif, a plastic RNA-binding platform to regulate post transcriptional gene expression. FEBS J 272(9):2118–2131

    Article  PubMed  CAS  Google Scholar 

  • Metzger E, Wissmann M, Yin N, Müller JM, Schneider R, Peters AH, Günther T, Buettner R, Schüle R (2005) LSD1 demethylates repressive histone marks to promote androgen-receptor-dependent transcription. Nature 437(7057):436–439

    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 

  • Mossessova E, Gulbis JM, Goldberg J (1998) Structure of the guanine nucleotide exchange factor Sec7 domain of human arno and analysis of the interaction with ARF GTPase. Cell 92(3):415–423

    Article  PubMed  CAS  Google Scholar 

  • Nguyen AT, Zhang Y (2011) The diverse functions of Dot1 and H3K79 methylation. GenesDev 25(13):1345–1358

    Article  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  PubMed Central  Google Scholar 

  • Park SJ, Kim JG, Son TG, Yi JM, Kim ND, Yang K, Heo K (2013) The histone demethylase JMJD1A regulates adrenomedullin-mediated cell proliferation in hepatocellular carcinoma under hypoxia. Biochem Biophys Res Commun 434(4):722–727

    Article  PubMed  CAS  Google Scholar 

  • Pasini D, Cloos PA, Walfridsson J, Olsson L, Bukowski JP, Johansen JV, Bak M, Tommerup N, Rappsilber J, Helin K (2010) JARID2 regulates binding of the Polycomb repressive complex 2 to target genes in ES cells. Nature 464(7286):306–310

    Article  PubMed  CAS  Google Scholar 

  • Patsialou A, Wilsker D, Moran E (2005) DNA-binding properties of ARID family proteins. Nucleic Acids Res 33(1):66–80

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Pilka ES, James T, Lisztwan JH (2015) Structural definitions of Jumonji family demethylase selectivity. Drug Discov Today. doi:10.1016/j.drudis.2014.12.013

    PubMed  Google Scholar 

  • Ponting CP, Blake DJ, Davies KE, Kendrick-Jones J, Winder SJ (1996) ZZ and TAZ: new putative zinc fingers in dystrophin and other proteins. Trends Biochem Sci 21(1):11–13

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Qi HH, Sarkissian M, Hu GQ, Wang Z, Bhattacharjee A, Gordon DB, Gonzales M, Lan F, Ongusaha PP, Huarte M, Yaghi NK, Lim H, Garcia BA, Brizuela L, Zhao K, Roberts TM, Shi Y (2010) Histone H4K20/H3K9 demethylase PHF8 regulates zebrafish brain and craniofacial development. Nature 466(7305):503–507

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Quan Z, Oliver SG, Zhang N (2011) JmjN interacts with JmjC to ensure selective proteolysis of Gis1 by the proteasome. Microbiology 157(Pt 9):2694–2701

    Article  PubMed  CAS  Google Scholar 

  • Rotili D, Mai A (2011) Targeting histone demethylases: a new avenue for the fight against cancer. Genes Cancer 2(6):663–679

    Article  PubMed  CAS  PubMed Central  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  PubMed Central  Google Scholar 

  • Secombe J, Eisenman RN (2007) The function and regulation of the JARID1 family of histone H3 lysine 4 demethylases: the Myc connection. Cell Cycle 6(11):1324–1328

    Article  PubMed  CAS  Google Scholar 

  • Shahbazian MD, Grunstein M (2007) Functions of site-specific histone acetylation and deacetylation. Annu Rev Biochem 76:75–100

    Article  PubMed  CAS  Google Scholar 

  • Shen Y, Conde E, Silva N, Audonnet L, Servet C, Wei W, Zhou DX (2014) Over-expression of histone H3K4 demethylase gene JMJ15 enhances salt tolerance in Arabidopsis. Front Plant Sci 5:290

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Smit JJ, Monteferrario D, Noordermeer SM, van Dijk WJ, van der Reijden BA, Sixma TK (2012) The E3 ligase HOIP specifies linear ubiquitin chain assembly through its RING-IBR-RING domain and the unique LDD extension. EMBO J 31(19):3833–3844

    Article  PubMed  CAS  PubMed Central  Google Scholar 

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

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Takeuchi T, Yamazaki Y, Katoh-Fukui Y, Tsuchiya R, Kondo S, Motoyama J, Higashinakagawa T (1995) Gene trap capture of a novel mouse gene, jumonji, required for neural tube formation. Genes Dev 9(10):1211–1222

    Article  PubMed  CAS  Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30(12):2725–2729

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Tee AE, Ling D, Nelson C, Atmadibrata B, Dinger ME, Xu N, Mizukami T, Liu PY, Liu B, Cheung B, Pasquier E, Haber M, Norris MD, Suzuki T, Marshall GM, Liu T (2014) The histone demethylase JMJD1A induces cell migration and invasion by up-regulating the expression of the long noncoding RNA MALAT1. Oncotarget 5(7):1793–1804

    Article  PubMed  PubMed Central  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  PubMed Central  Google Scholar 

  • Thorstensen T, Grini PE, Aalen RB (2011) SET domain proteins in plant development. Biochim Biophys Acta 1809(8):407–420

    Article  PubMed  CAS  Google Scholar 

  • Tschiersch B, Hofmann A, Krauss V, Dorn R, Korge G, Reuter G (1994) The protein encoded by the Drosophila position-effect variegation suppressor gene Su(var)3-9 combines domains of antagonistic regulators of homeotic gene complexes. EMBO J 13:3822–3831

    PubMed  CAS  PubMed Central  Google Scholar 

  • Tsukada Y, Fang J, Erdjument-Bromage H, Warren ME, Borchers CH, Tempst P, Zhang Y (2006) Histone demethylation by a family of JmjC domain-containing proteins. Nature 439(7078):811–816

    Article  PubMed  CAS  Google Scholar 

  • van Leeuwen F, Gottschling DE (2002) Genome-wide histone modifications: gaining specificity by preventing promiscuity. Curr Opin Cell Biol 14(6):756–762

    Article  PubMed  CAS  Google Scholar 

  • Wang L, Dong L, Zhang Y, Zhang Y, Wu W, Deng X, Xue Y (2004) Genome-wide analysis of S-Locus F-box-like genes in Arabidopsis thaliana. Plant Mol Biol 56(6):929–945

    Article  PubMed  CAS  Google Scholar 

  • Wang X, Wang H, Wang J, Sun R, Wu J, Liu S, Bai Y, Mun JH, Bancroft I, Cheng F, Huang S, Li X, Hua W, Wang J, Wang X, Freeling M, Pires JC, Paterson AH, Chalhoub B, Wang B, Hayward A, Sharpe AG, Park BS, Weisshaar B, Liu B, Li B, Liu B, Tong C, Song C, Duran C, Peng C, Geng C, Koh C, Lin C, Edwards D, Mu D, Shen D, Soumpourou E, Li F, Fraser F, Conant G, Lassalle G, King GJ, Bonnema G, Tang H, Wang H, Belcram H, Zhou H, Hirakawa H, Abe H, Guo H, Wang H, Jin H, Parkin IA, Batley J, Kim JS, Just J, Li J, Xu J, Deng J, Kim JA, Li J, Yu J, Meng J, Wang J, Min J, Poulain J, Wang J, Hatakeyama K, Wu K, Wang L, Fang L, Trick M, Links MG, Zhao M, Jin M, Ramchiary N, Drou N, Berkman PJ, Cai Q, Huang Q, Li R, Tabata S, Cheng S, Zhang S, Zhang S, Huang S, Sato S, Sun S, Kwon SJ, Choi SR, Lee TH, Fan W, Zhao X, Tan X, Xu X, Wang Y, Qiu Y, Yin Y, Li Y, Du Y, Liao Y, Lim Y, Narusaka Y, Wang Y, Wang Z, Li Z, Wang Z, Xiong Z, Zhang Z (2011) The genome of the mesopolyploid crop species Brassica rapa. Nat Genet 43(10):1035–1039

    Article  PubMed  CAS  Google Scholar 

  • Wang F, He L, Huangyang P, Liang J, Si W, Yan R, Han X, Liu S, Gui B, Li W, Miao D, Jing C, Liu Z, Pei F, Sun L, Shang Y (2014) JMJD6 promotes colon carcinogenesis through negative regulation of p53 by hydroxylation. PLoS Biol 12(3):e1001819

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Watanabe S, Watanabe K, Akimov V, Bartkova J, Blagoev B, Lukas J, Bartek J (2013) JMJD1C demethylates MDC1 to regulate the RNF8 and BRCA1-mediated chromatin response to DNA breaks. Nat Struct Mol Biol 20(12):1425–1433

    Article  PubMed  CAS  Google Scholar 

  • Wu CT, Morris JR (2001) Genes, genetics, and epigenetics: a correspondence. Science 293(5532):1103–1105

    Article  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 

  • Yang H, Mo H, Fan D, Cao Y, Cui S, Ma L (2012a) Overexpression of a histone H3K4 demethylase, JMJ15, accelerates flowering time in Arabidopsis. Plant Cell Rep 31(7):1297–1308

    Article  PubMed  CAS  Google Scholar 

  • Yang H, Han Z, Cao Y, Fan D, Li H, Mo H, Feng Y, Liu L, Wang Z, Yue Y, Cui S, Chen S, Chai J, Ma L (2012b) A companion cell-dominant and developmentally regulated H3K4 demethylase controls flowering time in Arabidopsis via the repression of FLC expression. PLoS Genet 8(4):e1002664

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Yu X, Li L, 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. PNAS 105(21):7618–7623

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Zhou X, Ma H (2008) Evolutionary history of histone demethylase families: distinct evolutionary patterns suggest functional divergence. BMC Evol Biol 8:294

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zhu H, Hu S, Baker J (2014) JMJD5 regulates cell cycle and pluripotency in human embryonic stem cells. Stem Cells 32(8):2098–2110

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

This work was funded in part by Open Fund of Innovation Platform in University of Hunan (14K046), Hunan Provincial Education Department of China (13B045) and Natural Science Foundation of Hunan Province of China (2015JJ3075).

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Correspondence to Yong Huang or Ying Ruan.

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This article does not contain any studies with animals performed by any of the authors.

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Communicated by S. Hohmann.

Authors Y. Huang and D. Chen contributed equally to this work.

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Huang, Y., Chen, D., Liu, C. et al. Evolution and conservation of JmjC domain proteins in the green lineage. Mol Genet Genomics 291, 33–49 (2016). https://doi.org/10.1007/s00438-015-1089-4

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