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H3K4 trimethylation dynamics impact diverse developmental and environmental responses in plants

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Abstract

Main conclusion

The H3K4me3 histone mark in plants functions in the regulation of gene expression and transcriptional memory, and influences numerous developmental processes and stress responses.

Abstract

Plants execute developmental programs and respond to changing environmental conditions via adjustments in gene expression, which are modulated in part by chromatin structure dynamics. Histone modifications alter chromatin in precise ways on a global scale, having the potential to influence the expression of numerous genes. Trimethylation of lysine 4 on histone H3 (H3K4me3) is a prominent histone modification that is dogmatically associated with gene activity, but more recently has also been linked to gene repression. As in other eukaryotes, the distribution of H3K4me3 in plant genomes suggests it plays a central role in gene expression regulation, however the underlying mechanisms are not fully understood. Transcript levels of many genes related to flowering, root, and shoot development are affected by dynamic H3K4me3 levels, as are those for a number of stress-responsive and stress memory-related genes. This review examines the current understanding of how H3K4me3 functions in modulating plant responses to developmental and environmental cues.

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References

  • Alonso C, Ramos-Cruz D, Becker C (2019) The role of plant epigenetics in biotic interactions. New Phytol 221(2):731–737

    Article  CAS  PubMed  Google Scholar 

  • 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(16):5199–5207

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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(8):627–637

    Article  CAS  PubMed  Google Scholar 

  • Alvarez-Venegas R, Abdallat AA, Guo M, Alfano JR, Avramova Z (2007) Epigenetic control of a transcription factor at the cross section of two antagonistic pathways. Epigenetics 2(2):106–113

    Article  PubMed  Google Scholar 

  • Avramova Z (2009) Evolution and pleiotropy of TRITHORAX function in Arabidopsis. Int J Dev Biol 53:371

    Article  CAS  PubMed  Google Scholar 

  • Barski A, Cuddapah S, Cui K, Roh T-Y, Schones DE, Wang Z, Wei G, Chepelev I, Zhao K (2007) High-resolution profiling of histone methylations in the human genome. Cell 129(4):823–837

    Article  CAS  PubMed  Google Scholar 

  • Bellegarde F, Maghiaoui A, Boucherez J, Krouk G, Lejay L, Bach L, Gojon A, Martin A (2019) The chromatin factor HNI9 and ELONGATED HYPOCOTYL5 maintain ROS homeostasis under high nitrogen provision. Plant Physiol 180(1):582–592. https://doi.org/10.1104/pp.18.01473

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bernstein BE, Humphrey EL, Erlich RL, Schneider R, Bouman P, Liu JS, Kouzarides T, Schreiber SL (2002) Methylation of histone H3 Lys 4 in coding regions of active genes. Proc Natl Acad Sci 99(13):8695–8700

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bernstein BE, Mikkelsen TS, Xie X, Kamal M, Huebert DJ, Cuff J, Fry B, Meissner A, Wernig M, Plath K, Jaenisch R, Wagschal A, Feil R, Schreiber SL, Lander ES (2006) A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell 125(2):315–326. https://doi.org/10.1016/j.cell.2006.02.041

    Article  CAS  PubMed  Google Scholar 

  • Berr A, Xu L, 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(3):1476–1485

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Berr A, McCallum EJ, Ménard R, Meyer D, Fuchs J, Dong A, Shen W-H (2010) Arabidopsis SET DOMAIN GROUP2 is required for H3K4 trimethylation and is crucial for both sporophyte and gametophyte development. Plant Cell 22(10):3232–3248

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bouyer D, Roudier F, Heese M, Andersen ED, Gey D, Nowack MK, Goodrich J, Renou JP, Grini PE, Colot V, Schnittger A (2011) Polycomb repressive complex 2 controls the embryo-to-seedling phase transition. PLoS Genet 7(3):e1002014. https://doi.org/10.1371/journal.pgen.1002014

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brusslan JA, Alvarez-Canterbury AMR, Nair NU, Rice JC, Hitchler MJ, Pellegrini M (2012) Genome-wide evaluation of histone methylation changes associated with leaf senescence in Arabidopsis. PLoS ONE 7(3):e33151

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brusslan JA, Bonora G, Rus-Canterbury AM, Tariq F, Jaroszewicz A, Pellegrini M (2015) A genome-wide chronological study of gene expression and two histone modifications, H3K4me3 and H3K9ac, during developmental leaf senescence. Plant Physiol 168(4):1246–1261

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cai H, Zhang M, Chai M, He Q, Huang X, Zhao L, Qin Y (2019) Epigenetic regulation of anthocyanin biosynthesis by an antagonistic interaction between H2A. Z and H3K4me3. New Phytol 221(1):295–308

    Article  CAS  PubMed  Google Scholar 

  • Calero G, Wilson KF, Ly T, Rios-Steiner JL, Clardy JC, Cerione RA (2002) Structural basis of m7G pppG binding to the nuclear cap-binding protein complex. Nat Struct Mol Biol 9(12):912–917

    Article  CAS  Google Scholar 

  • Carlone DL, Skalnik DG (2001) CpG binding protein is crucial for early embryonic development. Mol Cell Biol 21(22):7601–7606

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chandrika NNP, Sundaravelpandian K, Yu SM, Schmidt W (2013) ALFIN-LIKE 6 is involved in root hair elongation during phosphate deficiency in Arabidopsis. New Phytol 198(3):709–720

    Article  CAS  PubMed  Google Scholar 

  • Chen X, Hu Y (1809) Zhou D-X (2011) Epigenetic gene regulation by plant Jumonji group of histone demethylase. Biochimica et Biophysica Acta (BBA)-Gene Regulat Mech 8:421–426

    Google Scholar 

  • Chen L-T, Luo M, Wang Y-Y, Wu K (2010) Involvement of Arabidopsi s histone deacetylase HDA6 in ABA and salt stress response. J Exp Bot 61(12):3345–3353

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen K, Chen Z, Wu D, Zhang L, Lin X, Su J, Rodriguez B, Xi Y, Xia Z, Chen X (2015) Broad H3K4me3 is associated with increased transcription elongation and enhancer activity at tumor-suppressor genes. Nat Genet 47(10):1149

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen L, Luo J, Cui Z, Xue M, Wang L, Zhang X, Pawlowski WP, He Y (2017) ATX3, ATX4, and ATX5 encode putative H3K4 methyltransferases and are critical for plant development. Plant Physiol 174:1795

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Choi SC, Lee S, Kim S-R, Lee Y-S, Liu C, Cao X, An G (2014) Trithorax group protein Oryza sativa Trithorax1 controls flowering time in rice via interaction with early heading date3. Plant Physiol 164(3):1326–1337

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Clouaire T, Webb S, Skene P, Illingworth R, Kerr A, Andrews R, Lee J-H, Skalnik D, Bird A (2012) Cfp1 integrates both CpG content and gene activity for accurate H3K4me3 deposition in embryonic stem cells. Genes Dev 26(15):1714–1728

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Crevillen P, Yang H, Cui X, Greeff C, Trick M, Qiu Q, Cao X, Dean C (2014) Epigenetic reprogramming that prevents transgenerational inheritance of the vernalized state. Nature 515(7528):587–590. https://doi.org/10.1038/nature13722

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cruz C, Della Rosa M, Krueger C, Gao Q, Horkai D, King M, Field L, Houseley J (2018) Tri-methylation of histone H3 lysine 4 facilitates gene expression in ageing cells. Elife 7:e34081

    Article  PubMed  PubMed Central  Google Scholar 

  • Cui P, Liu W, Zhao Y, Lin Q, Ding F, Xin C, Geng J, Song S, Sun F, Hu S, Yu J (2012) The association between H3K4me3 and antisense transcription. Genom Proteom Bioinform 10(2):74–81. https://doi.org/10.1016/j.gpb.2012.05.001

    Article  CAS  Google Scholar 

  • Dai X, Bai Y, Zhao L, Dou X, Liu Y, Wang L, Li Y, Li W, Hui Y, Huang X (2017) H2A. Z Represses gene expression by modulating promoter nucleosome structure and enhancer histone modifications in arabidopsis. Molecular plant 10(10):1274–1292

    Article  CAS  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  CAS  PubMed  PubMed Central  Google Scholar 

  • Ding Y, Lapko H, Ndamukong I, Xia Y, Al-Abdallat A, Lalithambika S, Sadder M, Saleh A, Fromm M, Riethoven J-J (2009) The Arabidopsis chromatin modifier ATX1, the Myotubularin-like AtMTM, and the response to drought; a view from the other end of the pathway. Plant signal Behav 4(11):1049–1058

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ding Y, Avramova Z, Fromm M (2011a) The Arabidopsis trithorax-like factor ATX1 functions in dehydration stress responses via ABA-dependent and ABA-independent pathways. Plant J 66(5):735–744

    Article  CAS  PubMed  Google Scholar 

  • Ding Y, Avramova Z, Fromm M (2011b) Two distinct roles of ARABIDOPSIS HOMOLOG OF TRITHORAX1 (ATX1) at promoters and within transcribed regions of ATX1-regulated genes. Plant Cell 23(1):350–363

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ding Y, Fromm M, Avramova Z (2012a) Multiple exposures to drought’train’transcriptional responses in Arabidopsis. Nature Commun 3:740

    Article  Google Scholar 

  • Ding Y, Ndamukong I, Xu Z, Lapko H, Fromm M, Avramova Z (2012b) ATX1-generated H3K4me3 is required for efficient elongation of transcription, not initiation, at ATX1-regulated genes. PLoS Genet 8(12):e1003111

    Article  PubMed  PubMed Central  Google Scholar 

  • D’Urso A, Takahashi YH, Xiong B, Marone J, Coukos R, Randise-Hinchliff C, Wang JP, Shilatifard A, Brickner JH (2016) Set1/COMPASS and Mediator are repurposed to promote epigenetic transcriptional memory. Elife. https://doi.org/10.7554/eLife.16691

    Article  PubMed  PubMed Central  Google Scholar 

  • Engelhorn J, Blanvillain R, Kröner C, Parrinello H, Rohmer M, Posé D, Ott F, Schmid M, Carles CC (2017) Dynamics of H3K4me3 chromatin marks prevails over H3K27me3 for gene regulation during flower morphogenesis in Arabidopsis thaliana. Epigenomes 1(2):8

    Article  Google Scholar 

  • Foroozani M, Zahraeifard S, Oh D-H, Wang G, Dassanayake M, Smith A (2019) Defining chromatin state transitions predicts a network that modulates cell wall remodeling in phosphate-starved rice shoots. bioRxiv. https://doi.org/10.1101/706507

    Article  Google Scholar 

  • Greenberg MV, Deleris A, Hale CJ, Liu A, Feng S, Jacobsen SE (2013) Interplay between active chromatin marks and RNA-directed DNA methylation in Arabidopsis thaliana. PLoS Genet 9(11):e1003946

    Article  PubMed  PubMed Central  Google Scholar 

  • Greer EL, Shi Y (2012) Histone methylation: a dynamic mark in health, disease and inheritance. Nat Rev Genet 13(5):343–357. https://doi.org/10.1038/nrg3173

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guo L, Yu Y, Law JA, Zhang X (2010a) SET DOMAIN GROUP2 is the major histone H3 lysie 4 trimethyltransferase in Arabidopsis. Proc Natl Acad Sci 107:18557

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guo L, Yu Y, Law JA, Zhang X (2010b) SET DOMAIN GROUP2 is the major histone H3 lysine 4 trimethyltransferase in Arabidopsis. Proc Natl Acad Sci 107(43):18557–18562

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hou Y, Wang L, Wang L, Liu L, Li L, Sun L, Rao Q, Zhang J, Huang S (2015) JMJ704 positively regulates rice defense response against Xanthomonas oryzae pv. oryzae infection via reducing H3K4me2/3 associated with negative disease resistance regulators. BMC Plant Biol 15(1):286

    Article  PubMed  PubMed Central  Google Scholar 

  • Howe FS, Boubriak I, Sale MJ, Nair A, Clynes D, Grijzenhout A, Murray SC, Woloszczuk R, Mellor J (2014) Lysine acetylation controls local protein conformation by influencing proline isomerization. Mol Cell 55(5):733–744. https://doi.org/10.1016/j.molcel.2014.07.004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Howe FS, Fischl H, Murray SC, Mellor J (2017) Is H3K4me3 instructive for transcription activation? BioEssays 39(1):1–12. https://doi.org/10.1002/bies.201600095

    Article  CAS  PubMed  Google Scholar 

  • Huang S, Zhang A, Jin JB, Zhao B, Wang TJ, Wu Y, Wang S, Liu Y, Wang J, Guo P (2019) Arabidopsis histone H3K4 demethylase JMJ 17 functions in dehydration stress response. New Phytol 223(3):1372–1387

    Article  CAS  PubMed  Google Scholar 

  • Hussey SG, Loots MT, van der Merwe K, Mizrachi E, Myburg AA (2017) Integrated analysis and transcript abundance modelling of H3K4me3 and H3K27me3 in developing secondary xylem. Sci Rep 7(1):3370. https://doi.org/10.1038/s41598-017-03665-1

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jackson JD, Falciano VT, Gorovsky MA (1996) A likely histone H2A. F/Z variant in Saccharomyces cerevisiae. Trends Biochem Sci 21(12):466–467

    Article  CAS  PubMed  Google Scholar 

  • Jarillo JA, Pineiro M (2015) H2A. Z mediates different aspects of chromatin function and modulates flowering responses in Arabidopsis. Plant J 83(1):96–109. https://doi.org/10.1111/tpj.12873

    Article  CAS  PubMed  Google Scholar 

  • Jaskiewicz M, Conrath U, Peterhänsel C (2011) Chromatin modification acts as a memory for systemic acquired resistance in the plant stress response. EMBO Rep 12(1):50–55

    Article  CAS  PubMed  Google Scholar 

  • Jeong J-H, Song H-R, Ko J-H, Jeong Y-M, Kwon YE, Seol JH, Amasino RM, Noh B, Noh Y-S (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  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  CAS  PubMed  PubMed Central  Google Scholar 

  • Jiang D, Kong NC, Gu X, Li Z, He Y (2011) Arabidopsis COMPASS-like complexes mediate histone H3 lysine-4 trimethylation to control floral transition and plant development. PLoS Genet 7(3):e1001330

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jiang P, Wang S, Zheng H, Li H, Zhang F, Su Y, Xu Z, Lin H, Qian Q, Ding Y (2018) SIP 1 participates in regulation of flowering time in rice by recruiting OsTrx1 to Ehd1. New Phytol 219(1):422–435

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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(10):1580–1588

    Article  CAS  PubMed  Google Scholar 

  • Kohler A, Schwindling S, Conrath U (2002) Benzothiadiazole-induced priming for potentiated responses to pathogen infection, wounding, and infiltration of water into leaves requires the NPR1/NIM1 gene in Arabidopsis. Plant Physiol 128(3):1046–1056

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lämke J, Brzezinka K, Altmann S, Bäurle I (2016) A hit-and-run heat shock factor governs sustained histone methylation and transcriptional stress memory. The EMBO journal 35(2):162–175

    Article  PubMed  Google Scholar 

  • Lee I, Michaels SD, Masshardt AS, Amasino RM (1994) The late-flowering phenotype of FRIGIDA and mutations in LUMINIDEPENDENS is suppressed in the Landsberg erecta strain of Arabidopsis. Plant J 6(6):903–909

    Article  CAS  Google Scholar 

  • Lee WY, Lee D, Chung WI, Kwon CS (2009) Arabidopsis ING and Alfin1-like protein families localize to the nucleus and bind to H3K4me3/2 via plant homeodomain fingers. Plant J 58(3):511–524

    Article  CAS  PubMed  Google Scholar 

  • Lee BB, Choi A, Kim JH, Jun Y, Woo H, Ha SD, Yoon CY, Hwang J-T, Steinmetz L, Buratowski S (2018) Rpd3L HDAC links H3K4me3 to transcriptional repression memory. Nucleic Acids Res 46(16):8261–8274

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee K, Park O-S, Choi CY, Seo PJ (2019) ARABIDOPSIS TRITHORAX 4 facilitates shoot identity establishment during the plant regeneration process. Plant Cell Physiol 60(4):826–834

    Article  CAS  PubMed  Google Scholar 

  • Lenstra TL, Benschop JJ, Kim T, Schulze JM, Brabers NA, Margaritis T, van de Pasch LA, van Heesch SA, Brok MO, Koerkamp MJG (2011) The specificity and topology of chromatin interaction pathways in yeast. Mol Cell 42(4):536–549

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li X, Wang X, He K, Ma Y, Su N, He H, Stolc V, Tongprasit W, Jin W, Jiang J (2008) High-resolution mapping of epigenetic modifications of the rice genome uncovers interplay between DNA methylation, histone methylation, and gene expression. Plant Cell 20(2):259–276

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li Y, Mukherjee I, Thum KE, Tanurdzic M, Katari MS, Obertello M, Edwards MB, McCombie WR, Martienssen RA, Coruzzi GM (2015) The histone methyltransferase SDG8 mediates the epigenetic modification of light and carbon responsive genes in plants. Genome Biol 16:79. https://doi.org/10.1186/s13059-015-0640-2

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li Z, Jiang D, Fu X, Luo X, Liu R, He Y (2016) Coupling of histone methylation and RNA processing by the nuclear mRNA cap-binding complex. Nature Plants 2:16015

    Article  CAS  PubMed  Google Scholar 

  • Li D, Liu R, Singh D, Yuan X, Kachroo P, Raina R (2019) JMJ14 encoded H3K4 demethylase modulates immune responses by regulating defence gene expression and pipecolic acid levels. New Phytol 225:2108

    Article  PubMed  Google Scholar 

  • Liu CL, Kaplan T, Kim M, Buratowski S, Schreiber SL, Friedman N, Rando OJ (2005) Single-nucleosome mapping of histone modifications in S. cerevisiae. PLoS Biol 3(10):e328

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Liu N, Fromm M, Avramova Z (2014) H3K27me3 and H3K4me3 chromatin environment at super-induced dehydration stress memory genes of Arabidopsis thaliana. Molecular plant 7(3):502–513

    Article  CAS  PubMed  Google Scholar 

  • Liu X, Zhou S, Wang W, Ye Y, Zhao Y, Xu Q, Zhou C, Tan F, Cheng S, Zhou D-X (2015) Regulation of histone methylation and reprogramming of gene expression in the rice inflorescence meristem. Plant Cell 27(5):1428–1444

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu K, Yu Y, Dong A, Shen WH (2017) SET DOMAIN GROUP701 encodes a H3K4-methytransferase and regulates multiple key processes of rice plant development. New Phytol 215:609

    Article  CAS  PubMed  Google Scholar 

  • Liu P, Zhang S, Zhou B, Luo X, Zhou XF, Cai B, Jin YH, Niu D, Lin J, Cao X (2019) The histone H3K4 demethylase JMJ16 represses leaf senescence in Arabidopsis. Plant Cell 31(2):430–443

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lopez-Gonzalez L, Mouriz A, Narro-Diego L, Bustos R, Martinez-Zapater JM, Jarillo JA, Pineiro M (2014) Chromatin-dependent repression of the Arabidopsis floral integrator genes involves plant specific PHD-containing proteins. Plant Cell 26(10):3922–3938. https://doi.org/10.1105/tpc.114.130781

    Article  CAS  PubMed  PubMed Central  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(3):387

    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. https://doi.org/10.1038/ng.854

    Article  CAS  PubMed  Google Scholar 

  • Luger K, Mäder AW, Richmond RK, Sargent DF, Richmond TJ (1997) Crystal structure of the nucleosome core particle at 2.8 Å resolution. Nature 389(6648):251

    Article  CAS  PubMed  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 109(52):21540–21545

    Article  CAS  PubMed  PubMed Central  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mittler R, Finka A, Goloubinoff P (2012) How do plants feel the heat? Trends Biochem Sci 37(3):118–125. https://doi.org/10.1016/j.tibs.2011.11.007

    Article  CAS  PubMed  Google Scholar 

  • Molitor AM, Bu Z, Yu Y, Shen W-H (2014) Arabidopsis AL PHD-PRC1 complexes promote seed germination through H3K4me3-to-H3K27me3 chromatin state switch in repression of seed developmental genes. PLoS Genet 10(1):e1004091

    Article  PubMed  PubMed Central  Google Scholar 

  • Mozgova I, Wildhaber T, Liu Q, Abou-Mansour E, L’Haridon F, Metraux J-P, Gruissem W, Hofius D, Hennig L (2015a) Chromatin assembly factor CAF-1 represses priming of plant defence response genes. Nature plants 1(9):15127

    Article  CAS  PubMed  Google Scholar 

  • Mozgova I, Wildhaber T, Liu Q, Abou-Mansour E, L’Haridon F, Metraux J-P, Gruissem W, Hofius D, Hennig L (2015b) Chromatin assembly factor CAF-1 represses priming of plant defence response genes. Nature Plants 1(9):1–8

    Article  Google Scholar 

  • Murray SC, Lorenz P, Howe F, Wouters M, Brown T, Xi S, Fischl H, Khushaim W, Rayappu JR, Angel A (2019) H3K4me3 is neither instructive for, nor informed by, transcription. bioRxiv:709014

  • Mussig C, Kauschmann A, Clouse SD, Altmann T (2000) The Arabidopsis PHD-finger protein SHL is required for proper development and fertility. Mol Gen Genet 264(4):363–370. https://doi.org/10.1007/s004380000313

    Article  CAS  PubMed  Google Scholar 

  • Napsucialy-Mendivil S, Alvarez-Venegas R, Shishkova S, Dubrovsky JG (2014) ARABIDOPSIS HOMOLOG of TRITHORAX1 (ATX1) is required for cell production, patterning, and morphogenesis in root development. J Exp Bot 65(22):6373–6384

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ng DWK, Wang T, Chandrasekharan MB, Aramayo R, Kertbundit S, Hall TC (2007) Plant SET domain-containing proteins: Structure, function and regulation. Biochimica et Biophysica Acta (BBA): Gene Struct and Express 1769(5):316–329. https://doi.org/10.1016/j.bbaexp.2007.04.003

    Article  CAS  Google Scholar 

  • Ning Y-Q, Ma Z-Y, Huang H-W, Mo H, Zhao T-t, Li L, Cai T, Chen S, Ma L, He X-J (2015) Two novel NAC transcription factors regulate gene expression and flowering time by associating with the histone demethylase JMJ14. Nucleic Acids Res 43(3):1469–1484

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pan X, Fang Y, Yang X, Zheng D, Chen L, Wang L, Xiao J, Wang X-e, Wang K, Cheng Z (2017) Chromatin states responsible for the regulation of differentially expressed genes under 60 Co~ γ ray radiation in rice. BMC genomics 18(1):778

    Article  PubMed  PubMed Central  Google Scholar 

  • Park S, Kim GW, Kwon SH, Lee JS (2020) Broad domains of histone H3 lysine 4 trimethylation in transcriptional regulation and disease. FEBS J. https://doi.org/10.1111/febs.15219

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 trimethylation. Plant Cell 20(3):580–588

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pinon V, Yao X, Dong A, Shen W-H (2017) H3K4me3 is crucial for chromatin condensation and mitotic division during male gametogenesis. Plant physiol 174:1205

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Poethig RS (2010) The past, present, and future of vegetative phase change. Plant Physiol 154(2):541–544

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Qian S, Lv X, Scheid RN, Lu L, Yang Z, Chen W, Liu R, Boersma MD, Denu JM, Zhong X, Du J (2018) Dual recognition of H3K4me3 and H3K27me3 by a plant histone reader SHL. Nat Commun 9(1):2425. https://doi.org/10.1038/s41467-018-04836-y

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ram O, Goren A, Amit I, Shoresh N, Yosef N, Ernst J, Kellis M, Gymrek M, Issner R, Coyne M (2011) Combinatorial patterning of chromatin regulators uncovered by genome-wide location analysis in human cells. Cell 147(7):1628–1639

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Roberts MR, Sánchez AL (2019) Plant epigenetic mechanisms in response to biotic stress. In: Alvarez-Venegas R, De-la-Peña C, Casas-Mollano JA (eds) Epigenetics in plants of agronomic importance: Fundamentals and applications. Springer, pp 65–113

  • Roguev A, Schaft D, Shevchenko A, Pijnappel WP, Wilm M, Aasland R, Stewart AF (2001) The Saccharomyces cerevisiae Set1 complex includes an Ash2 homologue and methylates histone 3 lysine 4. The EMBO J 20(24):7137–7148

    Article  CAS  PubMed  Google Scholar 

  • Saleh A, Alvarez-Venegas R, Yilmaz M, Le O, Hou G, Sadder M, Al-Abdallat A, Xia Y, Lu G, Ladunga I (2008) The highly similar Arabidopsis homologs of trithorax ATX1 and ATX2 encode proteins with divergent biochemical functions. Plant Cell 20(3):568–579

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Santos-Rosa H, Schneider R, Bannister AJ, Sherriff J, Bernstein BE, Emre NT, Schreiber SL, Mellor J, Kouzarides T (2002) Active genes are tri-methylated at K4 of histone H3. Nature 419(6905):407–411

    Article  CAS  PubMed  Google Scholar 

  • Schneider J, Wood A, Lee J-S, Schuster R, Dueker J, Maguire C, Swanson SK, Florens L, Washburn MP, Shilatifard A (2005) Molecular regulation of histone H3 trimethylation by COMPASS and the regulation of gene expression. Mol Cell 19(6):849–856

    Article  CAS  PubMed  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  CAS  PubMed  PubMed Central  Google Scholar 

  • Sequeira-Mendes J, Aragüez I, Peiró R, Mendez-Giraldez R, Zhang X, Jacobsen SE, Bastolla U, Gutierrez C (2014) The functional topography of the Arabidopsis genome is organized in a reduced number of linear motifs of chromatin states. Plant Cell 26(6):2351–2366

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shen Y, Conde e Silva N, Audonnet L, Servet C, Wei W, Zhou D-X (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  CAS  PubMed  Google Scholar 

  • Shilatifard A (2012) The COMPASS family of histone H3K4 methylases: mechanisms of regulation in development and disease pathogenesis. Annu Rev Biochem 81:65–95

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sokol A, Kwiatkowska A, Jerzmanowski A, Prymakowska-Bosak M (2007) Up-regulation of stress-inducible genes in tobacco and Arabidopsis cells in response to abiotic stresses and ABA treatment correlates with dynamic changes in histone H3 and H4 modifications. Planta 227(1):245–254. https://doi.org/10.1007/s00425-007-0612-1

    Article  CAS  PubMed  Google Scholar 

  • Song Y, Ji D, Li S, Wang P, Li Q, Xiang F (2012) The dynamic changes of DNA methylation and histone modifications of salt responsive transcription factor genes in soybean. PLoS ONE 7(7):e41274

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Song T, Zhang Q, Wang H, Han J, Xu Z, Yan S, Zhu Z (2018) OsJMJ703, a rice histone demethylase gene, plays key roles in plant development and responds to drought stress. Plant Physiol Biochem 132:183–188

    Article  CAS  PubMed  Google Scholar 

  • Stief A, Altmann S, Hoffmann K, Pant BD, Scheible WR, Baurle I (2014) Arabidopsis miR156 regulates tolerance to recurring environmental stress through SPL transcription factors. Plant Cell 26(4):1792–1807. https://doi.org/10.1105/tpc.114.123851

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tamada Y, Yun J-Y, chul Woo S, 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  CAS  PubMed  PubMed Central  Google Scholar 

  • 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(7):995–1003

    Article  CAS  PubMed  Google Scholar 

  • Tsukada Y-i, 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

    Article  CAS  PubMed  Google Scholar 

  • Ueda M, Seki M (2020) Histone modifications form epigenetic regulatory networks to regulate abiotic stress response. Plant Physiol 182(1):15

    Article  CAS  PubMed  Google Scholar 

  • van Dijk K, Ding Y, Malkaram S, Riethoven J-JM, Liu R, Yang J, Laczko P, Chen H, Xia Y, Ladunga I (2010) Dynamic changes in genome-wide histone H3 lysine 4 methylation patterns in response to dehydration stress in Arabidopsis thaliana. BMC Plant Biol 10(1):238

    Article  PubMed  PubMed Central  Google Scholar 

  • Vastenhouw NL, Schier AF (2012) Bivalent histone modifications in early embryogenesis. Curr Opin Cell Biol 24(3):374–386. https://doi.org/10.1016/j.ceb.2012.03.009

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Widiez T, Girin T, Berr A, Ruffel S, Krouk G, Vayssières A, Shen W-H, Coruzzi GM, Gojon A, Lepetit M (2011) HIGH NITROGEN INSENSITIVE 9 (HNI9)-mediated systemic repression of root NO3− uptake is associated with changes in histone methylation. Proc Natl Acad Sci 108(32):13329–13334

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xia S, Cheng YT, Huang S, Win J, Soards A, Jinn T-L, Jones JD, Kamoun S, Chen S, Zhang Y (2013) Regulation of transcription of nucleotide-binding leucine-rich repeat-encoding genes SNC1 and RPP4 via H3K4 trimethylation. Plant Physiol 162(3):1694–1705

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xu M, Leichty AR, Hu T, Poethig RS (2018) H2A. Z promotes the transcription of MIR156A and MIR156C in Arabidopsis by facilitating the deposition of H3K4me3. Development 145(2):dev152868

    PubMed  PubMed Central  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  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Yang H, Han Z, Cao Y, Fan D, Li H, Mo H, Feng Y, Liu L, Wang Z, Yue Y (2012a) 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  CAS  PubMed  PubMed Central  Google Scholar 

  • Yao X, Feng H, Yu Y, Dong A, Shen W-H (2013) SDG2-mediated H3K4 methylation is required for proper Arabidopsis root growth and development. PLoS ONE 8(2):e56537

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yokoo T, Saito H, Yoshitake Y, Xu Q, Asami T, Tsukiyama T, Teraishi M, Okumoto Y, Tanisaka T (2014) Se14, encoding a JmjC domain-containing protein, plays key roles in long-day suppression of rice flowering through the demethylation of H3K4me3 of RFT1. PLoS ONE 9(4):e96064

    Article  PubMed  PubMed Central  Google Scholar 

  • You Y, Sawikowska A, Neumann M, Posé D, Capovilla G, Langenecker T, Neher RA, Krajewski P, Schmid M (2017) Temporal dynamics of gene expression and histone marks at the Arabidopsis shoot meristem during flowering. Nature communications 8:15120

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yu S, Cao L, Zhou C-M, Zhang T-Q, Lian H, Sun Y, Wu J, Huang J, Wang G, Wang J-W (2013) Sugar is an endogenous cue for juvenile-to-adult phase transition in plants. elife 2:e00269

    Article  PubMed  PubMed Central  Google Scholar 

  • 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(5):834–846

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zeng Z, Zhang W, Marand AP, Zhu B, Buell CR, Jiang J (2019) Cold stress induces enhanced chromatin accessibility and bivalent histone modifications H3K4me3 and H3K27me3 of active genes in potato. Genome Biol 20(1):123

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhang X, Bernatavichute YV, Cokus S, Pellegrini M, Jacobsen SE (2009) Genome-wide analysis of mono-, di-and trimethylation of histone H3 lysine 4 in Arabidopsis thaliana. Genome Biol 10(6):R62

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhang Z, Shi L, Dawany N, Kelsen J, Petri MA, Sullivan KE (2016) H3K4 tri-methylation breadth at transcription start sites impacts the transcriptome of systemic lupus erythematosus. Clin Epigenet 8:14. https://doi.org/10.1186/s13148-016-0179-4

    Article  CAS  Google Scholar 

  • Zhang K, Xu W, Wang C, Yi X, Zhang W, Su Z (2017) Differential deposition of H2A Z in combination with histone modifications within related genes in Oryza sativa callus and seedling. The Plant J 89(2):264–277

    Article  CAS  PubMed  Google Scholar 

  • Zheng D, Wang L, Chen L, Pan X, Lin K, Fang Y, Wang X-e, Zhang W (2019) Salt-responsive genes are differentially regulated at the chromatin levels between seedlings and roots in rice. Plant Cell Physiol 60:1790

    Article  CAS  PubMed  Google Scholar 

  • Zhou BO, Zhou J-Q (2011) Recent transcription-induced histone H3 lysine 4 (H3K4) methylation inhibits gene reactivation. J Biol Chem 286(40):34770–34776

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou H, Liu Y, Liang Y, Zhou D, Li S, Lin S, Dong H, Huang L (2020) The function of the histone lysine methylation related SET domain group (SDG) proteins in plants. Protein Sci 29:1120

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zong W, Zhong X, You J, Xiong L (2013) Genome-wide profiling of histone H3K4-tri-methylation and gene expression in rice under drought stress. Plant Mol Biol 81(1–2):175–188

    Article  CAS  PubMed  Google Scholar 

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Funding

This work was supported by the United States Department of Agriculture, National Institute of Food and Agriculture (USDA-NIFA grant no. 2016-10070) and the United States National Science Foundation, Division of Integrative Organismal Systems and Division of Molecular and Cellular Biosciences (NSF-IOS grant no. 1127051 and NSF-MCB grant no. 1616827).

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Foroozani, M., Vandal, M.P. & Smith, A.P. H3K4 trimethylation dynamics impact diverse developmental and environmental responses in plants. Planta 253, 4 (2021). https://doi.org/10.1007/s00425-020-03520-0

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