Arabidopsis Flower and Embryo Developmental Genes are Repressed in Seedlings by Different Combinations of Polycomb Group Proteins in Association with Distinct Sets of Cis-regulatory Elements
Polycomb repressive complexes (PRCs) play crucial roles in transcriptional repression and developmental regulation in both plants and animals. In plants, depletion of different members of PRCs causes both overlapping and unique phenotypic defects. However, the underlying molecular mechanism determining the target specificity and functional diversity is not sufficiently characterized. Here, we quantitatively compared changes of tri-methylation at H3K27 in Arabidopsis mutants deprived of various key PRC components. We show that CURLY LEAF (CLF), a major catalytic subunit of PRC2, coordinates with different members of PRC1 in suppression of distinct plant developmental programs. We found that expression of flower development genes is repressed in seedlings preferentially via non-redundant role of CLF, which specifically associated with LIKE HETEROCHROMATIN PROTEIN1 (LHP1). In contrast, expression of embryo development genes is repressed by PRC1-catalytic core subunits AtBMI1 and AtRING1 in common with PRC2-catalytic enzymes CLF or SWINGER (SWN). This context-dependent role of CLF corresponds well with the change in H3K27me3 profiles, and is remarkably associated with differential co-occupancy of binding motifs of transcription factors (TFs), including MADS box and ABA-related factors. We propose that different combinations of PRC members distinctively regulate different developmental programs, and their target specificity is modulated by specific TFs.
References
[1]
Bemer M, Grossniklaus U (2012) Dynamic regulation of Polycomb group activity during plant development. Curr Opin Plant Biol 15: 523–529. doi: 10.1016/j.pbi.2012.09.006. pmid:22999383
[2]
Mozgova I, Hennig L (2015) The Polycomb Group Protein Regulatory Network. Annu Rev Plant Biol. doi: 10.1146/annurev-arplant-043014-115627
[3]
Grossniklaus U, Paro R (2014) Transcriptional silencing by polycomb-group proteins. Cold Spring Harb Perspect Biol 6: a019331. doi: 10.1101/cshperspect.a019331. pmid:25367972
[4]
Xiao J, Wagner D (2015) Polycomb repression in the regulation of growth and development in Arabidopsis. Curr Opin Plant Biol 23C: 15–24. doi: 10.1016/j.pbi.2014.10.003
[5]
Goodrich J, Puangsomlee P, Martin M, Long D, Meyerowitz EM, et al. (1997) A Polycomb-group gene regulates homeotic gene expression in Arabidopsis. Nature 386: 44–51. pmid:9052779 doi: 10.1038/386044a0
[6]
Kinoshita T, Harada JJ, Goldberg RB, Fischer RL (2001) Polycomb repression of flowering during early plant development. Proc Natl Acad Sci U S A 98: 14156–14161. pmid:11698668 doi: 10.1073/pnas.241507798
[7]
Yang C, Bratzel F, Hohmann N, Koch M, Turck F, et al. (2013) VAL- and AtBMI1-mediated H2Aub initiate the switch from embryonic to postgerminative growth in Arabidopsis. Curr Biol 23: 1324–1329. doi: 10.1016/j.cub.2013.05.050. pmid:23810531
[8]
Shen LS, Thong ZH, Gong XM, Shen Q, Gan YB, et al. (2014) The putative PRC1 RING-finger protein AtRING1A regulates flowering through repressing MADS AFFECTING FLOWERING genes in Arabidopsis. Development 141: 1303–U1238. doi: 10.1242/dev.104513. pmid:24553292
[9]
Grossniklaus U, Vielle-Calzada JP, Hoeppner MA, Gagliano WB (1998) Maternal control of embryogenesis by MEDEA, a polycomb group gene in Arabidopsis. Science 280: 446–450. pmid:9545225 doi: 10.1126/science.280.5362.446
[10]
Gaudin V, Libault M, Pouteau S, Juul T, Zhao G, et al. (2001) Mutations in LIKE HETEROCHROMATIN PROTEIN 1 affect flowering time and plant architecture in Arabidopsis. Development 128: 4847–4858. pmid:11731464
[11]
Chanvivattana Y, Bishopp A, Schubert D, Stock C, Moon YH, et al. (2004) Interaction of Polycomb-group proteins controlling flowering in Arabidopsis. Development 131: 5263–5276. pmid:15456723 doi: 10.1242/dev.01400
[12]
Bratzel F, Lopez-Torrejon G, Koch M, Del Pozo JC, Calonje M (2010) Keeping cell identity in Arabidopsis requires PRC1 RING-finger homologs that catalyze H2A monoubiquitination. Curr Biol 20: 1853–1859. doi: 10.1016/j.cub.2010.09.046. pmid:20933424
Turck F, Roudier F, Farrona S, Martin-Magniette ML, Guillaume E, et al. (2007) Arabidopsis TFL2/LHP1 specifically associates with genes marked by trimethylation of histone H3 lysine 27. PLoS Genet 3: e86. pmid:17542647 doi: 10.1371/journal.pgen.0030086
[15]
Zhang X, Germann S, Blus BJ, Khorasanizadeh S, Gaudin V, et al. (2007) The Arabidopsis LHP1 protein colocalizes with histone H3 Lys27 trimethylation. Nat Struct Mol Biol 14: 869–871. pmid:17676062 doi: 10.1038/nsmb1283
[16]
Chen D, Molitor A, Liu C, Shen WH (2010) The Arabidopsis PRC1-like ring-finger proteins are necessary for repression of embryonic traits during vegetative growth. Cell Res 20: 1332–1344. doi: 10.1038/cr.2010.151. pmid:21060339
[17]
Derkacheva M, Steinbach Y, Wildhaber T, Mozgova I, Mahrez W, et al. (2013) Arabidopsis MSI1 connects LHP1 to PRC2 complexes. EMBO J 32: 2073–2085. doi: 10.1038/emboj.2013.145. pmid:23778966
[18]
Merini W, Calonje M (2015) PRC1 is taking the lead in PcG repression. Plant J Accepted Article. doi: 10.1111/tpj.12818
[19]
Molitor AM, Bu Z, Yu Y, Shen WH (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: e1004091. doi: 10.1371/journal.pgen.1004091. pmid:24465219
[20]
Wang Y, Gu X, Yuan W, Schmitz RJ, He Y (2014) Photoperiodic control of the floral transition through a distinct polycomb repressive complex. Dev Cell 28: 727–736. doi: 10.1016/j.devcel.2014.01.029. pmid:24613395
[21]
Lodha M, Marco CF, Timmermans MC (2013) The ASYMMETRIC LEAVES complex maintains repression of KNOX homeobox genes via direct recruitment of Polycomb-repressive complex2. Genes Dev 27: 596–601. doi: 10.1101/gad.211425.112. pmid:23468429
[22]
Liu X, Kim YJ, Muller R, Yumul RE, Liu C, et al. (2011) AGAMOUS terminates floral stem cell maintenance in Arabidopsis by directly repressing WUSCHEL through recruitment of Polycomb Group proteins. Plant Cell 23: 3654–3670. doi: 10.1105/tpc.111.091538. pmid:22028461
[23]
Liu C, Xi W, Shen L, Tan C, Yu H (2009) Regulation of floral patterning by flowering time genes. Dev Cell 16: 711–722. doi: 10.1016/j.devcel.2009.03.011. pmid:19460347
[24]
Heo JB, Sung S (2011) Vernalization-mediated epigenetic silencing by a long intronic noncoding RNA. Science 331: 76–79. doi: 10.1126/science.1197349. pmid:21127216
[25]
Swiezewski S, Liu F, Magusin A, Dean C (2009) Cold-induced silencing by long antisense transcripts of an Arabidopsis Polycomb target. Nature 462: 799–802. doi: 10.1038/nature08618. pmid:20010688
[26]
Adrian J, Farrona S, Reimer JJ, Albani MC, Coupland G, et al. (2010) cis-Regulatory elements and chromatin state coordinately control temporal and spatial expression of FLOWERING LOCUS T in Arabidopsis. Plant Cell 22: 1425–1440. doi: 10.1105/tpc.110.074682. pmid:20472817
[27]
Berger N, Dubreucq B, Roudier F, Dubos C, Lepiniec L (2011) Transcriptional regulation of Arabidopsis LEAFY COTYLEDON2 involves RLE, a cis-element that regulates trimethylation of histone H3 at lysine-27. Plant Cell 23: 4065–4078. doi: 10.1105/tpc.111.087866. pmid:22080598
[28]
Sun B, Looi LS, Guo S, He Z, Gan ES, et al. (2014) Timing mechanism dependent on cell division is invoked by Polycomb eviction in plant stem cells. Science 343: 1248559. doi: 10.1126/science.1248559. pmid:24482483
[29]
Crevillen P, Yang H, Cui X, Greeff C, Trick M, et al. (2014) Epigenetic reprogramming that prevents transgenerational inheritance of the vernalized state. Nature 515: 587–590. doi: 10.1038/nature13722. pmid:25219852
[30]
Roudier F, Ahmed I, Berard C, Sarazin A, Mary-Huard T, et al. (2011) Integrative epigenomic mapping defines four main chromatin states in Arabidopsis. EMBO J 30: 1928–1938. doi: 10.1038/emboj.2011.103. pmid:21487388
[31]
Bouyer D, Roudier F, Heese M, Andersen ED, Gey D, et al. (2011) Polycomb repressive complex 2 controls the embryo-to-seedling phase transition. PLoS Genet 7: e1002014. doi: 10.1371/journal.pgen.1002014. pmid:21423668
[32]
Kim SY, Lee J, Eshed-Williams L, Zilberman D, Sung ZR (2012) EMF1 and PRC2 cooperate to repress key regulators of Arabidopsis development. PLoS Genet 8: e1002512. doi: 10.1371/journal.pgen.1002512. pmid:22457632
[33]
Shao Z, Zhang Y, Yuan GC, Orkin SH, Waxman DJ (2012) MAnorm: a robust model for quantitative comparison of ChIP-Seq data sets. Genome Biol 13: R16. doi: 10.1186/gb-2012-13-3-r16. pmid:22424423
[34]
Xu J, Shao Z, Li D, Xie H, Kim W, et al. (2015) Developmental control of polycomb subunit composition by GATA factors mediates a switch to non-canonical functions. Mol Cell 57: 304–316. doi: 10.1016/j.molcel.2014.12.009. pmid:25578878
[35]
Xu J, Shao Z, Glass K, Bauer DE, Pinello L, et al. (2012) Combinatorial assembly of developmental stage-specific enhancers controls gene expression programs during human erythropoiesis. Dev Cell 23: 796–811. doi: 10.1016/j.devcel.2012.09.003. pmid:23041383
[36]
Das PP, Shao Z, Beyaz S, Apostolou E, Pinello L, et al. (2014) Distinct and combinatorial functions of Jmjd2b/Kdm4b and Jmjd2c/Kdm4c in mouse embryonic stem cell identity. Mol Cell 53: 32–48. doi: 10.1016/j.molcel.2013.11.011. pmid:24361252
[37]
Aubert D, Chen L, Moon YH, Martin D, Castle LA, et al. (2001) EMF1, a novel protein involved in the control of shoot architecture and flowering in Arabidopsis. Plant Cell 13: 1865–1875. pmid:11487698 doi: 10.1105/tpc.13.8.1865
[38]
Sneeringer CJ, Scott MP, Kuntz KW, Knutson SK, Pollock RM, et al. (2010) Coordinated activities of wild-type plus mutant EZH2 drive tumor-associated hypertrimethylation of lysine 27 on histone H3 (H3K27) in human B-cell lymphomas. Proc Natl Acad Sci U S A 107: 20980–20985. doi: 10.1073/pnas.1012525107. pmid:21078963
[39]
Stepanik VA, Harte PJ (2012) A mutation in the E(Z) methyltransferase that increases trimethylation of histone H3 lysine 27 and causes inappropriate silencing of active Polycomb target genes. Developmental Biology 364: 249–258. pmid:22182520 doi: 10.1016/j.ydbio.2011.12.007
[40]
Deng WW, Buzas DM, Ying H, Robertson M, Taylor J, et al. (2013) Arabidopsis Polycomb Repressive Complex 2 binding sites contain putative GAGA factor binding motifs within coding regions of genes. Bmc Genomics 14. doi: 10.1186/1471-2164-14-593
[41]
Lu FL, Cui X, Zhang SB, Jenuwein T, Cao XF (2011) Arabidopsis REF6 is a histone H3 lysine 27 demethylase. Nature Genetics 43: 715–U144. doi: 10.1038/ng.854. pmid:21642989
[42]
Schubert D, Primavesi L, Bishopp A, Roberts G, Doonan J, et al. (2006) Silencing by plant Polycomb-group genes requires dispersed trimethylation of histone H3 at lysine 27. Embo Journal 25: 4638–4649. pmid:16957776 doi: 10.1038/sj.emboj.7601311
[43]
Subramanian A, Tamayo P, Mootha VK, Mukherjee S, Ebert BL, et al. (2005) Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci U S A 102: 15545–15550. pmid:16199517 doi: 10.1073/pnas.0506580102
[44]
Jia H, Suzuki M, McCarty DR (2014) Regulation of the seed to seedling developmental phase transition by the LAFL and VAL transcription factor networks. Wiley Interdiscip Rev Dev Biol 3: 135–145. doi: 10.1002/wdev.126. pmid:24902838
[45]
Nambara E, Hayama R, Tsuchiya Y, Nishimura M, Kawaide H, et al. (2000) The role of ABI3 and FUS3 loci in Arabidopsis thaliana on phase transition from late embryo development to germination. Developmental Biology 220: 412–423. pmid:10753527 doi: 10.1006/dbio.2000.9632
[46]
West MAL, Yee KM, Danao J, Zimmerman JL, Fischer RL, et al. (1994) Leafy Cotyledon1 Is an Essential Regulator of Late Embryogenesis and Cotyledon Identity in Arabidopsis. Plant Cell 6: 1731–1745. pmid:12244233 doi: 10.2307/3869904
[47]
Baumbusch LO, Hughes DW, Galau GA, Jakobsen KS (2004) LEC1, FUS3, ABI3 and Em expression reveals no correlation with dormancy in Arabidopsis. Journal of Experimental Botany 55: 77–87. pmid:14676287 doi: 10.1093/jxb/erh014
[48]
Huang H, Mizukami Y, Hu Y, Ma H (1993) Isolation and characterization of the binding sequences for the product of the Arabidopsis floral homeotic gene AGAMOUS. Nucleic Acids Res 21: 4769–4776. pmid:7901838 doi: 10.1093/nar/21.20.4769
[49]
Riechmann JL, Wang M, Meyerowitz EM (1996) DNA-binding properties of Arabidopsis MADS domain homeotic proteins APETALA1, APETALA3, PISTILLATA and AGAMOUS. Nucleic Acids Res 24: 3134–3141. pmid:8774892 doi: 10.1093/nar/24.16.3134
[50]
Wang Y, Deng D, Zhang R, Wang S, Bian Y, et al. (2012) Systematic analysis of plant-specific B3 domain-containing proteins based on the genome resources of 11 sequenced species. Mol Biol Rep 39: 6267–6282. doi: 10.1007/s11033-012-1448-8. pmid:22302388
[51]
Pajoro A, Madrigal P, Muino JM, Matus JT, Jin J, et al. (2014) Dynamics of chromatin accessibility and gene regulation by MADS-domain transcription factors in flower development. Genome Biol 15: R41. doi: 10.1186/gb-2014-15-3-r41. pmid:24581456
[52]
DS OM, Wuest SE, Rae L, Raganelli A, Ryan PT, et al. (2013) Control of reproductive floral organ identity specification in Arabidopsis by the C function regulator AGAMOUS. Plant Cell 25: 2482–2503. doi: 10.1105/tpc.113.113209. pmid:23821642
[53]
Wuest SE, O'Maoileidigh DS, Rae L, Kwasniewska K, Raganelli A, et al. (2012) Molecular basis for the specification of floral organs by APETALA3 and PISTILLATA. Proc Natl Acad Sci U S A 109: 13452–13457. doi: 10.1073/pnas.1207075109. pmid:22847437
[54]
Smaczniak C, Immink RG, Muino JM, Blanvillain R, Busscher M, et al. (2012) Characterization of MADS-domain transcription factor complexes in Arabidopsis flower development. Proc Natl Acad Sci U S A 109: 1560–1565. doi: 10.1073/pnas.1112871109. pmid:22238427
[55]
Becker B, Marin B (2009) Streptophyte algae and the origin of embryophytes. Ann Bot 103: 999–1004. doi: 10.1093/aob/mcp044. pmid:19273476
[56]
Theissen G, Melzer R (2007) Molecular mechanisms underlying origin and diversification of the angiosperm flower. Ann Bot 100: 603–619. pmid:17670752 doi: 10.1093/aob/mcm143
[57]
Exner V, Aichinger E, Shu H, Wildhaber T, Alfarano P, et al. (2009) The Chromodomain of LIKE HETEROCHROMATIN PROTEIN 1 Is Essential for H3K27me3 Binding and Function during Arabidopsis Development. Plos One 4. doi: 10.1371/journal.pone.0005335
[58]
He C, Huang H, Xu L (2013) Mechanisms guiding Polycomb activities during gene silencing in Arabidopsis thaliana. Front Plant Sci 4: 454. doi: 10.3389/fpls.2013.00454. pmid:24312106
[59]
Gregis V, Andres F, Sessa A, Guerra RF, Simonini S, et al. (2013) Identification of pathways directly regulated by SHORT VEGETATIVE PHASE during vegetative and reproductive development in Arabidopsis. Genome Biol 14: R56. doi: 10.1186/gb-2013-14-6-r56. pmid:23759218
[60]
Gramzow L, Theissen G (2010) A hitchhiker's guide to the MADS world of plants. Genome Biol 11: 214. doi: 10.1186/gb-2010-11-6-214. pmid:20587009
[61]
Regad F, Lebas M, Lescure B (1994) Interstitial Telomeric Repeats within the Arabidopsis-Thaliana Genome. Journal of Molecular Biology 239: 163–169. pmid:8196051 doi: 10.1006/jmbi.1994.1360
[62]
Tremousaygue D, Garnier L, Bardet C, Dabos P, Herve C, et al. (2003) Internal telomeric repeats and 'TCP domain' protein-binding sites co-operate to regulate gene expression in Arabidopsis thaliana cycling cells. Plant Journal 33: 957–966. pmid:12631321 doi: 10.1046/j.1365-313x.2003.01682.x
[63]
Zhou Y, Hartwig B, Velikkakam JG, Schneeberger K, Turck F (2015) Complementary activities of TELOMERE REPEAT BINDING proteins and Polycomb Group complexes in transcriptional regulation of target genes. Plant Cell. doi: 10.1105/tpc.15.00787
[64]
Feng SH, Cokus SJ, Schubert V, Zhai JX, Pellegrini M, et al. (2014) Genome-wide Hi-C Analyses in Wild-Type and Mutants Reveal High-Resolution Chromatin Interactions in Arabidopsis. Molecular Cell 55: 694–707. doi: 10.1016/j.molcel.2014.07.008. pmid:25132175
[65]
Bannister AJ, Zegerman P, Partridge JF, Miska EA, Thomas JO, et al. (2001) Selective recognition of methylated lysine 9 on histone H3 by the HP1 chromo domain. Nature 410: 120–124. pmid:11242054 doi: 10.1038/35065138
[66]
Lachner M, O'Carroll D, Rea S, Mechtler K, Jenuwein T (2001) Methylation of histone H3 lysine 9 creates a binding site for HP1 proteins. Nature 410: 116–120. pmid:11242053 doi: 10.1038/35065132
[67]
Cao R, Wang L, Wang H, Xia L, Erdjument-Bromage H, et al. (2002) Role of histone H3 lysine 27 methylation in Polycomb-group silencing. Science 298: 1039–1043. pmid:12351676 doi: 10.1126/science.1076997
[68]
Min J, Zhang Y, Xu RM (2003) Structural basis for specific binding of Polycomb chromodomain to histone H3 methylated at Lys 27. Genes Dev 17: 1823–1828. pmid:12897052 doi: 10.1101/gad.269603
[69]
Francis NJ, Kingston RE, Woodcock CL (2004) Chromatin compaction by a polycomb group protein complex. Science 306: 1574–1577. pmid:15567868 doi: 10.1126/science.1100576
[70]
Mortz E, Krogh TN, Vorum H, Gorg A (2001) Improved silver staining protocols for high sensitivity protein identification using matrix-assisted laser desorption/ionization-time of flight analysis. Proteomics 1: 1359–1363. pmid:11922595 doi: 10.1002/1615-9861(200111)1:11<1359::aid-prot1359>3.3.co;2-h
[71]
Bouveret R, Schonrock N, Gruissem W, Hennig L (2006) Regulation of flowering time by Arabidopsis MSI1. Development 133: 1693–1702. pmid:16554362 doi: 10.1242/dev.02340
[72]
He CS, Chen XF, Huang H, Xu L (2012) Reprogramming of H3K27me3 Is Critical for Acquisition of Pluripotency from Cultured Arabidopsis Tissues. Plos Genetics 8. doi: 10.1371/journal.pgen.1002911
[73]
Larsson AS, Landberg K, Meeks-Wagner DR (1998) The TERMINAL FLOWER2 (TFL2) gene controls the reproductive transition and meristem identity in Arabidopsis thaliana. Genetics 149: 597–605. pmid:9611176
[74]
Li H, Durbin R (2009) Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25: 1754–1760. doi: 10.1093/bioinformatics/btp324. pmid:19451168
[75]
Kim D, Pertea G, Trapnell C, Pimentel H, Kelley R, et al. (2013) TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol 14: R36. doi: 10.1186/gb-2013-14-4-r36. pmid:23618408
[76]
Zhang Y, Liu T, Meyer CA, Eeckhoute J, Johnson DS, et al. (2008) Model-based analysis of ChIP-Seq (MACS). Genome Biol 9: R137. doi: 10.1186/gb-2008-9-9-r137. pmid:18798982
[77]
Ji H, Wong WH (2005) TileMap: create chromosomal map of tiling array hybridizations. Bioinformatics 21: 3629–3636. pmid:16046496 doi: 10.1093/bioinformatics/bti593
