Abstract
The Enhancer of Zeste Polycomb group proteins, which are encoded by a small gene family in Arabidopsis thaliana, participate to the control of plant development. In the tomato (Solanum lycopersicum), these proteins are encoded by three genes (SlEZ1, SlEZ2 and SlEZ3) that display specific expression profiles. Using a gene specific RNAi strategy, we demonstrate that repression of SlEZ2 correlates with a general reduction of H3K27me3 levels, indicating that SlEZ2 is part of an active PRC2 complex. Reduction of SlEZ2 gene expression impacts the vegetative development of tomato plants, consistent with SlEZ2 having retained at least some of the functions of the Arabidopsis CURLY LEAF (CLF) protein. Notwithstanding, we observed significant differences between transgenic SlEZ2 RNAi tomato plants and Arabidopsis clf mutants. First, we found that reduced SlEZ2 expression has dramatic effects on tomato fruit development and ripening, functions not described in Arabidopsis for the CLF protein. In addition, repression of SlEZ2 has no significant effect on the flowering time or the control of flower organ identity, in contrast to the Arabidopsis clf mutation. Taken together, our results are consistent with a diversification of the function of CLF orthologues in plants, and indicate that although partly conserved amongst plants, the function of EZ proteins need to be newly investigated for non-model plants because they might have been recruited to specific developmental processes.
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References
Ach RA, Taranto P, Gruissem W (1997) A conserved family of WD-40 proteins binds to the retinoblastoma protein in both plants and animals. The Plant Cell Online 9:1595–1606
Bar M, Ori N (2014) Leaf development and morphogenesis. Development 141:4219–4230
Beaudoin F, Wu X, Li F et al (2009) Functional characterization of the arabidopsis β-ketoacyl-coenzyme a reductase candidates of the fatty acid elongase. plant Physiol 150:1174–1191
Benvenuto G, Formiggini F, Laflamme P, Malakhov M, Bowler C (2002) The photomorphogenesis regulator DET1 binds the amino-terminal tail of histone H2B in a nucleosome context. Curr Biol 12:1529–1534
Berger Y, Harpaz-Saad S, Brand A, Melnik H, Sirding N, Alvarez JP, Zinder M, Samach A, Eshed Y, Ori N (2009) The NAC-domain transcription factor GOBLET specifies leaflet boundaries in compound tomato leaves. Development 136:823–832
Bird D, Beisson F, Brigham A et al (2007) Characterization of Arabidopsis ABCG11/WBC11, an ATP binding cassette (ABC) transporter that is required for cuticular lipid secretion. Plant J 52:485–498
Blackledge Neil P, Farcas Anca M, Kondo T, King Hamish W, McGouran Joanna F, Hanssen Lars L, Ito S, Cooper S, Kondo K, Koseki Y, Ishikura T, Long Hannah K, Sheahan Thomas W, Brockdorff N, Kessler Benedikt M, Koseki H, Klose Robert J (2014) Variant PRC1 complex-dependent H2A ubiquitylation drives PRC2 recruitment and polycomb domain formation. Cell 157:1445–1459
Bourdenx B, Bernard A, Domergue F, Pascal S, Léger A, Roby D, Pervent M, Vile D, Haslam RP, Napier JA, Lessire R, Joubés J (2011) Overexpression of Arabidopsis ECERIFERUM1 promotes wax very-long-chain alkane biosynthesis and influences plant response to biotic and abiotic stresses. Plant Physiol 156:29–45
Bouyer D, Roudier F, Heese M, Andersen ED, Gey D, Nowack MK, Goodrich J, Renou J-P, Grini PE, Colot V, Schnittger A (2011) Polycomb repressive complex 2 controls the embryo-to-seedling phase transition. PLoS Genet 7:e1002014
Butenko Y, Ohad N (2011) Polycomb-group mediated epigenetic mechanisms through plant evolution. Biochim Biophys Acta 1809:395–406
Cao R, Wang L, Wang H, Xia L, Erdjument-Bromage H, Tempst P, Jones RS, Zhang Y (2002) Role of histone H3 Lysine 27 methylation in polycomb-group silencing. Science 298:1039–1043
Chaïb J, Devaux M-F, Grotte M-G, Robini K, Causse M, Lahaye M, Marty I (2007) Physiological relationships among physical, sensory, and morphological attributes of texture in tomato fruits. J Exp Bot 58:1915–1925
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 131:5263–5276
Chaudhury AM, Ming L, Miller C, Craig S, Dennis ES, Peacock WJ (1997) Fertilization-independent seed development in Arabidopsis thaliana. Proc Natl Acad Sci USA 94:4223–4228
Chen W, Kong J, Qin C, Sheng Y, Tan J, Chen Y-r WuC, Wang H, Shi Y, Li C, Li B, Zhang P, Wang Y, Lai T, Yu Z, Zhang X, Shi N, Wang H, Osman T, Liu Y, Manning K, Jackson S, Rolin D, Zhong S, Seymour GB, Gallusci P, Hong Y (2015) Requirement of CHROMOMETHYLASE3 for somatic inheritance of spontaneous tomato epimutation Colourless non-ripening. Sci Rep 5:9192
Consortium TTG (2012) The tomato genome sequence provides insights into fleshy fruit evolution. Nature 485:635–641
Czermin B, Melfi R, McCabe D, Seitz V, Imhof A, Pirrotta V (2002) Drosophila enhancer of zeste/ESC complexes have a histone H3 methyltransferase activity that marks chromosomal polycomb sites. Cell 111:185–196
Danilevskaya ON, Hermon P, Hantke S, Muszynski MG, Kollipara K, Ananiev EV (2003) Duplicated fie genes in maize: expression pattern and imprinting suggest distinct functions. Plant Cell 15:425–438
Davuluri GR, van Tuinen A, Mustilli AC, Manfredonia A, Newman R, Burgess D, Brummell DA, King SR, Palys J, Uhlig J, Pennings HMJ, Bowler C (2004) Manipulation of DET1 expression in tomato results in photomorphogenic phenotypes caused by post-transcriptional gene silencing. Plant J 40:344–354
De Lucia F, Crevillen P, Jones AME, Greb T, Dean C (2008) A PHD-polycomb repressive complex 2 triggers the epigenetic silencing of FLC during vernalization. Proc Natl Acad Sci USA 105:16831–16836
Derkacheva M, Steinbach Y, Wildhaber T, Mozgová I, Mahrez W, Nanni P, Bischof S, Gruissem W, Hennig L (2013) Arabidopsis MSI1 connects LHP1 to PRC2 complexes. EMBO J 32:2073–2085
Domergue F, Vishwanath SJ, Joubés J, Ono J, Lee JA, Bourdon M, Alhattab R, Lowe C, Pascal S, Lessire R, Rowland O (2010) Three Arabidopsis fatty acyl-coenzyme a reductases, FAR1, FAR4, and FAR5, generate primary fatty alcohols associated with suberin deposition. Plant Physiol 153:1539–1554
Farrona S, Thorpe FL, Engelhorn J, Adrian J, Dong X, Sarid-Krebs L, Goodrich J, Turck F (2011) Tissue-specific expression of flowering locus T in arabidopsis is maintained independently of polycomb group protein repression. Plant Cell 23:3204–3214
Faure JD, Vittorioso P, Santoni V et al (1998) The PASTICCINO genes of Arabidopsis thaliana are involved in the control of cell division and differentiation. Development 125:909–918
Fei Z, Joung J-G, Tang X, Zheng Y, Huang M, Lee JM, McQuinn R, Tieman DM, Alba R, Klee HJ, Giovannoni JJ (2011) Tomato functional genomics database: a comprehensive resource and analysis package for tomato functional genomics. Nucl Acids Res 39:D1156–D1163
Gallusci P, Salamini F, Thompson RD (1994) Differences in cell type-specific expression of the gene Opaque 2 in maize and transgenic tobacco. Mol Gen Genet 244:391–400
Gendall AR, Levy YY, Wilson A, Dean C (2001) The vernalization 2 gene mediates the epigenetic regulation of vernalization in Arabidopsis. Cell 107:525–535
Gendrel A-V, Lippman Z, Martienssen R, Colot V (2005) Profiling histone modification patterns in plants using genomic tiling microarrays. Nat Methods 2:213–218
Giovannoni JJ (2007) Fruit ripening mutants yield insights into ripening control. Curr Opin Plant Biol 10:283–289
Gonzalez N, Gévaudant F, Hernould M, Chevalier C, Mouras A (2007) The cell cycle-associated protein kinase WEE1 regulates cell size in relation to endoreduplication in developing tomato fruit. Plant J 51:642–655
Goodrich J, Puangsomlee P, Martin M, Long D, Meyerowitz EM, Coupland G (1997) A polycomb-group gene regulates homeotic gene expression in Arabidopsis. Nature 386:44–51
Grimaud C, Negre N, Cavalli G (2006) From genetics to epigenetics: the tale of Polycomb group and trithorax group genes. Chromosome Res 14:363–375
Grossniklaus U, Vielle-Cazalda JP, Hoepner MA, Gagliano W (1998) maternal control of embryogenesis by MEDEA, a polycomb group gene in Arabidopsis thaliana. Science 280:448–449
Hagemann W, Gleissberg S (1996) Organogenetic capacity of leaves: the significance of marginal blastozones in angiosperms. Plant Syst Evol 199:121–152
Hennig L, Derkacheva M (2009) Diversity of Polycomb group complexes in plants: same rules, different players? Trends Genet 25:414–423
Hennig L, Taranto P, Walser M, Schonrock N, Gruissem W (2003) Arabidopsis MSI1 is required for epigenetic maintenance of reproductive development. Development 130:2555–2565
Hennig L, Bouveret R, Gruissem W (2005) MSI1-like proteins: an escort service for chromatin assembly and remodeling complexes. Trends Cell Biol 15:295–302
Holec S, Berger F (2012) Polycomb group complexes mediate developmental transitions in plants. Plant Physiol 158:35–43
How Kit A, Boureau L, Stammitti-Bert L, Rolin D, Teyssier E, Gallusci P (2010) Functional analysis of SlEZ1 a tomato enhancer of zeste (E(z)) gene demonstrates a role in flower development. Plant Mol Biol 74:201–213
Jasinski S, Tattersall A, Piazza P, Hay A, Martinez-Garcia JF, Schmitz G, Theres K, McCormick S, Tsiantis M (2008) PROCERA encodes a DELLA protein that mediates control of dissected leaf form in tomato. Plant j 56:603–612
Javelle M, Vernoud V, Rogowsky PM et al (2011) Epidermis: the formation and functions of a fundamental plant tissue. New Phytol 189:17–39
Jiang D, Wang Y, 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:e3404
Katz A, Oliva M, Mosquna A, Hakim O, Ohad N (2004) FIE and curly leaf polycomb proteins interact in the regulation of homeobox gene expression during sporophyte development. Plant J 37:707–719
Kim D-H, Sung S (2014) Polycomb-mediated gene silencing in Arabidopsis thaliana. Mol Cells 37:841–850
Kinoshita T, Harada JJ, Goldberg RB, Fischer RL (2001) Polycomb repression of flowering during early plant development. Proc Natl Acad Sci USA 98:14156–14161
Kiyosue T, Ohad N, Yadegari R, Hannon M, Dinneny J, Wells D, Katz A, Margossian L, Harada JJ, Goldberg RB, Fisher RL (1999) Control of fertilization independent endosperm development by the MEDEA polycomb gene in Arabidopsis. Proc Natl Acad Sci USA 96:4186–4191
Köhler C, Hennig L (2010) Regulation of cell identity by plant Polycomb and trithorax group proteins. Curr Opin Genet Dev 20:541–547
Köhler C, Villar CBR (2008) Programming of gene expression by Polycomb group proteins. Trends Cell Biol 18:236–243
Köhler C, Hennig L, Bouveret R, Gheyselinck J, Grossniklaus U, Gruissem W (2003) Arabidopsis MSI1 is a component of the MEA/FIE polycomb group complex and required for seed development. EMBO J 22:4804–4814
Kuzmichev ARD, Nishioka K, Erdjument-Bromage H, Tempst P, Reinberg D (2002) Histone methyltransferase activity associated with a human multiprotein complex containing the enhancer of Zeste protein. Genes Dev 16:2893–2905
Lafos M, Kroll P, Hohenstatt ML, Thorpe FL, Clarenz O, Schubert D (2011) Dynamic regulation of H3K27 trimethylation during Arabidopsis differentiation. PLoS Genet 7:e1002040
Lee E, Lucas JR, Goodrich J, Sack FD (2014) Arabidopsis guard cell integrity involves the epigenetic stabilization of the FLP and FAMA transcription factor genes. Plant J 78:566–577
Li S, Zhou B, Peng X, Kuang Q, Huang X, Yao J, Du B, Sun M-X (2013) OsFIE2 plays an essential role in the regulation of rice vegetative and reproductive development. New Phytol 201:66–79
Liu D-D, Dong Q-L, Fang M-J, Chen K-Q, Hao Y-J (2012) Ectopic expression of an apple apomixis-related gene MhFIE induces co-suppression and results in abnormal vegetative and reproductive development in tomato. J Plant Physiol 169:1866–1873
Liu R, How Kit A, Stammitti L et al (2015) A demeter-like DNA demethylase governs tomato fruit ripening. Proc Natl Acad Sci USA 112:10804–10809
Luo M, Bilodeau P, Koltunow A, Dennis ES, Peacock WJ, Chaudhury AM (1999) Genes controlling fertilization-independent seed development in Arabidopsis thaliana. Proc Natl Acad Sci USA 96:296–301
Luo M, Bilodeu P, Dennis ES, Peacock JW, Chaudhury AML (2000) Expression and parent-of-origin effects for FIS2, E(Z), and FIE in the endosperm and embryo of developing Arabidopsis seeds. Proc Natl Acad Sci USA 97:10637–10642
Manning K, Tör M, Poole M, Hong Y, Thompson AJ, King GJ, Giovannoni JJ, Seymour GB (2006) A naturally occuring epigenetic mutation in a gene encoding an SBP-box transcription factor inhibits tomato fruit ripening. Nature genet 38:948–952
Mayama T, Ohtsubo E, Tsuchimoto S (2003) Isolation and expression analysis of petunia curly leaf-like genes. Plant Cell Physiol 44:811–819
Miyake T, Takebayashi N, Wolf DE (2009) Possible diversifying selection in the imprinted gene, medea, in Arabidopsis. Mol Biol Evol 26:843–857
Molitor A, Shen W-H (2013) The polycomb complex PRC1: composition and function in plants. J Genet Genomics 40:231–238
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:e1004091
Mosquna A, Katz A, Decker EL, Rensing SA, Reski R, Ohad N (2009) Regulation of stem cell maintenance by the Polycomb protein FIE has been conserved during land plant evolution. Development 136:2433–2444
Moyle LC (2008) Ecological and evolutionary genomics in the wild tomatoes (Solanum sect. Lycopersicon). Evolution 62:2995–3013
Mozgova I, Köhler C, Hennig L (2015) Keeping the gate closed: functions of the polycomb repressive complex PRC2 in development. Plant J. doi:10.1111/tpj.12828
Müller J, Hart CM, Francis NJ, Vargas ML, Sengupta A, Wild B, Miller EL, O’Connor MB, Kingston RE, Simon JA (2002) Histone methyltransferase activity of a drosophila polycomb group repressor complex. Cell 111:197–208
Ohad N, Yadegari R, Margossian L, Hannon M, Michaeli D, Harada JJ, Goldberg RB, Fischer RL (1999) Mutations in FIE, a WD polycomb group gene, allow endosperm development without fertilization. Plant Cell 11:407–416
Orlando V, Paro R (1995) Chromatin multiprotein complexes involved in the maintenance of transcription patterns. Curr Opin Genet Dev 5:174–179
Panikashvili D, Savaldi-Goldstein S, Mandel T et al (2007) The Arabidopsis desperado/AtWBC11 transporter is required for cutin and wax secretion. Plant Physiol 145:1345–1360
Petit J, Bres C, Just D, Garcia V, Mauxion J-P, Marion D, Bakan B, Joubés J, Domergue F, Rothan C (2014) Analyses of tomato fruit brightness mutants uncover both cutin-deficient and cutin-abundant mutants and a new hypomorphic allele of GDSL lipase. Plant Physiol 164:888–906
Rodrigues JCM, Tucker MR, Johnson SD, Hrmova M, Koltunow AMG (2008) Sexual and apomictic seed formation in hieracium requires the plant polycomb-group gene fertilization independent endosperm. Plant cell 20:2372–2386
Schoeftner S, Sengupta AK, Kubicek S, Mechtler K, Spahn L, Koseki H, Jenuwein T, Wutz A (2006) Recruitment of PRC1 function at the initiation of X inactivation independent of PRC2 and silencing. EMBO J 25:3110–3122
Schubert D, Clarenz O, Goodrich J (2005) Epigenetic control of plant development by Polycomb-group proteins. Curr Opin Plant Biol 8:553–561
Shaver S, Casas-Mollano JA, Cerny RL, Cerutti H (2010) Origin of the polycomb repressive complex 2 and gene silencing by an E(z) homolog in the unicellular alga Chlamydomonas. Epigenetics 5:301–312
Spillane C, MacDougall C, Stock C, Kohler C, Vielle-Gazalda JP, Nunes SM, Grossniklaus U, Goodrich J (2000) Interaction of the Arabidopsis polycomb group proteins FIE and E(Z) mediates their common phenotypes. Curr Biol 10:1535–1538
Spillane C, Schmid KJ, Laoueille-Duprat S, Pien S, Escobar-Restrepo JM, Baroux C, Gagliardini V, Page DR, Wolfe KH, Grossniklaus U (2007) Positive darwinian selection at the imprinted MEDEA locus in plants. Nature 448:349–352
Tavares L, Dimitrova E, Oxley D, Webster J, Poot R, Demmers J, Bezstarosti K, Taylor S, Ura H, Koide H, Wutz A, Vidal M, Elderkin S, Brockdorff N (2012) RYBP-PRC1 complexes mediate H2A ubiquitylation at polycomb target sites independently of PRC2 and H3K27me3. Cell 148:664–678
Teyssier E, Bernacchia G, Maury S, How Kit A, Stammitti-Bert L, Rolin D, Gallusci P (2008) Tissue dependent variations of DNA methylation and endoreduplication levels during tomato fruit development and ripening. Planta 228:391–399
van der Knaap E, Chakrabarti M, Chu YH, Clevenger JP, Illa-Berenguer E, Huang Z, Keyhaninejad N, Mu Q, Sun L, Wang Y, Wu S (2014) What lies beyond the eye: the molecular mechanisms regulating tomato fruit weight and shape. Front Plant Sci 5:227
Wang H, Wang L, Erdjument-Bromage H, Vidal M, Tempst P, Jones RS, Zhang Y (2004) Role of histone H2A ubiquitination in polycomb silencing. Nature 431:873–878
Wang D, Tyson MD, Jackson SS, Yadegari R (2006) Partially redundant functions of two SET-domain polycomb-group proteins in controlling initiation of seed development in Arabidopsis. Proc Natl Acad Sci USA 103:13244–13249
Weinhofer I, Hehenberger E, Roszak P, Hennig L, Köhler C (2010) H3K27me3 profiling of the endosperm implies exclusion of polycomb group protein targeting by DNA methylation. PLoS Genet 6:e1001152
Wood CC, Robertson M, Tanner G, Peacock WJ, Dennis ES, Helliwell CA (2006) The Arabidopsis thaliana vernalization response requires a polycomb-like protein complex that also includes vernalization insensitive 3. Proc Natl Acad Sci USA 103:14631–14636
Xiao J, Wagner D (2015) Polycomb repression in the regulation of growth and development in Arabidopsis. Curr Opin Plant Biol 23:15–24
Yadegari R, Kinoshita T, Lotan O, Cohen G, Katz A, Choi Y, Nakashima K, Harada JJ, Goldberg RB, Fischer RL, Ohad N (2000) Mutations in the FIE and E(Z) genes that encode interacting polycomb proteins cause parent-of-origin effects on seed development by distinct mechanisms. Plant Cell 12:2367–2382
Yang C, Bratzel F, Hohmann N, Koch M, Turck F, Calonje M (2013) AL- and AtBMI1-mediated H2Aub initiate the switch from embryonic to postgerminative growth in Arabidopsis. Curr Biol 23:1324–1329
Yoshida N, Yanai Y, Chen L, Kato Y, Hiratsuka J, Miwa T, Sung ZR, Takahashi S (2001) Embryonic flower2, a novel polycomb group protein homolog, mediates shoot development and flowering in arabidopsis. Plant Cell Online 13:2471–2481
Zhong S, Fei Z, Chen Y-R, Zheng Y, Huang M, Vrebalov J, McQuinn R, Gapper N, Liu B, Xiang J, Shao Y, Giovannoni JJ (2013) Single-base resolution methylomes of tomato fruit development reveal epigenome modifications associated with ripening. Nat Biotech 31:154–159
Acknowledgments
LB and AHK were in receipt of a grant from the French Ministry of Research and Higher Education and MR from the Italian Ministry of Agriculture. Research work was in part funded by the French National Research Agency in the Frame of the ENDOREPIGENE project, by the Research Federation, Integrative Biology and Environment (FR BIE) and by the National Transgenic Program of China (2016ZX08009-001).
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Boureau, L., How-Kit, A., Teyssier, E. et al. A CURLY LEAF homologue controls both vegetative and reproductive development of tomato plants. Plant Mol Biol 90, 485–501 (2016). https://doi.org/10.1007/s11103-016-0436-0
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DOI: https://doi.org/10.1007/s11103-016-0436-0