Skip to main content
SpringerLink
Log in

EARLY FLOWERING IN SHORT DAYS (EFS) regulates the seed size in Arabidopsis

  • Research Paper
  • Published:
Science China Life Sciences Aims and scope Submit manuscript

Abstract

Post-transcriptional modifications, including histone modifications and DNA methylation, alter the chromatin landscape to regulate gene expression, thus control various cellular processes in plants. EARLY FLOWERING IN SHORT DAYS (EFS) is the major contributor for H3K36 methylation in Arabidopsis and is important for plant development. Here, we find that EFS is expressed in different stages of embryo morphogenesis, and the efs mutant produces larger embryo that results in enlarged seeds. Further analysis reveals that an imprinted gene MOP9.5 is hypomethylated at the promoter region and its expression is derepressed in efs mutant. MOP9.5 promoter is marked by various epigenetic modifications, and we find that following the increase of H3K36me3, H3K27me3 and H3K9me2 levels are reduced in efs mutant. This data indicates an antagonistic regulation between H3K36me3 and DNA methylation, and/or H3K27me3 at MOP9.5. Our results further show that both maternal and paternal EFS alleles are responsible for the seed size regulation, which unraveled a novel function of EFS in plant development.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Akhter, S., Uddin, M.N., Jeong, I.S., Kim, D.W., Liu, X.M., and Bahk, J.D. (2016). Role of Arabidopsis AtPI4Kγ3, a type II phosphoinositide 4- kinase, in abiotic stress responses and floral transition. Plant Biotechnol J 14, 215–230.

    Article  CAS  PubMed  Google Scholar 

  • Baroux, C., Gagliardini, V., Page, D.R., and Grossniklaus, U. (2006). Dynamic regulatory interactions of Polycomb group genes: MEDEA autoregulation is required for imprinted gene expression in Arabidopsis. Genes Dev 20, 1081–1086.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baubec, T., Colombo, D.F., Wirbelauer, C., Schmidt, J., Burger, L., Krebs, A.R., Akalin, A., and Schübeler, D. (2015). Genomic profiling of DNA methyltransferases reveals a role for DNMT3B in genic methylation. Nature 520, 243–247.

    Article  CAS  PubMed  Google Scholar 

  • Bernatavichute, Y.V., Zhang, X., Cokus, S., Pellegrini, M., and Jacobsen, S. E. (2008). Genome-wide association of histone H3 lysine nine methylation with CHG DNA methylation in Arabidopsis thaliana. PLoS ONE 3, e3156.

    Article  PubMed  PubMed Central  Google Scholar 

  • Berr, A., McCallum, E.J., Alioua, A., Heintz, D., Heitz, T., and Shen, W.H. (2010). Arabidopsis histone methyltransferase SET DOMAIN GROUP8 mediates induction of the jasmonate/ethylene pathway genes in plant defense response to necrotrophic fungi. Plant Physiol 154, 1403–1414.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Berr, A., Shafiq, S., Pinon, V., Dong, A., and Shen, W.H. (2015). The trxG family histone methyltransferase SET DOMAIN GROUP26 promotes flowering via a distinctive genetic pathway. Plant J 81, 316–328.

    Article  CAS  PubMed  Google Scholar 

  • Berr, A., Shafiq, S., and Shen, W.H. (2011). Histone modifications in transcriptional activation during plant development. Biochim Biophys Acta 1809, 567–576.

    Article  CAS  PubMed  Google Scholar 

  • Calarco, J.P., and Martienssen, R.A. (2012). Imprinting: DNA methyltransferases illuminate reprogramming. Curr Biol 22, R929–931.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cao, X., and Jacobsen, S.E. (2002). Role of the Arabidopsis DRM methyltransferases in de novo DNA methylation and gene silencing. Curr Biol 12, 1138–1144.

    Article  CAS  PubMed  Google Scholar 

  • Cartagena, J.A., Matsunaga, S., Seki, M., Kurihara, D., Yokoyama, M., Shinozaki, K., Fujimoto, S., Azumi, Y., Uchiyama, S., and Fukui, K. (2008). The Arabidopsis SDG4 contributes to the regulation of pollen tube growth by methylation of histone H3 lysines 4 and 36 in mature pollen. Dev Biol 315, 355–368.

    Article  CAS  PubMed  Google Scholar 

  • Cazzonelli, C.I., Cuttriss, A.J., Cossetto, S.B., Pye, W., Crisp, P., Whelan, J., Finnegan, E.J., Turnbull, C., and Pogson, B.J. (2009). Regulation of carotenoid composition and shoot branching in Arabidopsis by a chromatin modifying histone methyltransferase, SDG8. Plant Cell 21, 39–53.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cazzonelli, C.I., Nisar, N., Roberts, A.C., Murray, K.D., Borevitz, J.O., and Pogson, B.J. (2014). A chromatin modifying enzyme, SDG8, is involved in morphological, gene expression, and epigenetic responses to mechanical stimulation. Front Plant Sci 5, 533.

    Article  PubMed  PubMed Central  Google Scholar 

  • Cazzonelli, C.I., Roberts, A.C., Carmody, M.E., and Pogson, B.J. (2010). Transcriptional control of SET DOMAIN GROUP 8 and CAROTENOID ISOMERASE during Arabidopsis development. Mol Plant 3, 174–191.

    Article  CAS  PubMed  Google Scholar 

  • Cui, X., Jin, P., Cui, X., Gu, L., Lu, Z., Xue, Y., Wei, L., Qi, J., Song, X., Luo, M., An, G., and Cao, X. (2013). Control of transposon activity by a histone H3K4 demethylase in rice. Proc Natl Acad Sci USA 110, 1953–1958.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dhayalan, A., Rajavelu, A., Rathert, P., Tamas, R., Jurkowska, R.Z., Ragozin, S., and Jeltsch, A. (2010). The Dnmt3a PWWP domain reads histone 3 lysine 36 trimethylation and guides DNA methylation. J Biol Chem 285, 26114–26120.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dong, G., Ma, D.P., and Li, J. (2008). The histone methyltransferase SDG8 regulates shoot branching in Arabidopsis. Biochem BioPhys Res Commun 373, 659–664.

    Article  CAS  PubMed  Google Scholar 

  • Du, J., Johnson, L.M., Jacobsen, S.E., and Patel, D.J. (2015). DNA methylation pathways and their crosstalk with histone methylation. Nat Rev Mol Cell Biol 16, 519–532.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Du, J., Zhong, X., Bernatavichute, Y.V., Stroud, H., Feng, S., Caro, E., Vashisht, A.A., Terragni, J., Chin, H.G., Tu, A., Hetzel, J., Wohlschlegel, J.A., Pradhan, S., Patel, D.J., and Jacobsen, S.E. (2012). Dual binding of chromomethylase domains to H3K9me2-containing nucleosomes directs DNA methylation in plants. Cell 151, 167–180.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • FitzGerald, J., Luo, M., Chaudhury, A., and Berger, F. (2008). DNA methylation causes predominant maternal controls of plant embryo growth. PLoS ONE 3, e2298.

    Article  PubMed  PubMed Central  Google Scholar 

  • García-Aguilar, M., and Gillmor, C.S. (2015). Zygotic genome activation and imprinting: parent-of-origin gene regulation in plant embryogenesis. Curr Opin Plant Biol 27, 29–35.

    Article  PubMed  Google Scholar 

  • Gehring, M. (2013). Genomic imprinting: insights from plants. Annu Rev Genet 47, 187–208.

    Article  CAS  PubMed  Google Scholar 

  • Gehring, M., Huh, J.H., Hsieh, T.F., Penterman, J., Choi, Y., Harada, J.J., Goldberg, R.B., and Fischer, R.L. (2006). DEMETER DNA glycosylase establishes MEDEA Polycomb gene self-imprinting by allele-specific demethylation. Cell 124, 495–506.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Grini, P.E., Thorstensen, T., Alm, V., Vizcay-Barrena, G., Windju, S.S., Jørstad, T.S., Wilson, Z.A., and Aalen, R.B. (2009). The ASH1 HOMOLOG 2 (ASHH2) histone H3 methyltransferase is required for ovule and anther development in Arabidopsis. PLoS ONE 4, e7817.

    Article  PubMed  PubMed Central  Google Scholar 

  • He, G., Elling, A.A., and Deng, X.W. (2011). The epigenome and plant development. Annu Rev Plant Biol 62, 411–435.

    Article  CAS  PubMed  Google Scholar 

  • He, S., Sun, Y., Yang, Q., Zhang, X., Huang, Q., Zhao, P., Sun, M., Liu, J., Qian, W., Qin, G., Gu, H., and Qu, L.J. (2017). A novel imprinted gene NUWA controls mitochondrial function in early seed development in Arabidopsis. PLoS Genet 13, e1006553.

    Article  PubMed  PubMed Central  Google Scholar 

  • Hsieh, T.F., Shin, J., Uzawa, R., Silva, P., Cohen, S., Bauer, M.J., Hashimoto, M., Kirkbride, R.C., Harada, J.J., Zilberman, D., and Fischer, R. L. (2011). Regulation of imprinted gene expression in Arabidopsis endosperm. Proc Natl Acad Sci USA 108, 1755–1762.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kankel, M.W., Ramsey, D.E., Stokes, T.L., Flowers, S.K., Haag, J.R., Jeddeloh, J.A., Riddle, N.C., Verbsky, M.L., and Richards, E.J. (2003). Arabidopsis MET1 cytosine methyltransferase mutants. Genetics 163, 1109–1122.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kim, S.Y., He, Y., Jacob, Y., Noh, Y.S., Michaels, S., and Amasino, R. (2005). Establishment of the vernalization-responsive, winter-annual habit in Arabidopsis requires a putative histone H3 methyl transferase. Plant Cell 17, 3301–3310.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ko, J.H., Mitina, I., Tamada, Y., Hyun, Y., Choi, Y., Amasino, R.M., Noh, B., and Noh, Y.S. (2010). Growth habit determination by the balance of histone methylation activities in Arabidopsis. EMBO J 29, 3208–3215.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Köhler, C., Wolff, P., and Spillane, C. (2012). Epigenetic mechanisms underlying genomic imprinting in plants. Annu Rev Plant Biol 63, 331–352.

    Article  PubMed  Google Scholar 

  • Roszak, P., and Köhler, C. (2011). Polycomb group proteins are required to couple seed coat initiation to fertilization. Proc Natl Acad Sci USA 108, 20826–20831.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Law, J.A., and Jacobsen, S.E. (2010). Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nat Rev Genet 11, 204–220.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li, N., and Li, Y. (2016). Signaling pathways of seed size control in plants. Curr Opin Plant Biol 33, 23–32.

    Article  PubMed  Google Scholar 

  • Li, Y., Mukherjee, I., Thum, K.E., Tanurdzic, M., Katari, M.S., Obertello, M., Edwards, M.B., McCombie, W.R., Martienssen, R.A., and Coruzzi, G.M. (2015). The histone methyltransferase SDG8 mediates the epigenetic modification of light and carbon responsive genes in plants. Genome Biol 16, 79.

    Article  PubMed  PubMed Central  Google Scholar 

  • Lindroth, A.M., Cao, X., Jackson, J.P., Zilberman, D., McCallum, C.M., Henikoff, S., and Jacobsen, S.E. (2001). Requirement of CHROMOMETHYLASE3 for maintenance of CpXpG methylation. Science 292, 2077–2080.

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Matzke, M.A., and Mosher, R.A. (2014). RNA-directed DNA methylation: an epigenetic pathway of increasing complexity. Nat Rev Genet 15, 394–408.

    Article  CAS  PubMed  Google Scholar 

  • Ohnishi, T., Sekine, D., and Kinoshita, T. (2014). Genomic imprinting in plants: what makes the functions of paternal and maternal genes different in endosperm formation? Adv Genet 86, 1–25.

    CAS  PubMed  Google Scholar 

  • Orozco-Arroyo, G., Paolo, D., Ezquer, I., and Colombo, L. (2015). Networks controlling seed size in Arabidopsis. Plant Reprod 28, 17–32.

    Article  CAS  PubMed  Google Scholar 

  • Palma, K., Thorgrimsen, S., Malinovsky, F.G., Fiil, B.K., Nielsen, H.B., Brodersen, P., Hofius, D., Petersen, M., and Mundy, J. (2010). Autoimmunity in Arabidopsis acd11 is mediated by epigenetic regulation of an immune receptor. PLoS Pathog 6, e1001137.

    Article  PubMed  PubMed Central  Google Scholar 

  • Rodrigues, J.A., and Zilberman, D. (2015). Evolution and function of genomic imprinting in plants. Genes Dev 29, 2517–2531.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Shafiq, S., Berr, A., and Shen, W.H. (2014). Combinatorial functions of diverse histone methylations in Arabidopsis thaliana flowering time regulation. New Phytol 201, 312–322.

    Article  CAS  PubMed  Google Scholar 

  • Sun, Q., Csorba, T., Skourti-Stathaki, K., Proudfoot, N.J., and Dean, C. (2013). R-loop stabilization represses antisense transcription at the Arabidopsis FLC locus. Science 340, 619–621.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tang, X., Lim, M.H., Pelletier, J., Tang, M., Nguyen, V., Keller, W.A., Tsang, E.W.T., Wang, A., Rothstein, S.J., Harada, J.J., and Cui, Y. (2012). Synergistic repression of the embryonic programme by SET DOMAIN GROUP 8 and EMBRYONIC FLOWER 2 in Arabidopsis seedlings. J Exp Bot 63, 1391–1404.

    Article  CAS  PubMed  Google Scholar 

  • Vermeulen, M., Eberl, H.C., Matarese, F., Marks, H., Denissov, S., Butter, F., Lee, K.K., Olsen, J.V., Hyman, A.A., Stunnenberg, H.G., and Mann, M. (2010). Quantitative interaction proteomics and genome-wide profiling of epigenetic histone marks and their readers. Cell 142, 967–980.

    Article  CAS  PubMed  Google Scholar 

  • Vu, T.M., Nakamura, M., Calarco, J.P., Susaki, D., Lim, P.Q., Kinoshita, T., Higashiyama, T., Martienssen, R.A., and Berger, F. (2013). RNA-directed DNA methylation regulates parental genomic imprinting at several loci in Arabidopsis. Development 140, 2953–2960.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang, X., Chen, J., Xie, Z., Liu, S., Nolan, T., Ye, H., Zhang, M., Guo, H., Schnable, P.S., Li, Z., and Yin, Y. (2014). Histone lysine methyltransferase SDG8 is involved in brassinosteroid-regulated gene expression in Arabidopsis thaliana. Mol Plant 7, 1303–1315.

    Article  CAS  PubMed  Google Scholar 

  • Wendte, J.M., and Pikaard, C.S. (2017). The RNAs of RNA-directed DNA methylation. Biochim Biophys Acta 1860, 140–148.

    Article  CAS  PubMed  Google Scholar 

  • Wolff, P., Jiang, H., Wang, G., Santos-González, J., and Köhler, C. (2015). Paternally expressed imprinted genes establish postzygotic hybridization barriers in Arabidopsis thaliana. eLife 4, e10074.

    Article  PubMed Central  Google Scholar 

  • Xiao, W., Brown, R.C., Lemmon, B.E., Harada, J.J., Goldberg, R.B., and Fischer, R.L. (2006a). Regulation of seed size by hypomethylation of maternal and paternal genomes. Plant Physiol 142, 1160–1168.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xiao, W., Custard, K.D., Brown, R.C., Lemmon, B.E., Harada, J.J., Goldberg, R.B., and Fischer, R.L. (2006b). DNA methylation is critical for Arabidopsis embryogenesis and seed viability. Plant Cell 18, 805–814.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xu, L., Zhao, Z., Dong, A., Soubigou-Taconnat, L., Renou, J.P., Steinmetz, A., and Shen, W.H. (2008). Di- and Tri- but not monomethylation on histone H3 lysine 36 marks active transcription of genes involved in flowering time regulation and other processes in Arabidopsis thaliana. Mol Cell Biol 28, 1348–1360.

    Article  CAS  PubMed  Google Scholar 

  • Yang, H., Howard, M., and Dean, C. (2014). Antagonistic roles for H3- K36me3 and H3K27me3 in the cold-induced epigenetic switch at Arabidopsis FLC. Curr Biol 24, 1793–1797.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang, H., Tang, K., Wang, B., Duan, C.G., Lang, Z., and Zhu, J.K. (2014). Protocol: a beginner’s guide to the analysis of RNA-directed DNA methylation in plants. Plant Methods 10, 18.

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhang, X., Clarenz, O., Cokus, S., Bernatavichute, Y.V., Pellegrini, M., Goodrich, J., and Jacobsen, S.E. (2007). Whole-genome analysis of histone H3 lysine 27 trimethylation in Arabidopsis. PLoS Biol 5, e129.

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhao, X., Wang, Y., Wang, Y., Liu, Y., and Gao, S. (2017). Histone methyltransferase TXR1 is required for both H3 and H3.3 lysine 27 methylation in the well-known ciliated protist Tetrahymena thermophila. Sci China Life Sci 60, 264–270.

    Article  CAS  PubMed  Google Scholar 

  • Zhao, Z., Yu, Y., Meyer, D., Wu, C., and Shen, W.H. (2005). Prevention of early flowering by expression of FLOWERING LOCUS C requires methylation of histone H3 K36. Nat Cell Biol 7, 1256–1260.

    Article  PubMed  Google Scholar 

  • Zhu, H., Wang, G., and Qian, J. (2016). Transcription factors as readers and effectors of DNA methylation. Nat Rev Genet 17, 551–565.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We thank all the members of The Sun Lab for useful discussions, and Prof. Barry J. Pogson for sharing the pEFS::GUS seeds, and Dr. Wen-Hui Shen for the complementation line of pEFS:EFS in efs mutant. This work was supported by National Key R&D Program (2016YFA0500800), the National Natural Science Foundation of China (31571322), Tsinghua-Peking Joint Center for Life Sciences, and 1000 Young Talent Program of China. S. Shafiq and Wei Xu are supported by the postdoctoral fellowships from Tsinghua-Peking Joint Center for Life Sciences.

Author information

Authors and Affiliations

  1. Center for Plant Biology, and Tsinghua-Peking Joint Center for Life Sciences, School of Life Sciences, Tsinghua University, Beijing, 100084, China

    Lingling Cheng, Sarfraz Shafiq, Wei Xu & Qianwen Sun

Authors
  1. Lingling Cheng
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sarfraz Shafiq
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Wei Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Qianwen Sun
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Qianwen Sun.

Electronic supplementary material

Figure S1

DNA methylation screening of imprinted genes by Chop-PCR in flowers and buds of Col-0 and efs-3. McrBC is a methylation-sensitive enzyme that specifically digests methylated DNA, and the bands with McrBC treatment represent the non-methylation levels.

Figure S2mop9.5 has a normal seed size, while MOP9.5 is methylated and is the target of RNA Pol V.

Table S1

Primers information

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Cheng, L., Shafiq, S., Xu, W. et al. EARLY FLOWERING IN SHORT DAYS (EFS) regulates the seed size in Arabidopsis. Sci. China Life Sci. 61, 214–224 (2018). https://doi.org/10.1007/s11427-017-9236-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11427-017-9236-x

Keywords

Search

Navigation