Science China Life Sciences

, Volume 61, Issue 2, pp 225–234 | Cite as

Histone 3 lysine 36 to methionine mutations stably interact with and sequester SDG8 in Arabidopsis thaliana

Research Paper


Post-transcriptional modifications of histones play important roles in various biological processes. Here, we report that Arabidopsis plants overexpressing histone H3 lysine to methionine mutations at histone H3.1K36 (H3.1K36M) and H3.3K36 (H3.3K36M) have serious developmental defects with early-flowering and change in the modifications of endogenous histone H3, including acetylation at lysine 9 (H3K9ac), trimethylation at lysine 27 (H3K27me3), di- and tri-methylation at lysine 36 (H3K36me2 and H3K36me3). In addition, H3K36M mutation alters its subcellular localization and interacts with H3K36 methyltransferase SDG8. Our results support a model in which H3K36M stably interacts with SDG8, and inhibits the activity of SDG8 by sequestering SDG8, resulting in a dominant negative effect to affect the proper expression levels of a variety of genes and plant development.


histone H3 lysine to methionine mutation SDG8 dominant negative effect Arabidopsis 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.



This work was supported by the National Key Research and Development Program of China (2016YFD0100902) and Chinese Academy of Sciences (XDPB0403).

Supplementary material

11427_2017_9162_MOESM1_ESM.jpg (53 kb)
Figure S1 The chemical structure of lysine, methionine and isoleucine.
11427_2017_9162_MOESM2_ESM.docx (30 kb)
Table S1 The primers used in this study


  1. Baumbusch, L.O., Thorstensen, T., Krauss, V., Fischer, A., Naumann, K., Assalkhou, R., Schulz, I., Reuter, G., and Aalen, R.B. (2001). The Arabidopsis thaliana genome contains at least 29 active genes encoding SET domain proteins that can be assigned to four evolutionarily conserved classes. Nucleic Acids Res 29, 4319–4333.CrossRefPubMedPubMedCentralGoogle Scholar
  2. Behjati, S., Tarpey, P.S., Presneau, N., Scheipl, S., Pillay, N., Van Loo, P., Wedge, D.C., Cooke, S.L., Gundem, G., Davies, H., Nik-Zainal, S., Martin, S., McLaren, S., Goodie, V., Robinson, B., Butler, A., Teague, J.W., Halai, D., Khatri, B., Myklebost, O., Baumhoer, D., Jundt, G., Hamoudi, R., Tirabosco, R., Amary, M.F., Futreal, P.A., Stratton, M.R., Campbell, P.J., and Flanagan, A.M. (2013). Distinct H3F3A and H3F3B driver mutations define chondroblastoma and giant cell tumor of bone. Nat Genet 45, 1479–1482.CrossRefPubMedGoogle Scholar
  3. Berger, S.L. (2007). The complex language of chromatin regulation during transcription. Nature 447, 407–412.CrossRefPubMedGoogle Scholar
  4. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  5. 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.CrossRefPubMedGoogle Scholar
  6. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  7. Clough, S.J., and Bent, A.F. (1998). Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16, 735–743.CrossRefPubMedGoogle Scholar
  8. Fang, D., Gan, H., Lee, J.H., Han, J., Wang, Z., Riester, S.M., Jin, L., Chen, J., Zhou, H., Wang, J., Zhang, H., Yang, N., Bradley, E.W., Ho, T.H., Rubin, B.P., Bridge, J.A., Thibodeau, S.N., Ordog, T., Chen, Y., van Wijnen, A.J., Oliveira, A.M., Xu, R.M., Westendorf, J.J., and Zhang, Z. (2016). The histone H3.3K36M mutation reprograms the epigenome of chondroblastomas. Science 352, 1344–1348.CrossRefPubMedPubMedCentralGoogle Scholar
  9. Fang, Y., and Spector, D.L. (2007). Identification of nuclear dicing bodies containing proteins for microRNA biogenesis in living Arabidopsis plants. Curr Biol 17, 818–823.CrossRefPubMedPubMedCentralGoogle Scholar
  10. Fang, Y., and Spector, D.L. (2010). Live cell imaging of plants. In: Live Cell Imaging: A Laboratory Manual, 2th ed., R.D., Goldman, D.L., Spector, B.R., Masters, eds. (New York: Cold Spring Harbor Laboratory Press), pp. 371–386.Google Scholar
  11. Koriakov, D.E. (2006). Histone modification and regulation of chromatin function. Russian J Genet 42, 970–984.CrossRefGoogle Scholar
  12. Lewis, P.W., Müller, M.M., Koletsky, M.S., Cordero, F., Lin, S., Banaszynski, L.A., Garcia, B.A., Muir, T.W., Becher, O.J., and Allis, C.D. (2013). Inhibition of PRC2 activity by a gain-of-function H3 mutation found in pediatric glioblastoma. Science 340, 857–861.CrossRefPubMedPubMedCentralGoogle Scholar
  13. Li, M., and Fang, Y.D. (2015). Histone variants: the artists of eukaryotic chromatin. Sci China Life Sci 58, 232–239.CrossRefPubMedGoogle Scholar
  14. Liu, B., Berr, A., Chang, C., Liu, C., Shen, W.H., and Ruan, Y. (2016). Interplay of the histone methyltransferases SDG8 and SDG26 in the regulation of transcription and plant flowering and development. Biochim Biophys Acta 1859, 581–590.CrossRefPubMedGoogle Scholar
  15. Liu, C., Lu, F., Cui, X., and Cao, X. (2010). Histone methylation in higher plants. Annu Rev Plant Biol 61, 395–420.CrossRefPubMedGoogle Scholar
  16. Liu, Q., Yan, Q., Liu, Y., Hong, F., Sun, Z., Shi, L., Huang, Y., and Fang, Y. (2013). Complementation of hyponastic leaves1 by double-strand RNA-binding domains of dicer-like1 in nuclear dicing bodies. Plant Physiol 163, 108–117.CrossRefPubMedPubMedCentralGoogle Scholar
  17. Lu, F., Cui, X., Zhang, S., Jenuwein, T., and Cao, X. (2011). Arabidopsis REF6 is a histone H3 lysine 27 demethylase. Nat Genet 43, 715–719.CrossRefPubMedGoogle Scholar
  18. Luger, K., Mäder, A.W., Richmond, R.K., Sargent, D.F., and Richmond, T.J. (1997). Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature 389, 251–260.CrossRefPubMedGoogle Scholar
  19. Meller, V.H., Joshi, S.S., and Deshpande, N. (2015). Modulation of chromatin by noncoding RNA. Annu Rev Genet 49, 673–695.CrossRefPubMedGoogle Scholar
  20. Morris, S.A., Rao, B., Garcia, B.A., Hake, S.B., Diaz, R.L., Shabanowitz, J., Hunt, D.F., Allis, C.D., Lieb, J.D., and Strahl, B.D. (2007). Identification of histone H3 lysine 36 acetylation as a highly conserved histone modification. J Biol Chem 282, 7632–7640.CrossRefPubMedGoogle Scholar
  21. Narlikar, G.J., Sundaramoorthy, R., and Owen-Hughes, T. (2013). Mechanisms and functions of ATP-dependent chromatin-remodeling enzymes. Cell 154, 490–503.CrossRefPubMedPubMedCentralGoogle Scholar
  22. Okada, T., Endo, M., Singh, M.B., and Bhalla, P.L. (2005). Analysis of the histone H3 gene family in Arabidopsis and identification of the male-gamete-specific variant AtMGH3. Plant J 44, 557–568.CrossRefPubMedGoogle Scholar
  23. Qureshi, I.A., and Mehler, M.F. (2010). Emerging role of epigenetics in stroke: part 1: DNA methylation and chromatin modifications. Arch Neurol 67, 1316–1322.PubMedPubMedCentralGoogle Scholar
  24. Sanders, D., Qian, S., Fieweger, R., Lu, L., Dowell, J.A., Denu, J.M., and Zhong, X. (2017). Histone lysine-to-methionine mutations reduce histone methylation and cause developmental pleiotropy. Plant Physiol 173, 2243–2252.CrossRefPubMedPubMedCentralGoogle Scholar
  25. Schwartzentruber, J., Korshunov, A., Liu, X.Y., Jones, D.T.W., Pfaff, E., Jacob, K., Sturm, D., Fontebasso, A.M., Quang, D.A.K., Tönjes, M., Hovestadt, V., Albrecht, S., Kool, M., Nantel, A., Konermann, C., Lindroth, A., Jäger, N., Rausch, T., Ryzhova, M., Korbel, J.O., Hielscher, T., Hauser, P., Garami, M., Klekner, A., Bognar, L., Ebinger, M., Schuhmann, M.U., Scheurlen, W., Pekrun, A., Frühwald, M.C., Roggendorf, W., Kramm, C., Dürken, M., Atkinson, J., Lepage, P., Montpetit, A., Zakrzewska, M., Zakrzewski, K., Liberski, P.P., Dong, Z., Siegel, P., Kulozik, A.E., Zapatka, M., Guha, A., Malkin, D., Felsberg, J., Reifenberger, G., von Deimling, A., Ichimura, K., Collins, V.P., Witt, H., Milde, T., Witt, O., Zhang, C., Castelo-Branco, P., Lichter, P., Faury, D., Tabori, U., Plass, C., Majewski, J., Pfister, S.M., and Jabado, N. (2012). Driver mutations in histone H3.3 and chromatin remodelling genes in paediatric glioblastoma. Nature 482, 226–231.CrossRefPubMedGoogle Scholar
  26. Shi, L., Wang, J., Hong, F., Spector, D.L., and Fang, Y. (2011). Four amino acids guide the assembly or disassembly of Arabidopsis histone H3.3-containing nucleosomes. Proc Natl Acad Sci USA 108, 10574–10578.CrossRefPubMedPubMedCentralGoogle Scholar
  27. Strahl, B.D., and Allis, C.D. (2000). The language of covalent histone modifications. Nature 403, 41–45.CrossRefPubMedGoogle Scholar
  28. Wu, G., Broniscer, A., McEachron, T.A., Lu, C., Paugh, B.S., Becksfort, J., Qu, C., Ding, L., Huether, R., Parker, M., Zhang, J., Gajjar, A., Dyer, M.A., Mullighan, C.G., Gilbertson, R.J., Mardis, E.R., Wilson, R.K., Downing, J.R., Ellison, D.W., Zhang, J., Baker, S.J., and Baker, S.J. (2012). Somatic histone H3 alterations in pediatric diffuse intrinsic pontine gliomas and non-brainstem glioblastomas. Nat Genet 44, 251–253.CrossRefPubMedPubMedCentralGoogle Scholar
  29. 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.CrossRefPubMedGoogle Scholar
  30. Yan, Q., Xia, X., Sun, Z., and Fang, Y. (2017). Depletion of Arabidopsis SC35 and SC35-like serine/arginine-rich proteins affects the transcription and splicing of a subset of genes. PLoS Genet 13, e1006663.CrossRefPubMedPubMedCentralGoogle Scholar
  31. 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.CrossRefPubMedGoogle Scholar

Copyright information

© Science China Press and Springer-Verlag GmbH Germany, part of Springer Nature 2017

Authors and Affiliations

  1. 1.National key Laboratory of Plant Molecular Genetics, Chinese Academy of Sciences Center for Excellence in Molecular Plant Sciences, Institute of Plant Physiology and EcologyChinese Academy of Sciences; University of Chinese Academy of SciencesShanghaiChina

Personalised recommendations