Skip to main content
SpringerLink
Log in

Functions and mechanisms of plant histone deacetylases

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

Abstract

Lysine acetylation, one of the major types of post-translational modifications, plays critical roles in regulating gene expression and protein function. Histone deacetylases (HDACs) are responsible for removing acetyl groups from lysines of both histone and non-histone proteins. While tremendous progress has been made in understanding the function and mechanism of HDACs in animals in the past two decades, nearly half of the HDAC studies in plants were reported within the past five years. In this review, we summarize the major findings on plant HDACs, with a focus on the model plant Arabidopsis thaliana, and highlight the components, regulatory mechanisms, and biological functions of HDAC complexes.

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

  • Alinsug, M.V., Chen, F.F., Luo, M., Tai, R., Jiang, L., and Wu, K. (2012). Subcellular localization of class II HDAs in Arabidopsis thaliana: nucleocytoplasmic shuttling of HDA15 is driven by light. PLoS ONE 7, e30846.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Alinsug, M.V., Yu, C.W., and Wu, K. (2009). Phylogenetic analysis, subcellular localization, and expression patterns of RPD3/HDA1 family histone deacetylases in plants. BMC Plant Biol 9, 37.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Aufsatz, W., Mette, M.F., van der Winden, J., Matzke, M., and Matzke, A.J. (2002). HDA6, a putative histone deacetylase needed to enhance DNA methylation induced by double-stranded RNA. EMBO J 21, 6832–6841.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Aufsatz, W., Stoiber, T., Rakic, B., and Naumann, K. (2007). Arabidopsis histone deacetylase 6: a green link to RNA silencing. Oncogene 26, 5477–5488.

    Article  CAS  PubMed  Google Scholar 

  • Blevins, T., Pontvianne, F., Cocklin, R., Podicheti, R., Chandrasekhara, C., Yerneni, S., Braun, C., Lee, B., Rusch, D., Mockaitis, K., et al. (2014). A two-step process for epigenetic inheritance in Arabidopsis. Mol Cell 54, 30–42.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bosch-Presegue, L., and Vaquero, A. (2015). Sirtuin-dependent epigenetic regulation in the maintenance of genome integrity. FEBS J 282, 1745–1767.

    Article  CAS  PubMed  Google Scholar 

  • Bourque, S., Jeandroz, S., Grandperret, V., Lehotai, N., Aimé, S., Soltis, D. E., Miles, N.W., Melkonian, M., Deyholos, M.K., Leebens-Mack, J.H., et al. (2016). The evolution of HD2 proteins in green plants. Trends Plant Sci 21, 1008–1016.

    Article  CAS  PubMed  Google Scholar 

  • Buszewicz, D., Archacki, R., Palusiński, A., Kotliński, M., Fogtman, A., Iwanicka-Nowicka, R., Sosnowska, K., Kuciński, J., Pupel, P., Olȩdzki, J., et al. (2016). HD2C histone deacetylase and a SWI/SNF chromatin remodelling complex interact and both are involved in mediating the heat stress response in Arabidopsis. Plant Cell Environ 39, 2108–2122.

    Article  CAS  PubMed  Google Scholar 

  • Chen, L.T., and Wu, K. (2010). Role of histone deacetylases HDA6 and HDA19 in ABA and abiotic stress response. Plant Signal Behav 5, 1318–1320.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen, W.Q., Drapek, C., Li, D.X., Xu, Z.H., Benfey, P.N., and Bai, S.N. (2019). Histone deacetylase HDA19 affects root cortical cell fate by interacting with SCARECROW. Plant Physiol 180, 276–288.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen, X., Lu, L., Mayer, K.S., Scalf, M., Qian, S., Lomax, A., Smith, L.M., and Zhong, X. (2016). POWERDRESS interacts with HISTONE DEACETYLASE 9 to promote aging in Arabidopsis. eLife 5, e17214.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Chen, X., Lu, L., Qian, S., Scalf, M., Smith, L.M., and Zhong, X. (2018). Canonical and noncanonical actions of Arabidopsis histone deacetylases in ribosomal RNA processing. Plant Cell 30, 134–152.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cheng, L., Shafiq, S., Xu, W., and Sun, Q. (2018). EARLY FLOWERING IN SHORT DAYS (EFS) regulates the seed size in Arabidopsis. Sci China Life Sci 61, 214–224.

    Article  PubMed  Google Scholar 

  • Cigliano, R.A., Cremona, G., Paparo, R., Termolino, P., Perrella, G., Gutzat, R., Consiglio, M.F., and Conicella, C. (2013). Histone deacetylase AtHDA7 is required for female gametophyte and embryo development in Arabidopsis. Plant Physiol 163, 431–440.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ding, B., Bellizzi, M.R., Ning, Y., Meyers, B.C., and Wang, G.L. (2012). HDT701, a histone H4 deacetylase, negatively regulates plant innate immunity by modulating histone H4 acetylation of defense-related genes in rice. Plant Cell 24, 3783–3794.

    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., et al. (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 

  • Earley, K., Lawrence, R.J., Pontes, O., Reuther, R., Enciso, A.J., Silva, M., Neves, N., Gross, M., Viegas, W., and Pikaard, C.S. (2006). Erasure of histone acetylation by Arabidopsis HDA6 mediates large-scale gene silencing in nucleolar dominance. Genes Dev 20, 1283–1293.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Earley, K.W., Pontvianne, F., Wierzbicki, A.T., Blevins, T., Tucker, S., Costa-Nunes, P., Pontes, O., and Pikaard, C.S. (2010). Mechanisms of HDA6-mediated rRNA gene silencing: suppression of intergenic Pol II transcription and differential effects on maintenance versus siRNA-directed cytosine methylation. Genes Dev 24, 1119–1132.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gao, M.J., Li, X., Huang, J., Gropp, G.M., Gjetvaj, B., Lindsay, D.L., Wei, S., Coutu, C., Chen, Z., Wan, X.C., et al. (2015). SCARECROWLIKE15 interacts with HISTONE DEACETYLASE19 and is essential for repressing the seed maturation programme. Nat Commun 6, 7243.

    Article  PubMed  Google Scholar 

  • Gao, M.J., Parkin, I., Lydiate, D., and Hannoufa, A. (2004). An auxin-responsive SCARECROW-like transcriptional activator interacts with histone deacetylase. Plant Mol Biol 55, 417–431.

    Article  CAS  PubMed  Google Scholar 

  • Gong, F., and Miller, K.M. (2013). Mammalian DNA repair: HATs and HDACs make their mark through histone acetylation. Mutat Res/Fund Mol Mech Mutag 750, 23–30.

    Article  CAS  Google Scholar 

  • Gonzalez, D., Bowen, A.J., Carroll, T.S., and Conlan, R.S. (2007). The transcription corepressor LEUNIG interacts with the histone deacetylase HDA19 and mediator components MED14 (SWP) and CDK8 (HEN3) to repress transcription. Mol Cell Biol 27, 5306–5315.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Grunstein, M. (1997). Histone acetylation in chromatin structure and transcription. Nature 389, 349–352.

    Article  CAS  PubMed  Google Scholar 

  • Gu, D., Chen, C.Y., Zhao, M., Zhao, L., Duan, X., Duan, J., Wu, K., and Liu, X. (2017). Identification of HDA15-PIF1 as a key repression module directing the transcriptional network of seed germination in the dark. Nucleic Acids Res 45, 7137–7150.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guenther, M.G., Lane, W.S., Fischle, W., Verdin, E., Lazar, M.A., and Shiekhattar, R. (2000). A core SMRT corepressor complex containing HDAC3 and TBL1, a WD40-repeat protein linked to deafness. Genes Dev 14, 1048–1057.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Haberland, M., Montgomery, R.L., and Olson, E.N. (2009). The many roles of histone deacetylases in development and physiology: implications for disease and therapy. Nat Rev Genet 10, 32–42.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Han, Z., Yu, H., Zhao, Z., Hunter, D., Luo, X., Duan, J., and Tian, L. (2016). AtHD2D gene plays a role in plant growth, development, and response to abiotic stresses in Arabidopsis thaliana. Front Plant Sci 7.

  • Hao, Y., Wang, H., Qiao, S., Leng, L., and Wang, X. (2016). Histone deacetylase HDA6 enhances brassinosteroid signaling by inhibiting the BIN2 kinase. Proc Natl Acad Sci USA 113, 10418–10423.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hartl, M., Füßl, M., Boersema, P.J., Jost, J.O., Kramer, K., Bakirbas, A., Sindlinger, J., Plöchinger, M., Leister, D., Uhrig, G., et al. (2017). Lysine acetylome profiling uncovers novel histone deacetylase substrate proteins in Arabidopsis. Mol Syst Biol 13, 949.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hayakawa, T., and Nakayama, J.I. (2011). Physiological roles of class I HDAC complex and histone demethylase. J Biomed Biotech 2011(7), 1–10.

    Article  CAS  Google Scholar 

  • Hollender, C., and Liu, Z. (2008). Histone deacetylase genes in Arabidopsis development. J Integrat Plant Biol 50, 875–885.

    Article  CAS  Google Scholar 

  • Hong, J., Lee, H., Lee, J., Kim, H., and Ryu, H. (2019). ABSCISIC ACID-INSENSITIVE 3 is involved in brassinosteroid-mediated regulation of flowering in plants. Plant Physiol Biochem 139, 207–214.

    Article  CAS  PubMed  Google Scholar 

  • Hristova, E., Fal, K., Klemme, L., Windels, D., and Bucher, E. (2015). HISTONE DEACETYLASE6 controls gene expression patterning and DNA methylation-independent euchromatic silencing. Plant Physiol 168, 1298–1308.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huang, L., Sun, Q., Qin, F., Li, C., Zhao, Y., and Zhou, D.X. (2007). Down-regulation of a SILENT INFORMATION REGULATOR2-related histone deacetylase gene, OsSRT1, induces DNA fragmentation and cell death in rice. Plant Physiol 144, 1508–1519.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hung, F.Y., Chen, F.F., Li, C., Chen, C., Chen, J.H., Cui, Y., and Wu, K. (2019). The LDL1/2-HDA6 histone modification complex interacts with TOC1 and regulates the core circadian clock components in Arabidopsis. Front Plant Sci 10, 233.

    Article  PubMed  PubMed Central  Google Scholar 

  • Hung, F.Y., Chen, F.F., Li, C., Chen, C., Lai, Y.C., Chen, J.H., Cui, Y., and Wu, K. (2018). The Arabidopsis LDL1/2-HDA6 histone modification complex is functionally associated with CCA1/LHY in regulation of circadian clock genes. Nucleic Acids Res 20.

  • Jiang, H., Khan, S., Wang, Y., Charron, G., He, B., Sebastian, C., Du, J., Kim, R., Ge, E., Mostoslavsky, R., et al. (2013). SIRT6 regulates TNF-α secretion through hydrolysis of long-chain fatty acyl lysine. Nature 496, 110–113.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Joshi, P., Greco, T.M., Guise, A.J., Luo, Y., Yu, F., Nesvizhskii, A.I., and Cristea, I.M. (2013). The functional interactome landscape of the human histone deacetylase family. Mol Syst Biol 9, 672.

    Article  PubMed  PubMed Central  Google Scholar 

  • Kang, M.J., Jin, H.S., Noh, Y.S., and Noh, B. (2015). Repression of flowering under a noninductive photoperiod by the HDA9-AGL19-FT module in Arabidopsis. New Phytol 206, 281–294.

    Article  CAS  PubMed  Google Scholar 

  • Karagianni, P., and Wong, J. (2007). HDAC3: taking the SMRT-N-CoRrect road to repression. Oncogene 26, 5439–5449.

    Article  CAS  PubMed  Google Scholar 

  • Kim, H., Shim, D., Moon, S., Lee, J., Bae, W., Choi, H., Kim, K., and Ryu, H. (2019). Transcriptional network regulation of the brassinosteroid signaling pathway by the BES1-TPL-HDA19 co-repressor complex. Planta 250, 1371–1377.

    Article  CAS  PubMed  Google Scholar 

  • Kim, J.M., To, T.K., and Seki, M. (2012). An epigenetic integrator: new insights into genome regulation, environmental stress responses and developmental controls by histone deacetylase 6. Plant Cell Physiol 53, 794–800.

    Article  CAS  PubMed  Google Scholar 

  • Kim, K.C., Lai, Z., Fan, B., and Chen, Z. (2008). Arabidopsis WRKY38 and WRKY62 transcription factors interact with histone deacetylase 19 in basal defense. Plant Cell 20, 2357–2371.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim, W., Latrasse, D., Servet, C., and Zhou, D.X. (2013). Arabidopsis histone deacetylase HDA9 regulates flowering time through repression of AGL19. Biochem Biophys Res Commun 432, 394–398.

    Article  CAS  PubMed  Google Scholar 

  • Kim, Y.J., Wang, R., Gao, L., Li, D., Xu, C., Mang, H., Jeon, J., Chen, X., Zhong, X., Kwak, J.M., et al. (2016). POWERDRESS and HDA9 interact and promote histone H3 deacetylation at specific genomic sites in Arabidopsis. Proc Natl Acad Sci USA 113, 14858–14863.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim, Y.K., Kim, S., Shin, Y., Hur, Y.S., Kim, W.Y., Lee, M.S., Cheon, C.I., and Verma, D.P.S. (2014). Ribosomal protein S6, a target of rapamycin, is involved in the regulation of rRNA genes by possible epigenetic changes in Arabidopsis. J Biol Chem 289, 3901–3912.

    Article  CAS  PubMed  Google Scholar 

  • Konig, A.C., Hartl, M., Pham, P.A., Laxa, M., Boersema, P.J., Orwat, A., Kalitventseva, I., Plöchinger, M., Braun, H.P., Leister, D., et al. (2014). The Arabidopsis class II sirtuin is a lysine deacetylase and interacts with mitochondrial energy metabolism. Plant Physiol 164, 1401–1414.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kornberg, R.D. (1974). Chromatin structure: a repeating unit of histones and DNA. Science 184, 868–871.

    Article  CAS  PubMed  Google Scholar 

  • Kouzarides, T. (2007). Chromatin modifications and their function. Cell 128, 693–705.

    CAS  PubMed  Google Scholar 

  • Krogan, N.T., Hogan, K., and Long, J.A. (2012). APETALA2 negatively regulates multiple floral organ identity genes in Arabidopsis by recruiting the co-repressor TOPLESS and the histone deacetylase HDA19. Development 139, 4180–4190.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Latrasse, D., Jégu, T., Li, H., de Zelicourt, A., Raynaud, C., Legras, S., Gust, A., Samajova, O., Veluchamy, A., Rayapuram, N., et al. (2017). MAPK-triggered chromatin reprogramming by histone deacetylase in plant innate immunity. Genome Biol 18, 131.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lee, K., Mas, P., and Seo, P.J. (2019). The EC-HDA9 complex rhythmically regulates histone acetylation at the TOC1 promoter in Arabidopsis. Commun Biol 2, 143.

    Article  PubMed  PubMed Central  Google Scholar 

  • Lin, G., Zhou, Y., Li, M., and Fang, Y. (2018). Histone 3 lysine 36 to methionine mutations stably interact with and sequester SDG8 in Arabidopsis thaliana. Sci China Life Sci 61, 225–234.

    Article  CAS  PubMed  Google Scholar 

  • Liu, C., Li, L.C., Chen, W.Q., Chen, X., Xu, Z.H., and Bai, S.N. (2013a). HDA18 affects cell fate in Arabidopsis root epidermis via histone acetylation at four kinase genes. Plant Cell 25, 257–269.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu, R., Li, X., Chen, W., and Du, J. (2018). Structure and mechanism of plant histone mark readers. Sci China Life Sci 61, 170–177.

    Article  CAS  PubMed  Google Scholar 

  • Liu, X., Chen, C.Y., Wang, K.C., Luo, M., Tai, R., Yuan, L., Zhao, M., Yang, S., Tian, G., Cui, Y., et al. (2013b). PHYTOCHROME INTERACTING FACTOR3 associates with the histone deacetylase HDA15 in repression of chlorophyll biosynthesis and photosynthesis in etiolated Arabidopsis seedlings. Plant Cell 25, 1258–1273.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu, X., Luo, M., and Wu, K. (2012a). Epigenetic interplay of histone modifications and DNA methylation mediated by HDA6. Plant Signal Behav 7, 633–635.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu, X., Yu, C.W., Duan, J., Luo, M., Wang, K., Tian, G., Cui, Y., and Wu, K. (2012b). HDA6 directly interacts with DNA methyltransferase MET1 and maintains transposable element silencing in Arabidopsis. Plant Physiol 158, 119–129.

    Article  CAS  PubMed  Google Scholar 

  • Long, J.A., Ohno, C., Smith, Z.R., and Meyerowitz, E.M. (2006). TOPLESS regulates apical embryonic fate in Arabidopsis. Science 312, 1520–1523.

    Article  CAS  PubMed  Google Scholar 

  • Lu, L., Chen, X., Sanders, D., Qian, S., and Zhong, X. (2015). High-resolution mapping of H4K16 and H3K23 acetylation reveals conserved and unique distribution patterns in Arabidopsis and rice. Epigenetics 10, 1044–1053.

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 Å resolution. Nature 389, 251–260.

    Article  CAS  PubMed  Google Scholar 

  • Luo, M., Yu, C.W., Chen, F.F., Zhao, L., Tian, G., Liu, X., Cui, Y., Yang, J. Y., and Wu, K. (2012a). Histone deacetylase HDA6 is functionally associated with AS1 in repression of KNOX genes in Arabidopsis. PLoS Genet 8, e1003114.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Luo, M., Wang, Y.Y., Liu, X., Yang, S., Lu, Q., Cui, Y., and Wu, K. (2012b). HD2C interacts with HDA6 and is involved in ABA and salt stress response in Arabidopsis. J Exp Bot 63, 3297–3306.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Luo, M., Tai, R., Yu, C.W., Yang, S., Chen, C.Y., Lin, W.D., Schmidt, W., and Wu, K. (2015). Regulation of flowering time by the histone deacetylase HDA5 in Arabidopsis. Plant J 82, 925–936.

    Article  CAS  PubMed  Google Scholar 

  • Lusser, A., Brosch, G., Loidl, A., Haas, H., and Loidl, P. (1997). Identification of maize histone deacetylase HD2 as an acidic nucleolar phosphoprotein. Science 277, 88–91.

    Article  CAS  PubMed  Google Scholar 

  • Marks, P.A., Rifkind, R.A., Richon, V.M., Breslow, R., Miller, T., and Kelly, W.K. (2001). Histone deacetylases and cancer: causes and therapies. Nat Rev Cancer 1, 194–202.

    Article  CAS  PubMed  Google Scholar 

  • Marmorstein, R., and Zhou, M.M. (2014). Writers and readers of histone acetylation: structure, mechanism, and inhibition. Cold Spring Harb Perspect Biol 6, a018762.

    Article  PubMed  PubMed Central  Google Scholar 

  • Mayer, K.S., Chen, X., Sanders, D., Chen, J., Jiang, J., Nguyen, P., Scalf, M., Smith, L.M., and Zhong, X. (2019). HDA9-PWR-HOS15 is a core histone deacetylase complex regulating transcription and development. Plant Physiol 180, 342–355.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mehdi, S., Derkacheva, M., Ramström, M., Kralemann, L., Bergquist, J., and Hennig, L. (2016). The WD40 domain protein MSI1 functions in a histone deacetylase complex to fine-tune abscisic acid signaling. Plant Cell 28, 42–54.

    Article  CAS  PubMed  Google Scholar 

  • Murfett, J., Wang, X.J., Hagen, G., and Guilfoyle, T.J. (2001). Identification of Arabidopsis histone deacetylase HDA6 mutants that affect transgene expression. Plant Cell 13, 1047–1061.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ning, Y.Q., Chen, Q., Lin, R.N., Li, Y.Q., Li, L., Chen, S., and He, X.J. (2019). The HDA 19 histone deacetylase complex is involved in the regulation of flowering time in a photoperiod-dependent manner. Plant J 98, 448–464.

    Article  CAS  PubMed  Google Scholar 

  • Niu, D., Lin, X.L., Kong, X., Qu, G.P., Cai, B., Lee, J., and Jin, J.B. (2019). SIZ1-mediated SUMOylation of TPR1 suppresses plant immunity in Arabidopsis. Mol Plant 12, 215–228.

    Article  CAS  PubMed  Google Scholar 

  • Park, H.J., Baek, D., Cha, J.Y., Liao, X., Kang, S.H., McClung, C.R., Lee, S.Y., Yun, D.J., and Kim, W.Y. (2019). HOS15 interacts with the histone deacetylase HDA9 and the evening complex to epigenetically regulate the floral activator GIGANTEA. Plant Cell 31, 37–51.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Park, J., Chen, Y., Tishkoff, D.X., Peng, C., Tan, M., Dai, L., Xie, Z., Zhang, Y., Zwaans, B.M.M., Skinner, M.E., et al. (2013). SIRT5-mediated lysine desuccinylation impacts diverse metabolic pathways. Mol Cell 50, 919–930.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Park, J., Lim, C.J., Shen, M., Park, H.J., Cha, J.Y., Iniesto, E., Rubio, V., Mengiste, T., Zhu, J.K., Bressan, R.A., et al. (2018). Epigenetic switch from repressive to permissive chromatin in response to cold stress. Proc Natl Acad Sci USA 115, E5400–E5409.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Perrella, G., Lopez-Vernaza, M.A., Carr, C., Sani, E., Gosselé, V., Verduyn, C., Kellermeier, F., Hannah, M.A., and Amtmann, A. (2013). Histone deacetylase Complex1 expression level titrates plant growth and abscisic acid sensitivity in Arabidopsis. Plant Cell 25, 3491–3505.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pikaard, C.S. (2000). The epigenetics of nucleolar dominance. Trends Genet 16, 495–500.

    Article  CAS  PubMed  Google Scholar 

  • Pontes, O., Lawrence, R.J., Silva, M., Preuss, S., Costa-Nunes, P., Earley, K., Neves, N., Viegas, W., and Pikaard, C.S. (2007). Postembryonic establishment of megabase-scale gene silencing in nucleolar dominance. PLoS ONE 2, e1157.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Probst, A.V., Fagard, M., Proux, F., Mourrain, P., Boutet, S., Earley, K., Lawrence, R.J., Pikaard, C.S., Murfett, J., Furner, I., et al. (2004). Arabidopsis histone deacetylase HDA6 is required for maintenance of transcriptional gene silencing and determines nuclear organization of rDNA repeats. Plant Cell 16, 1021–1034.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Qian, S., Lv, X., Scheid, R.N., Lu, L., Yang, Z., Chen, W., Liu, R., Boersma, M.D., Denu, J.M., Zhong, X., et al. (2018). Dual recognition of H3K4me3 and H3K27me3 by a plant histone reader SHL. Nat Commun 9, 2425.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ryu, H., Cho, H., Bae, W., and Hwang, I. (2014). Control of early seedling development by BES1/TPL/HDA19-mediated epigenetic regulation of ABI3. Nat Commun 5, 4138.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Seto, E., and Yoshida, M. (2014). Erasers of histone acetylation: the histone deacetylase enzymes. Cold Spring Harb Perspect Biol 6, a018713.

    Article  PubMed  PubMed Central  Google Scholar 

  • Shen, Y., Lei, T., Cui, X., Liu, X., Zhou, S., Zheng, Y., Guérard, F., Issakidis-Bourguet, E., and Zhou, D.X. (2019). Arabidopsis histone deacetylase HDA 15 directly represses plant response to elevated ambient temperature. Plant J 100, 991–1006.

    Article  CAS  PubMed  Google Scholar 

  • Song, Y., Wu, K., Dhaubhadel, S., An, L., and Tian, L. (2010). Arabidopsis DNA methyltransferase AtDNMT2 associates with histone deacetylase AtHD2s activity. Biochem Biophys Res Commun 396, 187–192.

    Article  CAS  PubMed  Google Scholar 

  • Suzuki, M., Shinozuka, N., Hirakata, T., Nakata, M.T., Demura, T., Tsukaya, H., and Horiguchi, G. (2018). OLIGOCELLULA1/HIGH EXPRESSION OF OSMOTICALLY RESPONSIVE GENES15 promotes cell proliferation with HISTONE DEACETYLASE9 and POWERDRESS during leaf development in Arabidopsis thaliana. Front Plant Sci 9, 580.

    Article  PubMed  PubMed Central  Google Scholar 

  • Tanaka, M., Kikuchi, A., and Kamada, H. (2008). The Arabidopsis histone deacetylases HDA6 and HDA19 contribute to the repression of embryonic properties after germination. Plant Physiol 146, 149–161.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tang, Y., Liu, X., Liu, X., Li, Y., Wu, K., and Hou, X. (2017). Arabidopsis NF-YCs mediate the light-controlled hypocotyl elongation via modulating histone acetylation. Mol Plant 10, 260–273.

    Article  CAS  PubMed  Google Scholar 

  • Tasset, C., Singh Yadav, A., Sureshkumar, S., Singh, R., van der Woude, L., Nekrasov, M., Tremethick, D., van Zanten, M., and Balasubramanian, S. (2018). POWERDRESS-mediated histone deacetylation is essential for thermomorphogenesis in Arabidopsis thaliana. PLoS Genet 14, e1007280.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Taunton, J., Hassig, C.A., and Schreiber, S.L. (1996). A mammalian histone deacetylase related to the yeast transcriptional regulator Rpd3p. Science 272, 408–411.

    Article  CAS  PubMed  Google Scholar 

  • To, T.K., Kim, J.M., Matsui, A., Kurihara, Y., Morosawa, T., Ishida, J., Tanaka, M., Endo, T., Kakutani, T., Toyoda, T., et al. (2011). Arabidopsis HDA6 regulates locus-directed heterochromatin silencing in cooperation with MET1. PLoS Genet 7, e1002055.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tran, H.T., Nimick, M., Uhrig, R.G., Templeton, G., Morrice, N., Gourlay, R., DeLong, A., and Moorhead, G.B.G. (2012). Arabidopsis thaliana histone deacetylase 14 (HDA14) is an α-tubulin deacetylase that associates with PP2A and enriches in the microtubule fraction with the putative histone acetyltransferase ELP3. Plant J 71, 263–272.

    Article  CAS  PubMed  Google Scholar 

  • Unnikrishnan, A., Gafken, P.R., and Tsukiyama, T. (2010). Dynamic changes in histone acetylation regulate origins of DNA replication. Nat Struct Mol Biol 17, 430–437.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • van Zanten, M., Zöll, C., Wang, Z., Philipp, C., Carles, A., Li, Y., Kornet, N.G., Liu, Y., and Soppe, W.J.J. (2014). HISTONE DEACETYLASE 9 represses seedling traits in Arabidopsis thaliana dry seeds. Plant J 80, 475–488.

    Article  CAS  PubMed  Google Scholar 

  • Verdin, E., and Ott, M. (2015). 50 years of protein acetylation: from gene regulation to epigenetics, metabolism and beyond. Nat Rev Mol Cell Biol 16, 258–264.

    Article  CAS  PubMed  Google Scholar 

  • Vidal, M., and Gaber, R.F. (1991). RPD3 encodes a second factor required to achieve maximum positive and negative transcriptional states in Saccharomyces cerevisiae. Mol Cell Biol 11, 6317–6327.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wang, A., Kurdistani, S.K., and Grunstein, M. (2002). Requirement of Hos2 histone deacetylase for gene activity in yeast. Science 298, 1412–1414.

    Article  CAS  PubMed  Google Scholar 

  • Wang, B.B., and Brendel, V. (2004). The ASRG database: identification and survey of Arabidopsis thaliana genes involved in pre-mRNA splicing. Genome Biol 5, R102.

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang, C., Gao, F., Wu, J., Dai, J., Wei, C., and Li, Y. (2010). Arabidopsis putative deacetylase AtSRT2 regulates basal defense by suppressing PAD4, EDS5 and SID2 expression. Plant Cell Physiol 51, 1291–1299.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang, C., Zhu, B., and Xiong, J. (2018). Recruitment and reinforcement: maintaining epigenetic silencing. Sci China Life Sci 61, 515–522.

    Article  PubMed  CAS  Google Scholar 

  • Wang, Z., Cao, H., Sun, Y., Li, X., Chen, F., Carles, A., Li, Y., Ding, M., Zhang, C., Deng, X., et al. (2013). Arabidopsis paired amphipathic helix proteins SNL1 and SNL2 redundantly regulate primary seed dormancy via abscisic acid-ethylene antagonism mediated by histone deacetylation. Plant Cell 25, 149–166.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang, Z., Zang, C., Cui, K., Schones, D.E., Barski, A., Peng, W., and Zhao, K. (2009). Genome-wide mapping of HATs and HDACs reveals distinct functions in active and inactive genes. Cell 138, 1019–1031.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu, K., Malik, K., Tian, L., Brown, D., and Miki, B. (2000). Functional analysis of a RPD3 histone deacetylase homologue in Arabidopsis thaliana. Plant Mol Biol 44, 167–176.

    Article  CAS  PubMed  Google Scholar 

  • Yang, H., Liu, X., Xin, M., Du, J., Hu, Z., Peng, H.R., Rossi, V., Sun, Q., Ni, Z., and Yao, Y. (2016). Genome-wide mapping of targets of maize histone deacetylase HDA101 reveals its function and regulatory mechanism during seed development. Plant Cell 28, 629–645.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang, X.J., and Seto, E. (2003). Collaborative spirit of histone deacetylases in regulating chromatin structure and gene expression. Curr Opin Genet Dev 13, 143–153.

    Article  CAS  PubMed  Google Scholar 

  • Yang, Z., Qian, S., Scheid, R.N., Lu, L., Chen, X., Liu, R., Du, X., Lv, X., Boersma, M.D., Scalf, M., et al. (2018). EBS is a bivalent histone reader that regulates floral phase transition in Arabidopsis. Nat Genet 50, 1247–1253.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yu, C.W., Liu, X., Luo, M., Chen, C., Lin, X., Tian, G., Lu, Q., Cui, Y., and Wu, K. (2011). HISTONE DEACETYLASE6 interacts with FLOWERING LOCUS D and regulates flowering in Arabidopsis. Plant Physiol 156, 173–184.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yu, C.W., Tai, R., Wang, S.C., Yang, P., Luo, M., Yang, S., Cheng, K., Wang, W.C., Cheng, Y.S., and Wu, K. (2017). HISTONE DEACETYLASE6 acts in concert with histone methyltransferases SUVH4, SUVH5, and SUVH6 to regulate transposon silencing. Plant Cell 29, 1970–1983.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yuan, L., Chen, X., Chen, H., Wu, K., and Huang, S. (2019). Histone deacetylases HDA6 and HDA9 coordinately regulate valve cell elongation through affecting auxin signaling in Arabidopsis. Biochem Biophys Res Commun 508, 695–700.

    Article  CAS  PubMed  Google Scholar 

  • Yumul, R.E., Kim, Y.J., Liu, X., Wang, R., Ding, J., Xiao, L., and Chen, X. (2013). POWERDRESS and diversified expression of the MIR172 gene family bolster the floral stem cell network. PLoS Genet 9, e1003218.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yun, J., Kim, Y.S., Jung, J.H., Seo, P.J., and Park, C.M. (2012). The AT-hook motif-containing protein AHL22 regulates flowering initiation by modifying FLOWERING LOCUS T chromatin in Arabidopsis. J Biol Chem 287, 15307–15316.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zentner, G.E., and Henikoff, S. (2013). Regulation of nucleosome dynamics by histone modifications. Nat Struct Mol Biol 20, 259–266.

    Article  CAS  PubMed  Google Scholar 

  • Zhang, F., Wang, L., Ko, E.E., Shao, K., and Qiao, H. (2018). Histone deacetylases SRT1 and SRT2 interact with ENAP1 to mediate ethylene-induced transcriptional repression. Plant Cell 30, 153–166.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang, H., Zhao, Y., and Zhou, D.X. (2017). Rice NAD+-dependent histone deacetylase OsSRT1 represses glycolysis and regulates the moonlighting function of GAPDH as a transcriptional activator of glycolytic genes. Nucleic Acids Res 45, 12241–12255.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao, L., Peng, T., Chen, C.Y., Ji, R., Gu, D., Li, T., Zhang, D., Tu, Y.T., Wu, K., and Liu, X. (2019). HY5 interacts with the histone deacetylase HDA15 to repress hypocotyl cell elongation in photomorphogenesis. Plant Physiol 180, 1450–1466.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zheng, Y., Ding, Y., Sun, X., Xie, S., Wang, D., Liu, X., Su, L., Wei, W., Pan, L., and Zhou, D.X. (2016). Histone deacetylase HDA9 negatively regulates salt and drought stress responsiveness in Arabidopsis. J Exp Bot 67, 1703–1713.

    Article  CAS  PubMed  Google Scholar 

  • Zhong, X. (2016). Comparative epigenomics: a powerful tool to understand the evolution of DNA methylation. New Phytol 210, 76–80.

    Article  CAS  PubMed  Google Scholar 

  • Zhong, X., Zhang, H., Zhao, Y., Sun, Q., Hu, Y., Peng, H., and Zhou, D.X. (2013). The rice NAD+-dependent histone deacetylase OsSRT1 targets preferentially to stress- and metabolism-related genes and transposable elements. PLoS ONE 8, e66807.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou, R., Shang, R., Gong, D., Xu, X., and Liu, S. (2019). Characterization of H3 methylation in regulating oocyte development in cyprinid fish. Sci China Life Sci 62, 829–837.

    Article  CAS  PubMed  Google Scholar 

  • Zhou, Y., Tan, B., Luo, M., Li, Y., Liu, C., Chen, C., Yu, C.W., Yang, S., Dong, S., Ruan, J., et al. (2013). HISTONE DEACETYLASE19 interacts with HSL1 and participates in the repression of seed maturation genes in Arabidopsis seedlings. Plant Cell 25, 134–148.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu, G., Chang, Y., Xu, X., Tang, K., Chen, C., Lei, M., Zhu, J.K., and Duan, C.G. (2019). EXPORTIN 1A prevents transgene silencing in Arabidopsis by modulating nucleo-cytoplasmic partitioning of HDA6. J Integr Plant Biol jipb.12787.

  • Zhu, J., Jeong, J.C., Zhu, Y., Sokolchik, I., Miyazaki, S., Zhu, J.K., Hasegawa, P.M., Bohnert, H.J., Shi, H., Yun, D.J., et al. (2008). Involvement of Arabidopsis HOS15 in histone deacetylation and cold tolerance. Proc Natl Acad Sci USA 105, 4945–4950.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. State Key Laboratory of Hybrid Rice, College of Life Sciences, Wuhan University, Wuhan, 430072, China

    Xiangsong Chen

  2. Laboratory of Genetics & Wisconsin Institute for Discovery, University of Wisconsin-Madison, Madison, Wisconsin, 53706, USA

    Adeline B. Ding & Xuehua Zhong

Authors
  1. Xiangsong Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Adeline B. Ding
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Xuehua Zhong
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Xiangsong Chen or Xuehua Zhong.

Ethics declarations

The author(s) declare that they have no conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Chen, X., Ding, A.B. & Zhong, X. Functions and mechanisms of plant histone deacetylases. Sci. China Life Sci. 63, 206–216 (2020). https://doi.org/10.1007/s11427-019-1587-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11427-019-1587-x

Keywords

Search

Navigation