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Volume 48 Issue 5
May  2021
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Article Contents

Arabidopsis RPD3-like histone deacetylases form multiple complexes involved in stress response

doi: 10.1016/j.jgg.2021.04.004
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This work was supported by the National Natural Science Foundation of China (32025003) and by the National Key Research and Development Program of China (2016YFA0500801) from the Chinese Ministry of Science and Technology.

  • Received Date: 2021-02-20
  • Revised Date: 2021-03-31
  • Accepted Date: 2021-04-15
  • Publish Date: 2021-05-20
  • The Arabidopsis thaliana RPD3-type histone deacetylases have been known to form conserved SIN3-type histone deacetylase complexes, but whether they form other types of complexes is unknown. Here, we perform affinity purification followed by mass spectrometry and demonstrate that the Arabidopsis RPD3-type histone deacetylases HDA6 and HDA19 interact with several previously uncharacterized proteins, thereby forming three types of plant-specific histone deacetylase complexes, which we named SANT, ESANT, and ARID. RNA-seq indicates that the newly identified components function together with HDA6 and HDA19 and coregulate the expression of a number of genes. HDA6 and HDA19 were previously thought to repress gene transcription by histone deacetylation. We find that the histone deacetylase complexes can repress gene expression via both histone deacetylation-dependent and -independent mechanisms. In the mutants of histone deacetylase complexes, the expression of a number of stress-induced genes is up-regulated, and several mutants of the histone deacetylase complexes show severe retardation in growth. Considering that growth retardation is thought to be a trade-off for an increase in stress tolerance, we infer that the histone deacetylase complexes identified in this study prevent over-expression of stress-induced genes and thereby ensure normal growth of plants under nonstress conditions.
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  • Aceituno, F.F., Moseyko, N., Rhee, S.Y., Gutierrez, R.A., 2008. The rules of gene expression in plants:organ identity and gene body methylation are key factors for regulation of gene expression in Arabidopsis thaliana. BMC Genom. 9, 438.
    Ahringer, J., 2000. NuRD and SIN3:histone deacetylase complexes in development. Trends Genet. 16, 351-356.
    Aichinger, E., Villar, C.B., Di Mambro, R., Sabatini, S., Köhler, C., 2011. The CHD3 chromatin remodeler PICKLE and polycomb group proteins antagonistically regulate meristem activity in the Arabidopsis root. Plant Cell 23, 1047-1060.
    Alexandre, C., Möller-Steinbach, Y., Schönrock, N., Gruissem, W., Hennig, L., 2009. Arabidopsis MSI1 is required for negative regulation of the response to drought stress. Mol. Plant 2, 675-687.
    Allfrey, V.G., Faulkner, R., Mirsky, A., 1964. Acetylation and methylation of histones and their possible role in the regulation of RNA synthesis. Proc. Natl. Acad. Sci. U.S. A. 51, 786.
    Aufsatz, W., Stoiber, T., Rakic, B., Naumann, K., 2007. Arabidopsis histone deacetylase 6:a green link to RNA silencing. Oncogene 26, 5477-5488.
    Aufsatz, W., Mette, M.F., Winden, J.v.d., Matzke, M., Matzke, A.J.M., 2002. HDA6, a putative histone deacetylase needed to enhance DNA methylation induced by double-stranded RNA. EMBO J. 21, 6832-6841.
    Balciunaite, E., Spektor, A., Lents, N.H., Cam, H., te Riele, H., Scime, A., Rudnicki, M.A., Young, R., Dynlacht, B.D., 2005. Pocket protein complexes are recruited to distinct targets in quiescent and proliferating cells. Mol. Cell Biol. 25, 8166-8178.
    Barber, B.A., Rastegar, M., 2010. Epigenetic control of Hox genes during neurogenesis, development, and disease. Ann. Anat. 192, 261-274.
    Boyer, L.A., Latek, R.R., Peterson, C.L., 2004. The SANT domain:a unique histonetail-binding module? Nat. Rev. Mol. Cell Biol. 5, 158-163.
    Brownell, J.E., Zhou, J., Ranalli, T., Kobayashi, R., Edmondson, D.G., Roth, S.Y., Allis, C.D., 1996. Tetrahymena histone acetyltransferase A:a homolog to yeast Gcn5p linking histone acetylation to gene activation. Cell 84, 843-851.
    Choudhary, C., Kumar, C., Gnad, F., Nielsen, M.L., Rehman, M., Walther, T.C., Olsen, J.V., Mann, M., 2009. Lysine acetylation targets protein complexes and co-regulates major cellular functions. Science 325, 834-840.
    Clough, S.J., Bent, A.F., 1998. Floral dip:a simplified method for Agrobacteriummediated transformation of Arabidopsis thaliana. Plant J. 16, 735-743.
    Denslow, S., Wade, P., 2007. The human Mi-2/NuRD complex and gene regulation. Oncogene 26, 5433-5438.
    Derkacheva, M., Steinbach, Y., Wildhaber, T., Mozgova, I., Mahrez, W., Nanni, P., Bischof, S., Gruissem, W., Hennig, L., 2013. Arabidopsis MSI1 connects LHP1 to PRC2 complexes. EMBO J. 32, 2073-2085.
    Earley, K., Lawrence, R.J., Pontes, O., Reuther, R., Enciso, A.J., Silva, M., Neves, N., Gross, M., Viegas, W., Pikaard, C.S., 2006. Erasure of histone acetylation by Arabidopsis HDA6 mediates large-scale gene silencing in nucleolar dominance. Genes Dev. 20, 1283-1293.
    Fleischer, T.C., Yun, U.J., Ayer, D.E., 2003. Identification and characterization of three new components of the mSin3A corepressor complex. Mol. Cell Biol. 23, 3456-3467.
    Fukaki, H., Taniguchi, N., Tasaka, M., 2006. PICKLE is required for SOLITARY-ROOT/IAA14-mediated repression of ARF7 and ARF19 activity during Arabidopsis lateral root initiation. Plant J. 48, 380-389.
    Glozak, M.A., Sengupta, N., Zhang, X., Seto, E., 2005. Acetylation and deacetylation of non-histone proteins. Gene 363, 15-23.
    Gregoretti, I., Lee, Y.-M., Goodson, H.V., 2004. Molecular evolution of the histone deacetylase family:functional implications of phylogenetic analysis. J. Mol. Biol. 338, 17-31.
    Grozinger, C.M., Schreiber, S.L., 2002. Deacetylase enzymes-biological functions and the use of small-molecule inhibitors. Chem. Biol. 9, 3-16.
    Gu, X., Jiang, D., Yang, W., Jacob, Y., Michaels, S.D., He, Y., 2011. Arabidopsis homologs of retinoblastoma-associated protein 46/48 associate with a histone deacetylase to act redundantly in chromatin silencing. PLoS Genet. 7, e1002366.
    Haigis, M.C., Guarente, L.P., 2006. Mammalian sirtuinsd-merging roles in physiology, aging, and calorie restriction. Genes Dev. 20, 2913-2921.
    Hayakawa, T., Nakayama, J.-i., 2011. Physiological roles of class I HDAC complex and histone demethylase. J. Biomed. Biotechnol. 2011, 129383.
    Hendrich, B., Bird, A., 1998. Identification and characterization of a family of mammalian methyl CpG-binding proteins. Genet. Res. 72, 59-72.
    Hendrich, B., Tweedie, S., 2003. The methyl-CpG binding domain and the evolving role of DNA methylation in animals. Trends Genet. 19, 269-277.
    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.
    Hennig, L., Taranto, P., Walser, M., Schönrock, N., Gruissem, W., 2003. Arabidopsis MSI1 is required for epigenetic maintenance of reproductive development. Development 130, 2555-2565.
    Hollender, C., Liu, Z., 2008. Histone deacetylase genes in Arabidopsis development. J. Integr. Plant Biol. 50, 875-885.
    Huang, F., Yuan, W.Y., Tian, S., Zheng, Q.J., He, Y., 2019. SIN3 LIKE genes mediate long-day induction of flowering but inhibit the floral transition in short days through histone deacetylation in Arabidopsis. Plant J. 100, 101-113.
    Hubbert, C., Guardiola, A., Shao, R., Kawaguchi, Y., Ito, A., Nixon, A., Yoshida, M., Wang, X.-F., Yao, T.-P., 2002. HDAC6 is a microtubule-associated deacetylase. Nature 417, 455-458.
    Hung, F.Y., Chen, F.F., Li, C., Chen, C., Chen, J.H., Cui, Y., 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.
    Hung, F.Y., Chen, F.F., Li, C., Chen, C., Lai, Y.C., Chen, J.H., Cui, Y., 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. 46, 10669-10681.
    Itoh, T., Fairall, L., Muskett, F.W., Milano, C.P., Watson, P.J., Arnaudo, N., Saleh, A., Millard, C.J., El-Mezgueldi, M., Martino, F., 2015. Structural and functional characterization of a cell cycle associated HDAC1/2 complex reveals the structural basis for complex assembly and nucleosome targeting. Nucleic Acids Res. 43, 2033-2044.
    Iwahara, J., Clubb, R.T., 1999. Solution structure of the DNA binding domain from Dead ringer, a sequence-specific AT-rich interaction domain (ARID). EMBO J. 18, 6084-6094.
    Iwahara, J., Iwahara, M., Daughdrill, G.W., Ford, J., Clubb, R.T., 2002. The structure of the Dead ringereDNA complex reveals how AT-rich interaction domains(ARIDs) recognize DNA. EMBO J. 21, 1197-1209.
    Jing, Y., Zhang, D., Wang, X., Tang, W., Wang, W., Huai, J., Xu, G., Chen, D., Li, Y., Lin, R., 2013. Arabidopsis chromatin remodeling factor PICKLE interacts with transcription factor HY5 to regulate hypocotyl cell elongation. Plant Cell 25, 242-256.
    Karasov, T.L., Chae, E., Herman, J.J., Bergelson, J., 2017. Mechanisms to mitigate the trade-off between growth and defense. Plant Cell 29, 666-680.
    Kasten, M.M., Dorland, S., Stillman, D.J., 1997. A large protein complex containing the yeast Sin3p and Rpd3p transcriptional regulators. Mol. Cell Biol. 17, 4852-4858.
    Kaya, H., Shibahara, K.-i., Taoka, K.-i., Iwabuchi, M., Stillman, B., Araki, T., 2001. FASCIATA genes for chromatin assembly factor-1 in Arabidopsis maintain the cellular organization of apical meristems. Cell 104, 131-142.
    Kilian, J., Whitehead, D., Horak, J., Wanke, D., Weinl, S., Batistic, O., D'Angelo, C., Bornberg-Bauer, E., Kudla, J., Harter, K., 2007. The AtGenExpress global stress expression data set:protocols, evaluation and model data analysis of UV-B light, drought and cold stress responses. Plant J. 50, 347-363.
    Kim, D., Paggi, J.M., Park, C., Bennett, C., Salzberg, S.L., 2019. Graph-based genome alignment and genotyping with HISAT2 and HISAT-genotype. Nat. Biotechnol. 37, 907-915.
    Kim, J.M., To, T.K., Matsui, A., Tanoi, K., Kobayashi, N.I., Matsuda, F., Habu, Y., Ogawa, D., Sakamoto, T., Matsunaga, S., et al., 2017. Acetate-mediated novel survival strategy against drought in plants. Nat. Plants 3, 17097.
    Kim, Y.J., Wang, R.Z., Gao, L., Li, D.M., Xu, C., Mang, H., Jeon, J., Chen, X.S., Zhong, X.H., 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. U. S. A. 113, 14858-14863.
    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.
    Krueger, F., Andrews, S.R., 2011. Bismark:a flexible aligner and methylation caller for Bisulfite-Seq applications. Bioinformatics 27, 1571-1572.
    Kurita, K., Sakamoto, Y., Naruse, S., Matsunaga, T.M., Arata, H., Higashiyama, T., Habu, Y., Utsumi, Y., Utsumi, C., Tanaka, M., et al., 2019. Intracellular localization of histone deacetylase HDA6 in plants. J. Plant Res. 132, 629-640.
    Kuzmichev, A., Zhang, Y., Erdjument-Bromage, H., Tempst, P., Reinberg, D., 2002. Role of the Sin3-histone deacetylase complex in growth regulation by the candidate tumor suppressor p33(ING1). Mol. Cell Biol. 22, 835-848.
    Lai, A., Kennedy, B.K., Barbie, D.A., Bertos, N.R., Yang, X.J., Theberge, M.-C., Tsai, S.-C., Seto, E., Zhang, Y., Kuzmichev, A., 2001. RBP1 recruits the mSIN3-histone deacetylase complex to the pocket of retinoblastoma tumor suppressor family proteins found in limited discrete regions of the nucleus at growth arrest. Mol. Cell Biol. 21, 2918-2932.
    Langmead, B., Salzberg, S.L., 2012. Fast gapped-read alignment with Bowtie 2. Nat. Methods 9, 357.
    Lee, J.R., Lee, S.S., Jang, H.H., Lee, Y.M., Park, J.H., Park, S.-C., Moon, J.C., Park, S.K., Kim, S.Y., Lee, S.Y., 2009. Heat-shock dependent oligomeric status alters the function of a plant-specific thioredoxin-like protein, AtTDX. Proc. Natl. Acad. Sci. U. S. A. 106, 5978-5983.
    Liao, Y., Smyth, G.K., Shi, W., 2014. featureCounts:an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics 30, 923-930.
    Lin, J., Hung, F.-Y., Ye, C., Hong, L., Shih, Y.-H., Wu, K., Li, Q.Q., 2020. HDA6-dependent histone deacetylation regulates mRNA polyadenylation in Arabidopsis. Genome Res. 30, 1407-1417.
    Lin, Y.-y., Lu, J.-y., Zhang, J., Walter, W., Dang, W., Wan, J., Tao, S.-C., Qian, J., Zhao, Y., Boeke, J.D., 2009. Protein acetylation microarray reveals that NuA4 controls key metabolic target regulating gluconeogenesis. Cell 136, 1073-1084.
    Liu, Q., Kasuga, M., Sakuma, Y., Abe, H., Miura, S., Yamaguchi-Shinozaki, K., Shinozaki, K., 1998. Two transcription factors, DREB1 and DREB2, with an EREBP/AP2 DNA binding domain separate two cellular signal transduction pathways in drought-and low-temperature-responsive gene expression, respectively, in Arabidopsis. Plant Cell 10, 1391-1406.
    Liu, X., Yu, C.-W., Duan, J., Luo, M., Wang, K., Tian, G., Cui, Y., Wu, K., 2012. HDA6 directly interacts with DNA methyltransferase MET1 and maintains transposable element silencing in Arabidopsis. Plant Physiol. 158, 119-129.
    Luo, J., Su, F., Chen, D., Shiloh, A., Gu, W., 2000. Deacetylation of p53 modulates its effect on cell growth and apoptosis. Nature 408, 377-381.
    Luo, M., Wang, Y.-Y., Liu, X., Yang, S., Lu, Q., Cui, Y., Wu, K., 2012a. HD2C interacts with HDA6 and is involved in ABA and salt stress response in Arabidopsis. J. Exp. Bot. 63, 3297-3306.
    Luo, M., Yu, C.W., Chen, F.F., Zhao, L., Tian, G., Liu, X., Cui, Y., Yang, J.Y., Wu, K., 2012b. Histone deacetylase HDA6 is functionally associated with AS1 in repression of KNOX genes in Arabidopsis. PLoS Genet. 8, e1003114.
    Lusser, A., Brosch, G., Loidl, A., Haas, H., Loidl, P., 1997. Identification of maize histone deacetylase HD2 as an acidic nucleolar phosphoprotein. Science 277, 88-91.
    Mayer, K.S., Chen, X.S., Sanders, D., Chen, J.N., Jiang, J.J., Nguyen, P., Scalf, M., Smith, L.M., Zhong, X.H., 2019. HDA9-PWR-HOS15 is a ccore histone deacetylase complex regulating transcription and development. Plant Physiol. 180, 342-355.
    Mehdi, S., Derkacheva, M., Ramstrom, M., Kralemann, L., Bergquist, J., 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.
    Murfett, J., Wang, X.-J., Hagen, G., Guilfoyle, T.J., 2001. Identification of Arabidopsis histone deacetylase HDA6 mutants that affect transgene expression. Plant Cell 13, 1047-1061.
    Nakashima, K., Ito, Y., Yamaguchi-Shinozaki, K., 2009. Transcriptional regulatory networks in response to abiotic stresses in Arabidopsis and grasses. Plant Physiol. 149, 88-95.
    New, M., Olzscha, H., La Thangue, N.B., 2012. HDAC inhibitor-based therapies:can we interpret the code? Mol. Oncol. 6, 637-656.
    Ning, Y.Q., Chen, Q., Lin, R.N., Li, Y.Q., Li, L., Chen, S., He, X.J., 2019. The HDA19 histone deacetylase complex is involved in the regulation of flowering time in a photoperiod-dependent manner. Plant J. 98, 448-464.
    Ogas, J., Cheng, J.-C., Sung, Z.R., Somerville, C., 1997. Cellular differentiation regulated by gibberellin in the Arabidopsis thaliana pickle mutant. Science 277, 91-94.
    Park, H.J., Baek, D., Cha, J.Y., Liao, X.J., Kang, S.H., McClung, C.R., Lee, S.Y., Yun, D.J., 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.
    Perrella, G., Lopez-Vernaza, M.A., Carr, C., Sani, E., Gosselé, V., Verduyn, C., Kellermeier, F., Hannah, M.A., Amtmann, A., 2013. Histone deacetylase complex1 expression level titrates plant growth and abscisic acid sensitivity in Arabidopsis. Plant Cell 25, 3491-3505.
    Pontvianne, F., Blevins, T., Chandrasekhara, C., Mozgová, I., Hassel, C., Pontes, O.M., Tucker, S., Mokroš, P., Muchová, V., Fajkus, J., 2013. Subnuclear partitioning of rRNA genes between the nucleolus and nucleoplasm reflects alternative epiallelic states. Genes Dev. 27, 1545-1550.
    Ramírez, F., Ryan, D.P., Grüning, B., Bhardwaj, V., Kilpert, F., Richter, A.S., Heyne, S., Dündar, F., Manke, T., 2016. deepTools2:a next generation web server for deepsequencing data analysis. Nucleic Acids Res. 44, W160-W165.
    Rayman, J.B., Takahashi, Y., Indjeian, V.B., Dannenberg, J.-H., Catchpole, S., Watson, R.J., te Riele, H., Dynlacht, B.D., 2002. E2F mediates cell cycledependent transcriptional repression in vivo by recruitment of an HDAC1/mSin3B corepressor complex. Genes Dev. 16, 933-947.
    Robinson, M.D., McCarthy, D.J., Smyth, G.K., 2010. edgeR:a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26, 139-140.
    Rundlett, S.E., Carmen, A.A., Kobayashi, R., Bavykin, S., Turner, B.M., Grunstein, M., 1996. HDA1 and RPD3 are members of distinct yeast histone deacetylase complexes that regulate silencing and transcription. Proc. Natl. Acad. Sci. U. S. A. 93, 14503-14508.
    Saito, M., Ishikawa, F., 2002. The mCpG-binding domain of human MBD3 does not bind to mCpG but interacts with NuRD/Mi2 components HDAC1 and MTA2. J. Biol. Chem. 277, 35434-35439.
    Sang, S., Chen, Y., Yang, Q., Wang, P., 2017. Arabidopsis inositol polyphosphate multikinase delays flowering time through mediating transcriptional activation of Flowering Locus C. J. Exp. Bot. 68, 5787-5800.
    Seto, E., Yoshida, M., 2014. Erasers of histone acetylation:the histone deacetylase enzymes. Cold Spring Harb. Perspect. Biol. 6, a018713.
    Silverstein, R.A., Ekwall, K., 2005. Sin3:a flexible regulator of global gene expression and genome stability. Curr. Genet. 47, 1-17.
    Skowyra, D., Zeremski, M., Neznanov, N., Li, M., Choi, Y., Uesugi, M., Hauser, C.A., Gu, W., Gudkov, A.V., Qin, J., 2001. Differential association of products of alternative transcripts of the candidate tumor suppressor ING1 with the mSin3/HDAC1 transcriptional corepressor complex. J. Biol. Chem. 276, 8734-8739.
    Strahl, B.D., Allis, C.D., 2000. The language of covalent histone modifications. Nature 403, 41-45.
    Stroud, H., Greenberg, M.V., Feng, S., Bernatavichute, Y.V., Jacobsen, S.E., 2013. Comprehensive analysis of silencing mutants reveals complex regulation of the Arabidopsis methylome. Cell 152, 352-364.
    Tan, L.M., Liu, R., Gu, B.W., Zhang, C.J., Luo, J., Guo, J., Wang, Y., Chen, L., Du, X., Li, S., 2020. Dual recognition of H3K4me3 and DNA by the ISWI component ARID5 regulates the floral transition in Arabidopsis. Plant Cell 32, 2178-2195.
    Tan, L.M., Zhang, C.J., Hou, X.M., Shao, C.R., Lu, Y.J., Zhou, J.X., Li, Y.Q., Li, L., Chen, S., He, X.J., 2018. The PEAT protein complexes are required for histone deacetylation and heterochromatin silencing. EMBO J. 37, e98770.
    Tanaka, M., Kikuchi, A., Kamada, H., 2008. The Arabidopsis histone deacetylases HDA6 and HDA19 contribute to the repression of embryonic properties after germination. Plant Physiol. 146, 149-161.
    Taunton, J., Hassig, C.A., Schreiber, S.L., 1996. A mammalian histone deacetylase related to the yeast transcriptional regulator Rpd3p. Science 272, 408-411.
    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.
    Ueda, M., Matsui, A., Tanaka, M., Nakamura, T., Abe, T., Sako, K., Sasaki, T., Kim, J.M., Ito, A., Nishino, N., et al., 2017. The distinct roles of class I and II RPD3-like histone deacetylases in ssalinity stress response. Plant Physiol. 175, 1760-1773.
    Wang, L., Rajan, H., Pitman, J.L., McKeown, M., Tsai, C.-C., 2006. Histone deacetylase-associating Atrophin proteins are nuclear receptor corepressors. Genes Dev. 20, 525-530.
    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.
    Wang, Z., Chen, F., Li, X., Cao, H., Ding, M., Zhang, C., Zuo, J., Xu, C., Xu, J., Deng, X., 2016. Arabidopsis seed germination speed is controlled by SNL histone deacetylase-binding factor-mediated regulation of AUX1. Nat. Commun. 7, 1-14.
    Wang, Z.-P., Xing, H.-L., Dong, L., Zhang, H.-Y., Han, C.-Y., Wang, X.-C., Chen, Q.-J., 2015. Egg cell-specific promoter-controlled CRISPR/Cas9 efficiently generates homozygous mutants for multiple target genes in Arabidopsis in a single generation. Genome Biol. 16, 144.
    Wu, K., Zhang, L., Zhou, C., Yu, C.W., Chaikam, V., 2008. HDA6 is required for jasmonate response, senescence and flowering in Arabidopsis. J. Exp. Bot. 59, 225-234.
    Wu, R.-C., Jiang, M., Beaudet, A.L., Wu, M.-Y., 2013. ARID4A and ARID4B regulate male fertility, a functional link to the AR and RB pathways. Proc. Natl. Acad. Sci. U. S. A. 110, 4616-4621.
    Xue, Y., Wong, J., Moreno, G.T., Young, M.K., Côté, J., Wang, W., 1998. NURD, a novel complex with both ATP-dependent chromatin-remodeling and histone deacetylase activities. Mol. Cell 2, 851-861.
    Yang, J., Yuan, L., Yen, M.R., Zheng, F., Ji, R., Peng, T., Gu, D., Yang, S., Cui, Y., Chen, P.Y., Wu, K., Liu, X., 2020. SWI3B and HDA6 interact and are required for transposon silencing in Arabidopsis. Plant J. 102, 809-822.
    Yang, R., Zheng, Z., Chen, Q., Yang, L., Huang, H., Miki, D., Wu, W., Zeng, L., Liu, J., Zhou, J.-X., 2017. The developmental regulator PKL is required to maintain correct DNA methylation patterns at RNA-directed DNA methylation loci. Genome Biol. 18, 1-18.
    Yang, X.J., Seto, E., 2008. The Rpd3/Hda1 family of lysine deacetylases:from bacteria and yeast to mice and men. Nat. Rev. Mol. Cell Biol. 9, 206-218.
    Yu, C.W., Liu, X., Luo, M., Chen, C., Lin, X., Tian, G., Lu, Q., Cui, Y., Wu, K., 2011. HISTONE DEACETYLASE6 interacts with FLOWERING LOCUS D and regulates flowering in Arabidopsis. Plant Physiol. 156, 173-184.
    Yu, C.W., Tai, R., Wang, S.C., Yang, P., Luo, M., Yang, S., Cheng, K., Wang, W.C., Cheng, Y.S., Wu, K., 2017. Histone deacetylase 6 acts in concert with histone methyltransferases SUVH4, SUVH5, and SUVH6 to regulate transposon silencing. Plant Cell 29, 1970-1983.
    Zang, C., Schones, D.E., Zeng, C., Cui, K., Zhao, K., Peng, W., 2009. A clustering approach for identification of enriched domains from histone modification ChIPSeq data. Bioinformatics 25, 1952-1958.
    Zemach, A., Grafi, G., 2003. Characterization of Arabidopsis thaliana methyl-CpGbinding domain (MBD) proteins. Plant J. 34, 565-572.
    Zhang, C.J., Ning, Y.Q., Zhang, S.W., Chen, Q., Shao, C.-R., Guo, Y.W., Zhou, J.X., Li, L., Chen, S., He, X.J., 2012. IDN2 and its paralogs form a complex required for RNA-directed DNA methylation. PLoS Genet. 8, e1002693.
    Zhang, D., Jing, Y., Jiang, Z., Lin, R., 2014. The chromatin-remodeling factor PICKLE integrates brassinosteroid and gibberellin signaling during skotomorphogenic growth in Arabidopsis. Plant Cell 26, 2472-2485.
    Zhang, T., Cooper, S., Brockdorff, N., 2015. The interplay of histone modificationsewriters that read. EMBO Rep. 16, 1467-1481.
    Zhang, X., Yazaki, J., Sundaresan, A., Cokus, S., Chan, S.W.-L., Chen, H., Henderson, I.R., Shinn, P., Pellegrini, M., Jacobsen, S.E., 2006. Genome-wide high-resolution mapping and functional analysis of DNA methylation in Arabidopsis. Cell 126, 1189-1201.
    Zheng, B., He, H., Zheng, Y., Wu, W., McCormick, S., 2014. An ARID domaincontaining protein within nuclear bodies is required for sperm cell formation in Arabidopsis thaliana. PLoS Genet. 10, e1004421.
    Zhong, X., Hale, C.J., Law, J.A., Johnson, L.M., Feng, S., Tu, A., Jacobsen, S.E., 2012. DDR complex facilitates global association of RNA polymerase V to promoters and evolutionarily young transposons. Nat. Struct. Mol. Biol. 19, 870.
    Zhou, Y., Tergemina, E., Cui, H., Förderer, A., Hartwig, B., James, G.V., Schneeberger, K., Turck, F., 2017. Ctf4-related protein recruits LHP1-PRC2 to maintain H3K27me3 levels in dividing cells in Arabidopsis thaliana. Proc. Natl. Acad. Sci. U. S. A. 114, 4833-4838.
    Zhou, Y., Wang, Y., Krause, K., Yang, T., Dongus, J.A., Zhang, Y., Turck, F., 2018. Telobox motifs recruit CLF/SWN-PRC2 for H3K27me3 deposition via TRB factors in Arabidopsis. Nat. Genet. 50, 638-644.
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      沈阳化工大学材料科学与工程学院 沈阳 110142

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