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Histone acetylation is involved in GA-mediated 45S rDNA decondensation in maize aleurone layers

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Abstract

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The aleurone layer is crucial to seed germination. Using dissected aleurone layers, we found that GA increased histone acetylation accompanied by rDNA decondensation in aleurone layers during maize seed germination.

Abstract

Aleurone layers play an important role in cereal seed germination. In this study, we reported that rDNA chromatin was decondensed, accompanied with increased rDNA expression and genomic global hyperacetylation in gibberellin (GA)-treated maize-dissected aleurone layers. The activity analysis of histone acetyltransferase (HAT) and deacetylase (HDAC) showed that GA increased the level of histone acetylation by promoting the ratio of HAT/HDAC activity in aleurone layers. HDAC inhibitors TSA and CUDC-101 elevated the histone acetylation in aleurone layers accompanied by 45S rDNA decondensation. The further chromatin immunoprecipitation experiments showed that GA treatment promoted the level of histone acetylation in the promoter region of the rRNA and HAT/HDAC genes in aleurone layers. Taken together, these data indicated that histone acetylation mediates GA-regulated 45S rDNA chromatin decondensation in aleurone layers during maize seed germination.

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References

  • Bethke PC, Libourel IG, Aoyama N, Chung Y-Y, Still DW, Jones RL (2007) The Arabidopsis aleurone layer responds to nitric oxide, gibberellin, and abscisic acid and is sufficient and necessary for seed dormancy. Plant Physiol 143:1173–1188

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brownell JE, Allis CD (1996) Special HATs for special occasions: linking histone acetylation to chromatin assembly and gene activation. Curr Opin Genet Dev 6:176–184

    Article  CAS  PubMed  Google Scholar 

  • Chen H, Lin RJ, Xie W, Wilpitz D, Evans RM (1999) Regulation of hormone-induced histone hyperacetylation and gene activation via acetylation of an acetylase. Cell 98:675–686

    Article  CAS  PubMed  Google Scholar 

  • Chen L-T, Luo M, Wang Y-Y, Wu K (2010) Involvement of Arabidopsis histone deacetylase HDA6 in ABA and salt stress response. J Exp Bot 61:3345–3353

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chrispeels MJ, Varner J (1967) Hormonal control of enzyme synthesis: on the mode of action of gibberellic acid and abscisin in aleurone layers of barley. Plant Physiol 42:1008–1016

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dahl JA, Collas P (2008) A rapid micro chromatin immunoprecipitation assay (ChIP). Nat Protoc 3:1032

    Article  CAS  PubMed  Google Scholar 

  • De Ruijter AJ, Van Gennip AH, Caron HN, Stephan K, Van Kuilenburg AB (2003) Histone deacetylases (HDACs): characterization of the classical HDAC family. Biochem J 370:737–749

    Article  PubMed  PubMed Central  Google Scholar 

  • Domínguez F, Cejudo FJ (2014) Programmed cell death (PCD): an essential process of cereal seed development and germination. Front Plant Sci 5:366–377

    PubMed  PubMed Central  Google Scholar 

  • Durut N, Abou-Ellail M, Pontvianne F, Das S, Kojima H, Ukai S, de Bures A, Comella P, Nidelet S, Rialle S (2014) A duplicated NUCLEOLIN gene with antagonistic activity is required for chromatin organization of silent 45S rDNA in Arabidopsis. Plant Cell 26:1330–1344

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gómez-Cadenas A, Zentella R, Walker-Simmons MK, Ho T-HD (2001) Gibberellin/abscisic acid antagonism in barley aleurone cells: site of action of the protein kinase PKABA1 in relation to gibberellin signaling molecules. Plant Cell 13:667–679

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Hou H, Wang P, Zhang H, Wen H, Gao F, Ma N, Wang Q, Li L (2015) Histone acetylation is involved in GA-regulated sodCp gene expression in maize aleurone layers. Plant and Cell Physiology 56:2139–2149 (pcv126)

    CAS  PubMed  Google Scholar 

  • Huang M, Li H, Zhang L, Gao F, Wang P, Hu Y, Yan S, Zhao L, Zhang Q, Tan J (2012) Plant 45S rDNA clusters are fragile sites and their instability is associated with epigenetic alterations. PLoS One 7:e35139

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jones RL, Jacobsen JV (1991) Regulation of synthesis and transport of secreted proteins in cereal aleurone. Int Rev Cytol 126:49–88

    Article  CAS  PubMed  Google Scholar 

  • Lee DY, Hayes JJ, Pruss D, Wolffe AP (1993) A positive role for histone acetylation in transcription factor access to nucleosomal DNA. Cell 72:73–84

    Article  CAS  PubMed  Google Scholar 

  • Li L, Yang J, Tong Q, Zhao L, Song Y (2005) A novel approach to prepare extended DNA fibers in plants. Cytom Part A 63:114–117

    Article  CAS  Google Scholar 

  • Li H, Yan S, Zhao L, Tan J, Zhang Q, Gao F, Wang P, Hou H, Li L (2014) Histone acetylation associated up-regulation of the cell wall related genes is involved in salt stress induced maize root swelling. BMC Plant Biol 14:105

    Article  PubMed  PubMed Central  Google Scholar 

  • Ogawa M, Hanada A, Yamauchi Y, Kuwahara A, Kamiya Y, Yamaguchi S (2003) Gibberellin biosynthesis and response during Arabidopsis seed germination. Plant Cell 15:1591–1604

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pile LA, Wassarman DA (2000) Chromosomal localization links the SIN3–RPD3 complex to the regulation of chromatin condensation, histone acetylation and gene expression. EMBO J 19:6131–6140

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Probst AV, Fagard M, Proux F, Mourrain P, Boutet S, Earley K, Lawrence RJ, Pikaard CS, Murfett J, Furner I (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 

  • Rademacher W (2000) Growth retardants: effects on gibberellin biosynthesis and other metabolic pathways. Annu Rev Plant Biol 51:501–531

    Article  CAS  Google Scholar 

  • Richon VM, Sandhoff TW, Rifkind RA, Marks PA (2000) Histone deacetylase inhibitor selectively induces p21WAF1 expression and gene-associated histone acetylation. Proc Natl Acad Sci 97:10014–10019

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ruggero D (2013) Translational control in cancer etiology. Cold Spring Harbor Perspect Biol 5:a012336

    Article  Google Scholar 

  • Santoro R, Grummt I (2005) Epigenetic mechanism of rRNA gene silencing: temporal order of NoRC-mediated histone modification, chromatin remodeling, and DNA methylation. Mol Cell Biol 25:2539–2546

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Scheid OM, Probst AV, Afsar K, Paszkowski J (2002) Two regulatory levels of transcriptional gene silencing in Arabidopsis. Proc Natl Acad Sci 99:13659–13662

    Article  PubMed Central  Google Scholar 

  • Schneider R, Grosschedl R (2007) Dynamics and interplay of nuclear architecture, genome organization, and gene expression. Genes Dev 21:3027–3043

    Article  CAS  PubMed  Google Scholar 

  • Schübeler D, MacAlpine DM, Scalzo D, Wirbelauer C, Kooperberg C, Van Leeuwen F, Gottschling DE, O’Neill LP, Turner BM, Delrow J (2004) The histone modification pattern of active genes revealed through genome-wide chromatin analysis of a higher eukaryote. Genes Dev 18:1263–1271

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  Google Scholar 

  • Shahpiri A, Talaei N, Finnie C (2015) Spatio-temporal appearance of α-amylase and limit dextrinase in barley aleurone layer in response to gibberellic acid, abscisic acid and salicylic acid. J Sci Food Agric 95:141–147

    Article  CAS  PubMed  Google Scholar 

  • Shogren-Knaak M, Ishii H, Sun J-M, Pazin MJ, Davie JR, Peterson CL (2006) Histone H4-K16 acetylation controls chromatin structure and protein interactions. Science 311:844–847

    Article  CAS  PubMed  Google Scholar 

  • Sun CW, Callis J (1997) Independent modulation of Arabidopsis thaliana polyubiquitin mRNAs in different organs and in response to environmental changes. Plant J 11:1017–1027

    Article  CAS  PubMed  Google Scholar 

  • Tai HH, Tai GC, Beardmore T (2005) Dynamic histone acetylation of late embryonic genes during seed germination. Plant Mol Biol 59:909–925

    Article  CAS  PubMed  Google Scholar 

  • Vettese-Dadey M, Grant P, Hebbes T, Crane-Robinson C, Allis C, Workman J (1996) Acetylation of histone H4 plays a primary role in enhancing transcription factor binding to nucleosomal DNA in vitro. EMBO J 15:2508

    CAS  PubMed  PubMed Central  Google Scholar 

  • Vicente-Carbajosa J, Carbonero P (2004) Seed maturation: developing an intrusive phase to accomplish a quiescent state. Int J Dev Biol 49:645–651

    Article  Google Scholar 

  • Wang P, Zhao L, Hou H, Zhang H, Huang Y, Wang Y, Li H, Gao F, Yan S, Li L (2015) Epigenetic changes are associated with programmed cell death induced by heat stress in seedling leaves of Zea mays. Plant Cell Physiol 56:965–976

    Article  CAS  PubMed  Google Scholar 

  • Wang P, Zhang H, Hou H, Wang Q, Li Y, Huang Y, Xie L, Gao F, He S, Li L (2016) Cell cycle arrest induced by inhibitors of epigenetic modifications in maize (Zea mays) seedling leaves: characterization of the process and possible mechanisms involved. New Phytol 211:646–657

    Article  CAS  PubMed  Google Scholar 

  • Young TE, Gallie DR (2000) Programmed cell death during endosperm development. Plant Mol Biol 44:283–301

    Article  CAS  PubMed  Google Scholar 

  • Zhang L, Hu Y, Yan S, Li H, He S, Huang M, Li L (2012) ABA-mediated inhibition of seed germination is associated with ribosomal DNA chromatin condensation, decreased transcription, and ribosomal RNA gene hypoacetylation. Plant Mol Biol 79:285–293

    Article  CAS  PubMed  Google Scholar 

  • Zhang H, Wang P, Hou H, Wen H, Zhou H, Gao F, Wu J, Qiu Z, Li L (2016) Histone modification is involved in Okadaic acid (OA) induced DNA damage response and G 2-M transition arrest in maize. PLoS One 11:e0155852

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhao L, Wang P, Yan S, Gao F, Li H, Hou H, Zhang Q, Tan J, Li L (2014) Promoter-associated histone acetylation is involved in the osmotic stress-induced transcriptional regulation of the maize ZmDREB2A gene. Physiol Plant 151:459–467

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

This work was supported by the National Natural Science Foundation of China (No. 31571265).

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Authors and Affiliations

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

    Xueke Zheng, Haoli Hou, Hao Zhang, Mengxia Yue, Yan Hu & Lijia Li

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  1. Xueke Zheng
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  2. Haoli Hou
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  3. Hao Zhang
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  4. Mengxia Yue
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  5. Yan Hu
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  6. Lijia Li
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Correspondence to Lijia Li.

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Communicated by Tarek Hewezi.

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Zheng, X., Hou, H., Zhang, H. et al. Histone acetylation is involved in GA-mediated 45S rDNA decondensation in maize aleurone layers. Plant Cell Rep 37, 115–123 (2018). https://doi.org/10.1007/s00299-017-2207-z

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  • DOI: https://doi.org/10.1007/s00299-017-2207-z

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