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Regulation and Modification of the Epigenome for Enhanced Salinity Tolerance in Crop Plants

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Salinity Responses and Tolerance in Plants, Volume 2

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Abstract

Histone modifications (acetylation, methylation, phosphorylation, etc.), histone variants, regulatory RNAs, and DNA methylation represent the functional elements of epigenetics. They serve as a basis for regulating biological processes such as flowering and germination, as well as environmental stress responses in plants. Chromatin modifications can also function to prime plants to respond to adverse environmental conditions and act as short-term or long-term (transgenerational) stress memory, enabling to be preadapted to the prevailing environment. Recognition of the importance of epigenetic regulation in biological processes is increasing, including its role in salinity stress response, although many details are still lacking. To date, only a few studies in crop plants have provided evidence for epigenetic changes that occur in response to salinity and that result in increasing tolerance to salinity stress. In the current review, we discuss insights into the involvement of epigenetic regulatory elements, such as histone modifications, histone variants, regulatory RNAs, and DNA methylation, in salinity stress response based on studies in the model plant, Arabidopsis. In particular, knowledge of the involvement of histone acetylation in salt-stress response has increased, and various chemical compounds capable of regulating levels of histone acetylation have been identified. Based on the available evidence, we provide a perspective on the potential use of chemical epigenetic modifiers, which function as histone deacetylase (HDAC) inhibitors, for enhancing stress tolerance in crops such as cassava.

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Abbreviations

HDAC:

Histone deacetylase

HDC:

Histone deacetylation complex 1 (HDC1)

LEA:

Late embryogenesis abundant

lncRNA:

Long noncoding RNA

ncRNA:

Noncoding RNA

NHX:

Sodium hydrogen exchanger

RdDM:

RNA-directed DNA methylation

ROS1:

Repressor of transcriptional gene silencing 1 (ROS1)

siRNAs:

Short interfering RNA

References

  • Al-Lawati A, Al-Bahry S, Victor R, Al-Lawati AH, Yaish MW (2016) Salt stress alters DNA methylation levels in alfalfa (Medicago spp). Genet Mol Res 15:15018299

    Article  CAS  PubMed  Google Scholar 

  • Ammar R, Torti D, Tsui K, Gebbia M, Durbic T, Bader GD, Giaever G, Nislow C (2012) Chromatin is an ancient innovation conserved between Archaea and Eukarya. Elife 1:e00078

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Apse MP, Aharon GS, Snedden WA, Blumwald E (1999) Salt tolerance conferred by overexpression of a vacuolar Na+/H+ antiport in Arabidopsis. Science 285:1256–1258

    Article  CAS  PubMed  Google Scholar 

  • Asensi-Fabado MA, Amtmann A, Perrella G (2016) Plant responses to abiotic stress: the chromatin context of transcriptional regulation. Biochim Biophys Acta 1860:106–122

    Article  CAS  Google Scholar 

  • Bharti P, Mahajan M, Vishwakarma AK, Bhardwaj J, Yadav SK (2015) AtROS1 overexpression provides evidence for epigenetic regulation of genes encoding enzymes of flavonoid biosynthesis and antioxidant pathways during salt stress in transgenic tobacco. J Exp Bot 66:5959–5969

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bolden JE, Peart MJ, Johnstone RW (2006) Anticancer activities of histone deacetylase inhibitors. Nat Rev Drug Discov 5:769–784

    Article  CAS  PubMed  Google Scholar 

  • Brosch G, Lusser A, Goralik-Schramel M, Loidl P (1996) Purification and characterization of a high molecular weight histone deacetylase complex (HD2) of maize embryos. Biochemistry 35:15907–15914

    Article  CAS  PubMed  Google Scholar 

  • Chen LT, 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 LT, Luo M, Wang YY, 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 

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

    Google Scholar 

  • Choudhury FK, Rivero RM, Blumwald E, Mittler R (2017) Reactive oxygen species, abiotic stress and stress combination. Plant J 90:856–867

    Article  CAS  PubMed  Google Scholar 

  • Di C, Yuan J, Wu Y, Li J, Lin H, Hu L, Zhang T, Qi Y, Gerstein MB, Guo Y, Lu ZJ (2014) Characterization of stress-responsive lncRNAs in Arabidopsis thaliana by integrating expression, epigenetic and structural features. Plant J 80:848–861

    Article  CAS  PubMed  Google Scholar 

  • Downs JA, Nussenzweig MC, Nussenzweig A (2007) Chromatin dynamics and the preservation of genetic information. Nature 447:951–958

    Article  CAS  PubMed  Google Scholar 

  • Eddy SR (2001) Non-coding RNA genes and the modern RNA world. Nat Rev Genet 2:919–929

    Article  CAS  PubMed  Google Scholar 

  • Fahy J, Jeltsch A, Arimondo PB (2012) DNA methyltransferase inhibitors in cancer: a chemical and therapeutic patent overview and selected clinical studies. Expert Opin Ther Pat 22:1427–1442

    Article  CAS  PubMed  Google Scholar 

  • Gallusci P, Dai Z, Genard M, Gauffretau A, Leblanc-Fournier N, Richard-Molard C, Vile D, Brunel-Muguet S (2017) Epigenetics for plant improvement: current knowledge and modeling avenues. Trends Plant Sci 22:610–623

    Article  CAS  PubMed  Google Scholar 

  • Garg R, Narayana Chevala V, Shankar R, Jain M (2015) Divergent DNA methylation patterns associated with gene expression in rice cultivars with contrasting drought and salinity stress response. Sci Rep 5:14922

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Goyal K, Walton LJ, Tunnacliffe A (2005) LEA proteins prevent protein aggregation due to water stress. Biochem J 388:151–157

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gu X, Jiang D, Yang W, Jacob Y, Michaels SD, 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Han Z, Yu H, Zhao Z, Hunter D, Luo X, Duan J, Tian L (2016) AtHD2D gene plays a role in plant growth, development, and response to abiotic stresses in Arabidopsis thaliana. Front Plant Sci 7:310

    PubMed  PubMed Central  Google Scholar 

  • Hauser MT, Aufsatz W, Jonak C, Luschnig C (2011) Transgenerational epigenetic inheritance in plants. Biochim Biophys Acta 1809:459–468

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Heo JB, Sung S (2011) Vernalization-mediated epigenetic silencing by a long intronic noncoding RNA. Science 331:76–79

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Jablonka E, Lamb MJ (2002) The changing concept of epigenetics. Ann N Y Acad Sci 981:82–96

    Article  PubMed  Google Scholar 

  • Jenuwein T, Allis CD (2001) Translating the histone code. Science 293:1074–1080

    Article  CAS  PubMed  Google Scholar 

  • Jia H, Shao M, He Y, Guan R, Chu P, Jiang H (2015) Proteome dynamics and physiological responses to short-term salt stress in Brassica napus leaves. PLoS One 10:e0144808

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Julkowska MM, Testerink C (2015) Tuning plant signaling and growth to survive salt. Trends Plant Sci 20:586–594

    Article  CAS  PubMed  Google Scholar 

  • Kaldis A, Tsementzi D, Tanriverdi O, Vlachonasios KE (2011) Arabidopsis thaliana transcriptional co-activators ADA2b and SGF29a are implicated in salt stress responses. Planta 233:749–762

    Article  CAS  PubMed  Google Scholar 

  • Kim JM, To TK, Ishida J, Matsui A, Kimura H, Seki M (2012) Transition of chromatin status during the process of recovery from drought stress in Arabidopsis thaliana. Plant Cell Physiol 53:847–856

    Article  CAS  PubMed  Google Scholar 

  • Kim JM, Sasaki T, Ueda M, Sako K, Seki M (2015) Chromatin changes in response to drought, salinity, heat, and cold stresses in plants. Front Plant Sci 6:114

    PubMed  PubMed Central  Google Scholar 

  • Kishor P, Hong Z, Miao GH, Hu C, Verma D (1995) Overexpression of [delta]-pyrroline-5-carboxylate synthetase increases proline production and confers osmotolerance in transgenic plants. Plant Physiol 108:1387–1394

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Kovarik A, Koukalova B, Bezdek M, Opatrny Z (1997) Hypermethylation of tobacco heterochromatic loci in response to osmotic stress. Theor Appl Genet 95:301–306

    Article  Google Scholar 

  • Kumar SV, Wigge PA (2010) H2A.Z-containing nucleosomes mediate the thermosensory response in Arabidopsis. Cell 140:136–147

    Article  CAS  PubMed  Google Scholar 

  • Kung JT, Colognori D, Lee JT (2013) Long noncoding RNAs: past, present, and future. Genetics 193:651–669

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Law JA, Jacobsen SE (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 

  • Lee JT (2012) Epigenetic regulation by long noncoding RNAs. Science 338:1435–1439

    Article  CAS  PubMed  Google Scholar 

  • Li B, Carey M, Workman JL (2007) The role of chromatin during transcription. Cell 128:707–719

    Article  CAS  PubMed  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  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu C, Lu F, Cui X, Cao X (2010) Histone methylation in higher plants. Annu Rev Plant Biol 61:395–420

    Article  CAS  PubMed  Google Scholar 

  • Luger K, Mader AW, Richmond RK, Sargent DF, Richmond TJ (1997) Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature 389:251–260

    Article  CAS  PubMed  Google Scholar 

  • Luo M, Wang YY, Liu X, Yang S, Lu Q, Cui Y, Wu K (2012) 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 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Matsui A, Iida K, Tanaka M, Yamaguchi K, Mizuhashi K, Kim JM, Takahashi S, Kobayashi N, Shigenobu S, Shinozaki K, Seki M (2017) Novel stress-inducible antisense RNAs of protein-coding loci are synthesized by RNA-dependent RNA polymerase. Plant Physiol 175:457–472

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • McClintock B (1984) The significance of responses of the genome to challenge. Science 226:792–801

    Article  CAS  PubMed  Google Scholar 

  • McKersie BD, Bowley SR, Jones KS (1999) Winter survival of transgenic alfalfa overexpressing superoxide dismutase. Plant Physiol 119:839–848

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Moller IS, Gilliham M, Jha D, Mayo GM, Roy SJ, Coates JC, Haseloff J, Tester M (2009) Shoot Na+ exclusion and increased salinity tolerance engineered by cell type-specific alteration of Na+ transport in Arabidopsis. Plant Cell 21:2163–2178

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Munns R, Tester M (2008) Mechanisms of salinity tolerance. Ann Rev Plant Biol 59:651–681

    Article  CAS  Google Scholar 

  • Patanun O, Ueda M, Itouga M, Kato Y, Utsumi Y, Matsui A, Tanaka M, Utsumi C, Sakakibara H, Yoshida M, Narangajavana J, Seki M (2017) The histone deacetylase inhibitor suberoylanilide hydroxamic acid alleviates salinity stress in cassava. Front Plant Sci 7:2039

    Article  PubMed  PubMed Central  Google Scholar 

  • Perrella G, Lopez-Vernaza MA, Carr C, Sani E, Gossele V, Verduyn C, Kellermeier F, Hannah MA, 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 

  • Provart NJ, Alonso J, Assmann SM, Bergmann D, Brady SM, Brkljacic J, Browse J, Chapple C, Colot V, Cutler S, Dangl J, Ehrhardt D, Friesner JD, Frommer WB, Grotewold E, Meyerowitz E, Nemhauser J, Nordborg M, Pikaard C, Shanklin J, Somerville C, Stitt M, Torii KU, Waese J, Wagner D, McCourt P (2016) 50 years of Arabidopsis research: highlights and future directions. New Phytol 209:921–944

    Article  CAS  PubMed  Google Scholar 

  • Qin T, Zhao H, Cui P, Albesher N, Xiong L (2017) A nucleus-localized long non-coding RNA enhances drought and salt stress tolerance. Plant Physiol 175:1321–1336

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Roudier F, Teixeira FK, Colot V (2009) Chromatin indexing in Arabidopsis: an epigenomic tale of tails and more. Trends Genet 25:511–517

    Article  CAS  PubMed  Google Scholar 

  • Roxas VP, Smith RK Jr, Allen ER, Allen RD (1997) Overexpression of glutathione S-transferase/glutathione peroxidase enhances the growth of transgenic tobacco seedlings during stress. Nat Biotechnol 15:988–991

    Article  CAS  PubMed  Google Scholar 

  • Ryu H, Cho H, Bae W, 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 

  • Sakamoto A, Murata AN (1998) Metabolic engineering of rice leading to biosynthesis of glycinebetaine and tolerance to salt and cold. Plant Mol Biol 38:1011–1019

    Article  CAS  PubMed  Google Scholar 

  • Sako K, Kim JM, Matsui A, Nakamura K, Tanaka M, Kobayashi M, Saito K, Nishino N, Kusano M, Taji T, Yoshida M, Seki M (2016) Ky-2, a histone deacetylase inhibitor, enhances high-salinity stress tolerance in Arabidopsis thaliana. Plant Cell Physiol 57:776–783

    Article  CAS  PubMed  Google Scholar 

  • Sani E, Herzyk P, Perrella G, Colot V, Amtmann A (2013) Hyperosmotic priming of Arabidopsis seedlings establishes a long-term somatic memory accompanied by specific changes of the epigenome. Genome Biol 14:R59

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sequeira-Mendes J, Gutierrez C (2015) Links between genome replication and chromatin landscapes. Plant J 83:38–51

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shafi A, Chauhan R, Gill T, Swarnkar MK, Sreenivasulu Y, Kumar S, Kumar N, Shankar R, Ahuja PS, Singh AK (2015) Expression of SOD and APX genes positively regulates secondary cell wall biosynthesis and promotes plant growth and yield in Arabidopsis under salt stress. Plant Mol Biol 87:615–631

    Article  CAS  PubMed  Google Scholar 

  • Shahbazian MD, Grunstein M (2007) Functions of site-specific histone acetylation and deacetylation. Ann Rev Biochem 76:75–100

    Article  CAS  PubMed  Google Scholar 

  • Shen Y, Conde ESN, Audonnet L, Servet C, Wei W, Zhou DX (2014) Over-expression of histone H3K4 demethylase gene JMJ15 enhances salt tolerance in Arabidopsis. Front Plant Sci 5:290

    Article  PubMed  PubMed Central  Google Scholar 

  • Shi H, Lee BH, Wu SJ, Zhu JK (2003) Overexpression of a plasma membrane Na+/H+ antiporter gene improves salt tolerance in Arabidopsis thaliana. Nat Biotechnol 21:81–85

    Article  CAS  PubMed  Google Scholar 

  • Song Y, Ji D, Li S, Wang P, Li Q, Xiang F (2012) The dynamic changes of DNA methylation and histone modifications of salt responsive transcription factor genes in soybean. PLoS One 7:e41274

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sridha S, Wu K (2006) Identification of AtHD2C as a novel regulator of abscisic acid responses in Arabidopsis. Plant J 46:124–133

    Article  CAS  PubMed  Google Scholar 

  • Sura W, Kabza M, Karlowski WM, Bieluszewski T, Kus-Slowinska M, Paweloszek L, Sadowski J, Ziolkowski PA (2017) Dual role of the histone variant H2A.Z in transcriptional regulation of stress-response genes. Plant Cell 29:791–807

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Teperino R, Schoonjans K, Auwerx J (2010) Histone methyl transferases and demethylases; can they link metabolism and transcription? Cell Metab 12:321–327

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tran HT, Nimick M, Uhrig RG, Templeton G, Morrice N, Gourlay R, DeLong A, Moorhead GB (2012) Arabidopsis thaliana histone deacetylase 14 (HDA14) is an alpha-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 

  • Ueda M, Matsui A, Tanaka M, Nakamura T, Abe T, Sako K, Sasaki T, Kim JM, Ito A, Nishino N, Shimada H, Yoshida M, Seki M (2017) The distinct roles of class I and II RPD3-like histone deacetylases in salinity stress response. Plant Physiol 175:1760–1773

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Verdin E, 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 

  • Wang M, Qin L, Xie C, Li W, Yuan J, Kong L, Yu W, Xia G, Liu S (2014) Induced and constitutive DNA methylation in a salinity-tolerant wheat introgression line. Plant Cell Physiol 55:1354–1365

    Article  CAS  PubMed  Google Scholar 

  • Wang Z, Casas-Mollano JA, Xu J, Riethoven JJ, Zhang C, Cerutti H (2015) Osmotic stress induces phosphorylation of histone H3 at threonine 3 in pericentromeric regions of Arabidopsis thaliana. Proc Natl Acad Sci USA 112:8487–8492

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wibowo A, Becker C, Marconi G, Durr J, Price J, Hagmann J, Papareddy R, Putra H, Kageyama J, Becker J, Weigel D, Gutierrez-Marcos J (2016) Hyperosmotic stress memory in Arabidopsis is mediated by distinct epigenetically labile sites in the genome and is restricted in the male germline by DNA glycosylase activity. Elife 5:e13546

    Article  PubMed  PubMed Central  Google Scholar 

  • Xiao J, Lee US, Wagner D (2016) Tug of war: adding and removing histone lysine methylation in Arabidopsis. Curr Opin Plant Biol 34:41–53

    Article  CAS  PubMed  Google Scholar 

  • Xu D, Duan X, Wang B, Hong B, Ho T, Wu R (1996) Expression of a late embryogenesis abundant protein gene, HVA1, from barley confers tolerance to water deficit and salt stress in transgenic rice. Plant Physiol 110:249–257

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xu P, Hu G, Luo C, Liang Z (2016) DNA methyltransferase inhibitors: an updated patent review (2012–2015). Expert Opin Ther Pat 26:1017–1030

    Article  CAS  PubMed  Google Scholar 

  • Yang Q, Chen ZZ, Zhou XF, Yin HB, Li X, Xin XF, Hong XH, Zhu JK, Gong Z (2009) Overexpression of SOS (Salt Overly Sensitive) genes increases salt tolerance in transgenic Arabidopsis. Mol Plant 2:22–31

    Article  CAS  PubMed  Google Scholar 

  • Yang DL, Zhang G, Tang K, Li J, Yang L, Huang H, Zhang H, Zhu JK (2016) Dicer-independent RNA-directed DNA methylation in Arabidopsis. Cell Res 26:1264

    Article  PubMed  PubMed Central  Google Scholar 

  • Yao Y, Bilichak A, Golubov A, Kovalchuk I (2012) ddm1 plants are sensitive to methyl methane sulfonate and NaCl stresses and are deficient in DNA repair. Plant Cell Rep 31:1549–1561

    Article  CAS  PubMed  Google Scholar 

  • Zemach A, Kim MY, Hsieh PH, Coleman-Derr D, Eshed-Williams L, Thao K, Harmer SL, Zilberman D (2013) The Arabidopsis nucleosome remodeler DDM1 allows DNA methyltransferases to access H1-containing heterochromatin. Cell 153:193–205

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang X, Bernatavichute YV, Cokus S, Pellegrini M, Jacobsen SE (2009) Genome-wide analysis of mono-, di- and trimethylation of histone H3 lysine 4 in Arabidopsis thaliana. Genome Biol 10:R62

    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, Zhou DX (2016) Histone deacetylase HDA9 negatively regulates salt and drought stress responsiveness in Arabidopsis. J Exp Bot 67:1703–1713

    Article  CAS  PubMed  Google Scholar 

  • Zhu JK (2009) Active DNA demethylation mediated by DNA glycosylases. Ann Rev Genet 43:143–166

    Article  CAS  PubMed  Google Scholar 

  • Zilberman D, Cao X, Jacobsen SE (2003) ARGONAUTE4 control of locus-specific siRNA accumulation and DNA and histone methylation. Science 299:716–719

    Article  CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. Plant Genomic Network Research Team, RIKEN Center for Sustainable Resource Science, Yokohama, Kanagawa, Japan

    Minoru Ueda, Kaori Sako & Motoaki Seki

  2. Core Research for Evolutional Science and Technology (CREST), Japan Science and Technology Agency (JST), Kawaguchi, Saitama, Japan

    Minoru Ueda, Kaori Sako & Motoaki Seki

  3. Plant Epigenome Regulation Laboratory, RIKEN Cluster for Pioneering Research, Wako, Saitama, Japan

    Motoaki Seki

  4. Kihara Institute for Biological Research, Yokohama City University, Yokohama, Kanagawa, Japan

    Motoaki Seki

Authors
  1. Minoru Ueda
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  2. Kaori Sako
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  3. Motoaki Seki
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Correspondence to Motoaki Seki .

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Editors and Affiliations

  1. Department of Biotechnology, Modern College of Arts Science and Commerce, Savitribai Phule Pune University, Pune, India

    Vinay Kumar

  2. Genetics and Plant Breeding, Mountain Research Center for Field Crops, Khudwani, Anantnag, India

    Shabir Hussain Wani

  3. Nuclear Agriculture and Biotechnology Division, Bhabha Atomic Research Centre (BARC), Mumbai, India

    Penna Suprasanna

  4. Stress Adaptation Research Unit, RIKEN Center for Sustainable Resource Science, Yokohama, Japan

    Lam-Son Phan Tran

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Ueda, M., Sako, K., Seki, M. (2018). Regulation and Modification of the Epigenome for Enhanced Salinity Tolerance in Crop Plants. In: Kumar, V., Wani, S., Suprasanna, P., Tran, LS. (eds) Salinity Responses and Tolerance in Plants, Volume 2. Springer, Cham. https://doi.org/10.1007/978-3-319-90318-7_4

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