Rice Epigenomes: Characteristics, Regulatory Functions, and Reprogramming Mechanisms

Chapter

Abstract

Rice is one of the most important food crops in the world and has been established as a model for plant genomic and epigenomic study. In recent years accumulated data by high-throughput sequencing provide useful information on rice epigenomic characteristics. Exploring the function of various epigenetic regulators including writer, reader, and eraser of epigenomic information reveals the importance of epigenomic characteristics to genome activity. It has been also found that these regulators are involved in a diverse range of developmental and stress-responsive pathways. Analysis of different rice varieties indicates that some phenotypic differences are caused by epigenetic variations rather than DNA sequence mutations, which are referred to as epialleles. Significantly, several epialleles are identified to be related to important agronomic traits, which provide novel strategies to improve grain productivity in rice. In this chapter, we review features of rice epigenome, epigenetic regulation of gene expression, and its implication in rice development, stress response, agronomic traits, and yield.

Keywords

Rice Epigenome Regulation Development Stress 

References

  1. Ahmad A, Dong Y, Cao X (2011) Characterization of the PRMT gene family in rice reveals conservation of arginine methylation. PLoS One 6:e22664.  https://doi.org/10.1371/journal.pone.0022664 PubMedPubMedCentralCrossRefGoogle Scholar
  2. Chen X, Zhou DX (2013) Rice epigenomics and epigenetics: challenges and opportunities. Curr Opin Plant Biol 16:164–169.  https://doi.org/10.1016/j.pbi.2013.03.004 PubMedCrossRefGoogle Scholar
  3. Chen Q et al (2013) Structural basis of a histone H3 lysine 4 demethylase required for stem elongation in rice. PLoS Genet 9:e1003239.  https://doi.org/10.1371/journal.pgen.1003239 PubMedPubMedCentralCrossRefGoogle Scholar
  4. Chen X, Liu X, Zhao Y, Zhou DX (2015) Histone H3K4me3 and H3K27me3 regulatory genes control stable transmission of an epimutation in rice. Sci Rep 5:13251.  https://doi.org/10.1038/srep13251 PubMedPubMedCentralCrossRefGoogle Scholar
  5. Chodavarapu RK et al (2012) Transcriptome and methylome interactions in rice hybrids. Proc Natl Acad Sci U S A 109:12040–12045.  https://doi.org/10.1073/pnas.1209297109 PubMedPubMedCentralCrossRefGoogle Scholar
  6. Choi SC et al (2014) Trithorax group protein Oryza sativa trithorax1 controls flowering time in rice via interaction with early heading date3. Plant Physiol 164:1326–1337.  https://doi.org/10.1104/pp.113.228049 PubMedPubMedCentralCrossRefGoogle Scholar
  7. Coleman-Derr D, Zilberman D (2012) Deposition of histone variant H2A.Z within gene bodies regulates responsive genes. PLoS Genet 8:e1002988.  https://doi.org/10.1371/journal.pgen.1002988 PubMedPubMedCentralCrossRefGoogle Scholar
  8. Conrad LJ et al (2014) The polycomb group gene EMF2B is essential for maintenance of floral meristem determinacy in rice. Plant J Cell Mol Biol 80:883–894.  https://doi.org/10.1111/tpj.12688 CrossRefGoogle Scholar
  9. Cui X, Cao X (2014) Epigenetic regulation and functional exaptation of transposable elements in higher plants. Curr Opin Plant Biol 21:83–88.  https://doi.org/10.1016/j.pbi.2014.07.001 PubMedCrossRefGoogle Scholar
  10. Cui X et al (2013) Control of transposon activity by a histone H3K4 demethylase in rice. Proc Natl Acad Sci U S A 110:1953–1958.  https://doi.org/10.1073/pnas.1217020110 PubMedPubMedCentralCrossRefGoogle Scholar
  11. Deng Y et al (2017) Epigenetic regulation of antagonistic receptors confers rice blast resistance with yield balance. Science 355:962–965.  https://doi.org/10.1126/science.aai8898 PubMedCrossRefGoogle Scholar
  12. Ding B, Bellizzi Mdel R, Ning Y, Meyers BC, Wang GL (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.  https://doi.org/10.1105/tpc.112.101972 PubMedPubMedCentralCrossRefGoogle Scholar
  13. Du Z et al (2013) Genome-wide analysis of histone modifications: H3K4me2, H3K4me3, H3K9ac, and H3K27ac in Oryza sativa L. Mol Plant 6:1463–1472.  https://doi.org/10.1093/mp/sst018 PubMedPubMedCentralCrossRefGoogle Scholar
  14. Fang H, Liu X, Thorn G, Duan J, Tian L (2014) Expression analysis of histone acetyltransferases in rice under drought stress. Biochem Biophys Res Commun 443:400–405.  https://doi.org/10.1016/j.bbrc.2013.11.102 PubMedCrossRefGoogle Scholar
  15. Feng S et al (2010) Conservation and divergence of methylation patterning in plants and animals. Proc Natl Acad Sci U S A 107:8689–8694.  https://doi.org/10.1073/pnas.1002720107 PubMedPubMedCentralCrossRefGoogle Scholar
  16. Feng Q et al (2012) Salt and alkaline stress induced transgenerational alteration in DNA methylation of rice. Aust J Crop Sci 6:877–883Google Scholar
  17. Fu W, Wu K, Duan J (2007) Sequence and expression analysis of histone deacetylases in rice. Biochem Biophys Res Commun 356:843–850.  https://doi.org/10.1016/j.bbrc.2007.03.010 PubMedCrossRefGoogle Scholar
  18. Guo Z et al (2015) Global epigenomic analysis indicates that epialleles contribute to allele-specific expression via allele-specific histone modifications in hybrid rice. BMC Genomics 16:232.  https://doi.org/10.1186/s12864-015-1454-z PubMedPubMedCentralCrossRefGoogle Scholar
  19. He G et al (2010) Global epigenetic and transcriptional trends among two rice subspecies and their reciprocal hybrids. Plant Cell 22:17–33.  https://doi.org/10.1105/tpc.109.072041 PubMedPubMedCentralCrossRefGoogle Scholar
  20. Hou Y et al (2015) JMJ704 positively regulates rice defense response against Xanthomonas oryzae pv. oryzae infection via reducing H3K4me2/3 associated with negative disease resistance regulators. BMC Plant Biol 15:286.  https://doi.org/10.1186/s12870-015-0674-3 PubMedPubMedCentralCrossRefGoogle Scholar
  21. Hu Y, Lai Y (2015) Identification and expression analysis of rice histone genes. Plant Physiol Biochem: PPB 86:55–65.  https://doi.org/10.1016/j.plaphy.2014.11.012 PubMedCrossRefGoogle Scholar
  22. Hu Y et al (2009) Rice histone deacetylase genes display specific expression patterns and developmental functions. Biochem Biophys Res Commun 388:266–271.  https://doi.org/10.1016/j.bbrc.2009.07.162 PubMedCrossRefGoogle Scholar
  23. Hu Y et al (2012) CHD3 protein recognizes and regulates methylated histone H3 lysines 4 and 27 over a subset of targets in the rice genome. Proc Natl Acad Sci U S A 109:5773–5778.  https://doi.org/10.1073/pnas.1203148109 PubMedPubMedCentralCrossRefGoogle Scholar
  24. Hu L et al (2014) Mutation of a major CG methylase in rice causes genome-wide hypomethylation, dysregulated genome expression, and seedling lethality. Proc Natl Acad Sci U S A 111:10642–10647.  https://doi.org/10.1073/pnas.1410761111 PubMedPubMedCentralCrossRefGoogle Scholar
  25. Huang L et al (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.  https://doi.org/10.1104/pp.107.099473 PubMedPubMedCentralCrossRefGoogle Scholar
  26. Huang X et al (2016) Imprinted gene OsFIE1 modulates rice seed development by influencing nutrient metabolism and modifying genome H3K27me3. Plant J Cell Mol Biol 87:305–317.  https://doi.org/10.1111/tpj.13202 CrossRefGoogle Scholar
  27. Jang IC et al (2003) Structure and expression of the rice class-I type histone deacetylase genes OsHDAC1-3: OsHDAC1 overexpression in transgenic plants leads to increased growth rate and altered architecture. Plant J Cell Mol Biol 33:531–541CrossRefGoogle Scholar
  28. Jiao Y et al (2010) Regulation of OsSPL14 by OsmiR156 defines ideal plant architecture in rice. Nat Genet 42:541–544.  https://doi.org/10.1038/ng.591 PubMedCrossRefGoogle Scholar
  29. Jin J et al (2015) MORF-RELATED GENE702, a reader protein of Trimethylated histone H3 lysine 4 and histone H3 lysine 36, is involved in Brassinosteroid-regulated growth and flowering time control in Rice. Plant Physiol 168:1275–1285.  https://doi.org/10.1104/pp.114.255737 PubMedPubMedCentralCrossRefGoogle Scholar
  30. Kou HP et al (2011) Heritable alteration in DNA methylation induced by nitrogen-deficiency stress accompanies enhanced tolerance by progenies to the stress in rice (Oryza sativa L.) J Plant Physiol 168:1685–1693.  https://doi.org/10.1016/j.jplph.2011.03.017 PubMedCrossRefGoogle Scholar
  31. Kutateladze T, SnapShot G (2011) Histone readers. Cell 146:842–842. e841.  https://doi.org/10.1016/j.cell.2011.08.022 PubMedPubMedCentralCrossRefGoogle Scholar
  32. La H et al (2011) A 5-methylcytosine DNA glycosylase/lyase demethylates the retrotransposon Tos17 and promotes its transposition in rice. Proc Natl Acad Sci U S A 108:15498–15503.  https://doi.org/10.1073/pnas.1112704108 PubMedPubMedCentralCrossRefGoogle Scholar
  33. Law JA, Jacobsen SE (2010) Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nat Rev Genet 11:204–220.  https://doi.org/10.1038/nrg2719 PubMedPubMedCentralCrossRefGoogle Scholar
  34. Li C, Huang L, Xu C, Zhao Y, Zhou DX (2011a) Altered levels of histone deacetylase OsHDT1 affect differential gene expression patterns in hybrid rice. PLoS One 6:e21789.  https://doi.org/10.1371/journal.pone.0021789 PubMedPubMedCentralCrossRefGoogle Scholar
  35. Li W, Han Y, Tao F, Chong K (2011b) Knockdown of SAMS genes encoding S-adenosyl-l-methionine synthetases causes methylation alterations of DNAs and histones and leads to late flowering in rice. J Plant Physiol 168:1837–1843.  https://doi.org/10.1016/j.jplph.2011.05.020 PubMedCrossRefGoogle Scholar
  36. Li X et al (2012) Single-base resolution maps of cultivated and wild rice methylomes and regulatory roles of DNA methylation in plant gene expression. BMC Genomics 13:300.  https://doi.org/10.1186/1471-2164-13-300 PubMedPubMedCentralCrossRefGoogle Scholar
  37. Li T et al (2013) Jumonji C domain protein JMJ705-mediated removal of histone H3 lysine 27 trimethylation is involved in defense-related gene activation in rice. Plant Cell 25:4725–4736.  https://doi.org/10.1105/tpc.113.118802 PubMedPubMedCentralCrossRefGoogle Scholar
  38. Lindroth AM et al (2001) Requirement of CHROMOMETHYLASE3 for maintenance of CpXpG methylation. Science 292:2077–2080.  https://doi.org/10.1126/science.1059745 PubMedCrossRefGoogle Scholar
  39. Lindroth AM et al (2008) Antagonism between DNA and H3K27 methylation at the imprinted Rasgrf1 locus. PLoS Genet 4:e1000145.  https://doi.org/10.1371/journal.pgen.1000145 PubMedPubMedCentralCrossRefGoogle Scholar
  40. Lisch D (2009) Epigenetic regulation of transposable elements in plants. Annu Rev Plant Biol 60:43–66.  https://doi.org/10.1146/annurev.arplant.59.032607.092744 PubMedCrossRefGoogle Scholar
  41. Liu X et al (2012) Histone acetyltransferases in rice (Oryza sativa L.): phylogenetic analysis, subcellular localization and expression. BMC Plant Biol 12:145.  https://doi.org/10.1186/1471-2229-12-145 PubMedPubMedCentralCrossRefGoogle Scholar
  42. Liu X et al (2014) The rice enhancer of zeste [E(z)] genes SDG711 and SDG718 are respectively involved in long day and short day signaling to mediate the accurate photoperiod control of flowering time. Front Plant Sci 5:591.  https://doi.org/10.3389/fpls.2014.00591 PubMedPubMedCentralGoogle Scholar
  43. Liu X et al (2015) Regulation of histone methylation and reprogramming of gene expression in the rice inflorescence meristem. Plant Cell 27:1428–1444.  https://doi.org/10.1105/tpc.15.00201 PubMedPubMedCentralCrossRefGoogle Scholar
  44. Liu B et al (2016) SET DOMAIN GROUP 708, a histone H3 lysine 36-specific methyltransferase, controls flowering time in rice (Oryza sativa). New Phytol 210:577–588.  https://doi.org/10.1111/nph.13768 PubMedCrossRefGoogle Scholar
  45. Lu L, Chen X, Sanders D, Qian S, 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.  https://doi.org/10.1080/15592294.2015.1104446 PubMedPubMedCentralCrossRefGoogle Scholar
  46. Luo M, Platten D, Chaudhury A, Peacock WJ, Dennis ES (2009) Expression, imprinting, and evolution of rice homologs of the polycomb group genes. Mol Plant 2:711–723.  https://doi.org/10.1093/mp/ssp036 PubMedCrossRefGoogle Scholar
  47. Ma X et al (2015) CHR729 is a CHD3 protein that controls seedling development in rice. PLoS One 10:e0138934.  https://doi.org/10.1371/journal.pone.0138934 PubMedPubMedCentralCrossRefGoogle Scholar
  48. Mahrez W et al (2016) H3K36ac is an evolutionary conserved plant histone modification that marks active genes. Plant Physiol 170:1566–1577.  https://doi.org/10.1104/pp.15.01744 PubMedPubMedCentralGoogle Scholar
  49. Miura K et al (2010) OsSPL14 promotes panicle branching and higher grain productivity in rice. Nat Genet 42:545–549.  https://doi.org/10.1038/ng.592 PubMedCrossRefGoogle Scholar
  50. Nallamilli BR et al (2013) Polycomb group gene OsFIE2 regulates rice (Oryza sativa) seed development and grain filling via a mechanism distinct from Arabidopsis. PLoS Genet 9:e1003322.  https://doi.org/10.1371/journal.pgen.1003322 PubMedPubMedCentralCrossRefGoogle Scholar
  51. Ono A et al (2012) A null mutation of ROS1a for DNA demethylation in rice is not transmittable to progeny. Plant J Cell Mol Biol 71:564–574.  https://doi.org/10.1111/j.1365-313X.2012.05009.x CrossRefGoogle Scholar
  52. Ou X et al (2009) Spaceflight induces both transient and heritable alterations in DNA methylation and gene expression in rice (Oryza sativa L.) Mutat Res 662:44–53.  https://doi.org/10.1016/j.mrfmmm.2008.12.004 PubMedCrossRefGoogle Scholar
  53. Ou X et al (2012) Transgenerational inheritance of modified DNA methylation patterns and enhanced tolerance induced by heavy metal stress in rice (Oryza sativa L.) PLoS One 7:e41143.  https://doi.org/10.1371/journal.pone.0041143 PubMedPubMedCentralCrossRefGoogle Scholar
  54. Pang J, Dong M, Li N, Zhao Y, Liu B (2013) Functional characterization of a rice de novo DNA methyltransferase, OsDRM2, expressed in Escherichia coli and yeast. Biochem Biophys Res Commun 432:157–162.  https://doi.org/10.1016/j.bbrc.2013.01.067 PubMedCrossRefGoogle Scholar
  55. Qin FJ, Sun QW, Huang LM, Chen XS, Zhou DX (2010) Rice SUVH histone methyltransferase genes display specific functions in chromatin modification and retrotransposon repression. Mol Plant 3:773–782.  https://doi.org/10.1093/mp/ssq030 PubMedCrossRefGoogle Scholar
  56. Qiu SP, Huang J, Pan LJ, Wang MM, Zhang HS (2006) Salt induces expression of RH3.2A, encoding an H3.2-type histone H3 protein in rice (Oryza sativa L.) Yi Chuan Xue Bao = Acta Genet Sin 33:833–840.  https://doi.org/10.1016/S0379-4172(06)60117-0 PubMedGoogle Scholar
  57. Roy D et al (2014) Differential acetylation of histone H3 at the regulatory region of OsDREB1b promoter facilitates chromatin remodelling and transcription activation during cold stress. PLoS One 9:e100343.  https://doi.org/10.1371/journal.pone.0100343 PubMedPubMedCentralCrossRefGoogle Scholar
  58. Saze H, Mittelsten Scheid O, Paszkowski J (2003) Maintenance of CpG methylation is essential for epigenetic inheritance during plant gametogenesis. Nat Genet 34:65–69.  https://doi.org/10.1038/ng1138 PubMedCrossRefGoogle Scholar
  59. Sharma R et al (2009) Rice cytosine DNA methyltransferases – gene expression profiling during reproductive development and abiotic stress. FEBS J 276:6301–6311.  https://doi.org/10.1111/j.1742-4658.2009.07338.x PubMedCrossRefGoogle Scholar
  60. Shi Y et al (2004) Histone demethylation mediated by the nuclear amine oxidase homolog LSD1. Cell 119:941–953.  https://doi.org/10.1016/j.cell.2004.12.012 PubMedCrossRefGoogle Scholar
  61. Shi J, Dong A, Shen WH (2014) Epigenetic regulation of rice flowering and reproduction. Front Plant Sci 5:803.  https://doi.org/10.3389/fpls.2014.00803 PubMedGoogle Scholar
  62. Shindo H et al (2012) PHD finger of the SUMO ligase Siz/PIAS family in rice reveals specific binding for methylated histone H3 at lysine 4 and arginine 2. FEBS Lett 586:1783–1789.  https://doi.org/10.1016/j.febslet.2012.04.063 PubMedCrossRefGoogle Scholar
  63. Song X, Cao X (2017) Transposon-mediated epigenetic regulation contributes to phenotypic diversity and environmental adaptation in rice. Curr Opin Plant Biol 36:111–118.  https://doi.org/10.1016/j.pbi.2017.02.004 PubMedCrossRefGoogle Scholar
  64. Stroud H et al (2014) Non-CG methylation patterns shape the epigenetic landscape in Arabidopsis. Nat Struct Mol Biol 21:64–72.  https://doi.org/10.1038/nsmb.2735 PubMedCrossRefGoogle Scholar
  65. Sui P et al (2012) H3K36 methylation is critical for brassinosteroid-regulated plant growth and development in rice. Plant J Cell Mol Biol 70:340–347CrossRefGoogle Scholar
  66. Sun Q, Zhou DX (2008) Rice jmjC domain-containing gene JMJ706 encodes H3K9 demethylase required for floral organ development. Proc Natl Acad Sci U S A 105:13679–13684.  https://doi.org/10.1073/pnas.0805901105 PubMedPubMedCentralCrossRefGoogle Scholar
  67. Sun C et al (2012) The histone methyltransferase SDG724 mediates H3K36me2/3 deposition at MADS50 and RFT1 and promotes flowering in rice. Plant Cell 24:3235–3247.  https://doi.org/10.1105/tpc.112.101436 PubMedPubMedCentralCrossRefGoogle Scholar
  68. Tan F, Zhang K, Mujahid H, Verma DP, Peng Z (2011) Differential histone modification and protein expression associated with cell wall removal and regeneration in rice (Oryza sativa). J Proteome Res 10:551–563.  https://doi.org/10.1021/pr100748e PubMedCrossRefGoogle Scholar
  69. Tan F et al (2016) Analysis of chromatin regulators reveals specific features of rice DNA methylation pathways. Plant Physiol 171:2041–2054.  https://doi.org/10.1104/pp.16.00393 PubMedPubMedCentralCrossRefGoogle Scholar
  70. Tao Z et al (2009) A pair of allelic WRKY genes play opposite roles in rice-bacteria interactions. Plant Physiol 151:936–948.  https://doi.org/10.1104/pp.109.145623 PubMedPubMedCentralCrossRefGoogle Scholar
  71. Teerawanichpan P, Chandrasekharan MB, Jiang Y, Narangajavana J, Hall TC (2004) Characterization of two rice DNA methyltransferase genes and RNAi-mediated reactivation of a silenced transgene in rice callus. Planta 218:337–349.  https://doi.org/10.1007/s00425-003-1112-6 PubMedCrossRefGoogle Scholar
  72. Tsuji H, Saika H, Tsutsumi N, Hirai A, Nakazono M (2006) Dynamic and reversible changes in histone H3-Lys4 methylation and H3 acetylation occurring at submergence-inducible genes in rice. Plant Cell Physiol 47:995–1003.  https://doi.org/10.1093/pcp/pcj072 PubMedCrossRefGoogle Scholar
  73. Tsukada Y et al (2006) Histone demethylation by a family of JmjC domain-containing proteins. Nature 439:811–816.  https://doi.org/10.1038/nature04433 PubMedCrossRefGoogle Scholar
  74. Wang X, Weng Q, You A, Zhu L, He G (2003) Cloning and characterization of rice RH3 gene induced by brown planthopper. Chin Sci Bull 48:1976–1981Google Scholar
  75. Wang Y et al (2016) CRL6, a member of the CHD protein family, is required for crown root development in rice. Plant Physiol Biochem PPB 105:185–194.  https://doi.org/10.1016/j.plaphy.2016.04.022 PubMedCrossRefGoogle Scholar
  76. Weber CM, Henikoff S (2014) Histone variants: dynamic punctuation in transcription. Genes Dev 28:672–682.  https://doi.org/10.1101/gad.238873.114 PubMedPubMedCentralCrossRefGoogle Scholar
  77. Wei L et al (2014) Dicer-like 3 produces transposable element-associated 24-nt siRNAs that control agricultural traits in rice. Proc Natl Acad Sci U S A 111:3877–3882.  https://doi.org/10.1073/pnas.1318131111 PubMedPubMedCentralCrossRefGoogle Scholar
  78. Weinhofer I, Hehenberger E, Roszak P, Hennig L, Kohler C (2010) H3K27me3 profiling of the endosperm implies exclusion of polycomb group protein targeting by DNA methylation. PLoS Genet 6:e1001152.  https://doi.org/10.1371/journal.pgen.1001152 PubMedPubMedCentralCrossRefGoogle Scholar
  79. Yamauchi T et al (2008) Alternative splicing of the rice OsMET1 genes encoding maintenance DNA methyltransferase. J Plant Physiol 165:1774–1782.  https://doi.org/10.1016/j.jplph.2007.12.003 PubMedCrossRefGoogle Scholar
  80. Yamauchi T, Johzuka-Hisatomi Y, Terada R, Nakamura I, Iida S (2014) The MET1b gene encoding a maintenance DNA methyltransferase is indispensable for normal development in rice. Plant Mol Biol 85:219–232.  https://doi.org/10.1007/s11103-014-0178-9 PubMedCrossRefGoogle Scholar
  81. Yan H et al (2010) Genome-wide mapping of cytosine methylation revealed dynamic DNA methylation patterns associated with genes and centromeres in rice. Plant J Cell Mol Biol 63:353–365.  https://doi.org/10.1111/j.1365-313X.2010.04246.x CrossRefGoogle Scholar
  82. Yan D et al (2015) Curved chimeric palea 1 encoding an EMF1-like protein maintains epigenetic repression of OsMADS58 in rice palea development. Plant J Cell Mol Biol 82:12–24.  https://doi.org/10.1111/tpj.12784 CrossRefGoogle Scholar
  83. Yang J et al (2013) OsVIL2 functions with PRC2 to induce flowering by repressing OsLFL1 in rice. Plant J Cell Mol Biol 73:566–578.  https://doi.org/10.1111/tpj.12057 CrossRefGoogle Scholar
  84. Yin BL et al (2008) Integration of cytological features with molecular and epigenetic properties of rice chromosome 4. Mol Plant 1:816–829.  https://doi.org/10.1093/mp/ssn037 PubMedCrossRefGoogle Scholar
  85. Yokoo T et al (2014) Se14, encoding a JmjC domain-containing protein, plays key roles in long-day suppression of rice flowering through the demethylation of H3K4me3 of RFT1. PLoS One 9:e96064.  https://doi.org/10.1371/journal.pone.0096064 PubMedPubMedCentralCrossRefGoogle Scholar
  86. Yuan J et al (2017) Both maternally and paternally imprinted genes regulate seed development in rice. New Phytol.  https://doi.org/10.1111/nph.14510
  87. Zemach A et al (2010a) Local DNA hypomethylation activates genes in rice endosperm. Proc Natl Acad Sci U S A 107:18729–18734.  https://doi.org/10.1073/pnas.1009695107 PubMedPubMedCentralCrossRefGoogle Scholar
  88. Zemach A, McDaniel IE, Silva P, Zilberman D (2010b) Genome-wide evolutionary analysis of eukaryotic DNA methylation. Science 328:916–919.  https://doi.org/10.1126/science.1186366 PubMedCrossRefGoogle Scholar
  89. 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.  https://doi.org/10.1186/gb-2009-10-6-r62 PubMedPubMedCentralCrossRefGoogle Scholar
  90. Zhang W et al (2012a) High-resolution mapping of open chromatin in the rice genome. Genome Res 22:151–162.  https://doi.org/10.1101/gr.131342.111 PubMedPubMedCentralCrossRefGoogle Scholar
  91. Zhang L et al (2012b) Identification and characterization of an epi-allele of FIE1 reveals a regulatory linkage between two epigenetic marks in rice. Plant Cell 24:4407–4421.  https://doi.org/10.1105/tpc.112.102269 PubMedPubMedCentralCrossRefGoogle Scholar
  92. Zhang X, Sun J, Cao X, Song X (2015) Epigenetic mutation of RAV6 affects leaf angle and seed size in rice. Plant Physiol 169:2118–2128.  https://doi.org/10.1104/pp.15.00836 PubMedPubMedCentralGoogle Scholar
  93. Zhang H, Lu Y, Zhao Y, Zhou DX (2016a) OsSRT1 is involved in rice seed development through regulation of starch metabolism gene expression. Plant Sci Int J Exp Plant Biol 248:28–36.  https://doi.org/10.1016/j.plantsci.2016.04.004 Google Scholar
  94. Zhang H et al (2016b) Transposon-derived small RNA is responsible for modified function of WRKY45 locus. Nat Plant 2:16016.  https://doi.org/10.1038/nplants.2016.16 CrossRefGoogle Scholar
  95. Zhang K et al (2017a) Differential deposition of H2A.Z in combination with histone modifications within related genes in Oryza sativa callus and seedling. Plant J Cell Mol Biol 89:264–277.  https://doi.org/10.1111/tpj.13381 CrossRefGoogle Scholar
  96. Zhang L et al (2017b) A natural tandem array alleviates epigenetic repression of IPA1 and leads to superior yielding rice. Nat Commun 8:14789.  https://doi.org/10.1038/ncomms14789 PubMedPubMedCentralCrossRefGoogle Scholar
  97. Zhao C et al (2012) Molecular cloning and characterization of OsCHR4, a rice chromatin-remodeling factor required for early chloroplast development in adaxial mesophyll. Planta 236:1165–1176.  https://doi.org/10.1007/s00425-012-1667-1 PubMedCrossRefGoogle Scholar
  98. Zheng X et al (2013) Transgenerational variations in DNA methylation induced by drought stress in two rice varieties with distinguished difference to drought resistance. PLoS One 8:e80253.  https://doi.org/10.1371/journal.pone.0080253 PubMedPubMedCentralCrossRefGoogle Scholar
  99. Zheng M et al (2015) DEFORMED FLORAL ORGAN1 (DFO1) regulates floral organ identity by epigenetically repressing the expression of OsMADS58 in rice (Oryza sativa). New Phytol 206:1476–1490.  https://doi.org/10.1111/nph.13318 PubMedCrossRefGoogle Scholar
  100. Zhong X et al (2013) The rice NAD(+)-dependent histone deacetylase OsSRT1 targets preferentially to stress- and metabolism-related genes and transposable elements. PLoS One 8:e66807.  https://doi.org/10.1371/journal.pone.0066807 PubMedPubMedCentralCrossRefGoogle Scholar
  101. Zhou DX, Hu Y (2010) Regulatory function of histone modifications in controlling rice gene expression and plant growth. Rice 3:103–111CrossRefGoogle Scholar
  102. Zhou S et al (2016) Cooperation between the H3K27me3 chromatin mark and non-CG methylation in epigenetic regulation. Plant Physiol 172:1131–1141.  https://doi.org/10.1104/pp.16.01238 PubMedPubMedCentralGoogle Scholar
  103. Zhou S et al (2017) Rice homeodomain protein WOX11 recruits a histone acetyltransferase 1 complex to establish programs of cell proliferation of crown root meristem. Plant Cell (in press)Google Scholar
  104. Zong W, Zhong X, You J, Xiong L (2013) Genome-wide profiling of histone H3K4-tri-methylation and gene expression in rice under drought stress. Plant Mol Biol 81:175–188.  https://doi.org/10.1007/s11103-012-9990-2 PubMedCrossRefGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2018

Authors and Affiliations

  1. 1.Jingchu University of TechnologyJingmenChina
  2. 2.Institute of Plant Science Paris-SaclayUniversity Paris-sud 11OrsayFrance
  3. 3.National Key Laboratory of Crop Genetic ImprovementHuazhong Agricultural UniversityWuhanChina

Personalised recommendations