Rice Epigenomics: How Does Epigenetic Manipulation of Crops Contribute to Agriculture?

Part of the RNA Technologies book series (RNATECHN)


Production of rice (Oryza sativa)—the staple food of over half the world’s population, especially those living in poverty—must continue to increase to meet the rising demand. The availability of a wide variety of natural rice resources has enabled highly efficient breeding approaches that have successfully improved productivity as well as biotic and abiotic stress tolerances. However, recent changes in global climate tendencies are imposing additional pressures on rice production, with the need for varieties showing unprecedented characteristics to counter adverse environments calling for innovative responses from breeders and researchers. Recent developments in epigenetic research in Arabidopsis thaliana have provided a plethora of data on epigenetic regulation in gene expression and development, paving the way to crop improvement via epigenetic manipulation. At ~400 Mb, the rice genome is the smallest among cereal crops and is relatively tractable with current molecular genetics techniques. This chapter begins by comparing characteristics of the rice genome and epigenome with those of Arabidopsis, before presenting some examples of epigenetic regulation in plants, with the emphasis on agriculturally important traits including abiotic stress responses. Most molecular studies on epigenetic modifications affecting plant phenotypes have been done in Arabidopsis, but examples of epigenetic regulation of agriculturally important traits in rice are accumulating rapidly. Current problems and difficulties in applying epigenetic manipulation to rice and ensuring stable maintenance of the modified epigenetic states to secure given agricultural traits under natural conditions will then be discussed.


Abiotic stress Crop breeding Epigenome Rice Transgenerational epigenome inheritance 



I thank Helen Rothnie for comments on the manuscript and Rie Takahashi for technical assistance. This work was supported by a grant (CREST) from Japan Science and Technology Agency to YH.


  1. Akimoto K, Katakami H, Kim HJ et al (2007) Epigenetic inheritance in rice plants. Ann Bot 100:205–217PubMedPubMedCentralCrossRefGoogle Scholar
  2. Bender J, Fink GR (1995) Epigenetic control of an endogenous gene family is revealed by a novel blue fluorescent mutant of Arabidopsis. Cell 83:725–734PubMedCrossRefGoogle Scholar
  3. Blevins T, Pontvianne F, Cocklin R et al (2014) A two-step process for epigenetic inheritance in Arabidopsis. Mol Cell 54:30–42PubMedPubMedCentralCrossRefGoogle Scholar
  4. Boyko A, Kovalchuk I (2011) Genome instability and epigenetic modification-heritable responses to environmental stress? Curr Opin Plant Biol 14:260–266PubMedCrossRefGoogle Scholar
  5. Cabello JV, Lodeyro AF, Zurbriggen MD (2014) Novel perspectives for the engineering of abiotic stress tolerance in plants. Curr Opin Biotechnol 26:62–70PubMedCrossRefGoogle Scholar
  6. Campos EI, Stafford JM, Reinberg D (2014) Epigenetic inheritance: histone bookmarks across generations. Trends Cell Biol 24:664–674PubMedPubMedCentralCrossRefGoogle Scholar
  7. Cao X, Jacobsen SE (2002) Role of the Arabidopsis DRM methyltransferases in de novo DNA methylation and gene silencing. Curr Biol 12:1138–1144PubMedCrossRefGoogle Scholar
  8. Chen X (2009) Small RNAs and their roles in plant development. Annu Rev Cell Dev Biol 25:21–44PubMedPubMedCentralCrossRefGoogle Scholar
  9. Chen ZJ (2013) Genomic and epigenetic insights into the molecular bases of heterosis. Nat Rev Genet 14:471–482PubMedCrossRefGoogle Scholar
  10. Chen LT, Wu K (2010) Role of histone deacetylases HDA6 and HDA19 in ABA and abiotic stress response. Plant Signal Behav 5:1318–1320PubMedPubMedCentralCrossRefGoogle Scholar
  11. Chen X, Zhou DX (2013) Rice epigenomics and epigenetics: challenges and opportunities. Curr Opin Plant Biol 16:164–169PubMedCrossRefGoogle Scholar
  12. Chen LT, Luo M, Wang YY et al (2010) Involvement of Arabidopsis histone deacetylase HDA6 in ABA and salt stress response. J Exp Bot 61:3345–3353PubMedPubMedCentralCrossRefGoogle Scholar
  13. Chen X, Liu X, Zhao Y et al (2015) Histone H3K4me3 and H3K27me3 regulatory genes control stable transmission of an epimutation in rice. Sci Rep 5:13251PubMedPubMedCentralCrossRefGoogle Scholar
  14. Chinnusamy V, Zhu JK (2009) Epigenetic regulation of stress responses in plants. Curr Opin Plant Biol 12:133–139PubMedPubMedCentralCrossRefGoogle Scholar
  15. Chinnusamy V, Dalal M, Zhu JK (2014) Epigenetic regulation of abiotic stress responses in plants. In: Jenks MA, Hasegawa PM (eds) Plant abiotic stress, 2nd edn. Wiley, Ames, pp 203–229CrossRefGoogle Scholar
  16. Chung PJ, Kim JK (2009) Epigenetic interaction of OsHDAC1 with the OsNAC6 gene promoter regulates rice root growth. Plant Signal Behav 4:675–677PubMedPubMedCentralCrossRefGoogle Scholar
  17. Chung PJ, Kim YS, Jeong JS et al (2009) The histone deacetylase OsHDAC1 epigenetically regulates the OsNAC6 gene that controls seedling root growth in rice. Plant J 59:764–776PubMedCrossRefGoogle Scholar
  18. Cokus SJ, Feng S, Zhang X et al (2008) Shotgun bisulfite sequencing of the Arabidopsis genome reveals DNA methylation patterning. Nature 452:215–219PubMedPubMedCentralCrossRefGoogle Scholar
  19. Colomé-Tatché M, Cortijo S, Wardenaar R et al (2012) Features of the Arabidopsis recombination landscape resulting from the combined loss of sequence variation and DNA methylation. Proc Natl Acad Sci U S A 109:16240–16245PubMedPubMedCentralCrossRefGoogle Scholar
  20. Cubas P, Vincent C, Coen E (1999) An epigenetic mutation responsible for natural variation in floral symmetry. Nature 401:157–161PubMedCrossRefGoogle Scholar
  21. Cui X, Jin P, Cui X et al (2013) Control of transposon activity by a histone H3K4 demethylase in rice. Proc Natl Acad Sci U S A 110:1953–1958PubMedPubMedCentralCrossRefGoogle Scholar
  22. Dai A (2013) Increasing drought under global warming in observations and models. Nat Climate Change 3:52–58CrossRefGoogle Scholar
  23. Dapp M, Reinders J, Bédiée A et al (2015) Heterosis and inbreeding depression of epigenetic Arabidopsis hybrids. Nat Plants 1:15092PubMedCrossRefGoogle Scholar
  24. Devoto A, Nieto-Rostro M, Xie D et al (2002) COI1 links jasmonate signalling and fertility to the SCF ubiquitin-ligase complex in Arabidopsis. Plant J 32:457–466PubMedCrossRefGoogle Scholar
  25. Ding Y, Wang X, Su L et al (2007) SDG714, a histone H3K9 methyltransferase, is involved in Tos17 DNA methylation and transposition in rice. Plant Cell 19:9–22PubMedPubMedCentralCrossRefGoogle Scholar
  26. Ding B, del Rosario BM, Ning Y et al (2012) HDT701, a histone H4 deacetylase, negatively regulates plant innate immunity by modulating histone H4 acetylation of defense-related genes in rice. Plant Cell 24:3783–3794PubMedPubMedCentralCrossRefGoogle Scholar
  27. Duvick DN (2001) Biotechnology in the 1930s: the development of hybrid maize. Nat Rev Genet 2:69–74PubMedCrossRefGoogle Scholar
  28. Eamans A, Vaistij FE, Jones L (2008) NRPD1a and NRPD1b are required to maintain post-transcriptional RNA silencing and RNA-directed DNA methylation in Arabidopsis. Plant J 55:596–606CrossRefGoogle Scholar
  29. Early KW, Pontvianne F, Wierzbicki AT et al (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 24:1119–1132CrossRefGoogle Scholar
  30. Fedoroff NV (2013) The discovery of transposition. In: Fedoroff NV (ed) Plant transposons and genome dynamics in evolution. Wiley-Blackwell, Ames, pp 3–13CrossRefGoogle Scholar
  31. Feng S, Cokus SJ, Zhang X et al (2010) Conservation and divergence of methylation patterning in plants and animals. Proc Natl Acad Sci U S A 107:8689–8694PubMedPubMedCentralCrossRefGoogle Scholar
  32. Finnegan EJ, Dennis ES (1993) Isolation and identification by sequence homology of a putative cytosine methyltransferase from Arabidopsis thaliana. Nucleic Acids Res 21:2383–2388PubMedPubMedCentralCrossRefGoogle Scholar
  33. Fleury D, Langridge P (2014) QTL and association mapping for plant abiotic stress tolerance: trait characterization and introgression for crop improvement. In: Jenks MA, Hasegawa PM (eds) Plant abiotic stress, 2nd edn. Wiley, Ames, pp 257–287CrossRefGoogle Scholar
  34. Food and Agriculture Organization of the United Nations (2016a) Crop prospects and food situation. No. 2 Junee (
  35. Food and Agriculture Organization of the United Nations (2016b) Food outlook. June 2016 (
  36. Fu W, Wu K, Duan J (2007) Sequence and expression analysis of histone deacetylases in rice. Biochem Biophys Res Commun 356:843–850PubMedCrossRefGoogle Scholar
  37. Fuks F, Burgers WA, Brehm A et al (2000) DNA methyltransferase Dnmt1 associates with histone deacetylase activity. Nat Genet 24:88–91PubMedCrossRefGoogle Scholar
  38. Gerats AG, Huits H, Vrijlandt E et al (1990) Molecular characterization of a nonautonomous transposable element (dTph1) of petunia. Plant Cell 2:1121–1128PubMedPubMedCentralCrossRefGoogle Scholar
  39. Gong Z, Morales-Ruiz T, Ariza RR et al (2002) ROS1, a repressor of transcriptional gene silencing in Arabidopsis encodes a DNA glycosylase/lyase. Cell 111:803–814PubMedCrossRefGoogle Scholar
  40. Gowen JW (1952) Heterosis. A record of researches directed toward explaining and utilizing the vigor of hybrids. Iowa State College Press, AmesCrossRefGoogle Scholar
  41. Gu X, Jiang D, Yang W et al (2011) Arabidopsis homolog of retinoblastoma-associated protein 46/48 associate with a histone deacetylase to act redundantly in chromatin silencing. PLoS Genet 7:e1002366PubMedPubMedCentralCrossRefGoogle Scholar
  42. Habu Y, Ando T, Ito S et al (2015) Epigenomic modification in rice controls meiotic recombination and segregation distortion. Mol Breed 35:103CrossRefGoogle Scholar
  43. Hao Y, Wang H, Qiao S et al (2016) Histone deacetylase HDA6 enhances brassinosteroid signaling by inhibiting the BIN2 kinase. Proc Natl Acad Sci U S A 113:10418–10423PubMedPubMedCentralCrossRefGoogle Scholar
  44. Hauser MT, Aufsatz W, Jonak C et al (2011) Transgenerational epigenetic inheritance in plants. Biochem Biophys Acta 1809:459–468PubMedPubMedCentralGoogle Scholar
  45. He G, Zhu X, Elling AA et al (2010) Global epigenetic and transcriptional trends among two rice subspecies and their reciprocal hybrids. Plant Cell 22:17–33PubMedPubMedCentralCrossRefGoogle Scholar
  46. Hu Y, Qin F, Huang L et al (2009) Rice histone deacetylase genes display specific expression patterns and developmental functions. Biochem Biophys Res Commun 388:266–271PubMedCrossRefGoogle Scholar
  47. Hu L, Li N, Xu C 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 111:10642–10647PubMedPubMedCentralCrossRefGoogle Scholar
  48. Huang X, Yang S, Gong J et al (2016) Genomic architecture of heterosis for yield traits in rice. Nature 537:629–633PubMedCrossRefGoogle Scholar
  49. International Rice Genome Sequencing Project (2005) The map-based sequence of the rice genome. Nature 436:793–800CrossRefGoogle Scholar
  50. Ito H, Gaubert H, Bucher E et al (2011) An siRNA pathway prevents transgenerational retrotransposition in plants subjected to stress. Nature 472:115–119PubMedCrossRefGoogle Scholar
  51. Iwasaki M, Paszkowski J (2014a) Epigenetic memory in plants. EMBO J 33:1987–1998PubMedPubMedCentralCrossRefGoogle Scholar
  52. Iwasaki M, Paszkowski J (2014b) Identification of genes preventing transgenerational transmission of stress-induced epigenetic states. Proc Natl Acad Sci U S A 111:8547–8552PubMedPubMedCentralCrossRefGoogle Scholar
  53. Jang IC, Pahk YM, Song SI 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 33:531–541PubMedCrossRefGoogle Scholar
  54. Jenuwein T, Allis CD (2001) Translating the histone code. Science 293:1074–1080PubMedCrossRefGoogle Scholar
  55. Joshi R, Wani SH, Singh B et al (2016) Transcription factors and plants response to drought stress: current understanding and future directions. Front Plant Sci 7:1029PubMedPubMedCentralCrossRefGoogle Scholar
  56. Jung JH, Park JH, Lee S et al (2013) The cold signaling attenuator HIGH EXPRESSION OF OSMOTICALLY RESPONSIVE GENE1 activates FLOWERING LOCUS C transcription via chromatin remodeling under short-term cold stress in Arabidopsis. Plant Cell 25:4378–4390PubMedPubMedCentralCrossRefGoogle Scholar
  57. Kalisz S, Purugganan MD (2004) Epialleles via DNA methylation: consequences for plant evolution. Trends Ecol Evol 19:309–314PubMedCrossRefGoogle Scholar
  58. Kanno T, Habu Y (2011) siRNA-mediated chromatin maintenance and its function in Arabidopsis thaliana. Biochim Biophys Acta 1809:444–451PubMedCrossRefGoogle Scholar
  59. Kanno T, Yoshikawa M, Habu Y (2013) Locus-specific requirements of DDR complexes for gene-body methylation of TAS genes in Arabidopsis thaliana. Plant Mol Biol Rep 31:1048–1052CrossRefGoogle Scholar
  60. Kasai A, Kasai K, Yumoto S et al (2007) Structural features of GmIRCHS, candidate of the I gene inhibiting seed coat pigmentation in soybean: implications for inducing endogenous RNA silencing of chalcone synthase genes. Plant Mol Biol 64:467–479PubMedCrossRefGoogle Scholar
  61. Kawahara Y, de la Bastide M, Hamilton JP et al (2013) Improvement of the Oryza sativa Nipponbare reference genome using next generation sequence and optical map data. Rice 6:4PubMedPubMedCentralCrossRefGoogle Scholar
  62. Kim To T, Kim JM, Matsui A et al (2011) Arabidopsis HDA6 regulates locus-directed heterochromatin silencing in cooperation with MET1. PLoS Genet 7:e1002055CrossRefGoogle Scholar
  63. Kim W, Latrasse D, Servet C et al (2013) Arabidopsis histone deacetylase HDA9 regulates flowering time through repression of AGL19. Biochem Biophys Res Commun 432:394–398PubMedCrossRefGoogle Scholar
  64. Kim JM, Sasaki T, Ueda M et al (2015) Chromatin changes in response to drought, salinity, heat, and cold stresses in plants. Front Plant Sci 6:114PubMedPubMedCentralGoogle Scholar
  65. Kou HP, Li Y, Song XX et al (2011) Heritable alteration in DNA methylation induced by nitrogen-deficiency stress accompanies enhanced tolerance by progenies to the stress in rice. J Plant Physiol 168:1685–1693PubMedCrossRefGoogle Scholar
  66. Kouzarides T (2007) Chromatin modifications and their function. Cell 128:693–705PubMedCrossRefGoogle Scholar
  67. Krieger U, Lippman ZB, Zamir D (2010) The flowering gene SINGLE FLOWER TRUSS drives heterosis for yield in tomato. Nat Genet 42:459–463PubMedCrossRefGoogle Scholar
  68. Kusaba M, Miyahara K, Iida S et al (2003) Low glutelin content1: a dominant mutation that suppresses the glutelin multigene family via RNA silencing in rice. Plant Cell 15:1455–1467PubMedPubMedCentralCrossRefGoogle Scholar
  69. Law JA, Jacobsen SE (2010) Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nat Rev Genet 11:204–220PubMedPubMedCentralCrossRefGoogle Scholar
  70. Lee WK, Cho MH (2016) Telomere-binding protein regulates the chromosome ends through the interaction with histone deacetylases in Arabidopsis thaliana. Nucleic Acids Res 44:4610–4624PubMedPubMedCentralCrossRefGoogle Scholar
  71. Li X, Wang X, He K et al (2008) High-resolution mapping of epigenetic modifications of the rice genome uncovers interplay between DNA methylation, histone methylation, and gene expression. Plant Cell 20:259–276PubMedPubMedCentralCrossRefGoogle Scholar
  72. Li X, Zhu J, Hu F et al (2012) Single-base resolution maps of cultivated and wild rice methylomes and regulatory roles of DNA methylation on plant gene expression. BMC Genomics 13:300PubMedPubMedCentralCrossRefGoogle Scholar
  73. Lippman Z, Gendrel AV, Black M et al (2004) Role of transposable elements in heterochromatin and epigenetic control. Nature 430:471–476PubMedCrossRefGoogle Scholar
  74. Liu X, Yu CW, Duan J et al (2012) HDA6 directly interacts with DNA methyltransferase MET1 and maintains transposable element silencing in Arabidopsis. Plant Physiol 158:119–129PubMedCrossRefGoogle Scholar
  75. Loidl P (2004) A plant dialect of the histone language. Trends Plant Sci 9:84–90PubMedCrossRefGoogle Scholar
  76. Ma X, Lv S, Zhang C et al (2013) Histone deacetylases and their functions in plants. Plant Cell Rep 32:465–478PubMedCrossRefGoogle Scholar
  77. Mathieu O, Reinders J, Cáikovski M et al (2007) Transgenerational stability of the Arabidopsis epigenome is coordinated by CG methylation. Cell 130:851–862PubMedCrossRefGoogle Scholar
  78. Mehdi S, Derkacheva M, Ramström M et al (2016) The WD40 domain protein MSI1 functions in a histone deacetylase complex to fine-tune abscisic acid signaling. Plant Cell 28:42–54PubMedGoogle Scholar
  79. Melamed-Bessudo C, Levy AA (2012) Deficiency in DNA methylation increases meiotic crossover rates in euchromatic but not in heterochromatic regions in Arabidopsis. Proc Natl Acad Sci U S A 109:E981–E988PubMedPubMedCentralCrossRefGoogle Scholar
  80. Mirouze M, Reinders J, Bucher E et al (2009) Selective epigenetic control of retrotransposition in Arabidopsis. Nature 461:427–430PubMedCrossRefGoogle Scholar
  81. Mirouze M, Paszkowski J (2011) Epigenetic contribution to stress adaptation in plants. Curr Opin Plant Biol 14(3):267–274Google Scholar
  82. Mirouze M, Lieberman-Lazarovich M, Aversano R et al (2012) Loss of DNA methylation affects the recombination landscape in Arabidopsis. Proc Natl Acad Sci U S A 109:5880–5885PubMedPubMedCentralCrossRefGoogle Scholar
  83. Miura A, Yonebayashi S, Watanabe K et al (2001) Mobilization of transposons by a mutation abolishing full DNA methylation in Arabidopsis. Nature 411:212–214PubMedCrossRefGoogle Scholar
  84. Miura K, Agetsuma M, Kitano H et al (2009) A metastable DWARF1 epigenetic mutant affecting plant stature in rice. Proc Natl Acad Sci U S A 106:11218–11223PubMedPubMedCentralCrossRefGoogle Scholar
  85. Moritoh S, Eun CH, Ono A et al (2012) Targeted disruption of an orthologue of DOMAINS REARRANGED METHYLASE 2, OsDRM2, impairs the growth of rice plants by abnormal DNA methylation. Plant J 71:85–98PubMedCrossRefGoogle Scholar
  86. Nagaki K, Cheng Z, Ouyang S et al (2004) Sequencing of a rice centromere uncovers active genes. Nat Gent 36:138–145CrossRefGoogle Scholar
  87. Naito K, Cho E, Yang G et al (2006) Dramatic amplification of a rice transposable element during recent domestication. Proc Natl Acad Sci U S A 103:17620–17625PubMedPubMedCentralCrossRefGoogle Scholar
  88. Nakashima K, Yamaguchi-Shinozaki K, Shinozaki S (2014) The transcriptional regulatory network in the drought response and its crosstalk in abiotic stress responses including drought, cold, and heat. Front Plant Sci 5:170PubMedPubMedCentralCrossRefGoogle Scholar
  89. Nan X, Ng HH, Johnson CA et al (1998) Transcriptional repression by the methyl-CpG-binding protein MeCP2 involves a histone deacetylase complex. Nature 393:386–389PubMedCrossRefGoogle Scholar
  90. Numa H, Yamaguchi K, Shigenobu S et al (2015) Gene body CG and CHG methylation and suppression of centromeric CHH methylation are mediated by DECREASE IN DNA METHYLATION1 in rice. Mol Plant 8:1560–1562PubMedCrossRefGoogle Scholar
  91. Nuthikattu S, McCue AD, Panda K et al (2013) The initiation of epigenetic silencing of active transposable elements is triggered by RDR6 and 21-22 nucleotide small interfering RNAs. Plant Physiol 162:116–131PubMedPubMedCentralCrossRefGoogle Scholar
  92. Ong-Abdullah M, Ordway JM, Jiang N et al (2015) Loss of Karma transposon methylation underlies the mantled somaclonal variant of oil palm. Nature 525:533–537PubMedPubMedCentralCrossRefGoogle Scholar
  93. Ono A, Yamaguchi K, Fukada-Tanaka S et al (2012) A null mutation of ROS1a for DNA demethylation in rice is not transmittable to progeny. Plant J 71:564–574PubMedCrossRefGoogle Scholar
  94. Osakabe Y, Osakabe K (2015) Genome editing with engineered nucleases in plants. Plant Cell Physiol 56:389–400PubMedCrossRefGoogle Scholar
  95. Ou X, Zhang Y, Xu C 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:e41143PubMedPubMedCentralCrossRefGoogle Scholar
  96. Paszkowski J, Grossniklaus U (2011) Selected aspects of transgenerational epigenetic inheritance and resetting in plants. Curr Opin Plant Biol 14:195–203PubMedCrossRefGoogle Scholar
  97. Perrella G, Consiglio MF, Aiese-Cigliano R et al (2010) Histone hyperacetylation affects meiotic recombination and chromosome segregation in Arabidopsis. Plant J 62:796–806PubMedCrossRefGoogle Scholar
  98. Probst AV, Fagard M, Proux F et al (2004) Arabidopsis histone deacetylase HDA6 is required for maintenance of transcriptional gene silencing and determines nuclear organization of rDNA repeats. Plant Cell 16:1021–1034PubMedPubMedCentralCrossRefGoogle Scholar
  99. Qin FJ, Sun QW, Huang LM (2010) Rice SUVH histone methyltransferase genes display specific functions in chromatin modification and retrotransposon repression. Mol Plant 3:773–782PubMedCrossRefGoogle Scholar
  100. Sano H (2010) Inheritance of acquired traits in plants, reinstatement of Lamarck. Plant Signal Behav 5:346–348PubMedPubMedCentralCrossRefGoogle Scholar
  101. Sasaki T, Wu J, Mizuno H et al (2008) The rice genome sequence as an indispensable tool for crop improvement. In Hirano HY et al (eds) Rice biology in the genomics era. Biotechnology in agriculture and forestry. vol 62 Springer, Berlin, pp 3–12Google Scholar
  102. Saze H, Kakutani T (2007) Heritable epigenetic mutation of a transposon-flanked Arabidopsis gene due to lack of the chromatin-remodeling factor DDM1. EMBO J 26:3641–3652PubMedPubMedCentralCrossRefGoogle Scholar
  103. Shriram V, Kumar V, Devarumath RM et al (2016) MicroRNAs as potential targets for abiotic stress tolerance in plants. Front Plant Sci 7:817PubMedPubMedCentralCrossRefGoogle Scholar
  104. Singh D, Laxmi A (2015) transcriptional regulation of drought responses: a tortuous network of transcriptional factors. Front Plant Sci 6:895PubMedPubMedCentralGoogle Scholar
  105. Song X, Wang D, Ma L et al (2012) Rice RNA-dependent RNA polymerase 6 acts in small RNA biogenesis and spikelet development. Plant J 71:378–389PubMedGoogle Scholar
  106. Sridha S, Wu K (2006) Identification of AtHD2C as a novel regulator of abscisic acid responses in Arabidopsis. Plant J 46:124–133PubMedCrossRefGoogle Scholar
  107. Stokes TL, Richards EJ (2002) Induced instability of two Arabidopsis constitutive pathogen-response alleles. Proc Natl Acad Sci U S A 99:7792–7796PubMedPubMedCentralCrossRefGoogle Scholar
  108. Stroud H, Greenberg MVC, Feng S et al (2013) Comprehensive analysis of silencing mutants reveals complex regulation of the Arabidopsis methylome. Cell 152:352–364PubMedPubMedCentralCrossRefGoogle Scholar
  109. Tan F, Zhou C, Zhou Q et al (2016) Analysis of chromatin regulators reveals specific features of rice DNA methylation pathways. Plant Physiol 171:2041–2054PubMedCrossRefGoogle Scholar
  110. Till BJ, Cooper J, Tai TH et al (2007) Discovery of chemically induced mutations in rice by TILLING. BMC Plant Biol 7:19PubMedPubMedCentralCrossRefGoogle Scholar
  111. To TK, Nakaminami K, Kim JM et al (2011) Arabidopsis HDA6 is required for freezing tolerance. Biochem Biophys Res Commun 406:414–419PubMedCrossRefGoogle Scholar
  112. Todaka D, Shinozaki K, Yamaguchi-Shinozaki K (2015) Recent advances in the dissection of drought-stress regulation networks and strategies for development of drought-tolerant transgenic plants. Front Plant Sci 6:84PubMedPubMedCentralCrossRefGoogle Scholar
  113. Tsukahara S, Kobayashi A, Kawabe A et al (2009) Bursts of retrotransposition reproduced in Arabidopsis. Nature 461:423–426PubMedCrossRefGoogle Scholar
  114. Vaucheret H (2006) Post-transcriptional small RNA pathways in plants: mechanisms and regulations. Genes Dev 20:759–771PubMedCrossRefGoogle Scholar
  115. Vongs A, Kakutani T, Marienssen RA et al (1993) Arabidopsis thaliana DNA methylation mutants. Science 260:1926–1928PubMedCrossRefGoogle Scholar
  116. Vriet C, Henning L, Laloi C (2015) Stress-induced chromatin changes in plants: of memories, metabolites and crop improvement. Cell Mol Life Sci 72:1261–1273PubMedCrossRefGoogle Scholar
  117. Wang Z, Cao H, Chen F et al (2014) The roles of histone acetylation in seed performance and plant development. Plant Physiol Biochem 84:125–133PubMedCrossRefGoogle Scholar
  118. Wang N, Ning S, Wu J et al (2015) An epiallele ay cly1 affects the expression of floret closing (cleistogamy) in barley. Genetics 199:95–104PubMedCrossRefGoogle Scholar
  119. Wei L, Gu L, Sing X 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 111:3877–3882PubMedPubMedCentralCrossRefGoogle Scholar
  120. Wu K, Zhang L, Zhou C et al (2008) HDA6 is required for jasmonate response, senescence and flowering in Arabidopsis. J Exp Bot 59:225–234PubMedCrossRefGoogle Scholar
  121. Wu L, Zhou H, Zhang Q et al (2010) DNA methylation mediated by a microRNA pathway. Mol Cell 38:465–475PubMedCrossRefGoogle Scholar
  122. Wu L, Mao L, Qi Y (2012) Roles of DICER-LIKE and ARGONAUTE proteins in TAS-derived small interfering RNA-triggered DNA methylation. Plant Physiol 160:990–999Google Scholar
  123. Xue Y, Wong J, Moreno GT et al (1998) NURD, a novel complex with both ATP-dependent chromatin-remodeling and histone deacetylase activities. Mol Cell 2:851–861PubMedCrossRefGoogle Scholar
  124. Yamamoto T, Yano M (2008) Detection and molecular cloning of genes underlying quantitative phenotypic variations in rice. In: Hirano HY et al (eds) Rice biology in the genomics era, Biotechnology in agriculture and forestry, vol 62. Springer, Berlin, pp 295–308Google Scholar
  125. Yelina NE, Choi K, Chelysheva L et al (2012) Epigenetic remodeling of meiotic crossover frequency in Arabidopsis thaliana DNA methyltransferase mutants. PLoS Genet 8:e1002844PubMedPubMedCentralCrossRefGoogle Scholar
  126. Zemach A, McDaniel IE, Silva P et al (2010) Genome-wide evolutionary analysis of eukaryotic DNA methylation. Science 328:916–919PubMedCrossRefGoogle Scholar
  127. Zhang Y, Huang Y, Zhang L et al (2004) Structural features of the rice chromosome 4 centromere. Nucleic Acids Res 32:2023–2030PubMedPubMedCentralCrossRefGoogle Scholar
  128. Zhang L, Cheng Z, Qin R et al (2012) Identification and characterization of an epi-allele of FIE1 reveals a regulatory linkage between two epigenetic marks in rice. Plant Cell 24:4407–4421PubMedPubMedCentralCrossRefGoogle Scholar
  129. Zhang X, Sun J, Cao X et al (2015) Epigenetic mutation of RAV6 affects leaf angle and seed size in rice. Plant Physiol 169:2118–2128PubMedPubMedCentralGoogle Scholar
  130. Zhang Q, Li Y, Xu T et al (2016) The chromatin remodeler DDM1 promotes hybrid vigor by regulating salicylic acid metabolism. Cell Discov 2:16027PubMedPubMedCentralCrossRefGoogle Scholar
  131. Zhao Y, Zhou DX (2012) Epigenomic modification and epigenetic regulation in rice. J Genet Genomics 39:307–315PubMedCrossRefGoogle Scholar
  132. Zhao J, Li M, Gu D et al (2016) Involvement of rice histone deacetylase HDA705 in seed germination and in response to ABA and abiotic stresses. Biochem Biophys Res Commun 470:439–444PubMedCrossRefGoogle Scholar
  133. Zheng B, Wang Z, Li S et al (2009) Intergenic transcription by RNA polymerase II coordinates Pol IV and Pol V in siRNA-directed transcriptional gene silencing in Arabidopsis. Genes Dev 23:2850–2860PubMedPubMedCentralCrossRefGoogle Scholar
  134. Zheng Y, Ding Y, Sun X et al (2016) Histone deacetylase HDA9 negatively regulates salt and drought stress responsiveness in Arabidopsis. J Exp Bot 67:1703–1713PubMedCrossRefGoogle Scholar
  135. Zhong X, Zhang H, Zhao Y et al (2013) The rice NAD+-dependent histone deacetylase OsSRT1 targets preferentially to stress- and metabolism-related genes and transposable elements. PLoS One 8:e66807PubMedPubMedCentralCrossRefGoogle Scholar
  136. Zhou C, Zhang L, Duan J et al (2005) HISTONE DEACETYLASE19 is involved in jasmonic acid and ethylene signaling of pathogen response in Arabidopsis. Plant Cell 17:1196–1204PubMedPubMedCentralCrossRefGoogle Scholar
  137. Zhu Z, An F, Feng Y et al (2011) Derepression of ethylene-stabilized transcription factors (EIN3/EIL1) mediates jasmonate and ethylene signaling synergy in Arabidopsis. Proc Natl Acad Sci U S A 108:12539–12544PubMedPubMedCentralCrossRefGoogle Scholar
  138. Zuccolo A, Sebastian A, Talag J et al (2007) Transposable element distribution, abundance and role in genome size variation in the genus Oryza. BMC Evol Biol 7:152PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG 2017

Authors and Affiliations

  1. 1.Institute of Agrobiological Sciences, National Institute of Agriculture and Food Research OrganizationTsukubaJapan

Personalised recommendations