Advertisement

Journal of Genetics

, Volume 92, Issue 3, pp 629–666 | Cite as

Roles, and establishment, maintenance and erasing of the epigenetic cytosine methylation marks in plants

  • SUSHIL KUMAREmail author
  • RENU KUMARI
  • VISHAKHA SHARMA
  • VINAY SHARMA
Review Article

Abstract

Heritable information in plants consists of genomic information in DNA sequence and epigenetic information superimposed on DNA sequence. The latter is in the form of cytosine methylation at CG, CHG and CHH elements (where H = A, T or C) and a variety of histone modifications in nucleosomes. The epialleles arising from cytosine methylation marks on the nuclear genomic loci have better heritability than the epiallelic variation due to chromatin marks. Phenotypic variation is increased manifold by epiallele comprised methylomes. Plants (angiosperms) have highly conserved genetic mechanisms to establish, maintain or erase cytosine methylation from epialleles. The methylation marks in plants fluctuate according to the cell/tissue/organ in the vegetative and reproductive phases of plant life cycle. They also change according to environment. Epialleles arise by gain or loss of cytosine methylation marks on genes. The changes occur due to the imperfection of the processes that establish and maintain the marks and on account of spontaneous and stress imposed removal of marks. Cytosine methylation pattern acquired in response to abiotic or biotic stress is often inherited over one to several subsequent generations. Cytosine methylation marks affect physiological functions of plants via their effect(s) on gene expression levels. They also repress transposable elements that are abundantly present in plant genomes. The density of their distribution along chromosome lengths affects meiotic recombination rate, while their removal increases mutation rate. Transposon activation due to loss of methylation causes rearrangements such that new gene regulatory networks arise and genes for microRNAs may originate. Cytosine methylation dynamics contribute to evolutionary changes. This review presents and discusses the available evidence on origin, removal and roles of cytosine methylation and on related processes, such as RNA directed DNA methylation, imprinting, paramutation and transgenerational memory in plants.

Keywords

cytosine methylation DNA methylation mechanisms DNA demethylation mechanisms Darwinian-cum-Lamarckian evolution epialleles epigenetic modifications genetic recombination heritable induced defence mutational hotspots transgenerational inheritance 

Notes

Acknowledgments

Authors thank the Indian National Science Academy and the Council of Scientific and Industrial Research, Government of India, for the scientistship schemes to SK, and Department of Biotechnology and SKA Institution for Research, Education and Development for Postgraduate fellowships respectively to RK and VS.

References

  1. Agboola R. S., Kimatu J. N., Liao Y. C. and Liu B. 2012 Morphological and cytosine DNA methylation changes induced by combined effect of boron (B) and salt toxicity in Sorghum bicolor inbred line. Afr. J. Biotech. 11, 10874–10881.Google Scholar
  2. Agius F., Kapoor A. and Zhu J. K. 2006 Role of the Arabidopsis DNA glycosylases/lyase ROS1 in active DNA demethylation. Proc. Natl. Acad. Sci. USA 103, 11796–11801.PubMedGoogle Scholar
  3. Akimoto K., Katakami H., Kim H. J., Ogawa E., Sano C. M., Wada Y. and Sano H. 2007 Epigenetic inheritance in rice plants. Ann. Bot. (Lond.) 100, 205–217.Google Scholar
  4. Alina S., Sgorbati S., Santagostino A., Labra M., Ghiani A. and Citterio S. 2004 Specific hypomethylation of DNA is induced by heavy metals in white clover and industrial hemp. Physiol. Plant 121, 472–480.Google Scholar
  5. Alleman M., Sidorenko L., McGinnis K., Seshadri V., Dorweiler J. E., White J. et al. 2006 An RNA-dependent RNA polymerase is required for paramutation in maize. Nature 442, 295–298.PubMedGoogle Scholar
  6. Arber W. and Linn S. 1969 DNA modification and restriction. Annu. Rev. Biochem. 38, 467–500.PubMedGoogle Scholar
  7. Aufsatz W., Mette M. F., van der Winden J., Matzke M. and Matzke A. J. 2002 HDA6, a putative histone deacetylase needed to enhance DNA methylation induced by double-stranded RNA. EMBO J. 21, 6832–6841.PubMedGoogle Scholar
  8. Aufsatz W., Mette M. F., Matzke A. J. and Matzke M. 2004 The role of MET1 in RNA-directed de novo and maintenance methylation of CG dinucleotides. Plant Mol. Biol. 54, 793–804.PubMedGoogle Scholar
  9. Ausin I., Mockler T. C., Chory J. and Jacobsen S. E. 2009 IDN1 and IDN2 are required for de novo DNA methylation in Arabidopsis thaliana. Nat. Struct. Mol. Biol. 16, 1325–1327.PubMedCentralPubMedGoogle Scholar
  10. Avivi L. and Feldman M. 1980 Arrangement of chromosomes in the interphase nucleus of plants. Hum. Genet. 55, 281–295.PubMedGoogle Scholar
  11. Bairu M. W., Aremu A. O. and van Staden J. 2011 Somaclonal variation in plants: causes and detection methods. Plant Growth Regul. 63, 147–173.Google Scholar
  12. Bauer M. J. and Fischer R. L. 2011 Genome demethylation and imprinting in the endosperm. Curr. Opin. Plant Biol. 14, 162–167.PubMedCentralPubMedGoogle Scholar
  13. Becker C., Hagmann J., Muller J., Koenig D., Stegle O., Borgwardt K. and Weigel D. 2011 Spontaneous epigenetic variation in the Arabidopsis thaliana methylome. Nature 480, 245–249.PubMedGoogle Scholar
  14. Berger S. L. 2007 The complex language of chromatin regulation during transcription. Nature 447, 407–412.PubMedGoogle Scholar
  15. Berger F. and Twell D. 2011 Germline specification and function in plants. Ann. Rev. Plant Biol. 62, 461–484.Google Scholar
  16. Bernstein B. E., Meissner A. and Lander E. S. 2006 The mammalian epigenome. Cell 128, 669–681.Google Scholar
  17. Bhutani N., Burns D. M. and Blau H. M. 2011 DNA demethylation dynamics. Cell 146, 866–872.PubMedCentralPubMedGoogle Scholar
  18. Bies-Etheve N., Pontier D., Lahmy S., Picart C., Vega D., Cooke R. and Lagrange T. 2009 RNA-directed DNA methylation requires an AGO4-interacting member of SPT5 elongation factor. EMBO Rep. 10, 649–654.PubMedCentralPubMedGoogle Scholar
  19. Billichak A., Ilnystkyy Y., Hollunder J. and Kovalchuk I. 2012 The progeny of Arabidopsis thaliana plants exposed to salt exhibit changes in DNA methylation, histone modifications and gene expression. PLoS ONE 7, e30515.Google Scholar
  20. Boyko A., Kathiria P., Zemp F. J., Yao Y., Pogribny I. and Kovalchuk I. 2007 Transgenerational changes in the genome stability and methylation in pathogen-infected plants. Nucleic Acids Res. 35, 1714–1725.PubMedCentralPubMedGoogle Scholar
  21. Boyko A., Blevins T., Yao Y., Golubov A., Bilichak A., Ilnystkyy Y. et al. 2010 Transgenerational adaptation of Arabidopsis to stress requires DNA methylation and the functions of dicer-like proteins. PLoS ONE 5, e9514.Google Scholar
  22. Brenet F., Moh M., Funk P., Feierstein F., Viale A. J., Socci N. D. and Scandura J. M. 2011 DNA methylation of the first exon is tightly linked to transcriptional silencing. PLoS ONE 6, e14524.Google Scholar
  23. Brown J. C. L., De Decker M. M. and Fieldes M. A. 2008 A comparative analysis of developmental profiles for DNA methylation in 5-azacytidine-induced early flowering flax lines and their control. Plant Sci. 175, 217–225.Google Scholar
  24. Brutnell T. P., May B. P. and Dellaporta S. L. 1997 The Ac-st2 element of maize exhibits a positive dosage effect and epigenetic regulation. Genetics 147, 823–834.PubMedGoogle Scholar
  25. Brzeski J. and Jerzmanowski A. 2003 Deficient in DNA methylation 1 (DDM1) defines a noval family of chromatin remodelling factors. J. Biol. Chem. 278, 823–828.PubMedGoogle Scholar
  26. Calarco J. P., Borges F., Donoghue M. T., Van Ex F., Jullien P. E., Lopes T. et al. 2012 Reprogramming of DNA methylation in pollen guides epigenetic inheritance via small RNA. Cell 151, 194–205.PubMedCentralPubMedGoogle Scholar
  27. Calonji M. and Sung Z. R. 2006 Complexity beneath the silence. Curr. Opin. Plant Biol. 9, 530–537.Google Scholar
  28. Cao X. and Jacobsen S. E. 2002a Locus specific control of asymmetric and CpNpG methylation by DRM and CMT3 methyltransferase genes. Proc. Natl. Acad. Sci. USA 99, 16491–16498.PubMedGoogle Scholar
  29. Cao X. and Jacobsen S. E. 2002b Role of the Arabidopsis DRM methyltransferase in de novo DNA methylation and gene silencing. Curr. Biol. 12, 1138–1144.PubMedGoogle Scholar
  30. Cao X., Aufsatz W., Zilberman D., Mette M. F., Huang M. S., Matzke M. and Jacobsen S. E. 2003 Role of DRM and CMT3 methyltransferases in RNA-directed DNA methylation. Curr. Biol. 13, 2212–2217.PubMedGoogle Scholar
  31. Cao D., Gao X., Liu J., Kimatu J. N., Geng S., Wang X. et al. 2011 Methylation sensitive amplified polymorphism (MSAP) reveals that alkali stress triggers more DNA hypomethylation levels in cotton (Gossypium hirsutum L.) roots than salt stress. Afr. J. Biotech. 10, 18971–18980.Google Scholar
  32. Chan S. W., Henderson I. R. and Jacobsen S. E. 2005 Gardening the genome DNA methylation in Arabidopsis thaliana. Nat. Rev. Genet. 6, 351–360.PubMedGoogle Scholar
  33. Chan S. W., Henderson I. R., Zhang X., Shah G., Chien J. S. and Jacobsen S. E. 2006a RNAi, DRD1 and histone methylation actively target developmentally important non-CG DNA methylation in Arabidopsis. PLoS Genet. 2, e83.Google Scholar
  34. Chan S. W., Zhang X., Bernatavichute Y. V. and Jacobsen S. E. 2006b Two-step recruitment of RNA-directed DNA methylation to tandem repeats. PLoS Biol. 4, e363.Google Scholar
  35. Chandler V. L. 2007 Paramutation: from maize to mice. Cell 128, 641–645.PubMedGoogle Scholar
  36. Choi C. S. and Sano H. 2007 Abiotic-stress induces demethylation and transcriptional activation of a gene encoding a glycerophosphodiesterase-like protein in tobacco plants. Mol. Genet. Genomics 277, 589–600.PubMedGoogle Scholar
  37. Choi Y., Gehring M., Johnson L., Hannon M., Harada J. J., Goldberg R. B. et al. 2002 DEMETER, a DNA glycosylase domain protein, is required for endosperm gene imprinting and seed viability in Arabidopsis. Cell 110, 33–42.PubMedGoogle Scholar
  38. Chuck G. and O’Connor D. 2010 Small RNAs going the distance during plant development. Curr. Opin. Plant Biol. 13, 40–45.PubMedGoogle Scholar
  39. Colome-Tatche M., Cortijo S., Wardenaar R., Morgado L., Lahouze B., Sarazin A. et al. 2012 Features of the Arabidopsis recombination landscape resulting from the combined loss of sequence variation and DNA methylation. Proc. Natl. Acad. Sci. USA 109, 16240–16245.Google Scholar
  40. Coming D. E. 1980 Arrangement of chromatin in the nucleus. Hum. Genet. 53, 131–143.Google Scholar
  41. Conde D., Gonzalez-Melendi P. and Allona I. 2013 Poplar stems show opposite epigenetic patterns during winter dormancy and vegetative growth. Trees 27, 311–320.Google Scholar
  42. Cremer T., Cremer C., Schneider T., Baumann H., Hens L. and Kirsch-Volders M. 1982 Analysis of chromosome positions in the interphase nucleus of Chinese hamster cells by laser UV-microirradiation experiments. Hum. Genet. 62, 201–209.PubMedGoogle Scholar
  43. Cubas P., Vincent C. and Coen E. 1999 An epigenetic mutation responsible for natural variation in floral symmetry. Nature 401, 157–161.PubMedGoogle Scholar
  44. Dalakouras A., Dadami E., Zwiebel M., Krczal G. and Wassenegger M. 2012 Transgenerational maintenance of transgene body CG but not CHG and CHH methylation. Epigenetics 7, 1071–1078.PubMedGoogle Scholar
  45. Darwin C. 1859 On the origin of species, 1st edition. Murray, London, UK.Google Scholar
  46. Deal R. B. and Henikoff S. 2011 Histone variants and modifications in plant gene regulation. Curr. Opin. Plant Biol. 14, 116–122.PubMedCentralPubMedGoogle Scholar
  47. Dowen R. H., Pelizzola M., Schmitz R. J., Lister R., Dowen J. M., Nery J. R. et al. 2012 Widespread dynamic DNA methylation in response to biotic stress. Proc. Natl. Acad. Sci. USA 109, E2183–E2191.Google Scholar
  48. Duan C. G., Fang Y. Y., Zhou B. J., Zhao J. H., Hou W. N., Zhu H. et al. 2012 Suppression of Arabidopsis ARGONAUTE 1-mediated slicing, transgene-induced RNA silencing, and DNA methylation by distinct domains of the Cucumber mosaic virus 2b proteins. Plant Cell 24, 259–274.Google Scholar
  49. Dyachenko O. V., Zakharchenko N. S., Shevchuk T. V., Bohnert H. J., Cushman J. C. and Buryanov Y. I. 2006 Effect of hypermethylation of CCWGG sequences in DNA of Mesembryanthemum crystallinum plants on their adaptation to salt stress. Biochemistry (Moscow) 71, 461–465.Google Scholar
  50. El-Shami M., Pontier D., Lahmy S., Braun L., Picart C., Vega D. et al. 2007 Reiterated WG/GW motifs from functionally and evolutionarily conserved ARGONAUTE-binding platforms in RNAi-related components. Genes Dev. 21, 2539–2544.Google Scholar
  51. Erhard Jr K. F., Stonaker J. L., Parkinson S. E., Lim J. P., Hale C. J. and Hollick J. B. 2009 RNA polymerase IV functions in paramutation in Zea mays. Science 323, 1201–1205.PubMedGoogle Scholar
  52. Eun C. H., Takagi K., Park K. I., Maekawa M., Iida S. and Tsugano K. 2012 Activation and epigenetic regulation of DNA transposon nDart1 in rice. Plant Cell Physiol. 53, 857–868.PubMedGoogle Scholar
  53. Fang J. G. and Chao C. T. 2007 Methylation-sensitive amplification polymorphism in date palms (Phoenix dactylifera L.) and their off-shoots. Plant Biol. (Stuttg) 9, 526–533.Google Scholar
  54. Feng S., Jacobsen S. E. and Reik W. 2010 Epigenetic reprogramming in plant and animal development. Science 330, 622–627.PubMedCentralPubMedGoogle Scholar
  55. Finnegan E. J., Peacock W. J. and Dennis E. S. 1996 Reduced DNA methylation in Arabidopsis thaliana results in abnormal plant development. Proc. Natl. Acad. Sci. USA 93, 8449–8454.PubMedGoogle Scholar
  56. Fitz Gerald J. N., Hui P. S. and Berger F. 2009 Polycomb group-dependent imprinting of the actin regulator AtFH5 regulates morphogenesis in Arabidopsis thaliana. Development 136, 3399–3404.PubMedGoogle Scholar
  57. Floryszak-Wieczorek J., Arasimowicz-Jelonek M., Milczarek G., Janus L., Pawlak-Sprada S., Abramowskai D. et al. 2012 Nitric oxide-mediated stress imprints in potato as an effect of exposure to a priming agent. Mol. Plant Microbe Interact. 25, 1469–1477.Google Scholar
  58. Fu S., Gao Z., Birchler J. and Han F. 2012 Dicentric chromosome formation and epigenetics of centromere formation in plants. J. Genet. Genomics 39, 125–130.PubMedGoogle Scholar
  59. Fuchs J., Demidov D., Houben A. and Schubert I. 2006 Chromosomal histone modification patterns—from conservation to diversity. Trends Plant Sci. 11, 199–208.PubMedGoogle Scholar
  60. Gao Z., Liu H. L., Daxinger L., Pontes O., He X., Qian W. et al. 2010 An RNA polymerase II- and AGO4-associated protein acts in RNA-directed DNA methylation. Nature 465, 106–109.Google Scholar
  61. Garcia-Aguilar M., Michand C., Leblanc O. and Grimanelli D. 2010 Inactivation of a DNA methylation pathway in maize reproductive organs results in apomixis-like phenotypes. Plant Cell 22, 3249–3667.PubMedCentralPubMedGoogle Scholar
  62. Gazzani S., Gendall A. R., Lister C. and Dean C. 2003 Analysis of the molecular basis of flowering time variation in Arabidopsis accessions. Plant Physiol. 132, 1107–1114.PubMedCentralPubMedGoogle Scholar
  63. Gehring M., Bubb K. L. and Henikoff S. 2009 Extensive demethylation of repetitive elements during seed development underlies gene imprinting. Science 324, 1447–1451.PubMedCentralPubMedGoogle Scholar
  64. Gehring M., Huh J. H., Hsieh T. F., Penterman J., Choi Y., Harada J. J. et al. 2006 DEMETER DNA glycosylase establishes MEDEA polycomb gene self-imprinting by allele-specific demethylation. Cell 124, 495–506.Google Scholar
  65. Gehring M., Missirian V. and Henikoff S. 2011 Genomic analysis of parent-of-origin allelic expression in Arabidopsis thaliana seeds. PLoS ONE 6, e23687.Google Scholar
  66. Gong Z., Morales-Ruiz T., Ariza R. R., Roldan-Arjona T., David L. and Zhu J. K. 2002 ROS1, a repressor of transcriptional gene silencing in Arabidopsis, encodes a DNA glycosylase/lyase. Cell 111, 803–814.PubMedGoogle Scholar
  67. Greenberg M. V., Ausin I., Chan S. W., Cokus S. J., Cuperus J. T., Feng S. et al. 2011 Identification of genes required for de novo DNA methylation in Arabidopsis. Epigenetics 6, 344–354.Google Scholar
  68. Grewal S. I. and Elgin S. C. 2007 Transcription and RNA interference in the formation of heterochromatin. Nature 447, 399–406.PubMedCentralPubMedGoogle Scholar
  69. Gutierrez-Marcos J. F. and Dickinson H. G. 2012 Epigenetic reprogramming in plant reproductive lineages. Plant Cell Physiol. 53, 817–823.PubMedGoogle Scholar
  70. Haag J. R. and Pikaard C. S. 2011 Multisubunit RNA polymerases IV and V: purveyors of non-coding RNA for plant gene silencing. Nat. Rev. Mol. Cell Biol. 12, 483–492.PubMedGoogle Scholar
  71. Hashida S. N., Kitamura K., Mikami T. and Kishima Y. 2003 Temperature shift coordinately changes the activity and the methylation state of transposon Tam3 in Antirrhinum majus. Plant Physiol. 132, 1207–1216.PubMedCentralPubMedGoogle Scholar
  72. Hashida S. N., Uchiyama T., Martin C., Kishima Y., Sano Y. and Mikami T. 2006 The temperature-dependent change in methylation of the Antirrhinum transposon Tam3 is controlled, by the activity of its transposase. Plant Cell 18, 104–118.PubMedCentralPubMedGoogle Scholar
  73. He X. J., Hsu Y. F., Pontes O., Zhu J., Lu J., Bressan R. A. et al. 2009 NRPD4, a protein related to the RPB4 subunit of RNA polymerase II, is a component of RNA polymerase IV and V and is required for RNA-directed DNA methylation. Genes Dev. 23, 318–330.Google Scholar
  74. He G., Elling A. A. and Deng X. W. 2011 The epigenome and plant development. uAnnu. Rev. Plant Biol. 62, 411–435.PubMedGoogle Scholar
  75. Henderson I. R., Zhang X., Lu C., Johnson L., Meyers B. C., Green P. J. and Jacobsen S. E. 2006 Dissecting Arabidopsis thaliana DICER function in small RNA processing, gene silencing and DNA methylation patterning. Nature Gen. 38, 721–725.Google Scholar
  76. Henderson I. R. and Jacobsen S. E. 2007 Epigenetic inheritance in plants. Nature 447, 418–424.PubMedGoogle Scholar
  77. Henderson I. R. and Jacobsen S. E. 2008 Tandem repeats upstream of the Arabidopsis SDC recruit non-CG DNA methylation and initiate siRNA spreading. Genes Dev. 22, 1597–1606.PubMedGoogle Scholar
  78. Henderson I. R., Deleris A., Wong W., Zhong X., Chin H. G., Horwitz G. A. et al. 2010 The de novo cytosine methyltransferase DRM2 requires intact UBA domains and a catalytically mutated paralog DRM3 during RNA-directed DNA methylation in Arabidopsis thaliana. PLoS Genet. 6, e1001182.Google Scholar
  79. Henikoff S., Ahmad K. and Malik H. S. 2001 The centromere paradox: stable inheritance with rapidly evolving DNA. Science 293, 1098–1102.PubMedGoogle Scholar
  80. Herr A. J., Jensen M. B., Dalmay T. and Baulcombe D. C. 2005 RNA polymerase IV directs silencing of endogenous DNA. Science 308, 118–120.PubMedGoogle Scholar
  81. Hirochika H., Okamoto H. and Kakutani T. 2000 Silencing of retrotransposons in Arabidopsis and reactivation by the ddm1 mutation. Plant Cell 12, 357–369.PubMedCentralPubMedGoogle Scholar
  82. Holliday R. and Pugh J. E. 1975 DNA modification mechanism and gene activity during development. Science 187, 226–232.PubMedGoogle Scholar
  83. Hsieh T. F., Ibarra C. A., Silva P., Zemach A., Eshed-Williams L., Fischer R. L. and Zilberman D. 2009 Genome-wide demethylation of Arabidopsis endosperm. Science 324, 1451– 1454.PubMedGoogle Scholar
  84. Hsieh T. F., Shin J., Uzawa R., Silva P., Cohen S., Bauer M. J. et al. 2011 Regulation of imprinted gene expression in Arabidopsis endosperm. Proc. Natl. Acad. Sci. USA 108, 1755–1756.Google Scholar
  85. Huang L., Jones A. M., Searle I., Patel K., Vogler H., Hubner N. C. and Baulcombe D. C. 2009 An atypical RNA polymerase involved in RNA silencing shares small subunits with RNA polymerase II. Natl. Struct. Mol. Biol. 16, 91–93.Google Scholar
  86. Huff J. T. and Zilberman D. 2012 Regulation of biological accuracy, precision, and memory by plant chromatin organization. Curr. Opin. Genet. Dev. 22, 132–138.PubMedGoogle Scholar
  87. Ibarra C. A., Feng X., Schoft V. K., Hsieh T. F., Uzawa R., Rodrigues J. A. et al. 2012 Active DNA demethylation in plant companion cells reinforces transposon methylation in gametes. Science 337, 1360–1364.Google Scholar
  88. Ikeda Y. 2012 Plant imprinted genes identified by genome-wide approaches and their regulatory mechanisms. Plant Cell Physiol. 53, 809–816.PubMedGoogle Scholar
  89. Ikeda Y., Kobayashi Y., Yamaguchi A., Abe M. and Araki T. 2007 Molecular basis of late-flowering phenotype caused by dominant epi-alleles of the FWA locus in Arabidopsis. Plant Cell Physiol. 48, 205–220.PubMedGoogle Scholar
  90. Inagaki S., Miura-Kamio A., Nakamura Y., Lu F., Cui X., Cao X. et al. 2010 Autocatalytic differentiation of epigenetic modifications within the Arabidopsis genome. EMBO J. 29, 3496– 3506.Google Scholar
  91. Ito T., Seki M., Hayashida N., Shibata D. and Shinozaki K. 1999 Regional insertional mutagenesis of genes on Arabidopsis thaliana chromosome using the Ac/Ds transposition in combination with cDNA scanning method. Plant J. 17, 433–444.PubMedGoogle Scholar
  92. Ito H., Gaubert H., Bucher E., Mirouze M., Vaillant I. and Paszkowski J. 2011 An siRNA pathway prevents transgenerational retrotransposition in plants subjected to stress. Nature 472, 115–119.PubMedGoogle Scholar
  93. Jackson J. P., Lindroth A. M., Cao X. and Jacobsen S. E. 2002 Control of CpNpG methylation by the KRYPTONYTE histone H3 methyltransferase. Nature 416, 556–560.PubMedGoogle Scholar
  94. Jaenisch R. and Bird A. 2003 Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals. Nat. Genet. 33, 245–254.PubMedGoogle Scholar
  95. Jahnke S. and Scholten S. 2009 Epigenetic resetting of a gene imprinted in plant embryos. Curr. Biol. 19, 1677–1681.PubMedGoogle Scholar
  96. Jaligot E., Beule T., Baurens F. C., Billotte N. and Rival A. 2004 Search for methylation-sensitive amplification polymorphisms associated with the “mantled” variant phenotype in oil palm (Elaeis guineensis Jacq.) Genome 47, 224–228.Google Scholar
  97. Jiang H. and Kohler C. 2012 Evolution, function and regulation of genomic imprinting in plant seed development. J. Exp. Bot. 63, 4713–4722.PubMedGoogle Scholar
  98. Johannes F., Porcher E., Teixeira F. K., Saliba-Colombani V., Simon M., Agier N. et al. 2009 Assessing the impact of transgenerational epigenetic variation on complex traits. PLoS Genet. 5, e1000530.Google Scholar
  99. Johnson T. B. and Coghill R. D. 1925 Researches on pyrimidines CIII. The discovery of 5-methylcytosine in tuberculinic acid, the nucleic acid of the tubercle bacillus. J. Am. Chem. Soc. 47, 2838–2844.Google Scholar
  100. Johnson L. M., Bostick M., Zhang X., Kraft E., Henderson I., Callis J. and Jacobsen S. E. 2007 The SRA-methyl-cytosine-binding domain links DNA and histone methylation. Curr. Biol. 17, 379–384.PubMedCentralPubMedGoogle Scholar
  101. Johnson L. M., Law J. A., Khattar A., Henderson I. R. and Jacobsen S. E. 2008 SRA-domain proteins required for DRM2-mediated de novo DNA methylation. PLoS Genet. 4, e1000280.Google Scholar
  102. Jullien P. E. and Berger F. 2008 Parental genomic imprinting in plants: significance for reproduction. Med. Sci. 24, 753–757.Google Scholar
  103. Jullien P. E. and Berger F. 2010 Parental genome dosage imbalance deregulates imprinting in Arabidopsis. PLoS Genet. 6, e1000885.Google Scholar
  104. Jullien P. E., Kinoshita T., Ohad N. and Berger F. 2006 Maintenance of DNA methylation during the Arabidopsis life cycle is essential for parental imprinting. Plant Cell 18, 1360–1372.PubMedCentralPubMedGoogle Scholar
  105. Jullien P. E., Susaki D., Yelagandula R., Higashiyama T. and Berger F. 2012 DNA methylation dynamics during sexual reproduction in Arabidopsis thaliana. Curr. Biol. 22, 1825–1830.PubMedGoogle Scholar
  106. Kakutani T., Jeddeloh J. A., Flowers S. K., Munakata K. and Richards E. J. 1996 Developmental abnormalities and epimutations associated with DNA hypomethylation mutations. Proc. Natl. Acad. Sci. USA 29, 12406–12411.Google Scholar
  107. Kakutani T., Kato M., Kinoshita T. and Miura A. 2004 Control of development and transposon movement by DNA methylation in Arabidopsis thaliana. Cold Spring Harb. Symp. Quant. Biol. 69, 139–143.PubMedGoogle Scholar
  108. Kankel M. W., Rasey D. E., Stoke T. L., Flowers S. K., Haag J. R., Jeddeloh J. A. et al. 2003 MET1 cytosine methyltransferase mutants. Genetics 163, 1109–1122.Google Scholar
  109. Kanno T. and Habu Y. 2011 siRNA-mediated chromatin maintenance and its function in Arabidopsis thaliana. Biochim. Biophys. Acta 1809, 444–451.PubMedGoogle Scholar
  110. Kanno T., Mette M. F., Kreil D. P., Aufsatz W., Matzke M. and Matzke A. J. 2004 Involvement of putative SNF2 chromatin modelling protein DRD1 in RNA-directed DNA methylation. Curr. Biol. 14, 801–805.PubMedGoogle Scholar
  111. Kanno T., Bucher E., Daxinger L., Huettel B., Bohmdorfer G., Gregor W. et al. 2008 A structural-maintenance-of-chromosomes hinge domain-containing protein is required for RNA-directed DNA methylation. Nat. Genet. 40, 670–675.Google Scholar
  112. Kanno T., Bucher E., Daxinger L., Huettel B., Kreil D. P., Breinig F. et al. 2010 RNA-directed DNA methylation and plant development require an IWR1-type transcription factor. EMBO Rep. 11, 65–71.Google Scholar
  113. Karan R., DeLeon T., Biradar H. and Subudhi P. K. 2012 Salt stress induced variation in DNA methylation pattern and its influence on gene expression in contrasting rice genotypes. PLoS ONE 7, e40203.Google Scholar
  114. Kashkush K. and Khasdan V. 2007 Large-scale survey of cytosine methylation of retrotransposons and the impact of readout transcription from long terminal repeats on expression of adjacent rice genes. Genetics 177, 1975–1985.PubMedGoogle Scholar
  115. Kashkush K., Feldman M. and Levy A. A. 2003 Transcriptional activation of retrotransposons alters the expression of adjacent genes in wheat. Nat. Genet. 33, 102–106.PubMedGoogle Scholar
  116. Kathiria P., Sidler C., Golubov A., Kalischuk M., Kowchuk L. M. and Kovalchuk I. 2010 Tobacco mosaic virus infection results in an increase in recombination frequency and resistance to viral, bacterial and fungal pathogen in the progeny of infected plants. Plant Physiol. 153, 1859–1870.PubMedCentralPubMedGoogle Scholar
  117. Katiyar-Agarwal S., Morgan R., Dahlbeck D., Borsani O., Villegas Jr A., Zhu J. K. et al. 2006 A pathogen-inducible endogenous siRNA in plant immunity. Proc. Natl. Acad. Sci. USA 103, 18002–18007.Google Scholar
  118. Kato M., Miura A., Bender J., Jacobsen S. E. and Kakutani T. 2003 Role of CG and non-CG methylation in immobilization of transposons in Arabidopsis. Curr. Biol. 13, 421–426.PubMedGoogle Scholar
  119. Kim J. M., To T. K., Ishida J., Morosawa T., Kawashima M., Matsui A. et al. 2008 Alterations of lysine modifications on histone H3 N-tail under drought stress conditions in Arabidopsis thaliana. Plant Cell Physiol. 49, 1580–1588.Google Scholar
  120. Kim J. M., To T. K., Ishida J., Matsui A., Kimura H. and Seki M. 2012 Transition of chromatin status during the process of recovery from drought stress in Arabidopsis thaliana. Plant Cell Physiol. 53, 847–856.PubMedGoogle Scholar
  121. Kinoshita T., Yadagiri R., Harada J. J., Goldberg R. B. and Fischer R. L. 1999 Imprinting of the MEDEA polycomb gene in the Arabidopsis endosperm. Plant Cell 11, 1945–1952.PubMedCentralPubMedGoogle Scholar
  122. Kinoshita T., Miura A., Kinoshita Y., Cao X., Jacobsen S. E., Fischer R. L. and Kakutani T. 2004 One-way control of FWA imprinting in Arabidopsis endosperm by DNA methylation. Science 303, 521–523.PubMedGoogle Scholar
  123. Kinoshita Y., Saze H., Kinoshita T., Miura A., Soppe W. J., Koornneef M. and Kakutani T. 2007 Control of FWA gene silencing in Arabidopsis thaliana by SINE-related direct repeats. Plant J. 49, 38–45.PubMedGoogle Scholar
  124. Kohler C., Page D. R., Gagliardini V. and Grossniklaus U. 2005 The Arabidopsis thaliana MEDEA polycomb-group protein controls expression of PHERES 1 by parental imprinting. Nat. Genet. 37, 28–30.PubMedGoogle Scholar
  125. Koltunow A. M. and Grossniklaus V. 2003 Apomixis: a developmental perspective. Ann. Rev. Plant Biol. 54, 547–574.Google Scholar
  126. Koo D. H., Han F., Birchler J. A. and Jiang J. 2011 Distinct DNA methylation patterns associated with active and inactive centromeres of the maize B chromosome. Genome Res. 21, 908–914.PubMedGoogle Scholar
  127. Kou H. P., Li Y., Song X. X., Ou X. F., Xing S. C., Ma J. 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.Google Scholar
  128. Kouzarides T. 2007 Chromatin modifications and their function. Cell 128, 693–705.PubMedGoogle Scholar
  129. Kovalchuk O., Burke P., Arkhipov A., Kuchma N., James S. J., Kovalchuk I. and Pogribny I. 2003 Genome hypermethylation in Pinus silvestris of Chernobyl–a mechanism for radiation adaptation. Mut. Res. 529, 13–20.Google Scholar
  130. Kumar S. 2006 Progress in understanding of the genetic phenomenon paramutation. Curr. Sci. 91, 1002–1003.Google Scholar
  131. Kumar S. 2007 Mechanisms of heritable epigenetic variation mediated by cytosine methylation of nuclear genome in plants. Proc. Natl. Acad. Sci. India 77, 19–30.Google Scholar
  132. Kumar S. and Natarajan A. T. 1966 Kinetics of two-break chromosome exchanges and the spatial arrangement of chromosome strands in interphase nucleus. Nature 209, 796–797.PubMedGoogle Scholar
  133. Kumar S. V. and Wigge P. A. 2010 H2A.Z-containing nucleosomes mediate the thermosensory response in Arabidopsis. Cell 140, 136–147.Google Scholar
  134. Labra M., Ghiani A., Citterio S., Sgorbati S., Sala F., Vannini C. et al. 2002 Analysis of cytosine methylation pattern in response to water deficit in pea root tips. Plant Biol. 4, 694–699.Google Scholar
  135. Lamarck J. B. 1809 Philosophie zoologique., ou exposition des considerations relatives a I’histoire naturelle des animaux. Paris: Dentu.Google Scholar
  136. Latzel V., Zhang Y. Y., Moritz K. K., Fischer M. and Bossdorf O. 2012 Epigenetic variation in plant responses to defence hormones. Ann. Bot. 110, 1423–1428.PubMedGoogle Scholar
  137. Lauria M. and Rossi V. 2011 Epigenetic control of gene regulation in plants. Biochim. Biophys. Acta 1809, 369–378.PubMedGoogle Scholar
  138. Law J. A. and Jacobsen S. E. 2010 Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nat. Rev. Genet. 11, 204–220.PubMedCentralPubMedGoogle Scholar
  139. Law J. A., Ausin I., Johnson L. M., Vashisht A. A., Zhu J. K., Wohlschlegel J. A. and Jacobsen S. E. 2010 A protein complex required for polymerase V transcripts and RNA-directed DNA methylation in Arabidopsis. Curr. Biol. 20, 951–956.PubMedCentralPubMedGoogle Scholar
  140. Law J. A., Vashisht A. A., Wohlschlegel J. A. and Jacobsen S. E. 2011 SHH1, a homeodomain protein required for DNA methylation, as well as RDR2, RDM4, and chromatin remodeling factors, associate with RNA polymerase IV. PLoS Genet. 7, e1002195.Google Scholar
  141. Li C. F., Pontes O., El-Shami M., Henderson I. R., Bernatavichute Y. V., Chan S. W.-L. et al. 2006 An ARGONAUTE4-containing nuclear processing center colocalized with Cajal bodies in Arabidopsis thaliana. Cell 126, 93–106.Google Scholar
  142. Lindroth A. M., Cao X., Jackson J. P., Zilberman D., McCallum C. M., Henikoff S. and Jacobsen S. E. 2001 Requirement of CHROMOMETHYLASE 3 for maintenance of CpXpG methylation. Science 202, 2077–2080.Google Scholar
  143. Lindroth A. M., Shultis D., Jasencakova Z., Fuchs J., Johnson L., Schubert D. et al. 2004 Dual histone H3 methylation marks at lysine 9 and 27 required for interaction with CHROMOMETHYLASE 3. EMBO J. 23, 4286–4296.Google Scholar
  144. Lippman Z., Gendrel A. V., Black M., Vaughn M. W., Dedhia N., McCombie W. R. et al. 2004 Role of transposable elements in heterochromatin and epigenetic control. Nature 430, 471–476.Google Scholar
  145. Lira-Medeiros C. F., Parisod C., Fernandes R. A., Mata C. S., Cardosa M. A. and Ferreira P. C. 2010 Epigenetic variation in mangrove plants occurring in contrasting natural environment. PLoS ONE 5, e10326.Google Scholar
  146. Lisch D. 2009 Epigenetic regulation of transposable elements in plants. Ann. Rev. Plant Biol. 60, 43–66.Google Scholar
  147. Lisch D. and Bennetzen J. L. 2011 Transposable element origins of epigenetic regulation. Curr. Opin. Plant Biol. 14, 156–161.PubMedGoogle Scholar
  148. Lister R., O’Malley R. C., Tonti-Filippni J., Gregory B. D., Berry C. C., Millar A. H. and Ecker J. R. 2008 Highly integrated single-base resolution maps of the epigenome in Arabidopsis. Cell 133, 523–536.PubMedCentralPubMedGoogle Scholar
  149. Lu C., Kulkarni K., Souret F. F., MuthuValliappan R., Tej S. S., Poethig R. S. et al. 2006 MicroRNAs and other small RNAs enriched in the Arabidopsis RNA-dependent RNA Polymerase-2 mutant. Genome Res. 16, 1276–1288.Google Scholar
  150. Lu Y., Rong T. and Cao M. 2008 Analysis of DNA methylation in different maize tissues. J. Genet. Genomics 35, 41–48.PubMedGoogle Scholar
  151. Lucht J. M., Mauch-Mani B., Steiner H. Y., Metraux J. P., Ryals J. and Hohn B. 2002 Pathogen stress increases somatic recombination frequency in Arabidopsis. Nat. Genet. 30, 311–314.PubMedGoogle Scholar
  152. Luff B., Pawlowski L. and Bender J. 1999 An inverted repeat triggers cytosine methylation of identical sequences in Arabidopsis. Mol. Cell 3, 505–511.PubMedGoogle Scholar
  153. Luna E., Bruce T. J., Roberts M. R., Flors V. and Ton J. 2012 Next-generation systemic acquired resistance. Plant Physiol. 158, 844–853.PubMedCentralPubMedGoogle Scholar
  154. Luo C. and Lam E. 2010 ANCORP: a high-resolution approach that generates distinct chromatin state models from multiple genome-wide datasets. Plant J. 63, 339–351.PubMedGoogle Scholar
  155. Luo M., Taylor J. M., Spriggs A., Zhang H., Wu X., Russell S. et al. 2011 A genome-wide survey of imprinted genes in rice seeds reveals imprinting primarily occurs in the endosperm. PLoS Genet. 7, e1002125.Google Scholar
  156. Lyko F., Ramsahoye B. H. and Jaenisch R. 2000 DNA methylation in Drosophila melanogaster. Nature 408, 538–546.PubMedGoogle Scholar
  157. Ma J., Wing R. A., Bennetzen J. L. and Jackson S. A. 2007 Plant centromere organization: a dynamic structure with conserved functions. Trends Genet. 23, 134–139.PubMedGoogle Scholar
  158. Maloisel L. and Rossignol J. L. 1998 Suppression of crossing-over by DNA methylation in Ascobolus. Genes Dev. 12, 1381–1389.PubMedGoogle Scholar
  159. Manning K., Tor M., Poole M., Hong Y., Thompson A. J., King G. J. et al. 2006 A naturally occurring epigenetic mutation in a gene encoding an SBP-box transcription factor inhibits tomato fruit ripening. Nat. Genet. 38, 948–952.Google Scholar
  160. March-Diaz R., Garcia-Dominquez M., Lozano-Juste J., Leon J., Florencio F. J. and Reyes J. C. 2008 Histone H2A.Z and homologues of components of SWR1 complex are required to control immunity in Arabidopsis. Plant J. 53, 475–487.PubMedGoogle Scholar
  161. Margueron R. and Reinberg D. 2011 The polycomb complex PRC2 and its mark in life. Nature 469, 343–349.PubMedCentralPubMedGoogle Scholar
  162. Morris C. A. and Moazed D. 2007 Centromere assembly and propagation. Cell 128, 647–650.PubMedGoogle Scholar
  163. Martin A., Troadec C., Boualem A., Rajab M., Fernandez R., Morin H. et al. 2009 A transcription-induced epigenetic change leads to sex determination in melon. Nature 461, 1135–1138.Google Scholar
  164. Martinez-Macias M. I., Quin W., Miki D., Pontes O., Liu Y., Tang K. et al. 2012 A DNA 3 phosphatase functions in active DNA demethylation in Arabidopsis. Mol. Cell 45, 357–370.Google Scholar
  165. Matsunaga W., Kobayashi A., Kato A. and Ito H. 2012 The effects of heat induction and the siRNA biogenesis pathway on the transgenerational transcription of ONSEN, a copia-like retrotransposon in Arabidopsis thaliana. Plant Cell Physiol. 53, 824–833.PubMedGoogle Scholar
  166. Matzke M., Kanno T., Huettel B., Daxinger L. and Matzke A. J. 2007 Targets of RNA-directed DNA methylation. Curr. Opin. Plant Biol. 10, 512–519.PubMedGoogle Scholar
  167. Maunakea A. K., Nagarajan R. P., Bilenky M., Ballinger T. J., D’Souza C., Fouse S. D. et al. 2010 Conserved role of intragenic DNA methylation in regulating alternative promoters. Nature 466, 253–257.Google Scholar
  168. Maury S., Trap-Gentil M. V., Hebrard C., Weyens G., Delaunay A., Barnes S. et al. 2012 Genic DNA methylation changes during in vitro organogenesis: organ specificity and conservation between parental lines of epialleles. Physiol. Plant 146, 321–325.Google Scholar
  169. Mayr E. 1984 What is Darwinism today? Proceedings of the Biennial Meeting of the Philosophy of Science Association. Vol. 2. Symposia and Invited Papers, pp. 145–156, University of Chicago Press, Chicago, USA.Google Scholar
  170. Melquist S., Luff B. and Bender J. 1999 Arabidopsis PAI gene arrangements, cytosine methylation and expression. Genetics 153, 401–413.PubMedGoogle Scholar
  171. Messeguer R., Ganal M. W., Steffens J. C. and Tanksley S. D. 1991 Characterization of the level, target sites and inheritance of cytosine methylation in tomato nuclear DNA. Plant Mol. Biol. 16, 753–770.PubMedGoogle Scholar
  172. Mi S., Cai T., Hu Y., Chen Y., Hodges E., Ni F. et al. 2008 Sorting of small RNAs into Arabidopsis argonaute complex is directed by the 5 terminal nucleoide. Cell 133, 116–127.Google Scholar
  173. Mirouze M., Lieberman-Lazarovich M., Aversano R., Bucher E., Nicolet J., Reinders J. and Paszkowski J. 2012 Loss of DNA methylation affects the recombination landscape in Arabidopsis. Proc. Natl. Acad. Sci. USA 109, 5880–5885.PubMedGoogle Scholar
  174. Mirouze M., Reinders J., Bucher E., Nishimura T., Schneeberger K., Ossowski S. et al. 2009 Selective epigenetic control of retrotransposition in Arabidopsis. Nature 461, 427–430.Google Scholar
  175. Miura A., Yonebayashi S., Watanabe K., Toyama T., Shimada H. and Kakutani T. 2001 Mobilization of transposons by a mutation abolishing full DNA methylation in Arabidopsis. Nature 411, 212–214.PubMedGoogle Scholar
  176. Miura A., Nakamura M., Inagaki S., Kobayashi A., Saze H. and Kakutani T. 2009 An Arabidopsis jmjC domain protein protects transcribed genes from DNA methylation at CHG sites. EMBO J. 28, 1078–1086.PubMedGoogle Scholar
  177. Mizuguchi G., Shen X., Landry J., Wu W. H., Sen S. and Wu C. 2004 ATP-driven exchange of histone H2A.Z variant catalyzed by SWR1 chromatin remodelling complex. Science 303, 343–348.PubMedGoogle Scholar
  178. Mlynarova L., Nap J. P. and Bisseling T. 2007 The SWI/SNF chromatin-remodeling gene AtCHR12 mediates temporary growth arrest in Arabidopsis thaliana upon perceiving environmental stress. Plant J. 51, 874–885.PubMedGoogle Scholar
  179. Molinier J., Ries G., Zipfel C. and Hohn B. 2006 Transgeneration memory of stress in plants. Nature 442, 1046–1049.PubMedGoogle Scholar
  180. Morales-Ruiz T., Ortega-Galisteo A. P., Ponferrada-Marin M. I., Martinez-Macias M. I., Ariza R. R. and Roldan-Arjona T. 2006 DEMETER and REPRESSOR OF SILENCING 1 encode 5-methylcytosine DNA glycosylases. Proc. Natl. Acad. Sci. USA 103, 6853–6858.PubMedGoogle Scholar
  181. Nagaki K., Talbert P. B., Zhong C. X., Dawe R. K., Henikoff S. and Jiang J. 2003 Chromatin immunoprecipitation reveals that the 180-bp satellite repeat is the key functional DNA element of Arabidopsis thaliana centromeres. Genetics 163, 1221–1225.PubMedGoogle Scholar
  182. Naito K., Zhang F., Tsukiyama T., Saito H., Hancock C. N., Richardson A. O. et al. 2009 Unexpected consequences of a sudden and massive transposon amplification on rice gene expression. Nature 461, 1130–1134.Google Scholar
  183. Nakano Y., Steward N., Sekine M., Kusano T. and Sano H. 2000 A tobacco NtMET1 cDNA encoding a DNA methyltransferase: molecular characterization and abnormal phenotypes of transgenic tobacco plants. Plant Cell Physiol. 41, 448–457.PubMedGoogle Scholar
  184. Ng H. H., Jeppesen P. and Bird A. 2000 Active repression of methylated genes by the chromosomal protein MBD1. Mol. Cell Biol. 20, 1394–1406.PubMedCentralPubMedGoogle Scholar
  185. Nosaka M., Itoh J., Nagato Y., Ono A., Ishiwata A. and Sato Y. 2012 Role of transposon-derived small RNAs in the interplay between genomes and parasitic DNA in rice. PLoS Genet. 9, e1002953.Google Scholar
  186. Noutoshi Y., Ikeda M., Saito T., Osada H. and Shirasu K. 2012a Sulfonamides identified as plant-immune priming compounds in high-throughput chemical screening increase disease resistance in Arabidopsis thaliana. Front. Plant Sci. 3, 245.Google Scholar
  187. Noutoshi Y., Ikeda M. and Shirasu K. 2012b Diuretics prime plant immunity in Arabidopsis thaliana. PLoS ONE 7, e48443.Google Scholar
  188. Noutoshi Y., Okazaki M., Kida T., Nishina Y., Morishita Y., Ogawa T. et al. 2012c Novel plant immune-priming compounds identified via high-throughput chemical screening target salicylic glucosyl transferase in Arabidopsis. Plant Cell 24, 3795–3804.Google Scholar
  189. Olmedo-Monfil V., Duran-Figueroa N., Arteaga-Vazquez M., Demesa-Arevalo E., Autran D., Grimanelli D. et al. 2010 Control of female gamete formation by a small RNA pathway in Arabidopsis. Nature 464, 628–632.Google Scholar
  190. Onodera Y., Haag J. R., Ream T., Nunes P. C., Pontes O. and Pikaard C. S. 2005 Plant nuclear RNA polymerase IV mediates siRNA and DNA methylation-dependent heterochromatin formation. Cell 120, 613–622.PubMedGoogle Scholar
  191. Ortega-Galisteo A. P., Morales-Ruiz T., Ariza R. R. and Roldan-Arjona T. 2008 Arabidopsis DEMETER-LIKE proteins DML2 and DML3 are required for appropriate distribution of DNA methylation marks. Plant Mol. Biol. 67, 671–681.PubMedGoogle Scholar
  192. Ossowski S., Schneeberger K., Lucas-Lledo J. I., Warthmann N., Clark R. M., Shaw R. G. et al. 2010 The rate and molecular spectrum of spontaneous mutation in Arabidopsis thaliana. Science 327, 92–94.Google Scholar
  193. Ou X., Zhang Y., Xu C., Lin X., Zang Q., Zhuang T. 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.Google Scholar
  194. Papamichos-Chronakis M., Watanabe S., Rando O. J. and Peterson C. L. 2011 Global regulation of H2A.Z localization by the INO80 chromatin-remodeling enzyme is essential for genome integrity. Cell 144, 200–213.PubMedCentralPubMedGoogle Scholar
  195. Paun O., Bateman R. M., Fay M. F., Hedren M., Civeyrel L. and Chase M. W. 2010 Stable epigenetic effects impact adaptation in allopolyploid orchids (Dactylorhiza: Orchidaceae). Mol. Biol. Evol. 27, 2465–2473.PubMedGoogle Scholar
  196. Pavet V., Quintero C., Cecchini N. M., Rosa A. L. and Alvarez M. E. 2006 Arabidopsis displays centromeric DNA hypomethylation and cytological aleterations of heterochromatin upon attack by Pseudomonas syringae. MPMI 19, 577–587.PubMedGoogle Scholar
  197. Penterman J., Zilberman D., Huh J. H., Ballinger T., Henikoff S. and Fischer R. L. 2007 DNA demethylation in the Arabidopsis genome. Proc. Natl. Acad. Sci. USA 104, 6752–6757.PubMedGoogle Scholar
  198. Pfeifer G. P. 2006 Mutagenesis at methylated CpG sequences. CTMI 301, 259–281.Google Scholar
  199. Pick T., Jaskiewicz M., Peterhansel C. and Conrath U. 2012 Heat shock factor HsfB1 primes gene transcription and systemic acquired resistance in Arabidopsis. Plant Physiol. 159, 52–55.PubMedCentralPubMedGoogle Scholar
  200. Piegu B., Guyot R., Picault N., Roulin A., Sanyal A., Kim H. et al. 2006 Doublimg genome size without polyploidization: dynamics of retrotransposition-driven genomic expansions in Oryza australiensis, a wild relative of rice. Genome res. 16, 1262–1269.Google Scholar
  201. Pikaard C. S., Haag J. R., Ream T. and Wierzbicki A. T. 2008 Roles of RNA polymerase IV in gene silencing. Trends Plant Sci. 13, 390–397.PubMedCentralPubMedGoogle Scholar
  202. Ponferrada-Marin M. I., Roldan-Arjona T. and Ariza R. R. 2012 Demethylation initiated by ROS1 glycosylase involves random sliding along DNA. Nucleic Acids Res. 40, 11554–11562.PubMedCentralPubMedGoogle Scholar
  203. Pontes O., Li C. F., Costa Nunes P., Haag J., Ream T., Vitins A. et al. 2006 The Arabidopsis chromatin-modifying nuclear siRNA pathway involves a nucleolar RNA processing center. Cell 14, 79–92.Google Scholar
  204. Pontvianne F., Blevins T. and Pikaard C. S. 2010 Arabidopsis histone lysine methyltransferases. Adv. Bot. Res. 53, 1–22.PubMedCentralPubMedGoogle Scholar
  205. Probst A. V., Fagard M., Proux F., Mourrain P., Boutet S., Earley K. et al. 2004 Arabidopsis histone deacetylase HDA6 is required for maintenance of transcriptional gene and determines nuclear organization of rDNA repeats. Plant Cell 16, 1021–1034.Google Scholar
  206. Qi Y., He X., Wang X-J., Kohany O., Jurka J. and Hannon G. J. 2006 Distinct catalytic and non-catalytic roles of ARGONAUTE 4 in RNA-directed DNA methylation. Nature 443, 1006– 1012.Google Scholar
  207. Rabinowicz P. D., Palmer L. E., May B. P., Hemann M. T., Lowe S. W., McCombie W. R. and Martienssen R. A. 2003 Genes and transposons are differentially methylated in plants, but not in mammals. Genome Res. 13, 2658–2664.PubMedGoogle Scholar
  208. Raissig M. T., Baroux C. and Grossniklaus U. 2011 Regulation and flexibility of genomic imprinting during seed development. Plant Cell 23, 16–26.PubMedCentralPubMedGoogle Scholar
  209. Rangwala S. H. and Richards E. J. 2007 Differential epigenetic regulation within an Arabidopsis retrotransposon family. Genetics 176, 151–160.PubMedGoogle Scholar
  210. Rasmann S., De Vos M., Casteel C. L., Tian D., Halitschke R., Sun J. Y. et al. 2012 Herbivory in the previous generation primes plants for enhanced insect resistance. Plant Physiol. 158, 854–863.Google Scholar
  211. Ream T. S., Haag J. R., Wierzbicki A. T., Nicora C. D., Norbeck A. D., Zhu J. K. et al. 2009 Subunit compositions of the RNA-silencing enzymes Pol IV and Pol V reveal their origins as specialized forms of RNA polymerase II. Mol. Cell 33, 192–203.Google Scholar
  212. Reinders J., Wulff B. B., Mirouze M., Mari-Ordonez A., Dapp M., Rozhon W. et al. 2009 Compromised stability of DNA methylation and transposon immobilization in mosaic Arabidopsis epigenomes. Genes Dev. 23, 939–950.Google Scholar
  213. Reyes J. C. 2006 Chromatin modifiers that control plant development. Curr. Opin. Plant Biol. 9, 21–27.PubMedGoogle Scholar
  214. Rival A., Jaligot E., Beule T. and Finnegan E. J. 2008 Isolation and expression analysis of genes encoding MET, CMT and DRM methyltransferses in oil palm (Elaeis guineensis Jacq.) in relation to the ‘mantled’ somaclonal variation. J. Exp. Bot. 59, 3271–3281.PubMedGoogle Scholar
  215. Roudier F., Ahmed I., Berard C., Sarazin A., Mary-Huard T., Cortijo S. et al. 2011 Integrative epigenomic mapping defines four main chromatin states in Arabidopsis. EMBO J. 30, 1928–1938.Google Scholar
  216. Ruiz-Garcia L., Cervera M. T. and Martinez-Zapater J. M. 2005 DNA methylation increases throughtout Arabidopsis development. Planta 222, 301–306.PubMedGoogle Scholar
  217. Sano H., Kamada I., Youssefian S., Katsumi M. and Wabilko H. 1990 A single treatment of rice seedlings with 5-azacytidine induces heritable dwarfism and undermethylation of genomic DNA. Mol. Gen. Genet. 220, 441–447.Google Scholar
  218. Sasai N. and Defossez P. A. 2009 Many paths to one goal? The proteins that recognize methylated DNA in eukaryotes. Int. J. Dev. Biol. 53, 323–334.PubMedGoogle Scholar
  219. Sasaki T., Kobayashi A., Saze H. and Kakutani T. 2012a RNAi-independent de novo DNA methylation revealed in Arabidopsis mutants of chromatin remodeling gene DDM1. Plant J. 70, 750–758.PubMedGoogle Scholar
  220. Sasaki T., Naumann U., Forai P., Matzke A. J. and Matzke M. 2012b Unusual case of apparent hypermutation in Arabidopsis thaliana. Genetics 192, 1271–1280.PubMedGoogle Scholar
  221. Saze H. and 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– 3652.PubMedGoogle Scholar
  222. Saze H. and Kakutani T. 2011 Differentiation of epigenetic modifications between transposons and genes. Curr. Opin. Plant Biol. 14, 81–87.PubMedGoogle Scholar
  223. Saze H., Shiraishi A., Miura A. and Kakutani T. 2008 Control of genic DNA methylation by a jmjC domain-containing protein in Arabidopsis thaliana. Science 319, 462–465.PubMedGoogle Scholar
  224. Saze H., Tsugane K., Kanno T. and Nishimura T. 2012 DNA methylation in plants: relationship to small RNAs and histone modifications and functions in transposon inactivation. Plant Cell Physiol. 53, 766–784.PubMedGoogle Scholar
  225. Scebba F., Bernacchia G., De Bastiani M., Evangelista M., Cantoni R. M., Cella R. et al. 2003 Arabidopsis MBD proteins show different binding specificities and nuclear localization. Plant Mol. Biol. 53, 715–731.Google Scholar
  226. Schmitz R. J., Schultz M. D., Lawsey M. G., O’Malley R. C., Urich M. A., Libiger O. et al. 2011 Transgenerational epigenetic instability is a source of novel methylation variants. Science 334, 369–373.Google Scholar
  227. Scoville A. G., Barnett L. L., Bodbyl-Roels S., Kelly J. K. and Hileman L. C. 2011 Differential regulation of a MYB transcription factor is correlated with transgenerational epigenetic inheritance of trichome density in Mimulus guttatus. New Phytol. 191, 251–263.PubMedCentralPubMedGoogle Scholar
  228. Searle I. R., Pontes O., Melnyk C. W., Smith L. M. and Baulcombe D. C. 2010 JMJ14; a JmjC domain protein, is required for RNA silencing and cell-to-cell movement of an RNA silencing signal in Arabidopsis. Genes Dev. 24, 986–991.PubMedGoogle Scholar
  229. Sha A. H., Lin X. H., Huang J. B. and Zhang D. P. 2005 Analysis of DNA methylation related to rice adult plant resistance to bacterial blight based on methylation-sensitive AFLP (MSAP) analysis. Mol. Genet. Genomics 273, 484–490.PubMedGoogle Scholar
  230. Shaked H., Kashkush K., Ozkan H., Feldman M. and Levy A. A. 2001 Sequence elimination and cytosine methylation are rapid and reproducible responses of the genome to wide hybridization and allopolyploidy in wheat. Plant Cell 13, 1749–1759.PubMedCentralPubMedGoogle Scholar
  231. Shiba H., Kakizaki T., Iwano M., Tarutani Y., Watanabe M., Isogai A. and Takayama S. 2006 Dominance relationships between self-incompatibility alleles controlled by DNA methylation. Nat. Genet. 38, 297–299.PubMedGoogle Scholar
  232. Singh M., Goel S., Meeley R. B., Dantec C., Parrinello H., Michaud C. et al. 2011 Production of variable gametes without meiosis in maize deficient for an ARGONAUTE protein. Plant Cell 23, 443–458.Google Scholar
  233. Slaughter A., Daniel X., Flors V., Luna E., Hohn B. and Mauch-Mani B. 2012 Descendants of primed Arabidopsis plants exhibit resistance to biotic stress. Plant Physiol. 158, 835–843.PubMedCentralPubMedGoogle Scholar
  234. Slotkin R. K., Freeling M. and Lisch D. 2005 Heritable transposon silencing initiated by a naturally occurring transposon inverted duplication. Nat. Genet. 37, 641–644.PubMedGoogle Scholar
  235. Slotkin R. K., Vaughn M., Borges F., Tanurdzic M., Becker J. D., Feijo J. A. and Martienssen R. A. 2009 Epigenetic reprogramming and small RNA silencing of transposable elements in pollen. Cell 136, 461–472.PubMedCentralPubMedGoogle Scholar
  236. Smith L. M., Pontes O., Searle I., Yelina N., Yousafzai F. K., Herr A. J. et al. 2007 An SNF2 protein associated with nuclear RNA silencing and the spread of a silencing signal between cells in Arabidopsis. Plant Cell 19, 1507–1521.Google Scholar
  237. Song Y., Ji D., Li S., Wang P., Li Q. and Xiang F. 2012 The dynamic changes of DNA methylation and histone modifications of salt responsive transcription factor genes in soybean. PLoS ONE 7, e41274.Google Scholar
  238. Stam M., Belele C., Dorweiler J. E. and Chandler V. L. 2002 Differential chromatin structure within tandem array 100 kb upstream of the maize b1 locus is associated with paramutation. Genes Dev. 16, 1906–1918.PubMedGoogle Scholar
  239. Steward N., Kusano T. and Sano H. 2000 Expression of ZmMET1, a gene encoding a DNA methyltransferase from maize, is associated not only with DNA replication in actively proliferating cells, but also with altered DNA methylation status in cold-stressed quiescent cells. Nucleic Acids Res. 28, 3250–3259.PubMedCentralPubMedGoogle Scholar
  240. Steward N., Ito M., Yamaguchi Y., Koizumi N. and Sano H. 2002 Periodic DNA methylation in maize nucleosomes and demethylation by environmental stress. J. Biol. Chem. 277, 37741– 37746.PubMedGoogle Scholar
  241. Stonaker J. L., Lim J. P., Erhard Jr K. F. and Hollick J. B. 2009 Diversity of Pol IV function is defined by mutations at the maize rmr7 locus. PLoS Genet. 5, e1000706.Google Scholar
  242. Tarutani Y., Shiba H., Iwano M., Tarutani Y., Watanabe M., Isogai A. and Takayama S. 2010 Trans-acting small RNA determines dominance relationships in Brassica self-incompatibilty. Nature 466, 983–986.PubMedGoogle Scholar
  243. Teixeira F. K., Heredia F., Sarazin A., Roudier F., Boccara M., Ciaudo C. et al. 2009 A role for RNAi in the selective correction of DNA methylation defects. Science 323, 1600–1604.Google Scholar
  244. Tittel-Elmer M., Bucher E., Broger L., Mathieu O., Paszkowski J. and Valliank J. 2010 Stress-induced activation of heterochromatic transcription. PLoS ONE 6, e1001175.Google Scholar
  245. Tiwari S., Schulz R., Ikeda Y., Dytham L., Bravo J., Mathers L. et al. 2008 MATERNALLY EXPRESSED PAB C-TERMINAL., a novel imprinted gene in Arabidopsis, encodes the conserved C-terminal domain of polyadenylate binding proteins. Plant Cell 20, 2387–2398.Google Scholar
  246. To T. K., Kim J. M., Matsui A., Kurihara Y., Morosawa T., Ishida J. et al. 2011a Arabidopsis HDA6 regulated locus-directed heterochromatin silencing in cooperation with MET1. PLoS Genet 7, e1002055.Google Scholar
  247. To T. K., Nakaminami K., Kim J. M., Morosawa T., Ishida J., Tanaka M. et al. 2011b Arabidopsis HDA6 is required for freezing tolerance. Biochem. Biophys. Res. Commun. 406, 414–419.Google Scholar
  248. Topp C. N. and Dawe R. K. 2006 Reinterpreting pericentromeric heterochromatin. Curr. Opin. Plant Biol. 9, 647–653.PubMedGoogle Scholar
  249. Tsukahara S., Kobayashi A., Kawabe A., Mathieu O., Miura A. and Kakutani T. 2009 Bursts of retrotransposition reproduced in Arabidopsis. Nature 461, 423–426.PubMedGoogle Scholar
  250. Vanyushin B. F. 2006 DNA methylation in plants. Curr. Topics Microbiol. Immunol. 301, 67–122.Google Scholar
  251. Vaughn M. W., Tanurdzic M., Lippman Z., Jiang H., Carrasquillo R., Rabinowicz P. D. et al. 2007 Epigenetic natural variation in Arabidopsis thaliana. PLoS Biol. 5, e174.Google Scholar
  252. Verhoeven K. J., Jansen J. J., van Dijk P. J. and Biere A. 2010 Stress-induced DNA methylation changes and their heritability in asexual dandelions. New Phytol. 185, 1108–1118.Google Scholar
  253. Vielle-Calzada J. P., Thomas J., Spillane C., Coluccio A., Hoeppner M. A. and Grossniklaus U. 1999 Maintenance of genomic imprinting at the Arabidopsis medea locus requires zygotic DDM1 activity. Genes Dev. 13, 2971–2982.Google Scholar
  254. Vitte C. and Bennetzen J. L. 2006 Analysis of retrotransposon structural diversity uncovers properties and propensities in angiosperm genome evolution. Proc. Natl. Acad. Sci. USA 103, 17638–17643.PubMedGoogle Scholar
  255. Vogel F. and Schroeder T. M. 1974 The internal order of the interphase nucleus. Humangenetik 25, 265–297.PubMedGoogle Scholar
  256. Wada Y., Miyamoto K., Kusano H. and Sano H. 2004 Association between up-regulation of stress-responsive genes and hypomethylation of genomic DNA in tobacco plants. Mol. Genet. Genomics 271, 658–666.PubMedGoogle Scholar
  257. Walsh C. P. and Xu G. L. 2006 Cytosine methylation and DNA repair. Curr. Top Microbiol. Immunol. 301, 283–315.PubMedGoogle Scholar
  258. Wang W. S., Pan Y. J., Zhao X. Q., Dwivedi D., Zhu L. H., Ali J. et al. 2011 Drought-induced site-specific DNA methylation and its association with drought tolerance in rice (Oryza sativa L.). J. Exp. Bot. 62, 1951–1960.Google Scholar
  259. Wassenegger M. 2005 The role of the RNAi machinery in heterochromatin formation. Cell 122, 13–16.PubMedGoogle Scholar
  260. Wessler S. R. 1996 Turned on by stress. Plant retrotransposons. Curr. Biol. 6, 959–961.PubMedGoogle Scholar
  261. Wierzbicki A. T., Haag J. R. and Pikaard C. S. 2008 Non-coding transcription by RNA polymerase Pol IVb/Pol V mediates transcriptional silencing of overlapping and adjacent genes. Cell 135, 635–648.PubMedCentralPubMedGoogle Scholar
  262. Wierzbicki A. T., Ream T. S., Haag J. R. and Pikaard C. S. 2009 RNA polymerase V transcription guides ARGONAUTE4 to chromatin. Nat. Genet. 41, 630–634.PubMedCentralPubMedGoogle Scholar
  263. Wierzbicki A. T., Cocklin R., Mayampurath A., Lister R., Rowley M. J., Gregory B. D. et al. 2012 Spatial and functional relationships among Pol V-associated loci, Pol IV-dependent siRNAs, and cytosine methylation in the Arabidopsis epigenome. Genes Dev. 26, 1825–1836.Google Scholar
  264. Woo H. R. and Richards E. 2008 Natural variation in DNA methylation in ribosomal RNA genes of Arabidopsis thaliana. BMC Plant Biol. 8, 92.Google Scholar
  265. Woo H. R., Pontes O., Pikaard C. S. and Richards E. J. 2007 VIM1, a methylcytosine-binding protein required for centromeric heterochromatization. Genes Dev. 21, 267–277.PubMedGoogle Scholar
  266. Wu S. C. and Zhang Y. 2010 Active DNA demethylations: many roads lead to Rome. Nat. Rev. Mol. Cell Biol. 11, 607– 620.PubMedCentralPubMedGoogle Scholar
  267. Wu W. H., Alami S., Luk K., Wu C. H., Sen S., Mizuguchi G. et al. 2005 Swc2 is a widely conserved H2AZ-binding module essential for ATP-dependent histone exchange. Nat. Struct. Mol. Biol. 12, 1064–1071.Google Scholar
  268. Wu K., Zhang L., Zhou C., Yu C. W. and Chaikam V. 2008 HDA6 is required for jasmonate response, senescence and flowering in Arabidopsis. J. Exp. Biol. 59, 225–234.Google Scholar
  269. Xiao W. 2012 Specialized technologies for epigenetics in plants. Methods Mol. Biol. 925, 231–247.PubMedGoogle Scholar
  270. Xiao W., Custard K. D., Brown R. C., Lemmon B. E., Harada J. J., Goldberg R. B. and Fischer R. L. 2006 DNA methylation is critical for Arabidopsis embryogenesis and seed viability. Plant Cell 18, 805–814.PubMedCentralPubMedGoogle Scholar
  271. Xie Z., Johansen L. K., Gustafson A. M., Kasschau K. D., Lellis A. D., Zilberman D. et al. 2004 Genetic and functional diversification of small RNA pathways in plants. PLoS Biol. 2, e104.Google Scholar
  272. Xiong L. Z., Xu C. G., Saghai Maroof M. A. and Zhang Q. 1999 Patterns of cytosine methylation in an elite rice hybrid and its parental lines, detected by a methylation-sensitive amplification polymorphism technique. Mol. Gen. Genet. 261, 439–446.PubMedGoogle Scholar
  273. Yang Z., Ebright Y. W., Yu B. and Chen X. 2006 HEN1 recognizes 21–24 nt small RNA duplexes and deposits a methyl group on to the 2OH of the 3 terminal nucleotide. Nucleic Acids Res. 34, 667–675.PubMedCentralPubMedGoogle Scholar
  274. Yao Y. and Kovalchuk I. 2011 Abiotic stress leads to somatic and heritable changes in homologous recombination frequency, point mutation frequency and microsatellite stability in Arabidopsis plants. Mut. Res. 707, 61–66.Google Scholar
  275. You W., Tyczewska A., Spencer M., Daxinger L., Schmid M. W., Grossniklaus U. et al. 2012 Atypical DNA methylation of genes encoding cysteine-rich peptides in Arabidopsis thaliana. BMC Plant Biol. 12, 51–65.Google Scholar
  276. Yu B., Yang Z., Li J., Minakhina S., Yang M., Padgett R. W., Steward R. and Chen X. 2005 Methylation as a crucial step in plant microRNA biogenesis. Science 307, 932–935.PubMedGoogle Scholar
  277. Yu A., Lepere G., Jay F., Wang J., Bapaume L., Wang Y. et al. 2013 Dynamics and biological relevance of DNA demethylation in Arabidopsis antibacterial defense. PNAS 110, 2389–2394.Google Scholar
  278. Zemach A. and Grafi G. 2003 Characterization of Arabidopsis thaliana methyl-CpG-binding domain proteins. Plant J. 34, 565–572.PubMedGoogle Scholar
  279. Zemach A. and Grafi G. 2007 Methyl-CpG-binding domain protein in plants: interpreters of DNA methylation. Trends Plant Sci. 12, 80–85.PubMedGoogle Scholar
  280. Zemach A., Li Y., Wayburn B., Ben-Meir H., Kiss V., Avivi Y. et al. 2005 DDM1 binds Arabidopsis methyl-CpG binding domain proteins and affects their subnuclear localization. Plant Cell 17, 1549–1558.Google Scholar
  281. Zemach A., McDaniel I. E., Silva P. and Zilberman D. 2010 Genome-wide evolutionary analysis of eukaryotic DNA methylation. Science 328, 916–919.PubMedGoogle Scholar
  282. Zhang X. 2008 The epigenetic landscape of plants. Science 320, 489–492.PubMedGoogle Scholar
  283. Zhang X., Henderson I. R., Lu C., Green P. J. and Jacobsen S. E. 2007 Role of RNA polymerase IV in plant small RNA metabolism. Proc. Natl. Acad. Sci. USA 104, 4536–4541.PubMedGoogle Scholar
  284. Zhang X., Bernatavichute Y. V., Cokus S., Pellegrini M. and Jacobsen S. E. 2009 Genome-wide analysis of mono-, di- and tri-methylation of histone H3 lysine 4 in Arabidopsis thaliana. Genome Biol. 10, R62.Google Scholar
  285. Zhang W., Friebe B., Gill B. S. and Jiang J. 2010 Centromere inactivation and epigenetic modifications of a plant chromosome with three functional centromeres. Chromosoma 119, 553–563.PubMedGoogle Scholar
  286. Zhang M., Zhao H., Xie S., Chen J., Xu Y., Wang K. et al. 2011 Extensive, clustered parental imprinting of protein-coding and noncoding RNAs in developing maize endosperm. Proc. Natl. Acad. Sci. USA 108, 20042–20047.Google Scholar
  287. Zhao Y., Yu S., Xing C., Fan S. and Song M. 2008 DNA methylation in cotton hybrids and their parents. Mol. Biol. 42, 169–178.Google Scholar
  288. Zhao Y., Yu S., Ye W., Wang H., Wang J. and Fang B. 2010 Study on DNA cytosine methylation of cotton (Gossypium hirsutum L.) genome and its implications for salt tolerance. Agri. Sci. China 9, 783–791.Google Scholar
  289. Zheng B. and Chen X. 2011 Dynamics of histone H3 lysine 27 trimethylation in plant development. Curr. Opin. Plant Biol. 14, 123–129.PubMedCentralPubMedGoogle Scholar
  290. Zheng X., Zhu J., Kapoor A. and Zhu J. K. 2007 Roles of Arabidopsis AGO6 in siRNA accumulation, DNA methylation and transcriptional gene silencing. EMBO J. 26, 1691–1701.PubMedGoogle Scholar
  291. Zheng X., Pontes O., Zhu J., Miki D., Zhang F., Li W. X. et al. 2008 ROS3 is an RNA-binding protein required for DNA demethylation in Arabidopsis. Nature 455, 1259–1262.Google Scholar
  292. Zheng B., Wang Z., Li S., Yu B., Liu J. Y. and Chen X. 2009 Intergenic transcription by RNA polymerase II coordinates pol IV and pol V in siRNA-directed transcriptional gene silencing in Arabidopsis. Genes Dev. 23, 2850–2860.PubMedGoogle Scholar
  293. Zheng Z., Xing Y., He X. J., Li W., Hu Y., Yadav S. K. et al. 2010 An SGS3-like protein functions in RNA-directed DNA methylation and transcriptional gene silencing in Arabidopsis. Plant J. 62, 92–99.Google Scholar
  294. Zhong L., Xu Y.-H. and Wang J.-B. 2009 DNA-methylation changes induced by salt stress in wheat, Triticum aestivum. Afr. J. Biotech. 8, 6201–6207.Google Scholar
  295. Zhu J. K. 2009 Active DNA methylation mediated by DNA glycosylases. Ann. Rev. Genet. 43, 143–166.PubMedCentralPubMedGoogle Scholar
  296. Zhu J., Kapoor A., Sridhar V. V., Agius F. and Zhu J. K. 2007 The DNA glycosylase/lyase ROS1 functions in pruning DNA methylation patterns in Arabidopsis. Curr. Biol. 17, 54–59.PubMedGoogle Scholar
  297. Zhu R., Shevchenko O., Ma C., Maury S., Freitag M. and Strauss S. H. 2013 Poplars with a PtDDM-RNAi transgene have reduced DNA methylation and show aberrant post-dormancy morphology. Planta 237, 1483–1493.PubMedGoogle Scholar
  298. Zilberman D., Cao X. and Jacobsen S. E. 2003 ARGONAUTE 4 control of locus-specific siRNA accumulation and DNA histone methylation. Science 299, 716–719.PubMedGoogle Scholar
  299. Zilberman D., Cao X., Johansen L. K., Xie Z., Carrington J. C. and Jacobsen S. E. 2004 Role of Arabidopsis ARGONAUTE4 in RNA-directed DNA methylation triggered by inverted repeats. Curr. Biol. 14, 1214–1220.PubMedGoogle Scholar
  300. Zilberman D., Coleman-Derr D., Ballinger T. and Henikoff S. 2008 Histone H2A.Z and DNA methylation are mutually antagonistic chromatin marks. Nature 456, 125–129.PubMedCentralPubMedGoogle Scholar
  301. Zubko E., Gentry M., Kunova A. and Meyer P. 2012 De novo DNA methylation activity of METHYLTRANSFERASE 1 (MET1) partially restores body methylation in Arabidopsis thaliana. Plant J. 71, 1029–1037.PubMedGoogle Scholar

Copyright information

© Indian Academy of Sciences 2013

Authors and Affiliations

  • SUSHIL KUMAR
    • 1
    • 2
    Email author
  • RENU KUMARI
    • 1
    • 3
  • VISHAKHA SHARMA
    • 1
    • 2
  • VINAY SHARMA
    • 3
  1. 1.National Institute of Plant Genome Research (NIPGR)New DelhiIndia
  2. 2.SKA Institution for Research, Education and Development (SKAIRED)New DelhiIndia
  3. 3.Banasthali UniversityBanasthaliIndia

Personalised recommendations