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Epigenomic landscape and epigenetic regulation in maize


Key message

Epigenetic regulation has been implicated in the control of multiple agronomic traits in maize. Here, we review current advances in our understanding of epigenetic regulation, which has great potential for improving agronomic traits and the environmental adaptability of crops.


Epigenetic regulation plays vital role in the control of complex agronomic traits. Epigenetic variation could contribute to phenotypic diversity and can be used to improve the quality and productivity of crops. Maize (Zea mays L.), one of the most widely cultivated crops for human food, animal feed, and ethanol biofuel, is a model plant for genetic studies. Recent advances in high-throughput sequencing technology have made possible the study of epigenetic regulation in maize on a genome-wide scale. In this review, we discuss recent epigenetic studies in maize many achieved by Chinese research groups. These studies have explored the roles of DNA methylation, posttranslational modifications of histones, chromatin remodeling, and noncoding RNAs in the regulation of gene expression in plant development and environment response. We also provide our future prospects for manipulating epigenetic regulation to improve crops.

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  1. Alejandri-Ramirez ND, Chavez-Hernandez EC, Contreras-Guerra JL, Reyes JL, Dinkova TD (2018) Small RNA differential expression and regulation in Tuxpeno maize embryogenic callus induction and establishment. Plant Physiol Biochem 122:78–89

  2. Anderson SN, Stitzer MC, Brohammer AB, Zhou P, Noshay JM, O’Connor CH, Hirsch CD, Ross-Ibarra J, Hirsch CN, Springer NM (2019) Transposable elements contribute to dynamic genome content in maize. Plant J 100:1052–1065

  3. Annemieke JM, De Ruijter AJ, van Gennip AH, Caron HN, Andre SK, Kuilenburg BP (2003) Histone deacetylases HDACs: characterization of the classical HDAC family. Biochem J 370:737–749

  4. Aravind J, Rinku S, Pooja B, Shikha M, Kaliyugam S, Mallikarjuna MG, Kumar A, Rao AR, Nepolean T (2017) Identification, characterization, and functional validation of drought-responsive MicroRNAs in subtropical maize inbreds. Front Plant Sci 8:941

  5. Bartel DP (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116:281–297

  6. Bartels A, Han Q, Nair P, Stacey L, Gaynier H, Mosley M, Huang QQ, Pearson JK, Hsieh TF, An YC, Xiao W (2018) Dynamic DNA Methylation in plant growth and development. Int J Mol Sci 19:2144

  7. Bartolomei MS, Ferguson-Smith AC (2011) Mammalian genomic imprinting. Cold Spring Harb Perspect Biol 3:a002592

  8. Berdasco M, Ropero S, Setien F, Fraga MF, Lapunzina P, Losson R, Alaminos M, Cheung NK, Rahman N, Esteller M (2009) Epigenetic inactivation of the Sotos overgrowth syndrome gene histone methyltransferase NSD1 in human neuroblastoma and glioma. Proc Natl Acad Sci U S A 106:21830–21835

  9. Bernatavichute YV, Zhang X, Cokus S, Pellegrini M, Jacobsen SE (2008) Genome-wide association of histone H3 lysine nine methylation with CHG DNA methylation in Arabidopsis thaliana. PLoS ONE 3:e3156

  10. Berr A, Shafiq S, Shen WH (2011) Histone modifications in transcriptional activation during plant development. Biochim Biophys Acta 1809:567–576

  11. Bheda P, Schneider R (2014) Epigenetics reloaded: the single-cell revolution. Trends Cell Biol 24:712–723

  12. Bird A (2002) DNA methylation patterns and epigenetic memory. Genes Dev 16:6–21

  13. Candaele J, Demuynck K, Mosoti D, Beemster GT, Inze D, Nelissen H (2014) Differential methylation during maize leaf growth targets developmentally regulated genes. Plant Physiol 164:1350–1364

  14. Cao X, Springer NM, Muszynski MG, Phillips RL, Kaeppler S, Jacobsen SE (2000) Conserved plant genes with similarity to mammalian de novo DNA methyltransferases. Proc Natl Acad Sci U S A 97:4979–4984

  15. Cao R, Tsukada Y, Zhang Y (2005) Role of Bmi-1 and Ring1A in H2A ubiquitylation and Hox gene silencing. Mol Cell 20:845–854

  16. Capitao C, Paiva JA, Santos DM, Fevereiro P (2011) In Medicago truncatula, water deficit modulates the transcript accumulation of components of small RNA pathways. BMC Plant Biol 11:79

  17. Carrington JC, Ambros V (2003) Role of microRNAs in plant and animal development. Science 301:336–338

  18. Chan SW, Henderson IR, Jacobsen SE (2005) Gardening the genome: DNA methylation in Arabidopsis thaliana. Nat Rev Genet 6:351–360

  19. Chandler V, Walbot V (1986) DNA modification of a maize transposable element correlates with loss of activity. PNAS 83:1767–1771

  20. Charron JB, He H, Elling AA, Deng XW (2009) Dynamic landscapes of four histone modifications during deetiolation in Arabidopsis. Plant Cell 21:3732–3748

  21. Chavez-Hernandez EC, Alejandri-Ramirez ND, Juarez-Gonzalez VT, Dinkova TD (2015) Maize miRNA and target regulation in response to hormone depletion and light exposure during somatic embryogenesis. Front Plant Sci 6:555

  22. Chen L, Ding X, Zhang H, He T, Li Y, Wang T, Li X, Jin L, Song Q, Yang S, Gai J (2018) Comparative analysis of circular RNAs between soybean cytoplasmic male-sterile line NJCMS1A and its maintainer NJCMS1B by high-throughput sequencing. BMC Genom 19:663

  23. Chinnusamy V, Zhu JK (2009) Epigenetic regulation of stress responses in plants. Curr Opin Plant Biol 12:133–139

  24. Choi Y, Gehring M, Johnson L, Hannon M, Harada JJ, Goldberg RB, Jacobsen SE, Fischer RL (2002) DEMETER, a DNA glycosylase domain protein, is required for endosperm gene imprinting and seed viability in arabidopsis. Cell 110:33–42

  25. Ci D, Tian M, Song Y, Du Q, Quan M, Xuan A, Yu J, Yuan Z, Zhang D (2019) Indole-3-acetic acid has long-term effects on long non-coding RNA gene methylation and growth in Populus tomentosa. Mol Genet Genom 294:1511–1525

  26. Clapier CR, Cairns BR (2009) The biology of chromatin remodeling complexes. Annu Rev Biochem 78:273–304

  27. Creyghton MP, Cheng AW, Welstead GG, Kooistra T, Carey BW, Steine EJ, Hanna J, Lodato MA, Frampton GM, Sharp PA, Boyer LA, Young RA, Jaenisch R (2010) Histone H3K27ac separates active from poised enhancers and predicts developmental state. Proc Natl Acad Sci U S A 107:21931–21936

  28. Cui X, Jin P, Cui X, Gu L, Lu Z, Xue Y, Wei L, Qi J, Song X, Luo M, An G, Cao X (2013) Control of transposon activity by a histone H3K4 demethylase in rice. Proc Natl Acad Sci U S A 110:1953–1958

  29. Cui X, Liang Z, Shen L, Zhang Q, Bao S, Geng Y, Zhang B, Leo V, Vardy LA, Lu T, Gu X, Yu H (2017) 5-methylcytosine RNA methylation in Arabidopsis thaliana. Mol Plant 10:1387–1399

  30. Dai J, Sultan S, Taylor SS, Higgins JM (2005) The kinase haspin is required for mitotic histone H3 Thr 3 phosphorylation and normal metaphase chromosome alignment. Genes Dev 19:472–488

  31. Danilevskaya ON (2003) Duplicated fie genes in maize: expression pattern and imprinting suggest distinct functions. Plant Cell 15:425–438

  32. Danilevskaya ON, Meng X, Hou Z, Ananiev EV, Simmons CR (2008) A genomic and expression compendium of the expanded PEBP gene family from maize. Plant Physiol 146:250–264

  33. Darbani B, Noeparvar S, Borg S (2016) Identification of circular RNAs from the parental genes involved in multiple aspects of cellular metabolism in barley. Front Plant Sci 7:776

  34. Deal RB, Henikoff S (2011) The INTACT method for cell type-specific gene expression and chromatin profiling in Arabidopsis thaliana. Nat Protoc 6:56–68

  35. Deng X, Song X, Wei L, Liu C, Cao X (2016) Epigenetic regulation and epigenomic landscape in rice. Natl Sci Rev 3:309–327

  36. Ding Y, Wang X, Su L, Zhai J, Cao S, Zhang D, Liu C, Bi Y, Qian Q, Cheng Z, Chu C, Cao X (2007) SDG714, a histone H3K9 methyltransferase, is involved in Tos17 DNA methylation and transposition in rice. Plant Cell 19:9–22

  37. Ding D, Wang Y, Han M, Fu Z, Li W, Liu Z, Hu Y, Tang J (2012) MicroRNA transcriptomic analysis of heterosis during maize seed germination. PLoS ONE 7:e39578

  38. Ding D, Li W, Han M, Wang Y, Fu Z, Wang B, Tang J (2014a) Identification and characterisation of maize microRNAs involved in developing ears. Plant Biol (Stuttg) 16:9–15

  39. Ding H, Gao J, Qin C, Ma H, Huang H, Song P, Luo X, Lin H, Shen Y, Pan G, Zhang Z (2014b) The dynamics of DNA methylation in maize roots under Pb stress. Int J Mol Sci 15:23537–23554

  40. Dion MF, Altschuler SJ, Wu LF, Rando OJ (2005) Genomic characterization reveals a simple histone H4 acetylation code. Proc Natl Acad Sci U S A 102:5501–5506

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

  42. Dong X, Zhang M, Chen J, Peng L, Zhang N, Wang X, Lai J (2017) Dynamic and antagonistic allele-specific epigenetic modifications controlling the expression of imprinted genes in maize endosperm. Mol Plant 10:442–455

  43. Dong X, Chen J, Li T, Li E, Zhang X, Zhang M, Song W, Zhao H, Lai J (2018) Parent-of-origin-dependent nucleosome organization correlates with genomic imprinting in maize. Genome Res 28:1020–1028

  44. Dotto MC, Petsch KA, Aukerman MJ, Beatty M, Hammell M, Timmermans MC (2014) Genome-wide analysis of leafbladeless1-regulated and phased small RNAs underscores the importance of the TAS3 ta-siRNA pathway to maize development. PLoS Genet 10:e1004826

  45. Doyon Y, Cayrou C, Ullah M, Landry AJ, Cote V, Selleck W, Lane WS, Tan S, Yang XJ, Cote J (2006) ING tumor suppressor proteins are critical regulators of chromatin acetylation required for genome expression and perpetuation. Mol Cell 21:51–64

  46. Du J, Zhong X, Bernatavichute YV, Stroud H, Feng S, Caro E, Vashisht AA, Terragni J, Chin HG, Tu A, Hetzel J, Wohlschlegel JA, Pradhan S, Patel DJ, Jacobsen SE (2012) Dual binding of chromomethylase domains to H3K9me2-containing nucleosomes directs DNA methylation in plants. Cell 151:167–180

  47. Du J, Johnson LM, Jacobsen SE, Patel DJ (2015) DNA methylation pathways and their crosstalk with histone methylation. Nat Rev Mol Cell Biol 16:519–532

  48. Du Q, Wang K, Zou C, Xu C, Li WX (2018) The PILNCR1-miR399 regulatory module is important for low phosphate tolerance in maize. Plant Physiol 177:1743–1753

  49. Duan HC, Wei LH, Zhang C, Wang Y, Chen L, Lu ZK, Chen PR, He C, Jia GF (2017) ALKBH10B Is an RNA N-6-methyladenosine demethylase affecting Arabidopsis floral transition. Plant Cell 29:2995–3011

  50. Duan CG, Zhu JK, Cao X (2018) Retrospective and perspective of plant epigenetics in China. J Genet Genom 45:621–638

  51. Eberharter A, Becker PB (2002) Histone acetylation_ a switch between repressive and permissive chromatin. Second in review series on chromatin dynamics. EMBO Rep 3:224–229

  52. Eichten SR, Springer NM (2015) Minimal evidence for consistent changes in maize DNA methylation patterns following environmental stress. Front Plant Sci 6:308

  53. Eichten SR, Swanson-Wagner RA, Schnable JC, Waters AJ, Hermanson PJ, Liu S, Yeh CT, Jia Y, Gendler K, Freeling M, Schnable PS, Vaughn MW, Springer NM (2011) Heritable epigenetic variation among maize inbreds. PLoS Genet 7:e1002372

  54. Eichten SR, Ellis NA, Makarevitch I, Yeh CT, Gent JI, Guo L, McGinnis KM, Zhang X, Schnable PS, Vaughn MW, Dawe RK, Springer NM (2012) Spreading of heterochromatin is limited to specific families of maize retrotransposons. PLoS Genet 8:e1003127

  55. Eichten SR, Briskine R, Song J, Li Q, Swanson-Wagner R, Hermanson PJ, Waters AJ, Starr E, West PT, Tiffin P, Myers CL, Vaughn MW, Springer NM (2013a) Epigenetic and genetic influences on DNA methylation variation in maize populations. Plant Cell 25:2783–2797

  56. Eichten SR, Vaughn MW, Hermanson PJ, Springer NM (2013b) Variation in DNA methylation patterns is more common among maize inbreds than among tissues. Plant Genome 6:1–10

  57. Erhard KF Jr, Stonaker JL, Parkinson SE, Lim JP, Hale CJ, Hollick JB (2009) RNA polymerase IV functions in paramutation in Zea mays. Science 323:1201–1205

  58. Fahlgren N, Montgomery TA, Howell MD, Allen E, Dvorak SK, Alexander AL, Carrington JC (2006) Regulation of AUXIN RESPONSE FACTOR3 by TAS3 ta-siRNA affects developmental timing and patterning in Arabidopsis. Curr Biol 16:939–944

  59. Fan C, Hao Z, Yan J, Li G (2015) Genome-wide identification and functional analysis of lincRNAs acting as miRNA targets or decoys in maize. BMC Genom 16:793

  60. Ferguson-Smith AC (2011) Genomic imprinting: the emergence of an epigenetic paradigm. Nat Rev Genet 12:565–575

  61. Fire A, Xu S, Montgomery MK, Kostas SA, Driver SE, Mello CC (1998) Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 391:806–811

  62. Forestan C, Farinati S, Rouster J, Lassagne H, Lauria M, Dal Ferro N, Varotto S (2018) Control of maize vegetative and reproductive development, fertility, and rRNAs silencing by histone deacetylase 108. Genetics 208:1443–1466

  63. Fritsch TE, Siqueira FM, Schrank IS (2018) Global analysis of sRNA target genes in Mycoplasma hyopneumoniae. BMC Genom 19:767

  64. Fu R, Zhang M, Zhao Y, He X, Ding C, Wang S, Feng Y, Song X, Li P, Wang B (2017) Identification of salt tolerance-related microRNAs and their targets in maize (Zea mays L.) using high-throughput sequencing and degradome analysis. Front Plant Sci 8:864

  65. Fuchs J, Demidov D, Houben A, Schubert I (2006) Chromosomal histone modification patterns–from conservation to diversity. Trends Plant Sci 11:199–208

  66. Gao Z, Li J, Luo M, Li H, Chen Q, Wang L, Song S, Zhao L, Xu W, Zhang C, Wang S, Ma C (2019) Characterization and cloning of grape circular RNAs identified the cold resistance-related Vv-circATS1. Plant Physiol 180:966–985

  67. Gayon J (2016) From mendel to epigenetics: history of genetics. Comptes Rendus Biol 339:225–230

  68. Ge F, Huang X, Hu H, Zhang Y, Li Z, Zou C, Peng H, Li L, Gao S, Pan G, Shen Y (2017) Endogenous small interfering RNAs associated with maize embryonic callus formation. PLoS ONE 12:e0180567

  69. Gehring M (2013) Genomic imprinting: insights from plants. Annu Rev Genet 47:187–208

  70. Gehring M, Choi Y, Fischer RL (2004) Imprinting and seed development. Plant Cell 16(Suppl):S203–S213

  71. Gehring M, Huh JH, Hsieh TF, Penterman J, Choi Y, Harada JJ, Goldberg RB, Fischer RL (2006) DEMETER DNA glycosylase establishes MEDEA polycomb gene self-imprinting by allele-specific demethylation. Cell 124:495–506

  72. Genger RK, Kovac KA, Dennis ES, Peacock WJ, Finnegan EJ (1999) Multiple DNA methyltransferase genes in Arabidopsis thaliana. Plant Mol Biol 41:269–278

  73. Gent JI, Dong Y, Jiang J, Dawe RK (2012) Strong epigenetic similarity between maize centromeric and pericentromeric regions at the level of small RNAs, DNA methylation and H3 chromatin modifications. Nucleic Acids Res 40:1550–1560

  74. Gent JI, Ellis NA, Guo L, Harkess AE, Yao Y, Zhang X, Dawe RK (2013) CHH islands: de novo DNA methylation in near-gene chromatin regulation in maize. Genome Res 23:628–637

  75. Gent JI, Madzima TF, Bader R, Kent MR, Zhang X, Stam M, McGinnis KM, Dawe RK (2014) Accessible DNA and relative depletion of H3K9me2 at maize loci undergoing RNA-directed DNA methylation. Plant Cell 26:4903–4917

  76. Ghorbani A, Izadpanah K, Peters JR, Dietzgen RG, Mitter N (2018) Detection and profiling of circular RNAs in uninfected and maize Iranian mosaic virus-infected maize. Plant Sci 274:402–409

  77. Grossniklaus U, Paro R (2014) Transcriptional silencing by polycomb-group proteins. Cold Spring Harb Perspect Biol 6:a019331

  78. Gruber JJ, Geller B, Lipchik AM, Chen J, Salahudeen AA, Ram AN, Ford JM, Kuo CJ, Snyder MP (2019) HAT1 coordinates histone production and acetylation via H4 promoter binding. Mol Cell 75(711–724):e715

  79. Gu Y, Liu Y, Zhang J, Liu H, Hu Y, Du H, Li Y, Chen J, Wei B, Huang Y (2013) Identification and characterization of microRNAs in the developing maize endosperm. Genomics 102:472–478

  80. Gutierrez-Marcos JF, Costa LM, Biderre-Petit C, Khbaya B, O’Sullivan DM, Wormald M, Perez P, Dickinson HG (2004) Maternally expressed gene1 is a novel maize endosperm transfer cell-specific gene with a maternal parent-of-origin pattern of expression. Plant Cell 16:1288–1301

  81. Gutierrez-Marcos JF, Costa LM, Dal Pra M, Scholten S, Kranz E, Perez P, Dickinson HG (2006) Epigenetic asymmetry of imprinted genes in plant gametes. Nat Genet 38:876–878

  82. Guttman M, Russell P, Ingolia NT, Weissman JS, Lander ES (2013) Ribosome profiling provides evidence that large noncoding RNAs do not encode proteins. Cell 154:240–251

  83. Han Z, Crisp PA, Stelpflug S, Kaeppler SM, Li Q, Springer NM (2018) Heritable epigenomic changes to the maize methylome resulting from tissue culture. Genetics 209:983–995

  84. Haring M, Bader R, Louwers M, Schwabe A, van Driel R, Stam M (2010) The role of DNA methylation, nucleosome occupancy and histone modifications in paramutation. Plant J 63:366–378

  85. Haun WJ, Springer NM (2008) Maternal and paternal alleles exhibit differential histone methylation and acetylation at maize imprinted genes. Plant J 56:903–912

  86. Haun WJ, Laoueille-Duprat S, O’Connell MJ, Spillane C, Grossniklaus U, Phillips AR, Kaeppler SM, Springer NM (2007) Genomic imprinting, methylation and molecular evolution of maize Enhancer of zeste (Mez) homologs. Plant J 49:325–337

  87. He Y (2012) Chromatin regulation of flowering. Trends Plant Sci 17:556–562

  88. He G, Zhu X, Elling AA, Chen L, Wang X, Guo L, Liang M, He H, Zhang H, Chen F, Qi Y, Chen R, Deng XW (2010) Global epigenetic and transcriptional trends among two rice subspecies and their reciprocal hybrids. Plant Cell 22:17–33

  89. He G, Elling AA, Deng XW (2011) The epigenome and plant development. Annu Rev Plant Biol 62:411–435

  90. He G, Chen B, Wang X, Li X, Li J, He H, Yang M, Lu L, Qi Y, Wang X, Deng XW (2013) Conservation and divergence of transcriptomic and epigenomic variation in maize hybrids. Genome Biol 14:R57

  91. He X, Guo S, Wang Y, Wang L, Shu S, Sun J (2019) Systematic identification and analysis of heat-stress-responsive lncRNAs, circRNAs and miRNAs with associated co-expression and ceRNA networks in cucumber (Cucumis sativus L.). Physiol Plant.

  92. Hernando CE, Sanchez SE, Mancini E, Yanovsky MJ (2015) Genome wide comparative analysis of the effects of PRMT5 and PRMT4/CARM1 arginine methyltransferases on the Arabidopsis thaliana transcriptome. BMC Genom 16:192

  93. Horst I, Offermann S, Dreesen B, Niessen M, Peterhansel C (2009) Core promoter acetylation is not required for high transcription from the phosphoenolpyruvate carboxylase promoter in maize. Epigenetics Chromatin 2:17

  94. Hossfeld U, Jacobsen HJ, Plass C, Brors B, Wackernagel W (2017) 150 years of Johann Gregor Mendel’s “Versuche uber Pflanzen-Hybriden”. Mol Genet Genom 292:1–3

  95. Hou H, Zheng X, Zhang H, Yue M, Hu Y, Zhou H, Wang Q, Xie C, Wang P, Li L (2017) Histone deacetylase is required for GA-induced programmed cell death in maize aleurone layers. Plant Physiol 175:1484–1496

  96. Hou J, Lu D, Mason AS, Li B, Xiao M, An S, Fu D (2019) Non-coding RNAs and transposable elements in plant genomes: emergence, regulatory mechanisms and roles in plant development and stress responses. Planta 250:23–40

  97. Hsu FM, Yen MR, Wang CT, Lin CY, Wang CR, Chen PY (2017) Optimized reduced representation bisulfite sequencing reveals tissue-specific mCHH islands in maize. Epigenetics Chromatin 10:42

  98. Hu Y, Zhang L, Zhao L, Li J, He S, Zhou K, Yang F, Huang M, Jiang L, Li L (2011) Trichostatin A selectively suppresses the cold-induced transcription of the ZmDREB1 gene in maize. PLoS One 6:e22132

  99. Hu Y, Zhang L, He S, Huang M, Tan J, Zhao L, Yan S, Li H, Zhou K, Liang Y, Li L (2012) Cold stress selectively unsilences tandem repeats in heterochromatin associated with accumulation of H3K9ac. Plant Cell Environ 35:2130–2142

  100. Huanca-Mamani W, Arias-Carrasco R, Cardenas-Ninasivincha S, Rojas-Herrera M, Sepulveda-Hermosilla G, Caris-Maldonado JC, Bastias E, Maracaja-Coutinho V (2018) Long non-coding RNAs responsive to salt and boron stress in the hyper-arid Lluteno maize from Atacama Desert. Genes (Basel) 9:170

  101. Huang J, Lynn JS, Schulte L, Vendramin S, McGinnis K (2017) Epigenetic control of gene expression in maize. Int Rev Cell Mol Biol 328:25–48

  102. Hughes CM, Rozenblatt-Rosen O, Milne TA, Copeland TD, Levine SS, Lee JC, Hayes DN, Shanmugam KS, Bhattacharjee A, Biondi CA, Kay GF, Hayward NK, Hess JL, Meyerson M (2004) Menin associates with a trithorax family histone methyltransferase complex and with the hoxc8 locus. Mol Cell 13:587–597

  103. Iqbal MS, Jabbar B, Sharif MN, Ali Q, Husnain T, Nasir IA (2017) In silico MCMV silencing concludes potential host-derived miRNAs in maize. Front Plant Sci 8:372

  104. Jasencakova Z, Meister A, Walter J, Turner BM, Schubert I (2000) Histone H4 acetylation of euchromatin and heterochromatin is cell cycle dependent and correlated with replication rather than with transcription. Plant Cell 12:2087–2100

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

  106. Ji L, Neumann DA, Schmitz RJ (2015) Crop epigenomics: identifying, unlocking, and harnessing cryptic variation in crop genomes. Mol Plant 8:860–870

  107. Jiang F, Doudna JA (2017) CRISPR-Cas9 structures and mechanisms. Annu Rev Biophys 46:505–529

  108. Jiang P, Wang S, Ikram AU, Xu Z, Jiang H, Cheng B, Ding Y (2018) SDG721 and SDG705 are required for rice growth. J Integr Plant Biol 60:530–535

  109. Jin X, Fu Z, Lv P, Peng Q, Ding D, Li W, Tang J (2015) Identification and characterization of microRNAs during maize grain filling. PLoS One 10:e0125800

  110. Jullien PE, Kinoshita T, Ohad N, Berger F (2006) Maintenance of DNA methylation during the Arabidopsis life cycle is essential for parental imprinting. Plant Cell 18:1360–1372

  111. Kaeppler SM, Phillips RL (1993) Tissue culture-induced DNA methylation variation in maize. Proc Natl Acad Sci U S A 90:8773–8776

  112. Kang M, Zhao Q, Zhu D, Yu J (2012) Characterization of microRNAs expression during maize seed development. BMC Genom 13:360

  113. Kermicle J (1970) Dependence of the R-mottled aleurone phenotype in maize on mode of sexual transmission. Genetics 66:69–85

  114. Kermicle JL, Alleman M (1990) Gametic imprinting in maize in relation to the angiosperm life cycle. Dev Suppl 108:9–14

  115. Kim DH, Sung S (2014) Polycomb-mediated gene silencing in Arabidopsis thaliana. Mol Cells 37:841–850

  116. Kim JM, To TK, Ishida J, Morosawa T, Kawashima M, Matsui A, Toyoda T, Kimura H, Shinozaki K, Seki M (2008) Alterations of lysine modifications on the histone H3 N-tail under drought stress conditions in Arabidopsis thaliana. Plant Cell Physiol 49:1580–1588

  117. Kim JS, Mizoi J, Yoshida T, Fujita Y, Nakajima J, Ohori T, Todaka D, Nakashima K, Hirayama T, Shinozaki K, Yamaguchi-Shinozaki K (2011) An ABRE promoter sequence is involved in osmotic stress-responsive expression of the DREB2A gene, which encodes a transcription factor regulating drought-inducible genes in Arabidopsis. Plant Cell Physiol 52:2136–2146

  118. Kim YJ, Wang R, Gao L, Li D, Xu C, Mang H, Jeon J, Chen X, Zhong X, Kwak JM, Mo B, Xiao L, Chen X (2016) POWERDRESS and HDA9 interact and promote histone H3 deacetylation at specific genomic sites in Arabidopsis. Proc Natl Acad Sci U S A 113:14858–14863

  119. Kinoshita T, Miura A, Choi Y, Kinoshita Y, Cao X, Jacobsen SE, Fischer RL, Kakutani T (2004) One-way control of FWA imprinting in Arabidopsis endosperm by DNA methylation. Science 303:521–523

  120. Klose RJ, Zhang Y (2007) Regulation of histone methylation by demethylimination and demethylation. Nat Rev Mol Cell Biol 8:307–318

  121. Kong X, Zhang M, Xu X, Li X, Li C, Ding Z (2014) System analysis of microRNAs in the development and aluminium stress responses of the maize root system. Plant Biotechnol J 12:1108–1121

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

  123. Krebs JE (2007) Moving marks: dynamic histone modifications in yeast. Mol Biosyst 3:590–597

  124. Kuo YM, Andrews AJ (2013) Quantitating the specificity and selectivity of Gcn5-mediated acetylation of histone H3. PLoS One 8:e54896

  125. Lai X, Bazin J, Webb S, Crespi M, Zubieta C, Conn SJ (2018) CircRNAs in Plants. Adv Exp Med Biol 1087:329–343

  126. Lario LD, Ramirez-Parra E, Gutierrez C, Spampinato CP, Casati P (2013) ANTI-SILENCING FUNCTION1 proteins are involved in ultraviolet-induced DNA damage repair and are cell cycle regulated by E2F transcription factors in Arabidopsis. Plant Physiol 162:1164–1177

  127. Lauria M, Rupe M, Guo M, Kranz E, Pirona R, Viotti A, Lund G (2004) Extensive maternal DNA hypomethylation in the endosperm of Zea mays. Plant Cell 16:510–522

  128. Lauria M, Echegoyen-Nava RA, Rodriguez-Rios D, Zaina S, Lund G (2017) Inter-individual variation in DNA methylation is largely restricted to tissue-specific differentially methylated regions in maize. BMC Plant Biol 17:52

  129. Law JA, Jacobsen SE (2010) Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nat Rev Genet 11:204–220

  130. Lazakis CM, Coneva V, Colasanti J (2011) ZCN8 encodes a potential orthologue of Arabidopsis FT florigen that integrates both endogenous and photoperiod flowering signals in maize. J Exp Bot 62:4833–4842

  131. Li E, Zhang Y (2014) DNA methylation in mammals. Cold Spring Harb Perspect Biol 6:a019133

  132. Li X, Wang X, He K, Ma Y, Su N, He H, Stolc V, Tongprasit W, Jin W, Jiang J, Terzaghi W, Li S, Deng XW (2008) High-resolution mapping of epigenetic modifications of the rice genome uncovers interplay between DNA methylation, histone methylation, and gene expression. Plant Cell 20:259–276

  133. Li W, Liu H, Cheng ZJ, Su YH, Han HN, Zhang Y, Zhang XS (2011) DNA methylation and histone modifications regulate de novo shoot regeneration in Arabidopsis by modulating WUSCHEL expression and auxin signaling. PLoS Genet 7:e1002243

  134. Li J, Guo G, Guo W, Guo G, Tong D, Ni Z, Sun Q, Yao Y (2012) miRNA164-directed cleavage of ZmNAC1 confers lateral root development in maize (Zea mays L.). BMC Plant Biol 12:220

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

  136. Li L, Eichten SR, Shimizu R, Petsch K, Yeh CT, Wu W, Chettoor AM, Givan SA, Cole RA, Fowler JE, Evans MM, Scanlon MJ, Yu J, Schnable PS, Timmermans MC, Springer NM, Muehlbauer GJ (2014b) Genome-wide discovery and characterization of maize long non-coding RNAs. Genome Biol 15:R40

  137. Li Q, Eichten SR, Hermanson PJ, Springer NM (2014c) Inheritance patterns and stability of DNA methylation variation in maize near-isogenic lines. Genetics 196:667–676

  138. Li Q, Eichten SR, Hermanson PJ, Zaunbrecher VM, Song J, Wendt J, Rosenbaum H, Madzima TF, Sloan AE, Huang J, Burgess DL, Richmond TA, McGinnis KM, Meeley RB, Danilevskaya ON, Vaughn MW, Kaeppler SM, Jeddeloh JA, Springer NM (2014d) Genetic perturbation of the maize methylome. Plant Cell 26:4602–4616

  139. Li Q, Gent JI, Zynda G, Song J, Makarevitch I, Hirsch CD, Hirsch CN, Dawe RK, Madzima TF, McGinnis KM, Lisch D, Schmitz RJ, Vaughn MW, Springer NM (2015a) RNA-directed DNA methylation enforces boundaries between heterochromatin and euchromatin in the maize genome. Proc Natl Acad Sci U S A 112:14728–14733

  140. Li Q, Song J, West PT, Zynda G, Eichten SR, Vaughn MW, Springer NM (2015b) Examining the causes and consequences of context-specific differential DNA methylation in maize. Plant Physiol 168:1262–1274

  141. Li D, Liu Z, Gao L, Wang L, Gao M, Jiao Z, Qiao H, Yang J, Chen M, Yao L, Liu R, Kan Y (2016a) Genome-wide identification and characterization of microRNAs in developing grains of Zea mays L. PLoS One 11:e0153168

  142. Li Z, Zhang X, Liu X, Zhao Y, Wang B, Zhang J (2016b) miRNA alterations are important mechanism in maize adaptations to low-phosphate environments. Plant Sci 252:103–117

  143. Li H, Peng T, Wang Q, Wu Y, Chang J, Zhang M, Tang G, Li C (2017a) Development of incompletely fused carpels in maize ovary revealed by miRNA, target gene and phytohormone analysis. Front Plant Sci 8:463

  144. Li S, Castillo-Gonzalez C, Yu B, Zhang X (2017b) The functions of plant small RNAs in development and in stress responses. Plant J 90:654–670

  145. Li Y, Dong XM, Jin F, Shen Z, Chao Q, Wang BC (2017c) Histone acetylation modifications affect tissue-dependent expression of poplar homologs of C4 photosynthetic enzyme genes. Front Plant Sci 8:950

  146. Li A, Li G, Zhao Y, Meng Z, Zhao M, Li C, Zhang Y, Li P, Ma CL, Xia H, Zhao S, Hou L, Zhao C, Wang X (2018a) Combined small RNA and gene expression analysis revealed roles of miRNAs in maize response to rice black-streaked dwarf virus infection. Sci Rep 8:13502

  147. Li X, Harris CJ, Zhong Z, Chen W, Liu R, Jia B, Wang Z, Li S, Jacobsen SE, Du J (2018b) Mechanistic insights into plant SUVH family H3K9 methyltransferases and their binding to context-biased non-CG DNA methylation. Proc Natl Acad Sci U S A 115:E8793–E8802

  148. Li S, Cai J, Lu H, Mao S, Dai S, Hu J, Wang L, Hua X, Xu H, Tian B, Zhao Y, Hua Y (2019) N(4)-cytosine DNA methylation is involved in the maintenance of genomic stability in Deinococcus radiodurans. Front Microbiol 10:1905

  149. Liang Z, Shen L, Cui X, Bao S, Geng Y, Yu G, Liang F, Xie S, Lu T, Gu X, Yu H (2018) DNA N(6)-adenine methylation in Arabidopsis thaliana. Dev Cell 45(406–416):e403

  150. Lippman Z, Gendrel AV, Black M, Vaughn MW, Dedhia N, McCombie WR, Lavine K, Mittal V, May B, Kasschau KD, Carrington JC, Doerge RW, Colot V, Martienssen R (2004) Role of transposable elements in heterochromatin and epigenetic control. Nature 430:471–476

  151. Liu S, Yu Y, Ruan Y, Meyer D, Wolff M, Xu L, Wang N, Steinmetz A, Shen WH (2007) Plant SET- and RING-associated domain proteins in heterochromatinization. Plant J 52:914–926

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

  153. Liu Y, Ye N, Liu R, Chen M, Zhang J (2010b) H2O2 mediates the regulation of ABA catabolism and GA biosynthesis in Arabidopsis seed dormancy and germination. J Exp Bot 61:2979–2990

  154. Liu P, Yan K, Lei YX, Xu R, Zhang YM, Yang GD, Huang JG, Wu CA, Zheng CC (2013) Transcript profiling of microRNAs during the early development of the maize brace root via Solexa sequencing. Genomics 101:149–156

  155. Liu H, Qin C, Chen Z, Zuo T, Yang X, Zhou H, Xu M, Cao S, Shen Y, Lin H, He X, Zhang Y, Li L, Ding H, Lubberstedt T, Zhang Z, Pan G (2014) Identification of miRNAs and their target genes in developing maize ears by combined small RNA and degradome sequencing. BMC Genom 15:25

  156. Liu H, Ma L, Yang X, Zhang L, Zeng X, Xie S, Peng H, Gao S, Lin H, Pan G, Wu Y, Shen Y (2017a) Integrative analysis of DNA methylation, mRNAs, and small RNAs during maize embryo dedifferentiation. BMC Plant Biol 17:105

  157. Liu SR, Zhou JJ, Hu CG, Wei CL, Zhang JZ (2017b) MicroRNA-mediated gene silencing in plant defense and viral counter-defense. Front Microbiol 8:1801

  158. Long JC, Xia AA, Liu JH, Jing JL, Wang YZ, Qi CY, He Y (2019) Decrease in DNA methylation 1 (DDM1) is required for the formation of (m) CHH islands in maize. J Integr Plant Biol 61:749–764

  159. Lu Y, Rong T, Cao M (2008) Analysis of DNA methylation in different maize tissues. J Genet Genom 35:41–48

  160. Lu F, Cui X, Zhang S, Jenuwein T, Cao X (2011) Arabidopsis REF6 is a histone H3 lysine 27 demethylase. Nat Genet 43:715–719

  161. Lu X, Wang W, Ren W, Chai Z, Guo W, Chen R, Wang L, Zhao J, Lang Z, Fan Y, Zhao J, Zhang C (2015) Genome-wide epigenetic regulation of gene transcription in maize seeds. PLoS One 10:e0139582

  162. Luan M, Xu M, Lu Y, Zhang L, Fan Y, Wang L (2015) Expression of zma-miR169 miRNAs and their target ZmNF-YA genes in response to abiotic stress in maize leaves. Gene 555:178–185

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

  164. Lun AT, Perry M, Ing-Simmons E (2016) Infrastructure for genomic interactions: bioconductor classes for Hi-C, ChIA-PET and related experiments. F1000Res 5:950

  165. Lunardon A, Forestan C, Farinati S, Axtell MJ, Varotto S (2016) Genome-wide characterization of maize small RNA Loci and their regulation in the required to maintain repression6-1 (rmr6-1) mutant and long-term abiotic stresses. Plant Physiol 170:1535–1548

  166. Luo GZ, MacQueen A, Zheng G, Duan H, Dore LC, Lu Z, Liu J, Chen K, Jia G, Bergelson J, He C (2014) Unique features of the m6A methylome in Arabidopsis thaliana. Nat Commun 5:5630

  167. Luo J, Wang Y, Wang M, Zhang L, Peng H, Zhou Y, Jia G, He Y (2019a) Natural variation in RNA m6A methylation and its relationship with translational status. Plant Physiol 182:332–344

  168. Luo Z, Han L, Qian J, Li L (2019b) Circular RNAs exhibit extensive intraspecific variation in maize. Planta 250:69–78

  169. Lv Y, Liang Z, Ge M, Qi W, Zhang T, Lin F, Peng Z, Zhao H (2016) Genome-wide identification and functional prediction of nitrogen-responsive intergenic and intronic long non-coding RNAs in maize (Zea mays L.). BMC Genom 17:350

  170. Majeran W, Friso G, Ponnala L, Connolly B, Huang M, Reidel E, Zhang C, Asakura Y, Bhuiyan NH, Sun Q, Turgeon R, van Wijk KJ (2010) Structural and metabolic transitions of C4 LEAF DEVELOPMENT AND differentiation defined by microscopy and quantitative proteomics in maize. Plant Cell 22:3509–3542

  171. Makarevitch I, Eichten SR, Briskine R, Waters AJ, Danilevskaya ON, Meeley RB, Myers CL, Vaughn MW, Springer NM (2013) Genomic distribution of maize facultative heterochromatin marked by trimethylation of H3K27. Plant Cell 25:780–793

  172. Mao Y, Pavangadkar KA, Thomashow MF, Triezenberg SJ (2006a) Physical and functional interactions of Arabidopsis ADA2 transcriptional coactivator proteins with the acetyltransferase GCN5 and with the cold-induced transcription factor CBF1. Biochim Biophys Acta 1759:69–79

  173. Mao Y, Pavangadkar KA, Thomashow MF, Triezenberg SJ (2006b) Physical and functional interactions of ADA2 transcriptional coactivator proteins with the acetyltransferase GCN5 and with the cold-induced transcription factor CBF1. Biochim et Biophys Acta (BBA) Gene Struct Expr 1759:69–79

  174. Mao H, Wang H, Liu S, Li Z, Yang X, Yan J, Li J, Tran LS, Qin F (2015) A transposable element in a NAC gene is associated with drought tolerance in maize seedlings. Nat Commun 6:8326

  175. Mascheretti I, Battaglia R, Mainieri D, Altana A, Lauria M, Rossi V (2013) The WD40-repeat proteins NFC101 and NFC102 regulate different aspects of maize development through chromatin modification. Plant Cell 25:404–420

  176. Mascheretti I, Turner K, Brivio RS, Hand A, Colasanti J, Rossi V (2015) Florigen-encoding genes of day-neutral and photoperiod-sensitive maize are regulated by different chromatin modifications at the floral transition. Plant Physiol 168:1351–1363

  177. Meng X, Muszynski MG, Danilevskaya ON (2011) The FT-like ZCN8 gene functions as a floral activator and is involved in photoperiod sensitivity in maize. Plant Cell 23:942–960

  178. Meyer P (2011) DNA methylation systems and targets in plants. FEBS Lett 585:2008–2015

  179. Millar AA, Waterhouse PM (2005) Plant and animal microRNAs: similarities and differences. Funct Integr Genom 5:129–135

  180. Millar CB, Grunstein M (2006) Genome-wide patterns of histone modifications in yeast. Nat Rev Mol Cell Biol 7:657–666

  181. Mirouze M, Vitte C (2014) Transposable elements, a treasure trove to decipher epigenetic variation: insights from Arabidopsis and crop epigenomes. J Exp Bot 65:2801–2812

  182. Ng DW, Wang T, Chandrasekharan MB, Aramayo R, Kertbundit S, Hall TC (2007) Plant SET domain-containing proteins: structure, function and regulation. Biochim Biophys Acta 1769:316–329

  183. Nie Z, Ren Z, Wang L, Su S, Wei X, Zhang X, Wu L, Liu D, Tang H, Liu H, Zhang S, Gao S (2016) Genome-wide identification of microRNAs responding to early stages of phosphate deficiency in maize. Physiol Plant 157:161–174

  184. Offermann S, Danker T, Dreymuller D, Kalamajka R, Topsch S, Weyand K, Peterhansel C (2006) Illumination is necessary and sufficient to induce histone acetylation independent of transcriptional activity at the C4-specific phosphoenolpyruvate carboxylase promoter in maize. Plant Physiol 141:1078–1088

  185. Offermann S, Dreesen B, Horst I, Danker T, Jaskiewicz M, Peterhansel C (2008) Developmental and environmental signals induce distinct histone acetylation profiles on distal and proximal promoter elements of the C4-Pepc gene in maize. Genetics 179:1891–1901

  186. Okamoto H, Hirochika H (2001) Silencing of transposable elements in plants. Trends Plant Sci 6:527–534

  187. Olejniczak M, Kotowska-Zimmer A, Krzyzosiak W (2018) Stress-induced changes in miRNA biogenesis and functioning. Cell Mol Life Sci 75:177–191

  188. Papa CM, Springer NM, Muszynski MG, Meeley R, Kaeppler SM (2001) Maize chromomethylase Zea methyltransferase2 is required for CpNpG methylation. Plant Cell 13:1919–1928

  189. Pei L, Jin Z, Li K, Yin H, Wang J, Yang A (2013) Identification and comparative analysis of low phosphate tolerance-associated microRNAs in two maize genotypes. Plant Physiol Biochem 70:221–234

  190. Perduns R, Horst-Niessen I, Peterhansel C (2015) Photosynthetic genes and genes associated with the C4 trait in maize are characterized by a unique class of highly regulated histone acetylation peaks on upstream promoters. Plant Physiol 168:1378–1388

  191. Probst AV, Dunleavy E, Almouzni G (2009) Epigenetic inheritance during the cell cycle. Nat Rev Mol Cell Biol 10:192–206

  192. Qin F, Kakimoto M, Sakuma Y, Maruyama K, Osakabe Y, Tran LS, Shinozaki K, Yamaguchi-Shinozaki K (2007) Regulation and functional analysis of ZmDREB2A in response to drought and heat stresses in Zea mays L. Plant J 50:54–69

  193. Ravindran S (2012) Barbara McClintock and the discovery of jumping genes. Proc Natl Acad Sci U S A 109:20198–20199

  194. Regulski M, Lu Z, Kendall J, Donoghue MT, Reinders J, Llaca V, Deschamps S, Smith A, Levy D, McCombie WR, Tingey S, Rafalski A, Hicks J, Ware D, Martienssen RA (2013) The maize methylome influences mRNA splice sites and reveals widespread paramutation-like switches guided by small RNA. Genome Res 23:1651–1662

  195. Rhee Y, Sekhon RS, Chopra S, Kaeppler S (2010) Tissue culture-induced novel epialleles of a Myb transcription factor encoded by pericarp color1 in maize. Genetics 186:843–855

  196. Roguev A, Schaft D, Shevchenko A, Pijnappel WW, Wilm M, Aasland R, Stewart AF (2001) The Saccharomyces cerevisiae Set1 complex includes an Ash2 homologue and methylates histone 3 lysine 4. EMBO J 20:7137–7148

  197. Rossi V, Locatelli S, Varotto S, Donn G, Pirona R, Henderson DA, Hartings H, Motto M (2007) Maize histone deacetylase hda101 is involved in plant development, gene transcription, and sequence-specific modulation of histone modification of genes and repeats. Plant Cell 19:1145–1162

  198. Rusk N (2014) CRISPRs and epigenome editing. Nat Methods 11:28

  199. Saze H, Shiraishi A, Miura A, Kakutani T (2008) Control of genic DNA methylation by a jmjC domain-containing protein in Arabidopsis thaliana. Science 319:462–465

  200. Shen LS, Liang Z, Gu XF, Chen Y, Teo ZWN, Hou XL, Cai WM, Dedon PC, Liu L, Yu H (2016) N-6-methyladenosine RNA modification regulates shoot stem cell fate in Arabidopsis. Dev Cell 38:186–200

  201. Songa Z-T, Suna L, Lua S-J, Tianb Y, Dingb Y, Liua J-X (2015) Transcription factor interaction with COMPASS-like complex regulates histone H3K4 trimethylation for specific gene expression in plants. Proc Natl Acad Sci 112:2900–2905

  202. Stelpflug SC, Eichten SR, Hermanson PJ, Springer NM, Kaeppler SM (2014) Consistent and heritable alterations of DNA methylation are induced by tissue culture in maize. Genetics 198:209–218

  203. Stoddard CI, Feng S, Campbell MG, Liu W, Wang H, Zhong X, Bernatavichute Y, Cheng Y, Jacobsen SE, Narlikar GJ (2019) A nucleosome bridging mechanism for activation of a maintenance DNA methyltransferase. Mol Cell 73(73–83):e76

  204. Strahl BD, Allis CD (2000) The language of covalent histone modifications. Nature 403:41–45

  205. Swanson-Wagner RA, Jia Y, DeCook R, Borsuk LA, Nettleton D, Schnable PS (2006) All possible modes of gene action are observed in a global comparison of gene expression in a maize F1 hybrid and its inbred parents. Proc Natl Acad Sci U S A 103:6805–6810

  206. Swygert SG, Peterson CL (2014) Chromatin dynamics: interplay between remodeling enzymes and histone modifications. Biochim Biophys Acta 1839:728–736

  207. Tachibana M, Ueda J, Fukuda M, Takeda N, Ohta T, Iwanari H, Sakihama T, Kodama T, Hamakubo T, Shinkai Y (2005) Histone methyltransferases G9a and GLP form heteromeric complexes and are both crucial for methylation of euchromatin at H3-K9. Genes Dev 19:815–826

  208. Tamburini BA, Tyler JK (2005) Localized histone acetylation and deacetylation triggered by the homologous recombination pathway of double-strand DNA repair. Mol Cell Biol 25:4903–4913

  209. Tang B, Hao Z, Zhu Y, Zhang H, Li G (2018) Genome-wide identification and functional analysis of circRNAs in Zea mays. PLoS One 13:e0202375

  210. Thorstensen T, Grini PE, Aalen RB (2011) SET domain proteins in plant development. Bba-Gene Regul Mech 1809:407–420

  211. Tolley BJ, Woodfield H, Wanchana S, Bruskiewich R, Hibberd JM (2012) Light-regulated and cell-specific methylation of the maize PEPC promoter. J Exp Bot 63:1381–1390

  212. Trevisan S, Begheldo M, Nonis A, Quaggiotti S (2012a) The miRNA-mediated post-transcriptional regulation of maize response to nitrate. Plant Signal Behav 7:822–826

  213. Trevisan S, Nonis A, Begheldo M, Manoli A, Palme K, Caporale G, Ruperti B, Quaggiotti S (2012b) Expression and tissue-specific localization of nitrate-responsive miRNAs in roots of maize seedlings. Plant Cell Environ 35:1137–1155

  214. Turner BM (2002) Cellular memory and the histone code. Cell 111:285–291

  215. Vaissiere T, Sawan C, Herceg Z (2008) Epigenetic interplay between histone modifications and DNA methylation in gene silencing. Mutat Res 659:40–48

  216. Vaquero A, Scher MB, Lee DH, Sutton A, Cheng HL, Alt FW, Serrano L, Sternglanz R, Reinberg D (2006) SirT2 is a histone deacetylase with preference for histone H4 Lys 16 during mitosis. Genes Dev 20:1256–1261

  217. Varotto S, Locatelli S, Canova S, Pipal A, Motto M, Rossi V (2003) Expression profile and cellular localization of maize Rpd3-type histone deacetylases during plant development. Plant Physiol 133:606–617

  218. Vilperte V, Agapito-Tenfen SZ, Wikmark OG, Nodari RO (2016) Levels of DNA methylation and transcript accumulation in leaves of transgenic maize varieties. Environ Sci Eur 28:29

  219. Wang X, Elling AA, Li X, Li N, Peng Z, He G, Sun H, Qi Y, Liu XS, Deng XW (2009) Genome-wide and organ-specific landscapes of epigenetic modifications and their relationships to mRNA and small RNA transcriptomes in maize. Plant Cell 21:1053–1069

  220. Wang L, Liu H, Li D, Chen H (2011) Identification and characterization of maize microRNAs involved in the very early stage of seed germination. BMC Genom 12:154

  221. Wang PL, Bao Y, Yee MC, Barrett SP, Hogan GJ, Olsen MN, Dinneny JR, Brown PO, Salzman J (2014) Circular RNA is expressed across the eukaryotic tree of life. PLoS One 9:e90859

  222. Wang P, Xia H, Zhang Y, Zhao S, Zhao C, Hou L, Li C, Li A, Ma C, Wang X (2015a) Genome-wide high-resolution mapping of DNA methylation identifies epigenetic variation across embryo and endosperm in Maize (Zea may). BMC Genom 16:21

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

  224. Wang J, Yu Y, Tao F, Zhang J, Copetti D, Kudrna D, Talag J, Lee S, Wing RA, Fan C (2016a) DNA methylation changes facilitated evolution of genes derived from Mutator-like transposable elements. Genome Biol 17:92

  225. Wang Y, Yang M, Wei S, Qin F, Zhao H, Suo B (2016b) Identification of circular RNAs and their targets in leaves of Triticum aestivum L. under dehydration stress. Front Plant Sci 7:2024

  226. Wang C, Yang Q, Wang W, Li Y, Guo Y, Zhang D, Ma X, Song W, Zhao J, Xu M (2017a) A transposon-directed epigenetic change in ZmCCT underlies quantitative resistance to Gibberella stalk rot in maize. New Phytol 215:1503–1515

  227. Wang D, Qu Z, Yang L, Zhang Q, Liu ZH, Do T, Adelson DL, Wang ZY, Searle I, Zhu JK (2017b) Transposable elements (TEs) contribute to stress-related long intergenic noncoding RNAs in plants. Plant J 90:133–146

  228. Wang J, Meng X, Dobrovolskaya OB, Orlov YL, Chen M (2017c) Non-coding RNAs and their roles in stress response in plants. Genom Proteom Bioinform 15:301–312

  229. Wang Y, Wang Y, Zhao J, Huang J, Shi Y, Deng D (2018) Unveiling gibberellin-responsive coding and long noncoding RNAs in maize. Plant Mol Biol 98:427–438

  230. Wang B, Cheng D, Chen Z, Zhang M, Zhang G, Jiang M, Tan M (2019) Bioinformatic exploration of the targets of Xylem Sap miRNAs in Maize under cadmium stress. Int J Mol Sci 20:1474

  231. Waters AJ, Makarevitch I, Eichten SR, Swanson-Wagner RA, Yeh CT, Xu W, Schnable PS, Vaughn MW, Gehring M, Springer NM (2011) Parent-of-origin effects on gene expression and DNA methylation in the maize endosperm. Plant Cell 23:4221–4233

  232. Waters AJ, Bilinski P, Eichten SR, Vaughn MW, Ross-Ibarra J, Gehring M, Springer NM (2013) Comprehensive analysis of imprinted genes in maize reveals allelic variation for imprinting and limited conservation with other species. Proc Natl Acad Sci U S A 110:19639–19644

  233. Wei X, Wang X (2013) A computational workflow to identify allele-specific expression and epigenetic modification in maize. Genom Proteom Bioinform 11:247–252

  234. Wei LH, Song PZ, Wang Y, Lu ZK, Tang Q, Yu Q, Xiao Y, Zhang X, Duan HC, Jia GF (2018) The m(6)A reader ECT2 controls trichome morphology by Affecting mRNA stability in arabidopsis([OPEN]). Plant Cell 30:968–985

  235. Wendte JM, Haag JR, Pontes OM, Singh J, Metcalf S, Pikaard CS (2019) The Pol IV largest subunit CTD quantitatively affects siRNA levels guiding RNA-directed DNA methylation. Nucleic Acids Res 47:9024–9036

  236. West PT, Li Q, Ji L, Eichten SR, Song J, Vaughn MW, Schmitz RJ, Springer NM (2014) Genomic distribution of H3K9me2 and DNA methylation in a maize genome. PLoS One 9:e105267

  237. Whetstine JR, Nottke A, Lan F, Huarte M, Smolikov S, Chen Z, Spooner E, Li E, Zhang G, Colaiacovo M, Shi Y (2006) Reversal of histone lysine trimethylation by the JMJD2 family of histone demethylases. Cell 125:467–481

  238. Wierzbicki AT, Cocklin R, Mayampurath A, Lister R, Rowley MJ, Gregory BD, Ecker JR, Tang H, Pikaard CS (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

  239. Wu FY, Tang CY, Guo YM, Yang MK, Yang RW, Lu GH, Yang YH (2016) Comparison of miRNAs and their targets in seed development between two maize inbred lines by high-throughput sequencing and degradome analysis. PLoS One 11:e0159810

  240. Xia Z, Peng J, Li Y, Chen L, Li S, Zhou T, Fan Z (2014) Characterization of small interfering RNAs derived from Sugarcane mosaic virus in infected maize plants by deep sequencing. PLoS One 9:e97013

  241. Xia Z, Zhao Z, Chen L, Li M, Zhou T, Deng C, Zhou Q, Fan Z (2016) Synergistic infection of two viruses MCMV and SCMV increases the accumulations of both MCMV and MCMV-derived siRNAs in maize. Sci Rep 6:20520

  242. Xia Z, Zhao Z, Jiao Z, Xu T, Wu Y, Zhou T, Fan Z (2018a) Virus-derived small interfering RNAs affect the accumulations of viral and host transcripts in maize. Viruses 10:664

  243. Xia Z, Zhao Z, Li M, Chen L, Jiao Z, Wu Y, Zhou T, Yu W, Fan Z (2018b) Identification of miRNAs and their targets in maize in response to Sugarcane mosaic virus infection. Plant Physiol Biochem 125:143–152

  244. Xiang L, Cai C, Cheng J, Wang L, Wu C, Shi Y, Luo J, He L, Deng Y, Zhang X, Yuan Y, Cai Y (2018) Identification of circularRNAs and their targets in Gossypium under Verticillium wilt stress based on RNA-seq. PeerJ 6:e4500

  245. Xie W, Schultz MD, Lister R, Hou Z, Rajagopal N, Ray P, Whitaker JW, Tian S, Hawkins RD, Leung D, Yang H, Wang T, Lee AY, Swanson SA, Zhang J, Zhu Y, Kim A, Nery JR, Urich MA, Kuan S, Yen CA, Klugman S, Yu P, Suknuntha K, Propson NE, Chen H, Edsall LE, Wagner U, Li Y, Ye Z, Kulkarni A, Xuan Z, Chung WY, Chi NC, Antosiewicz-Bourget JE, Slukvin I, Stewart R, Zhang MQ, Wang W, Thomson JA, Ecker JR, Ren B (2013) Epigenomic analysis of multilineage differentiation of human embryonic stem cells. Cell 153:1134–1148

  246. Xin M, Yang R, Yao Y, Ma C, Peng H, Sun Q, Wang X, Ni Z (2014) Dynamic parent-of-origin effects on small interfering RNA expression in the developing maize endosperm. BMC Plant Biol 14:192

  247. Xin M, Yang G, Yao Y, Peng H, Hu Z, Sun Q, Wang X, Ni Z (2015) Temporal small RNA transcriptome profiling unraveled partitioned miRNA expression in developing maize endosperms between reciprocal crosses. Front Plant Sci 6:744

  248. Xing L, Zhu M, Zhang M, Li W, Jiang H, Zou J, Wang L, Xu M (2017) High-throughput sequencing of small RNA transcriptomes in maize kernel identifies miRNAs involved in embryo and endosperm development. Genes (Basel) 8:385

  249. Xu Z, Zhong S, Li X, Li W, Rothstein SJ, Zhang S, Bi Y, Xie C (2011) Genome-wide identification of microRNAs in response to low nitrate availability in maize leaves and roots. PLoS One 6:e28009

  250. Xu D, Huang W, Li Y, Wang H, Huang H, Cui X (2012) Elongator complex is critical for cell cycle progression and leaf patterning in Arabidopsis. Plant J 69:792–808

  251. Xu J, Chen G, Hermanson PJ, Xu Q, Sun C, Chen W, Kan Q, Li M, Crisp PA, Yan J, Li L, Springer NM, Li Q (2019) Population-level analysis reveals the widespread occurrence and phenotypic consequence of DNA methylation variation not tagged by genetic variation in maize. Genome Biol 20:243

  252. Yamada M (2017) Functions of long intergenic non-coding (linc) RNAs in plants. J Plant Res 130:67–73

  253. Yamane K, Toumazou C, Tsukada Y, Erdjument-Bromage H, Tempst P, Wong J, Zhang Y (2006) JHDM2A, a JmjC-containing H3K9 demethylase, facilitates transcription activation by androgen receptor. Cell 125:483–495

  254. Yang F, Zhang L, Li J, Huang J, Wen R, Ma L, Zhou D, Li L (2010) Trichostatin A and 5-azacytidine both cause an increase in global histone H4 acetylation and a decrease in global DNA and H3K9 methylation during mitosis in maize. BMC Plant Biol 10:178

  255. Yang H, Qi Y, Goley ME, Huang J, Ivashuta S, Zhang Y, Sparks OC, Ma J, van Scoyoc BM, Caruano-Yzermans AL, King-Sitzes J, Li X, Pan A, Stoecker MA, Wiggins BE, Varagona MJ (2018a) Endogenous tassel-specific small RNAs-mediated RNA interference enables a novel glyphosate-inducible male sterility system for commercial production of hybrid seed in Zea mays L. PLoS One 13:e0202921

  256. Yang Z, Qiu Q, Chen W, Jia B, Chen X, Hu H, He K, Deng X, Li S, Tao WA, Cao X, Du J (2018b) Structure of the Arabidopsis JMJ14-H3K4me3 complex provides insight into the substrate specificity of KDM5 subfamily histone demethylases. Plant Cell 30:167–177

  257. Ye J, Zhong T, Zhang D, Ma C, Wang L, Yao L, Zhang Q, Zhu M, Xu M (2019) The auxin-regulated protein ZmAuxRP1 coordinates the balance between root growth and stalk rot disease resistance in maize. Mol Plant 12:360–373

  258. Yoo KH, Hennighausen L (2012) EZH2 methyltransferase and H3K27 methylation in breast cancer. Int J Biol Sci 8:59–65

  259. Yu X, Jiang L, Wu R, Meng X, Zhang A, Li N, Xia Q, Qi X, Pang J, Xu ZY, Liu B (2016) The core subunit of A chromatin-remodeling complex, ZmCHB101, plays essential roles in maize growth and development. Sci Rep 6:38504

  260. Yu X, Meng X, Liu Y, Li N, Zhang A, Wang TJ, Jiang L, Pang J, Zhao X, Qi X, Zhang M, Wang S, Liu B, Xu ZY (2018) The chromatin remodeler ZmCHB101 impacts expression of osmotic stress-responsive genes in maize. Plant Mol Biol 97:451–465

  261. Zhang B, Wang Q, Pan X (2007) MicroRNAs and their regulatory roles in animals and plants. J Cell Physiol 210:279–289

  262. Zhang M, Xie S, Dong X, Zhao X, Zeng B, Chen J, Li H, Yang W, Zhao H, Wang G, Chen Z, Sun S, Hauck A, Jin W, Lai J (2014a) Genome-wide high resolution parental-specific DNA and histone methylation maps uncover patterns of imprinting regulation in maize. Genome Res 24:167–176

  263. Zhang W, Han Z, Guo Q, Liu Y, Zheng Y, Wu F, Jin W (2014b) Identification of maize long non-coding RNAs responsive to drought stress. PLoS One 9:e98958

  264. Zhang W, Garcia N, Feng Y, Zhao H, Messing J (2015) Genome-wide histone acetylation correlates with active transcription in maize. Genomics 106:214–220

  265. Zhang H, Wang P, Hou H, Wen H, Zhou H, Gao F, Wu J, Qiu Z, Li L (2016) Histone modification is involved in okadaic acid (OA) induced DNA damage response and G2-M transition arrest in maize. PLoS One 11:e0155852

  266. Zhang H, Zhang JS, Lang ZB, Botella JR, Zhu JK (2017a) Genome editing-principles and applications for functional genomics research and crop improvement. Crit Rev Plant Sci 36:291–309

  267. Zhang Q, Wang P, Hou H, Zhang H, Tan J, Huang Y, Li Y, Wu J, Qiu Z, Li L (2017b) Histone acetylation and reactive oxygen species are involved in the preprophase arrest induced by sodium butyrate in maize roots. Protoplasma 254:167–179

  268. Zhang H, Yue M, Zheng X, Gautam M, He S, Li L (2018a) The role of promoter-associated histone acetylation of Haem Oxygenase-1 (HO-1) and Giberellic Acid-Stimulated Like-1 (GSL-1) genes in heat-induced lateral root primordium inhibition in maize. Front Plant Sci 9:1520

  269. Zhang Q, Liang Z, Cui X, Ji C, Li Y, Zhang P, Liu J, Riaz A, Yao P, Liu M, Wang Y, Lu T, Yu H, Yang D, Zheng H, Gu X (2018b) N(6)-methyladenine DNA methylation in Japonica and Indica rice genomes and its association with gene expression, plant development, and stress responses. Mol Plant 11:1492–1508

  270. Zhang M, An P, Li H, Wang X, Zhou J, Dong P, Zhao Y, Wang Q, Li C (2019a) The miRNA-mediated post-transcriptional regulation of maize in response to high temperature. Int J Mol Sci 20:1754

  271. Zhang P, Fan Y, Sun X, Chen L, Terzaghi W, Bucher E, Li L, Dai M (2019b) A large-scale circular RNA profiling reveals universal molecular mechanisms responsive to drought stress in maize and Arabidopsis. Plant J 98:697–713

  272. Zhang TQ, Xu ZG, Shang GD, Wang JW (2019c) A single-cell RNA sequencing profiles the developmental landscape of Arabidopsis root. Mol Plant 12:648–660

  273. Zhang Z, Wang B, Wang S, Lin T, Yang L, Zhao Z, Zhang Z, Huang S, Yang X (2019d) Genome-wide target mapping shows histone deacetylase complex 1 regulates cell proliferation in cucumber fruit. Plant Physiol.

  274. Zhao M, Tai H, Sun S, Zhang F, Xu Y, Li WX (2012) Cloning and characterization of maize miRNAs involved in responses to nitrogen deficiency. PLoS One 7:e29669

  275. Zhao Y, Xu Z, Mo Q, Zou C, Li W, Xu Y, Xie C (2013) Combined small RNA and degradome sequencing reveals novel miRNAs and their targets in response to low nitrate availability in maize. Ann Bot 112:633–642

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

  277. Zheng X, Hou H, Zhang H, Yue M, Hu Y, Li L (2018) Histone acetylation is involved in GA-mediated 45S rDNA decondensation in maize aleurone layers. Plant Cell Rep 37:115–123

  278. Zheng L, Zhang X, Zhang H, Gu Y, Huang X, Huang H, Liu H, Zhang J, Hu Y, Li Y, Yu G, Liu Y, Lawson SS, Huang Y (2019) The miR164-dependent regulatory pathway in developing maize seed. Mol Genet Genom 294:501–517

  279. Zhong S, Jansen C, She QB, Goto H, Inagaki M, Bode AM, Ma WY, Dong Z (2001) Ultraviolet B-induced phosphorylation of histone H3 at serine 28 is mediated by MSK1. J Biol Chem 276:33213–33219

  280. Zhou DX (2009) Regulatory mechanism of histone epigenetic modifications in plants. Epigenetics 4:15–18

  281. Zhou Y, Xu Z, Duan C, Chen Y, Meng Q, Wu J, Hao Z, Wang Z, Li M, Yong H, Zhang D, Zhang S, Weng J, Li X (2016) Dual transcriptome analysis reveals insights into the response to Rice black-streaked dwarf virus in maize. J Exp Bot 67:4593–4609

  282. Zhou S, Jiang W, Zhao Y, Zhou DX (2019) Single-cell three-dimensional genome structures of rice gametes and unicellular zygotes. Nat Plants 5:795–800

  283. Zhu B, Zheng Y, Pham AD, Mandal SS, Erdjument-Bromage H, Tempst P, Reinberg D (2005) Monoubiquitination of human histone H2B: the factors involved and their roles in HOX gene regulation. Mol Cell 20:601–611

  284. Zhu M, Zhang M, Xing L, Li W, Jiang H, Wang L, Xu M (2017) Transcriptomic analysis of long non-coding RNAs and coding genes uncovers a complex regulatory network that is involved in maize seed development. Genes (Basel) 8:274

  285. Zippo A, Serafini R, Rocchigiani M, Pennacchini S, Krepelova A, Oliviero S (2009) Histone crosstalk between H3S10ph and H4K16ac generates a histone code that mediates transcription elongation. Cell 138:1122–1136

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This work was supported by the National Transgenic Major Program (2019ZX08010-004), the National Natural Science Foundation of China (31872805), the National Key Research and Development Program of China (2016YFD0100103), and the Innovation Program of Chinese Academy of Agricultural Sciences.

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LP conceived and outlined the review; all authors wrote the manuscript; and LP revised the manuscript.

Correspondence to Li Pu.

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Communicated by Mingliang Xu.

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Yu, J., Xu, F., Wei, Z. et al. Epigenomic landscape and epigenetic regulation in maize. Theor Appl Genet (2020).

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