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Epigenomic landscape and epigenetic regulation in maize

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Abstract

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.

Abstract

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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References

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    PubMed  PubMed Central  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed Central  Google Scholar 

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

    PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    PubMed  PubMed Central  Google Scholar 

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

    PubMed  CAS  Google Scholar 

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

    PubMed  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  PubMed Central  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  PubMed Central  Google Scholar 

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

    PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    PubMed  PubMed Central  Google Scholar 

  • 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

    Google Scholar 

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

    PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  PubMed Central  CAS  Google Scholar 

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

    PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    PubMed  PubMed Central  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

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

    CAS  Google Scholar 

  • 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

    PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    PubMed  PubMed Central  Google Scholar 

  • 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

    PubMed  PubMed Central  CAS  Google Scholar 

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

    PubMed  PubMed Central  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    PubMed  PubMed Central  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    PubMed  PubMed Central  CAS  Google Scholar 

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

    Google Scholar 

  • 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

    PubMed  PubMed Central  CAS  Google Scholar 

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

    PubMed  PubMed Central  Google Scholar 

  • 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

    PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  PubMed Central  CAS  Google Scholar 

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

    CAS  Google Scholar 

  • 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

    PubMed  PubMed Central  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  PubMed Central  Google Scholar 

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

    Google Scholar 

  • 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

    PubMed  PubMed Central  Google Scholar 

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

    PubMed  CAS  Google Scholar 

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

    PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    PubMed  PubMed Central  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

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

    PubMed  PubMed Central  Google Scholar 

  • 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

    Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  PubMed Central  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  PubMed Central  Google Scholar 

  • 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. https://doi.org/10.1111/ppl.12997

    Article  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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

    PubMed  PubMed Central  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  PubMed Central  Google Scholar 

  • 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

    PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  PubMed Central  Google Scholar 

  • 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

    PubMed  PubMed Central  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  PubMed Central  Google Scholar 

  • 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

    PubMed  PubMed Central  CAS  Google Scholar 

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

    PubMed  PubMed Central  CAS  Google Scholar 

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

    CAS  Google Scholar 

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

    PubMed  PubMed Central  CAS  Google Scholar 

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

    Google Scholar 

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

    PubMed  PubMed Central  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

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

    PubMed  PubMed Central  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    PubMed  PubMed Central  Google Scholar 

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

    PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    PubMed  PubMed Central  CAS  Google Scholar 

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

    PubMed  PubMed Central  Google Scholar 

  • 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

    PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    PubMed  PubMed Central  Google Scholar 

  • 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

    PubMed  PubMed Central  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  PubMed Central  Google Scholar 

  • 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

    PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    PubMed  PubMed Central  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  PubMed Central  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  PubMed Central  Google Scholar 

  • 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

    PubMed  PubMed Central  Google Scholar 

  • 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

    PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    PubMed  PubMed Central  Google Scholar 

  • 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

    Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    PubMed  PubMed Central  Google Scholar 

  • 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

    PubMed  PubMed Central  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  PubMed Central  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  PubMed Central  Google Scholar 

  • 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

    PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  PubMed Central  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    PubMed  PubMed Central  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

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

    CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    PubMed  PubMed Central  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  PubMed Central  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

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

    PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    PubMed  PubMed Central  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  PubMed Central  CAS  Google Scholar 

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

    PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    PubMed  PubMed Central  CAS  Google Scholar 

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

    CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    PubMed  PubMed Central  Google Scholar 

  • 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

    PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    PubMed  PubMed Central  Google Scholar 

  • 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

    Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  PubMed Central  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed Central  CAS  Google Scholar 

  • 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

    PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    PubMed  PubMed Central  CAS  Google Scholar 

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

    Google Scholar 

  • 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

    PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    PubMed  PubMed Central  Google Scholar 

  • 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

    PubMed  PubMed Central  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    PubMed  PubMed Central  Google Scholar 

  • 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

    PubMed  PubMed Central  Google Scholar 

  • 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

    PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    PubMed Central  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  PubMed Central  Google Scholar 

  • 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

    PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    PubMed  PubMed Central  Google Scholar 

  • 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

    PubMed  PubMed Central  Google Scholar 

  • 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

    Google Scholar 

  • 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

    PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  PubMed Central  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  PubMed Central  Google Scholar 

  • 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

    PubMed  PubMed Central  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    PubMed  PubMed Central  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  PubMed Central  Google Scholar 

  • 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

    Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  PubMed Central  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed Central  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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. https://doi.org/10.1104/pp.19.00532

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

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Acknowledgements

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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  1. Jia Yu, Fan Xu, Ziwei Wei, and Xiangxiang Zhang have contributed equally to this work.

Authors and Affiliations

  1. Biotechnology Research Institute, Chinese Academy of Agricultural Sciences, Beijing, China

    Jia Yu, Fan Xu, Xiangxiang Zhang & Li Pu

  2. School of Life Sciences, Anhui Agricultural University, Hefei, China

    Ziwei Wei

  3. College of Life and Environmental Sciences, Hangzhou Normal University, Hangzhou, China

    Tao Chen

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

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Yu, J., Xu, F., Wei, Z. et al. Epigenomic landscape and epigenetic regulation in maize. Theor Appl Genet 133, 1467–1489 (2020). https://doi.org/10.1007/s00122-020-03549-5

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