Skip to main content
SpringerLink
Log in

Understanding epigenomics based on the rice model

  • Review
  • Published:
Theoretical and Applied Genetics Aims and scope Submit manuscript

Abstract

Key message

The purpose of this paper provides a comprehensive overview of the recent researches on rice epigenomics, including DNA methylation, histone modifications, noncoding RNAs, and three-dimensional genomics. The challenges and perspectives for future research in rice are discussed.

Abstract

Rice as a model plant for epigenomic studies has much progressed current understanding of epigenetics in plants. Recent results on rice epigenome profiling and three-dimensional chromatin structure studies reveal specific features and implication in gene regulation during rice plant development and adaptation to environmental changes. Results on rice chromatin regulator functions shed light on mechanisms of establishment, recognition, and resetting of epigenomic information in plants. Cloning of several rice epialleles associated with important agronomic traits highlights importance of epigenomic variation in rice plant growth, fitness, and yield. In this review, we summarize and analyze recent advances in rice epigenomics and discuss challenges and directions for future research in the field.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  • Amin NM, Greco TM, Kuchenbrod LM, Rigney MM, Chung MI, Wallingford JB, Cristea IM, Conlon FL (2014) Proteomic profiling of cardiac tissue by isolation of nuclei tagged in specific cell types (INTACT). Development 141:962–973

    PubMed  PubMed Central  CAS  Google Scholar 

  • Arikit S, Zhai J, Meyers BC (2013) Biogenesis and function of rice small RNAs from non-coding RNA precursors. Curr Opin Plant Biol 16:170–179

    PubMed  CAS  Google Scholar 

  • Axtell MJ (2013) Classification and comparison of small RNAs from plants. Annu Rev Plant Biol 64:137–159

    PubMed  CAS  Google Scholar 

  • Bajic M, Maher KA, Deal RB (2018) Identification of open chromatin regions in plant genomes using ATAC-Seq. Methods Mol Biol 1675:183–201

    PubMed  PubMed Central  CAS  Google Scholar 

  • Banerjee A, Roychoudhury A (2018) The gymnastics of epigenomics in rice. Plant Cell Rep 37:25–49

    PubMed  CAS  Google Scholar 

  • Benoit M, Simon L, Desset S, Duc C, Cotterell S, Poulet A, Le Goff S, Tatout C, Probst AV (2019) Replication-coupled histone H3.1 deposition determines nucleosome composition and heterochromatin dynamics during Arabidopsis seedling development. New Phytol 221:385–398

    PubMed  CAS  Google Scholar 

  • Birchler JA, Han F (2013) Centromere epigenetics in plants. J Genet Genomics 40:201–204

    PubMed  Google Scholar 

  • Bologna NG, Voinnet O (2014) The diversity, biogenesis, and activities of endogenous silencing small RNAs in Arabidopsis. Annu Rev Plant Biol 65:473–503

    PubMed  CAS  Google Scholar 

  • Boyle AP, Davis S, Shulha HP, Meltzer P, Margulies EH, Weng Z, Furey TS, Crawford GE (2008) High-resolution mapping and characterization of open chromatin across the genome. Cell 132:311–322

    PubMed  PubMed Central  CAS  Google Scholar 

  • Buenrostro JD, Giresi PG, Zaba LC, Chang HY, Greenleaf WJ (2013) Transposition of native chromatin for fast and sensitive epigenomic profiling of open chromatin, DNA-binding proteins and nucleosome position. Nat Methods 10:1213–1218

    PubMed  PubMed Central  CAS  Google Scholar 

  • Calarco JP, Borges F, Donoghue MT, Van Ex F, Jullien PE, Lopes T, Gardner R, Berger F, Feijo JA, Becker JD, Martienssen RA (2012) Reprogramming of DNA methylation in pollen guides epigenetic inheritance via small RNA. Cell 151:194–205

    PubMed  PubMed Central  CAS  Google Scholar 

  • Cantu D, Vanzetti LS, Sumner A, Dubcovsky M, Matvienko M, Distelfeld A, Michelmore RW, Dubcovsky J (2010) Small RNAs, DNA methylation and transposable elements in wheat. BMC Genomics 11:408

    PubMed  PubMed Central  Google Scholar 

  • Chen X, Zhou DX (2013) Rice epigenomics and epigenetics: challenges and opportunities. Curr Opin Plant Biol 16:164–169

    CAS  PubMed  Google Scholar 

  • Chen Q, Chen X, Wang Q, Zhang F, Lou Z, Zhang Q, Zhou DX (2013) Structural basis of a histone H3 lysine 4 demethylase required for stem elongation in rice. PLoS Genet 9:e1003239

    PubMed  PubMed Central  CAS  Google Scholar 

  • Chen X, Liu X, Zhao Y, Zhou DX (2015) Histone H3K4me3 and H3K27me3 regulatory genes control stable transmission of an epimutation in rice. Sci Rep 5:13251

    PubMed  PubMed Central  CAS  Google Scholar 

  • Chen Y, Muller F, Rieu I, Winter P (2016) Epigenetic events in plant male germ cell heat stress responses. Plant Reprod 29:21–29

    PubMed  CAS  Google Scholar 

  • Chen C, Li C, Wang Y, Renaud J, Tian G, Kambhampati S, Saatian B, Nguyen V, Hannoufa A, Marsolais F, Yuan ZC, Yu K, Austin RS, Liu J, Kohalmi SE, Wu K, Huang S, Cui Y (2017) Cytosolic acetyl-CoA promotes histone acetylation predominantly at H3K27 in Arabidopsis. Nat Plants 3:814–824

    PubMed  CAS  Google Scholar 

  • Chen L, Shi S, Jiang N, Khanzada H, Wassan GM, Zhu C, Peng X, Xu J, Chen Y, Yu Q, He X, Fu J, Chen X, Hu L, Ouyang L, Sun X, He H, Bian J (2018) Genome-wide analysis of long non-coding RNAs affecting roots development at an early stage in the rice response to cadmium stress. BMC Genomics 19:460

    PubMed  PubMed Central  Google Scholar 

  • Cheng C, Tarutani Y, Miyao A, Ito T, Yamazaki M, Sakai H, Fukai E, Hirochika H (2015) Loss of function mutations in the rice chromomethylase OsCMT3a cause a burst of transposition. Plant J 83:1069–1081

    PubMed  CAS  Google Scholar 

  • Cheng S, Tan F, Lu Y, Liu X, Li T, Yuan W, Zhao Y, Zhou DX (2018) WOX11 recruits a histone H3K27me3 demethylase to promote gene expression during shoot development in rice. Nucleic Acids Res 46:2356–2369

    PubMed  PubMed Central  CAS  Google Scholar 

  • Chinnusamy V, Zhu JK (2009) RNA-directed DNA methylation and demethylation in plants. Sci China C Life Sci 52:331–343

    PubMed  CAS  Google Scholar 

  • Cho J (2018) Transposon-derived non-coding RNAs and their function in plants. Front Plant Sci 9:600

    PubMed  PubMed Central  Google Scholar 

  • Chodavarapu RK, Feng S, Ding B, Simon SA, Lopez D, Jia Y, Wang GL, Meyers BC, Jacobsen SE, Pellegrini M (2012) Transcriptome and methylome interactions in rice hybrids. Proc Natl Acad Sci USA 109:12040–12045

    PubMed  CAS  PubMed Central  Google Scholar 

  • Cong W, Miao Y, Xu L, Zhang Y, Yuan C, Wang J, Zhuang T, Lin X, Jiang L, Wang N, Ma J, Sanguinet KA, Liu B, Rustgi S, Ou X (2019) Transgenerational memory of gene expression changes induced by heavy metal stress in rice (Oryza sativa L.). BMC Plant Biol 19:282

  • Creyghton MP, Markoulaki S, Levine SS, Hanna J, Lodato MA, Sha K, Young RA, Jaenisch R, Boyer LA (2008) H2AZ is enriched at polycomb complex target genes in ES cells and is necessary for lineage commitment. Cell 135:649–661

    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 USA 110:1953–1958

    PubMed  CAS  PubMed Central  Google Scholar 

  • Cui J, Zhang Z, Shao Y, Zhang K, Leng P, Liang Z (2015) Genome-wide identification, evolutionary, and expression analyses of histone H3 variants in plants. Biomed Res Int 2015:341598

    PubMed  PubMed Central  Google Scholar 

  • Dai X, Bai Y, Zhao L, Dou X, Liu Y, Wang L, Li Y, Li W, Hui Y, Huang X, Wang Z, Qin Y (2017) H2A.Z represses gene expression by modulating promoter nucleosome structure and enhancer histone modifications in Arabidopsis. Mol Plant 10:1274–1292

    PubMed  CAS  Google Scholar 

  • Davis-Richardson AG, Russell JT, Dias R, McKinlay AJ, Canepa R, Fagen JR, Rusoff KT, Drew JC, Kolaczkowski B, Emerich DW, Triplett EW (2016) Integrating DNA methylation and gene expression data in the development of the soybean-bradyrhizobium N2-fixing symbiosis. Front Microbiol 7:518

    PubMed  PubMed Central  Google Scholar 

  • Dekker J, Marti-Renom MA, Mirny LA (2013) Exploring the three-dimensional organization of genomes: interpreting chromatin interaction data. Nat Rev Genet 14:390–403

    PubMed  PubMed Central  CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Deng P, Muhammad S, Cao M, Wu L (2018) Biogenesis and regulatory hierarchy of phased small interfering RNAs in plants. Plant Biotechnol J 16:965–975

    PubMed  PubMed Central  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 B, Zhu Y, Bu ZY, Shen WH, Yu Y, Dong AW (2010) SDG714 regulates specific gene expression and consequently affects plant growth via H3K9 dimethylation. J Integr Plant Biol 52:420–430

    PubMed  CAS  Google Scholar 

  • Ding B, Bellizzi Mdel R, Ning Y, Meyers BC, Wang GL (2012a) HDT701, a histone H4 deacetylase, negatively regulates plant innate immunity by modulating histone H4 acetylation of defense-related genes in rice. Plant Cell 24:3783–3794

    PubMed  PubMed Central  CAS  Google Scholar 

  • Ding J, Lu Q, Ouyang Y, Mao H, Zhang P, Yao J, Xu C, Li X, Xiao J, Zhang Q (2012b) A long noncoding RNA regulates photoperiod-sensitive male sterility, an essential component of hybrid rice. Proc Natl Acad Sci USA 109:2654–2659

    PubMed  CAS  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 Q, Li N, Li X, Yuan Z, Xie D, Wang X, Li J, Yu Y, Wang J, Ding B, Zhang Z, Li C, Bian Y, Zhang A, Wu Y, Liu B, Gong L (2018) Genome-wide Hi-C analysis reveals extensive hierarchical chromatin interactions in rice. Plant J 94:1141–1156

    PubMed  CAS  Google Scholar 

  • Dong P, Tu X, Li H, Zhang J, Grierson D, Li P, Zhong S (2019) Tissue-specific Hi-C analyses of rice, foxtail millet and maize suggest non-canonical function of plant chromatin domains. J Integr Plant Biol. https://doi.org/10.1111/jipb.12809

    Article  PubMed  Google Scholar 

  • Du Z, Li H, Wei Q, Zhao X, Wang C, Zhu Q, Yi X, Xu W, Liu XS, Jin W, Su Z (2013) Genome-wide analysis of histone modifications: H3K4me2, H3K4me3, H3K9ac, and H3K27ac in Oryza sativa L. Japonica. Mol Plant 6:1463–1472

    PubMed  CAS  Google Scholar 

  • Ehrlich M, Wang RY (1981) 5-Methylcytosine in eukaryotic DNA. Science 212:1350–1357

    PubMed  CAS  Google Scholar 

  • Erdmann RM, Satyaki PRV, Klosinska M, Gehring M (2017) A small RNA pathway mediates allelic dosage in endosperm. Cell Rep 21:3364–3372

    PubMed  CAS  Google Scholar 

  • Fan Y, Yang J, Mathioni SM, Yu J, Shen J, Yang X, Wang L, Zhang Q, Cai Z, Xu C, Li X, Xiao J, Meyers BC, Zhang Q (2016) PMS1T, producing phased small-interfering RNAs, regulates photoperiod-sensitive male sterility in rice. Proc Natl Acad Sci USA 113:15144–15149

    PubMed  CAS  PubMed Central  Google Scholar 

  • Fang C, Zhang H, Wan J, Wu Y, Li K, Jin C, Chen W, Wang S, Wang W, Zhang H, Zhang P, Zhang F, Qu L, Liu X, Zhou DX, Luo J (2016a) Control of leaf senescence by an MeOH-jasmonates cascade that is epigenetically regulated by OsSRT1 in rice. Mol Plant 9:1366–1378

    PubMed  CAS  Google Scholar 

  • Fang Y, Wang L, Wang X, You Q, Pan X, Xiao J, Wang XE, Wu Y, Su Z, Zhang W (2016b) Histone modifications facilitate the coexpression of bidirectional promoters in rice. BMC Genomics 17:768

    PubMed  PubMed Central  Google Scholar 

  • Fang Y, Wang X, Wang L, Pan X, Xiao J, Wang XE, Wu Y, Zhang W (2016c) Functional characterization of open chromatin in bidirectional promoters of rice. Sci Rep 6:32088

    PubMed  PubMed Central  CAS  Google Scholar 

  • Fatland BL, Nikolau BJ, Wurtele ES (2005) Reverse genetic characterization of cytosolic acetyl-CoA generation by ATP-citrate lyase in Arabidopsis. Plant Cell 17:182–203

    PubMed  PubMed Central  CAS  Google Scholar 

  • Fei Q, Xia R, Meyers BC (2013) Phased, secondary, small interfering RNAs in posttranscriptional regulatory networks. Plant Cell 25:2400–2415

    PubMed  PubMed Central  CAS  Google Scholar 

  • Fei Q, Yang L, Liang W, Zhang D, Meyers BC (2016) Dynamic changes of small RNAs in rice spikelet development reveal specialized reproductive phasiRNA pathways. J Exp Bot 67:6037–6049

    PubMed  PubMed Central  CAS  Google Scholar 

  • Feng S, Cokus SJ, Schubert V, Zhai J, Pellegrini M, Jacobsen SE (2014) Genome-wide Hi-C analyses in wild-type and mutants reveal high-resolution chromatin interactions in Arabidopsis. Mol Cell 55:694–707

    PubMed  PubMed Central  CAS  Google Scholar 

  • Frerichs A, Engelhorn J, Altmuller J, Gutierrez-Marcos J, Werr W (2019) Specific chromatin changes mark lateral organ founder cells in the Arabidopsis inflorescence meristem. J Exp Bot 70:3867–3879

    PubMed  PubMed Central  CAS  Google Scholar 

  • Fu Y, Luo GZ, Chen K, Deng X, Yu M, Han D, Hao Z, Liu J, Lu X, Dore LC, Weng X, Ji Q, Mets L, He C (2015) N6-methyldeoxyadenosine marks active transcription start sites in Chlamydomonas. Cell 161:879–892

    PubMed  PubMed Central  CAS  Google Scholar 

  • Fullwood MJ, Liu MH, Pan YF, Liu J, Xu H, Mohamed YB, Orlov YL, Velkov S, Ho A, Mei PH, Chew EG, Huang PY, Welboren WJ, Han Y, Ooi HS, Ariyaratne PN, Vega VB, Luo Y, Tan PY, Choy PY, Wansa KD, Zhao B, Lim KS, Leow SC, Yow JS, Joseph R, Li H, Desai KV, Thomsen JS, Lee YK, Karuturi RK, Herve T, Bourque G, Stunnenberg HG, Ruan X, Cacheux-Rataboul V, Sung WK, Liu ET, Wei CL, Cheung E, Ruan Y (2009) An oestrogen-receptor-alpha-bound human chromatin interactome. Nature 462:58–64

    PubMed  PubMed Central  CAS  Google Scholar 

  • Ganguly DR, Crisp PA, Eichten SR, Pogson BJ (2017) The Arabidopsis DNA methylome is stable under transgenerational drought stress. Plant Physiol 175:1893–1912

    PubMed  PubMed Central  CAS  Google Scholar 

  • Gibcus JH, Dekker J (2013) The hierarchy of the 3D genome. Mol Cell 49:773–782

    PubMed  PubMed Central  CAS  Google Scholar 

  • Goudarzi A, Zhang D, Huang H, Barral S, Kwon OK, Qi S, Tang Z, Buchou T, Vitte AL, He T, Cheng Z, Montellier E, Gaucher J, Curtet S, Debernardi A, Charbonnier G, Puthier D, Petosa C, Panne D, Rousseaux S, Roeder RG, Zhao Y, Khochbin S (2016) Dynamic competing histone H4 K5K8 acetylation and butyrylation are hallmarks of highly active gene promoters. Mol Cell 62:169–180

    PubMed  PubMed Central  CAS  Google Scholar 

  • Greaves IK, Groszmann M, Ying H, Taylor JM, Peacock WJ, Dennis ES (2012) Trans chromosomal methylation in Arabidopsis hybrids. Proc Natl Acad Sci USA 109:3570–3575

    PubMed  CAS  PubMed Central  Google Scholar 

  • Greaves IK, Groszmann M, Wang A, Peacock WJ, Dennis ES (2014) Inheritance of trans chromosomal methylation patterns from Arabidopsis F1 hybrids. Proc Natl Acad Sci USA 111:2017–2022

    PubMed  CAS  PubMed Central  Google Scholar 

  • Greaves IK, Gonzalez-Bayon R, Wang L, Zhu A, Liu PC, Groszmann M, Peacock WJ, Dennis ES (2015) Epigenetic changes in hybrids. Plant Physiol 168:1197–1205

    PubMed  PubMed Central  CAS  Google Scholar 

  • Greaves IK, Eichten SR, Groszmann M, Wang A, Ying H, Peacock WJ, Dennis ES (2016) Twenty-four-nucleotide siRNAs produce heritable trans-chromosomal methylation in F1 Arabidopsis hybrids. Proc Natl Acad Sci USA 113:E6895–E6902

    PubMed  CAS  PubMed Central  Google Scholar 

  • Greer EL, Blanco MA, Gu L, Sendinc E, Liu J, Aristizabal-Corrales D, Hsu CH, Aravind L, He C, Shi Y (2015) DNA methylation on N6-adenine in C. elegans. Cell 161:868–878

    PubMed  PubMed Central  CAS  Google Scholar 

  • Guo Z, Song G, Liu Z, Qu X, Chen R, Jiang D, Sun Y, Liu C, Zhu Y, Yang D (2015) Global epigenomic analysis indicates that epialleles contribute to Allele-specific expression via Allele-specific histone modifications in hybrid rice. BMC Genomics 16:232

    PubMed  PubMed Central  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 

  • Hong H, Liu Y, Zhang H, Xiao J, Li X, Wang S (2015) Small RNAs and gene network in a durable disease resistance gene-mediated defense responses in rice. PLoS ONE 10:e0137360

    PubMed  PubMed Central  Google Scholar 

  • Hou Y, Wang L, Wang L, Liu L, Li L, Sun L, Rao Q, Zhang J, Huang S (2015) JMJ704 positively regulates rice defense response against Xanthomonas oryzae pv. oryzae infection via reducing H3K4me2/3 associated with negative disease resistance regulators. BMC Plant Biol 15:286

  • Hu Y, Liu D, Zhong X, Zhang C, Zhang Q, Zhou DX (2012) CHD3 protein recognizes and regulates methylated histone H3 lysines 4 and 27 over a subset of targets in the rice genome. Proc Natl Acad Sci USA 109:5773–5778

    PubMed  CAS  PubMed Central  Google Scholar 

  • Hu L, Li N, Xu C, Zhong S, Lin X, Yang J, Zhou T, Yuliang A, Wu Y, Chen YR, Cao X, Zemach A, Rustgi S, von Wettstein D, Liu B (2014) Mutation of a major CG methylase in rice causes genome-wide hypomethylation, dysregulated genome expression, and seedling lethality. Proc Natl Acad Sci USA 111:10642–10647

    PubMed  CAS  PubMed Central  Google Scholar 

  • Huang L, Sun Q, Qin F, Li C, Zhao Y, Zhou DX (2007) Down-regulation of a SILENT INFORMATION REGULATOR2-related histone deacetylase gene, OsSRT1, induces DNA fragmentation and cell death in rice. Plant Physiol 144:1508–1519

    PubMed  PubMed Central  CAS  Google Scholar 

  • Huang H, Sabari BR, Garcia BA, Allis CD, Zhao Y (2014) SnapShot: histone modifications. Cell 159(458–458):e451

    Google Scholar 

  • Huang J, Wang R, Dai X, Feng J, Zhang H, Zhao PX (2019) A microRNA biogenesis-like pathway for producing phased small interfering RNA from a long non-coding RNA in rice. J Exp Bot 70:1767–1774

    PubMed  CAS  Google Scholar 

  • Ibarra CA, Feng X, Schoft VK, Hsieh TF, Uzawa R, Rodrigues JA, Zemach A, Chumak N, Machlicova A, Nishimura T, Rojas D, Fischer RL, Tamaru H, Zilberman D (2012) Active DNA demethylation in plant companion cells reinforces transposon methylation in gametes. Science 337:1360–1364

    PubMed  PubMed Central  CAS  Google Scholar 

  • Jabnoune M, Secco D, Lecampion C, Robaglia C, Shu Q, Poirier Y (2013) A rice cis-natural antisense RNA acts as a translational enhancer for its cognate mRNA and contributes to phosphate homeostasis and plant fitness. Plant Cell 25:4166–4182

    PubMed  PubMed Central  CAS  Google Scholar 

  • Jain P, Sharma V, Dubey H, Singh PK, Kapoor R, Kumari M, Singh J, Pawar DV, Bisht D, Solanke AU, Mondal TK, Sharma TR (2017) Identification of long non-coding RNA in rice lines resistant to Rice blast pathogen Maganaporthe oryzae. Bioinformation 13:249–255

    PubMed  PubMed Central  Google Scholar 

  • Jiang J (2015) The 'dark matter' in the plant genomes: non-coding and unannotated DNA sequences associated with open chromatin. Curr Opin Plant Biol 24:17–23

    PubMed  Google Scholar 

  • Johnson C, Kasprzewska A, Tennessen K, Fernandes J, Nan GL, Walbot V, Sundaresan V, Vance V, Bowman LH (2009) Clusters and superclusters of phased small RNAs in the developing inflorescence of rice. Genome Res 19:1429–1440

    PubMed  PubMed Central  CAS  Google Scholar 

  • Johnson C, Conrad LJ, Patel R, Anderson S, Li C, Pereira A, Sundaresan V (2018) Reproductive long intergenic noncoding RNAs exhibit male gamete specificity and polycomb repressive complex 2-mediated repression. Plant Physiol 177:1198–1217

    PubMed  PubMed Central  CAS  Google Scholar 

  • Jung I, Ahn H, Shin SJ, Kim J, Kwon HB, Jung W, Kim S (2016) Clustering and evolutionary analysis of small RNAs identify regulatory siRNA clusters induced under drought stress in rice. BMC Syst Biol 10:115

    PubMed  PubMed Central  Google Scholar 

  • Kakrana A, Mathioni SM, Huang K, Hammond R, Vandivier L, Patel P, Arikit S, Shevchenko O, Harkess AE, Kingham B, Gregory BD, Leebens-Mack JH, Meyers BC (2018) Plant 24-nt reproductive phasiRNAs from intramolecular duplex mRNAs in diverse monocots. Genome Res 28:1333–1344

    PubMed  PubMed Central  CAS  Google Scholar 

  • Kawanabe T, Ishikura S, Miyaji N, Sasaki T, Wu LM, Itabashi E, Takada S, Shimizu M, Takasaki-Yasuda T, Osabe K, Peacock WJ, Dennis ES, Fujimoto R (2016) Role of DNA methylation in hybrid vigor in Arabidopsis thaliana. Proc Natl Acad Sci USA 113:E6704–E6711

    PubMed  CAS  PubMed Central  Google Scholar 

  • Kiegle EA, Garden A, Lacchini E, Kater MM (2018) A genomic view of alternative splicing of long non-coding RNAs during rice seed development reveals extensive splicing and lncRNA gene families. Front Plant Sci 9:115

    PubMed  PubMed Central  Google Scholar 

  • Kim MY, Ono A, Scholten S, Kinoshita T, Zilberman D, Okamoto T, Fischer RL (2019) DNA demethylation by ROS1a in rice vegetative cells promotes methylation in sperm. Proc Natl Acad Sci USA 116:9652–9657

    PubMed  CAS  PubMed Central  Google Scholar 

  • Komiya R (2017) Biogenesis of diverse plant phasiRNAs involves an miRNA-trigger and Dicer-processing. J Plant Res 130:17–23

    PubMed  CAS  Google Scholar 

  • Komiya R, Ohyanagi H, Niihama M, Watanabe T, Nakano M, Kurata N, Nonomura K (2014) Rice germline-specific Argonaute MEL1 protein binds to phasiRNAs generated from more than 700 lincRNAs. Plant J 78:385–397

    PubMed  CAS  Google Scholar 

  • Koziol MJ, Bradshaw CR, Allen GE, Costa ASH, Frezza C, Gurdon JB (2016) Identification of methylated deoxyadenosines in vertebrates reveals diversity in DNA modifications. Nat Struct Mol Biol 23:24–30

    PubMed  CAS  Google Scholar 

  • La H, Ding B, Mishra GP, Zhou B, Yang H, Bellizzi Mdel R, Chen S, Meyers BC, Peng Z, Zhu JK, Wang GL (2011) A 5-methylcytosine DNA glycosylase/lyase demethylates the retrotransposon Tos17 and promotes its transposition in rice. Proc Natl Acad Sci USA 108:15498–15503

    PubMed  CAS  PubMed Central  Google Scholar 

  • Lang Z, Wang Y, Tang K, Tang D, Datsenka T, Cheng J, Zhang Y, Handa AK, Zhu JK (2017) Critical roles of DNA demethylation in the activation of ripening-induced genes and inhibition of ripening-repressed genes in tomato fruit. Proc Natl Acad Sci USA 114:E4511–E4519

    PubMed  CAS  PubMed Central  Google Scholar 

  • Lauss K, Wardenaar R, Oka R, van Hulten MHA, Guryev V, Keurentjes JJB, Stam M, Johannes F (2018) Parental DNA methylation states are associated with heterosis in epigenetic hybrids. Plant Physiol 176:1627–1645

    PubMed  CAS  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 

  • Le TN, Schumann U, Smith NA, Tiwari S, Au PC, Zhu QH, Taylor JM, Kazan K, Llewellyn DJ, Zhang R, Dennis ES, Wang MB (2014) DNA demethylases target promoter transposable elements to positively regulate stress responsive genes in Arabidopsis. Genome Biol 15:458

    PubMed  PubMed Central  Google Scholar 

  • Lewsey MG, Hardcastle TJ, Melnyk CW, Molnar A, Valli A, Urich MA, Nery JR, Baulcombe DC, Ecker JR (2016) Mobile small RNAs regulate genome-wide DNA methylation. Proc Natl Acad Sci USA 113:E801–810

    PubMed  CAS  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 C, Huang L, Xu C, Zhao Y, Zhou DX (2011) Altered levels of histone deacetylase OsHDT1 affect differential gene expression patterns in hybrid rice. PLoS ONE 6:e21789

    PubMed  PubMed Central  CAS  Google Scholar 

  • Li X, Zhu JD, Hu FY, Ge S, Ye MZ, Xiang H, Zhang GJ, Zheng XM, Zhang HY, Zhang SL, Li Q, Luo RB, Yu C, Yu J, Sun JF, Zou XY, Cao XF, Xie XF, Wang J, Wang W (2012) Single-base resolution maps of cultivated and wild rice methylomes and regulatory roles of DNA methylation in plant gene expression. BMC Genomics 13

  • Li T, Chen X, Zhong X, Zhao Y, Liu X, Zhou S, Cheng S, Zhou DX (2013) Jumonji C domain protein JMJ705-mediated removal of histone H3 lysine 27 trimethylation is involved in defense-related gene activation in rice. Plant Cell 25:4725–4736

    PubMed  PubMed Central  CAS  Google Scholar 

  • Li X, Luo OJ, Wang P, Zheng M, Wang D, Piecuch E, Zhu JJ, Tian SZ, Tang Z, Li G, Ruan Y (2017a) Long-read ChIA-PET for base-pair-resolution mapping of haplotype-specific chromatin interactions. Nat Protoc 12:899–915

    PubMed  PubMed Central  CAS  Google Scholar 

  • Li Y, Zhao D, Chen Z, Li H (2017b) YEATS domain: linking histone crotonylation to gene regulation. Transcription 8:9–14

    PubMed  CAS  Google Scholar 

  • Li C, Liu Y, Shen WH, Yu Y, Dong A (2018a) Chromatin-remodeling factor OsINO80 is involved in regulation of gibberellin biosynthesis and is crucial for rice plant growth and development. J Integr Plant Biol 60:144–159

    PubMed  CAS  Google Scholar 

  • Li F, Wan M, Zhang B, Peng Y, Zhou Y, Pi C, Xu X, Ye L, Zhou X, Zheng L (2018b) Bivalent histone modifications and development. Curr Stem Cell Res Ther 13:83–90

    PubMed  Google Scholar 

  • Li N, Xu C, Zhang A, Lv R, Meng X, Lin X, Gong L, Wendel JF, Liu B (2019a) DNA methylation repatterning accompanying hybridization, whole genome doubling and homoeolog exchange in nascent segmental rice allotetraploids. New Phytol 223:979–992

    PubMed  CAS  Google Scholar 

  • Li P, Yang H, Wang L, Liu H, Huo H, Zhang C, Liu A, Zhu A, Hu J, Lin Y, Liu L (2019b) Physiological and transcriptome analyses reveal short-term responses and formation of memory under drought stress in rice. Front Genet 10:55

    PubMed  PubMed Central  CAS  Google Scholar 

  • Lin H, Su X, He B (2012) Protein lysine acylation and cysteine succination by intermediates of energy metabolism. ACS Chem Biol 7:947–960

    PubMed  PubMed Central  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Liu X, Zhou C, Zhao Y, Zhou S, Wang W, Zhou DX (2014) The rice enhancer of zeste [E(z)] genes SDG711 and SDG718 are respectively involved in long day and short day signaling to mediate the accurate photoperiod control of flowering time. Front Plant Sci 5:591

    PubMed  PubMed Central  Google Scholar 

  • Liu X, Zhou S, Wang W, Ye Y, Zhao Y, Xu Q, Zhou C, Tan F, Cheng S, Zhou DX (2015) Regulation of histone methylation and reprogramming of gene expression in the rice inflorescence meristem. Plant Cell 27:1428–1444

    PubMed  PubMed Central  CAS  Google Scholar 

  • Liu B, Wei G, Shi J, Jin J, Shen T, Ni T, Shen WH, Yu Y, Dong A (2016a) SET DOMAIN GROUP 708, a histone H3 lysine 36-specific methyltransferase, controls flowering time in rice (Oryza sativa). New Phytol 210:577–588

    CAS  PubMed  Google Scholar 

  • Liu J, Zhu Y, Luo GZ, Wang X, Yue Y, Wang X, Zong X, Chen K, Yin H, Fu Y, Han D, Wang Y, Chen D, He C (2016b) Abundant DNA 6mA methylation during early embryogenesis of zebrafish and pig. Nat Commun 7:13052

    PubMed  PubMed Central  CAS  Google Scholar 

  • Liu C, Cheng YJ, Wang JW, Weigel D (2017a) Prominent topologically associated domains differentiate global chromatin packing in rice from Arabidopsis. Nat Plants 3:742–748

    PubMed  CAS  Google Scholar 

  • Liu K, Yu Y, Dong A, Shen WH (2017b) SET DOMAIN GROUP701 encodes a H3K4-methytransferase and regulates multiple key processes of rice plant development. New Phytol 215:609–623

    CAS  PubMed  Google Scholar 

  • Liu S, Xue C, Fang Y, Chen G, Peng X, Zhou Y, Chen C, Liu G, Gu M, Wang K, Zhang W, Wu Y, Gong Z (2018a) Global involvement of lysine crotonylation in protein modification and transcription regulation in rice. Mol Cell Proteomics 17:1922–1936

    PubMed  PubMed Central  CAS  Google Scholar 

  • Liu X, Li D, Zhang D, Yin D, Zhao Y, Ji C, Zhao X, Li X, He Q, Chen R, Hu S, Zhu L (2018b) A novel antisense long noncoding RNA, TWISTED LEAF, maintains leaf blade flattening by regulating its associated sense R2R3-MYB gene in rice. New Phytol 218:774–788

    PubMed  CAS  Google Scholar 

  • Liu H, Wang R, Mao B, Zhao B, Wang J (2019) Identification of lncRNAs involved in rice ovule development and female gametophyte abortion by genome-wide screening and functional analysis. BMC Genomics 20:90

    PubMed  PubMed Central  CAS  Google Scholar 

  • Lu L, Chen X, Sanders D, Qian S, Zhong X (2015) High-resolution mapping of H4K16 and H3K23 acetylation reveals conserved and unique distribution patterns in Arabidopsis and rice. Epigenetics 10:1044–1053

    PubMed  PubMed Central  Google Scholar 

  • Lu Z, Hofmeister BT, Vollmers C, DuBois RM, Schmitz RJ (2017) Combining ATAC-seq with nuclei sorting for discovery of cis-regulatory regions in plant genomes. Nucleic Acids Res 45:e41

    PubMed  Google Scholar 

  • Lu Y, Xu Q, Liu Y, Yu Y, Cheng ZY, Zhao Y, Zhou DX (2018a) Dynamics and functional interplay of histone lysine butyrylation, crotonylation, and acetylation in rice under starvation and submergence. Genome Biol 19:144

    PubMed  PubMed Central  Google Scholar 

  • Lu Z, Ricci WA, Schmitz RJ, Zhang X (2018b) Identification of cis-regulatory elements by chromatin structure. Curr Opin Plant Biol 42:90–94

    PubMed  CAS  Google Scholar 

  • Lu Z, Marand AP, Ricci WA, Ethridge CL, Zhang X, Schmitz RJ (2019) The prevalence, evolution and chromatin signatures of plant regulatory elements. Nat Plants

  • Ma L, Bajic VB, Zhang Z (2013) On the classification of long non-coding RNAs. RNA Biol 10:925–933

    PubMed  Google Scholar 

  • Maher KA, Bajic M, Kajala K, Reynoso M, Pauluzzi G, West DA, Zumstein K, Woodhouse M, Bubb K, Dorrity MW, Queitsch C, Bailey-Serres J, Sinha N, Brady SM, Deal RB (2018) Profiling of Accessible Chromatin Regions across Multiple Plant Species and Cell Types Reveals Common Gene Regulatory Principles and New Control Modules. Plant Cell 30:15–36

    PubMed  CAS  Google Scholar 

  • Mahrez W, Arellano MS, Moreno-Romero J, Nakamura M, Shu H, Nanni P, Kohler C, Gruissem W, Hennig L (2016) H3K36ac Is an Evolutionary Conserved Plant Histone Modification That Marks Active Genes. Plant Physiol 170:1566–1577

    PubMed  PubMed Central  CAS  Google Scholar 

  • Martinez G, Panda K, Kohler C, Slotkin RK (2016) Silencing in sperm cells is directed by RNA movement from the surrounding nurse cell. Nat Plants 2:16030

    PubMed  CAS  Google Scholar 

  • Matzke M, Kanno T, Daxinger L, Huettel B, Matzke AJ (2009) RNA-mediated chromatin-based silencing in plants. Curr Opin Cell Biol 21:367–376

    PubMed  CAS  Google Scholar 

  • Matzke MA, Kanno T, Matzke AJ (2015) RNA-Directed DNA Methylation: The Evolution of a Complex Epigenetic Pathway in Flowering Plants. Annu Rev Plant Biol 66:243–267

    PubMed  CAS  Google Scholar 

  • Melnyk CW, Molnar A, Bassett A, Baulcombe DC (2011a) Mobile 24 nt small RNAs direct transcriptional gene silencing in the root meristems of Arabidopsis thaliana. Curr Biol 21:1678–1683

    PubMed  CAS  Google Scholar 

  • Melnyk CW, Molnar A, Baulcombe DC (2011b) Intercellular and systemic movement of RNA silencing signals. EMBO J 30:3553–3563

    PubMed  PubMed Central  CAS  Google Scholar 

  • Meyers BC, Axtell MJ, Bartel B, Bartel DP, Baulcombe D, Bowman JL, Cao X, Carrington JC, Chen X, Green PJ, Griffiths-Jones S, Jacobsen SE, Mallory AC, Martienssen RA, Poethig RS, Qi Y, Vaucheret H, Voinnet O, Watanabe Y, Weigel D, Zhu JK (2008) Criteria for annotation of plant MicroRNAs. Plant Cell 20:3186–3190

    PubMed  PubMed Central  CAS  Google Scholar 

  • Millard CJ, Varma N, Saleh A, Morris K, Watson PJ, Bottrill AR, Fairall L, Smith CJ, Schwabe JW (2016) The structure of the core NuRD repression complex provides insights into its interaction with chromatin. Elife 5:e13941

    PubMed  PubMed Central  Google Scholar 

  • Miura K, Agetsuma M, Kitano H, Yoshimura A, Matsuoka M, Jacobsen SE, Ashikari M (2009) A metastable DWARF1 epigenetic mutant affecting plant stature in rice. Proc Natl Acad Sci USA 106:11218–11223

    PubMed  CAS  PubMed Central  Google Scholar 

  • Molnar A, Melnyk CW, Bassett A, Hardcastle TJ, Dunn R, Baulcombe DC (2010) Small silencing RNAs in plants are mobile and direct epigenetic modification in recipient cells. Science 328:872–875

    PubMed  CAS  Google Scholar 

  • Moraga F, Aquea F (2015) Composition of the SAGA complex in plants and its role in controlling gene expression in response to abiotic stresses. Front Plant Sci 6:865

    PubMed  PubMed Central  Google Scholar 

  • Moritoh S, Eun CH, Ono A, Asao H, Okano Y, Yamaguchi K, Shimatani Z, Koizumi A, Terada R (2012) Targeted disruption of an orthologue of DOMAINS REARRANGED METHYLASE 2, OsDRM2, impairs the growth of rice plants by abnormal DNA methylation. Plant J 71:85–98

    PubMed  CAS  Google Scholar 

  • Muerdter F, Boryn LM, Arnold CD (2015) STARR-seq—principles and applications. Genomics 106:145–150

    PubMed  CAS  Google Scholar 

  • Nekrasov M, Amrichova J, Parker BJ, Soboleva TA, Jack C, Williams R, Huttley GA, Tremethick DJ (2012) Histone H2A.Z inheritance during the cell cycle and its impact on promoter organization and dynamics. Nat Struct Mol Biol 19:1076–1083

    PubMed  CAS  Google Scholar 

  • Niu D, Zhang X, Song X, Wang Z, Li Y, Qiao L, Wang Z, Liu J, Deng Y, He Z, Yang D, Liu R, Wang Y, Zhao H (2018) Deep Sequencing Uncovers Rice Long siRNAs and Its Involvement in Immunity Against Rhizoctonia solani. Phytopathology 108:60–69

    PubMed  CAS  Google Scholar 

  • Oka R, Zicola J, Weber B, Anderson SN, Hodgman C, Gent JI, Wesselink JJ, Springer NM, Hoefsloot HCJ, Turck F, Stam M (2017) Genome-wide mapping of transcriptional enhancer candidates using DNA and chromatin features in maize. Genome Biol 18:137

    PubMed  PubMed Central  Google Scholar 

  • Ono S, Liu H, Tsuda K, Fukai E, Tanaka K, Sasaki T, Nonomura KI (2018) EAT1 transcription factor, a non-cell-autonomous regulator of pollen production, activates meiotic small RNA biogenesis in rice anther tapetum. PLoS Genet 14:e1007238

    PubMed  PubMed Central  Google Scholar 

  • Otero S, Desvoyes B, Gutierrez C (2014) Histone H3 dynamics in plant cell cycle and development. Cytogenet Genome Res 143:114–124

    PubMed  CAS  Google Scholar 

  • Ou X, Zhang Y, Xu C, Lin X, Zang Q, Zhuang T, Jiang L, von Wettstein D, Liu B (2012) Transgenerational inheritance of modified DNA methylation patterns and enhanced tolerance induced by heavy metal stress in rice (Oryza sativa L.). PLoS One 7:e41143

  • Park K, Kim MY, Vickers M, Park JS, Hyun Y, Okamoto T, Zilberman D, Fischer RL, Feng X, Choi Y, Scholten S (2016) DNA demethylation is initiated in the central cells of Arabidopsis and rice. Proc Natl Acad Sci USA 113:15138–15143

    PubMed  CAS  PubMed Central  Google Scholar 

  • Patel P, Mathioni S, Kakrana A, Shatkay H, Meyers BC (2018) Reproductive phasiRNAs in grasses are compositionally distinct from other classes of small RNAs. New Phytol 220:851–864

    PubMed  CAS  Google Scholar 

  • Peng Y, Xiong D, Zhao L, Ouyang W, Wang S, Sun J, Zhang Q, Guan P, Xie L, Li W, Li G, Yan J, Li X (2019) Chromatin interaction maps reveal genetic regulation for quantitative traits in maize. Nat Commun 10:2632

    PubMed  PubMed Central  Google Scholar 

  • Qin FJ, Sun QW, Huang LM, Chen XS, Zhou DX (2010) Rice SUVH histone methyltransferase genes display specific functions in chromatin modification and retrotransposon repression. Mol Plant 3:773–782

    CAS  PubMed  Google Scholar 

  • Qiu SP, Huang J, Pan LJ, Wang MM, Zhang HS (2006) Salt induces expression of RH3.2A, encoding an H3.2-type histone H3 protein in rice (Oryza sativa L.). Yi Chuan Xue Bao 33:833–840

    PubMed  CAS  Google Scholar 

  • Ricci WA, Lu Z, Ji L, Marand AP, Ethridge CL, Murphy NG, Noshay JM, Galli M, Mejia-Guerra MK, Colome-Tatche M, Johannes F, Rowley MJ, Corces VG, Zhai J, Scanlon MJ, Buckler ES, Gallavotti A, Springer NM, Schmitz RJ, Zhang X (2019) Widespread long-range cis-regulatory elements in the maize genome. Nat Plants

  • Rodrigues JA, Ruan R, Nishimura T, Sharma MK, Sharma R, Ronald PC, Fischer RL, Zilberman D (2013) Imprinted expression of genes and small RNA is associated with localized hypomethylation of the maternal genome in rice endosperm. Proc Natl Acad Sci USA 110:7934–7939

    PubMed  CAS  PubMed Central  Google Scholar 

  • Ruan B, Hua Z, Zhao J, Zhang B, Ren D, Liu C, Yang S, Zhang A, Jiang H, Yu H, Hu J, Zhu L, Chen G, Shen L, Dong G, Zhang G, Zeng D, Guo L, Qian Q, Gao Z (2019) OsACL-A2 negatively regulates cell death and disease resistance in rice. Plant Biotechnol J 17:1344–1356

    PubMed  PubMed Central  CAS  Google Scholar 

  • Sabari BR, Tang Z, Huang H, Yong-Gonzalez V, Molina H, Kong HE, Dai L, Shimada M, Cross JR, Zhao Y, Roeder RG, Allis CD (2015) Intracellular crotonyl-CoA stimulates transcription through p300-catalyzed histone crotonylation. Mol Cell 58:203–215

    PubMed  PubMed Central  CAS  Google Scholar 

  • Sabari BR, Zhang D, Allis CD, Zhao Y (2017) Metabolic regulation of gene expression through histone acylations. Nat Rev Mol Cell Biol 18:90–101

    PubMed  CAS  Google Scholar 

  • Sarkies P, Selkirk ME, Jones JT, Blok V, Boothby T, Goldstein B, Hanelt B, Ardila-Garcia A, Fast NM, Schiffer PM, Kraus C, Taylor MJ, Koutsovoulos G, Blaxter ML, Miska EA (2015) Ancient and novel small RNA pathways compensate for the loss of piRNAs in multiple independent nematode lineages. PLoS Biol 13:e1002061

    PubMed  PubMed Central  Google Scholar 

  • Seitz H (2009) Redefining microRNA targets. Curr Biol 19:870–873

    PubMed  CAS  Google Scholar 

  • Shen Y, Wei W, Zhou DX (2015) Histone Acetylation Enzymes Coordinate Metabolism and Gene Expression. Trends Plant Sci 20:614–621

    PubMed  CAS  Google Scholar 

  • Shen Y, Issakidis-Bourguet E, Zhou DX (2016) Perspectives on the interactions between metabolism, redox, and epigenetics in plants. J Exp Bot 67:5291–5300

    PubMed  CAS  Google Scholar 

  • Shin SY, Jeong JS, Lim JY, Kim T, Park JH, Kim JK, Shin C (2018) Transcriptomic analyses of rice (Oryza sativa) genes and non-coding RNAs under nitrogen starvation using multiple omics technologies. BMC Genomics 19:532

    PubMed  PubMed Central  Google Scholar 

  • Sijacic P, Bajic M, McKinney EC, Meagher RB, Deal RB (2018) Changes in chromatin accessibility between Arabidopsis stem cells and mesophyll cells illuminate cell type-specific transcription factor networks. Plant J 94:215–231

    PubMed  CAS  PubMed Central  Google Scholar 

  • Slotkin RK, Vaughn M, Borges F, Tanurdzic M, Becker JD, Feijo JA, Martienssen RA (2009) Epigenetic reprogramming and small RNA silencing of transposable elements in pollen. Cell 136:461–472

    PubMed  PubMed Central  CAS  Google Scholar 

  • Song Q, Chen ZJ (2015) Epigenetic and developmental regulation in plant polyploids. Curr Opin Plant Biol 24:101–109

    PubMed  PubMed Central  CAS  Google Scholar 

  • Song X, Li P, Zhai J, Zhou M, Ma L, Liu B, Jeong DH, Nakano M, Cao S, Liu C, Chu C, Wang XJ, Green PJ, Meyers BC, Cao X (2012a) Roles of DCL4 and DCL3b in rice phased small RNA biogenesis. Plant J 69:462–474

    PubMed  CAS  Google Scholar 

  • Song X, Wang D, Ma L, Chen Z, Li P, Cui X, Liu C, Cao S, Chu C, Tao Y, Cao X (2012b) Rice RNA-dependent RNA polymerase 6 acts in small RNA biogenesis and spikelet development. Plant J 71:378–389

    PubMed  CAS  Google Scholar 

  • Song X, Li Y, Cao X, Qi Y (2019) MicroRNAs and Their Regulatory Roles in Plant-Environment Interactions. Annu Rev Plant Biol 70:489–525

    PubMed  CAS  Google Scholar 

  • Stroud H, Ding B, Simon SA, Feng S, Bellizzi M, Pellegrini M, Wang GL, Meyers BC, Jacobsen SE (2013) Plants regenerated from tissue culture contain stable epigenome changes in rice. Elife 2:e00354

    PubMed  PubMed Central  Google Scholar 

  • Sui P, Jin J, Ye S, Mu C, Gao J, Feng H, Shen WH, Yu Y, Dong A (2012) H3K36 methylation is critical for brassinosteroid-regulated plant growth and development in rice. Plant J 70:340–347

    CAS  PubMed  Google Scholar 

  • Sui P, Shi J, Gao X, Shen WH, Dong A (2013) H3K36 methylation is involved in promoting rice flowering. Mol Plant 6:975–977

    PubMed  CAS  Google Scholar 

  • Sun Q, Zhou DX (2008) Rice jmjC domain-containing gene JMJ706 encodes H3K9 demethylase required for floral organ development. Proc Natl Acad Sci USA 105:13679–13684

    PubMed  CAS  PubMed Central  Google Scholar 

  • Sun C, Fang J, Zhao T, Xu B, Zhang F, Liu L, Tang J, Zhang G, Deng X, Chen F, Qian Q, Cao X, Chu C (2012) The histone methyltransferase SDG724 mediates H3K36me2/3 deposition at MADS50 and RFT1 and promotes flowering in rice. Plant Cell 24:3235–3247

    PubMed  PubMed Central  CAS  Google Scholar 

  • Sun J, He N, Niu L, Huang Y, Shen W, Zhang Y, Li L, Hou C (2019) Global quantitative mapping of enhancers in rice by STARR-seq. Genomics Proteom Bioinform 17:140–153

    PubMed  PubMed Central  Google Scholar 

  • Sura W, Kabza M, Karlowski WM, Bieluszewski T, Kus-Slowinska M, Paweloszek L, Sadowski J, Ziolkowski PA (2017) Dual role of the histone variant H2A.Z in transcriptional regulation of stress-response genes. Plant Cell 29:791–807

    PubMed  PubMed Central  CAS  Google Scholar 

  • Talbert PB, Henikoff S (2010) Histone variants–ancient wrap artists of the epigenome. Nat Rev Mol Cell Biol 11:264–275

    PubMed  CAS  Google Scholar 

  • Tan F, Zhou C, Zhou Q, Zhou S, Yang W, Zhao Y, Li G, Zhou DX (2016) Analysis of chromatin regulators reveals specific features of rice DNA methylation pathways. Plant Physiol 171:2041–2054

    PubMed  PubMed Central  CAS  Google Scholar 

  • Tan F, Lu Y, Jiang W, Wu T, Zhang R, Zhao Y, Zhou DX (2018) DDM1 represses noncoding RNA expression and RNA-directed DNA methylation in heterochromatin. Plant Physiol 177:1187–1197

    PubMed  PubMed Central  CAS  Google Scholar 

  • Tang Z, Xu M, Ito H, Cai J, Ma X, Qin J, Yu D, Meng Y (2019) Deciphering the non-coding RNA-level response to arsenic stress in rice (Oryza sativa). Plant Signal Behav 1–11

  • Tannenbaum M, Sarusi-Portuguez A, Krispil R, Schwartz M, Loza O, Benichou JIC, Mosquna A, Hakim O (2018) Regulatory chromatin landscape in Arabidopsis thaliana roots uncovered by coupling INTACT and ATAC-seq. Plant Methods 14:113

    PubMed  PubMed Central  CAS  Google Scholar 

  • Ullah F, Hamilton M, Reddy ASN, Ben-Hur A (2018) Exploring the relationship between intron retention and chromatin accessibility in plants. BMC Genomics 19:21

    PubMed  PubMed Central  Google Scholar 

  • Van Ex F, Jacob Y, Martienssen RA (2011) Multiple roles for small RNAs during plant reproduction. Curr Opin Plant Biol 14:588–593

    PubMed  PubMed Central  Google Scholar 

  • Virlouvet L, Avenson TJ, Du Q, Zhang C, Liu N, Fromm M, Avramova Z, Russo SE (2018) Dehydration stress memory: gene networks linked to physiological responses during repeated stresses of Zea mays. Front Plant Sci 9:1058

    PubMed  PubMed Central  Google Scholar 

  • Voigt P, Tee WW, Reinberg D (2013) A double take on bivalent promoters. Genes Dev 27:1318–1338

    PubMed  PubMed Central  CAS  Google Scholar 

  • Voinnet O (2009) Origin, biogenesis, and activity of plant microRNAs. Cell 136:669–687

    PubMed  CAS  Google Scholar 

  • Wagner EJ, Carpenter PB (2012) Understanding the language of Lys36 methylation at histone H3. Nat Rev Mol Cell Biol 13:115–126

    PubMed  PubMed Central  CAS  Google Scholar 

  • Wakasa Y, Kawakatsu T, Harada T, Takaiwa F (2018) Transgene-independent heredity of RdDM-mediated transcriptional gene silencing of endogenous genes in rice. Plant Biotechnol J 16:2007–2015

    PubMed  PubMed Central  CAS  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 H, Niu QW, Wu HW, Liu J, Ye J, Yu N, Chua NH (2015) Analysis of non-coding transcriptome in rice and maize uncovers roles of conserved lncRNAs associated with agriculture traits. Plant J 84:404–416

    PubMed  CAS  Google Scholar 

  • Wang M, Wang P, Tu L, Zhu S, Zhang L, Li Z, Zhang Q, Yuan D, Zhang X (2016) Multi-omics maps of cotton fibre reveal epigenetic basis for staged single-cell differentiation. Nucleic Acids Res 44:4067–4079

    PubMed  PubMed Central  CAS  Google Scholar 

  • Wang D, Qu Z, Yang L, Zhang Q, Liu ZH, Do T, Adelson DL, Wang ZY, Searle I, Zhu JK (2017a) 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 X, Zhang Z, Fu T, Hu L, Xu C, Gong L, Wendel JF, Liu B (2017b) Gene-body CG methylation and divergent expression of duplicate genes in rice. Sci Rep 7:2675

    PubMed  PubMed Central  Google Scholar 

  • Wang Y, Chen X, Sheng Y, Liu Y, Gao S (2017c) N6-adenine DNA methylation is associated with the linker DNA of H2A.Z-containing well-positioned nucleosomes in Pol II-transcribed genes in Tetrahymena. Nucleic Acids Res 45:11594–11606

    PubMed  PubMed Central  CAS  Google Scholar 

  • Wang Y, Luo X, Sun F, Hu J, Zha X, Su W, Yang J (2018) Overexpressing lncRNA LAIR increases grain yield and regulates neighbouring gene cluster expression in rice. Nat Commun 9:3516

    PubMed  PubMed Central  Google Scholar 

  • Wei L, Gu L, Song X, Cui X, Lu Z, Zhou M, Wang L, Hu F, Zhai J, Meyers BC, Cao X (2014) Dicer-like 3 produces transposable element-associated 24-nt siRNAs that control agricultural traits in rice. Proc Natl Acad Sci USA 111:3877–3882

    PubMed  CAS  PubMed Central  Google Scholar 

  • Wei W, Liu X, Chen J, Gao S, Lu L, Zhang H, Ding G, Wang Z, Chen Z, Shi T, Li J, Yu J, Wong J (2017a) Class I histone deacetylases are major histone decrotonylases: evidence for critical and broad function of histone crotonylation in transcription. Cell Res 27:898–915

    PubMed  PubMed Central  CAS  Google Scholar 

  • Wei X, Song X, Wei L, Tang S, Sun J, Hu P, Cao X (2017b) An epiallele of rice AK1 affects photosynthetic capacity. J Integr Plant Biol 59:158–163

    PubMed  CAS  Google Scholar 

  • Wollmann H, Holec S, Alden K, Clarke ND, Jacques PE, Berger F (2012) Dynamic deposition of histone variant H3.3 accompanies developmental remodeling of the Arabidopsis transcriptome. PLoS Genet 8:e1002658

  • Wollmann H, Stroud H, Yelagandula R, Tarutani Y, Jiang D, Jing L, Jamge B, Takeuchi H, Holec S, Nie X, Kakutani T, Jacobsen SE, Berger F (2017) The histone H3 variant H3.3 regulates gene body DNA methylation in Arabidopsis thaliana. Genome Biol 18:94

  • Wu L, Zhou H, Zhang Q, Zhang J, Ni F, Liu C, Qi Y (2010) DNA methylation mediated by a microRNA pathway. Mol Cell 38:465–475

    PubMed  CAS  Google Scholar 

  • Wu Y, Kikuchi S, Yan H, Zhang W, Rosenbaum H, Iniguez AL, Jiang J (2011) Euchromatic subdomains in rice centromeres are associated with genes and transcription. Plant Cell 23:4054–4064

    PubMed  PubMed Central  CAS  Google Scholar 

  • Wu HJ, Wang ZM, Wang M, Wang XJ (2013) Widespread long noncoding RNAs as endogenous target mimics for microRNAs in plants. Plant Physiol 161:1875–1884

    PubMed  PubMed Central  CAS  Google Scholar 

  • Wu TP, Wang T, Seetin MG, Lai Y, Zhu S, Lin K, Liu Y, Byrum SD, Mackintosh SG, Zhong M, Tackett A, Wang G, Hon LS, Fang G, Swenberg JA, Xiao AZ (2016) DNA methylation on N(6)-adenine in mammalian embryonic stem cells. Nature 532:329–333

    PubMed  PubMed Central  CAS  Google Scholar 

  • Xia R, Xu J, Meyers BC (2017) The emergence, evolution, and diversification of the miR390-TAS3-ARF pathway in land plants. Plant Cell 29:1232–1247

    PubMed  PubMed Central  CAS  Google Scholar 

  • Xing MQ, Zhang YJ, Zhou SR, Hu WY, Wu XT, Ye YJ, Wu XX, Xiao YP, Li X, Xue HW (2015) Global analysis reveals the crucial roles of DNA methylation during rice seed development. Plant Physiol 168:1417–1432

    PubMed  PubMed Central  CAS  Google Scholar 

  • Yan Y, Zhang Y, Yang K, Sun Z, Fu Y, Chen X, Fang R (2011) Small RNAs from MITE-derived stem-loop precursors regulate abscisic acid signaling and abiotic stress responses in rice. Plant J 65:820–828

    PubMed  CAS  Google Scholar 

  • Yan W, Chen D, Schumacher J, Durantini D, Engelhorn J, Chen M, Carles CC, Kaufmann K (2019) Dynamic control of enhancer activity drives stage-specific gene expression during flower morphogenesis. Nat Commun 10:1705

    PubMed  PubMed Central  Google Scholar 

  • Yang M, Xu Z, Zhao W, Liu Q, Li Q, Lu L, Liu R, Zhang X, Cui F (2018a) Rice stripe virus-derived siRNAs play different regulatory roles in rice and in the insect vector Laodelphax striatellus. BMC Plant Biol 18:219

    PubMed  PubMed Central  CAS  Google Scholar 

  • Yang Z, Qian S, Scheid RN, Lu L, Chen X, Liu R, Du X, Lv X, Boersma MD, Scalf M, Smith LM, Denu JM, Du J, Zhong X (2018b) EBS is a bivalent histone reader that regulates floral phase transition in Arabidopsis. Nat Genet 50:1247–1253

    PubMed  PubMed Central  CAS  Google Scholar 

  • Yao B, Cheng Y, Wang Z, Li Y, Chen L, Huang L, Zhang W, Chen D, Wu H, Tang B, Jin P (2017) DNA N6-methyladenine is dynamically regulated in the mouse brain following environmental stress. Nat Commun 8:1122

    PubMed  PubMed Central  Google Scholar 

  • Yin BL, Guo L, Zhang DF, Terzaghi W, Wang XF, Liu TT, He H, Cheng ZK, Deng XW (2008) Integration of cytological features with molecular and epigenetic properties of rice chromosome 4. Mol Plant 1:816–829

    PubMed  CAS  Google Scholar 

  • Yokoo T, Saito H, Yoshitake Y, Xu Q, Asami T, Tsukiyama T, Teraishi M, Okumoto Y, Tanisaka T (2014) Se14, encoding a JmjC domain-containing protein, plays key roles in long-day suppression of rice flowering through the demethylation of H3K4me3 of RFT1. PLoS ONE 9:e96064

    PubMed  PubMed Central  Google Scholar 

  • Young MD, Willson TA, Wakefield MJ, Trounson E, Hilton DJ, Blewitt ME, Oshlack A, Majewski IJ (2011) ChIP-seq analysis reveals distinct H3K27me3 profiles that correlate with transcriptional activity. Nucleic Acids Res 39:7415–7427

    PubMed  PubMed Central  CAS  Google Scholar 

  • Yu M, Ren B (2017) The three-dimensional organization of mammalian genomes. Annu Rev Cell Dev Biol 33:265–289

    PubMed  PubMed Central  CAS  Google Scholar 

  • Yuan J, Li J, Yang Y, Tan C, Zhu Y, Hu L, Qi Y, Lu ZJ (2018) Stress-responsive regulation of long non-coding RNA polyadenylation in Oryza sativa. Plant J 93:814–827

    PubMed  CAS  Google Scholar 

  • Zahraeifard S, Foroozani M, Sepehri A, Oh DH, Wang G, Mangu V, Chen B, Baisakh N, Dassanayake M, Smith AP (2018) Rice H2A.Z negatively regulates genes responsive to nutrient starvation but promotes expression of key housekeeping genes. J Exp Bot 69:4907–4919

    PubMed  PubMed Central  CAS  Google Scholar 

  • Zemach A, Kim MY, Silva P, Rodrigues JA, Dotson B, Brooks MD, Zilberman D (2010a) Local DNA hypomethylation activates genes in rice endosperm. Proc Natl Acad Sci USA 107:18729–18734

    PubMed  CAS  PubMed Central  Google Scholar 

  • Zemach A, McDaniel IE, Silva P, Zilberman D (2010b) Genome-wide evolutionary analysis of eukaryotic DNA methylation. Science 328:916–919

    PubMed  CAS  Google Scholar 

  • Zhai J, Zhang H, Arikit S, Huang K, Nan GL, Walbot V, Meyers BC (2015) Spatiotemporally dynamic, cell-type-dependent premeiotic and meiotic phasiRNAs in maize anthers. Proc Natl Acad Sci USA 112:3146–3151

    PubMed  CAS  PubMed Central  Google Scholar 

  • Zhang W, Jiang J (2015) Genome-wide mapping of DNase I hypersensitive sites in plants. Methods Mol Biol 1284:71–89

    PubMed  CAS  Google Scholar 

  • Zhang X, Bernatavichute YV, Cokus S, Pellegrini M, Jacobsen SE (2009) Genome-wide analysis of mono-, di- and trimethylation of histone H3 lysine 4 in Arabidopsis thaliana. Genome Biol 10:R62

    PubMed  PubMed Central  Google Scholar 

  • Zhang L, Cheng Z, Qin R, Qiu Y, Wang JL, Cui X, Gu L, Zhang X, Guo X, Wang D, Jiang L, Wu CY, Wang H, Cao X, Wan J (2012a) Identification and characterization of an epi-allele of FIE1 reveals a regulatory linkage between two epigenetic marks in rice. Plant Cell 24:4407–4421

    PubMed  PubMed Central  CAS  Google Scholar 

  • Zhang W, Wu Y, Schnable JC, Zeng Z, Freeling M, Crawford GE, Jiang J (2012b) High-resolution mapping of open chromatin in the rice genome. Res 22:151–162

    CAS  Google Scholar 

  • Zhang YC, Liao JY, Li ZY, Yu Y, Zhang JP, Li QF, Qu LH, Shu WS, Chen YQ (2014) Genome-wide screening and functional analysis identify a large number of long noncoding RNAs involved in the sexual reproduction of rice. Genome Biol 15:512

    PubMed  PubMed Central  Google Scholar 

  • Zhang G, Huang H, Liu D, Cheng Y, Liu X, Zhang W, Yin R, Zhang D, Zhang P, Liu J, Li C, Liu B, Luo Y, Zhu Y, Zhang N, He S, He C, Wang H, Chen D (2015a) N6-methyladenine DNA modification in Drosophila. Cell 161:893–906

    PubMed  CAS  Google Scholar 

  • Zhang J, Liu Y, Xia EH, Yao QY, Liu XD, Gao LZ (2015b) Autotetraploid rice methylome analysis reveals methylation variation of transposable elements and their effects on gene expression. Proc Natl Acad Sci USA 112:E7022–7029

    PubMed  CAS  PubMed Central  Google Scholar 

  • Zhang X, Sun J, Cao X, Song X (2015c) Epigenetic mutation of RAV6 affects leaf angle and seed size in rice. Plant Physiol 169:2118–2128

    PubMed  PubMed Central  CAS  Google Scholar 

  • Zhang H, Lu Y, Zhao Y, Zhou DX (2016a) OsSRT1 is involved in rice seed development through regulation of starch metabolism gene expression. Plant Sci 248:28–36

    PubMed  CAS  Google Scholar 

  • Zhang H, Tao Z, Hong H, Chen Z, Wu C, Li X, Xiao J, Wang S (2016b) Transposon-derived small RNA is responsible for modified function of WRKY45 locus. Nat Plants 2:16016

    PubMed  CAS  Google Scholar 

  • Zhang Q, Wang D, Lang Z, He L, Yang L, Zeng L, Li Y, Zhao C, Huang H, Zhang H, Zhang H, Zhu JK (2016c) Methylation interactions in Arabidopsis hybrids require RNA-directed DNA methylation and are influenced by genetic variation. Proc Natl Acad Sci USA 113:E4248–4256

    PubMed  CAS  PubMed Central  Google Scholar 

  • Zhang T, Marand AP, Jiang J (2016d) PlantDHS: a database for DNase I hypersensitive sites in plants. Nucleic Acids Res 44:D1148–D1153

    PubMed  CAS  Google Scholar 

  • Zhang K, Xu W, Wang C, Yi X, Su Z (2017a) Differential deposition of H2A.Z in rice seedling tissue during the day-night cycle. Plant Signal Behav 12:e1286438

    PubMed  PubMed Central  Google Scholar 

  • Zhang K, Xu W, Wang C, Yi X, Zhang W, Su Z (2017) Differential deposition of H2A.Z in combination with histone modifications within related genes in Oryza sativa callus and seedling. Plant J 89:264–277

    PubMed  CAS  Google Scholar 

  • Zhang H, Lang Z, Zhu JK (2018a) Dynamics and function of DNA methylation in plants. Nat Rev Mol Cell Biol 19:489–506

    PubMed  CAS  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 

  • Zhao Y, Zhou DX (2012) Epigenomic modification and epigenetic regulation in rice. J Genet Genomics 39:307–315

    PubMed  CAS  Google Scholar 

  • Zhao J, Zhang J, Zhang W, Wu K, Zheng F, Tian L, Liu X, Duan J (2014) Expression and functional analysis of the plant-specific histone deacetylase HDT701 in rice. Front Plant Sci 5:764

    PubMed  Google Scholar 

  • Zhao L, Wang S, Cao Z, Ouyang W, Zhang Q, Xie L, Zheng R, Guo M, Ma M, Hu Z, Sung WK, Zhang Q, Li G, Li X (2019a) Chromatin loops associated with active genes and heterochromatin shape rice genome architecture for transcriptional regulation. Nat Commun 10:3640

    PubMed  PubMed Central  Google Scholar 

  • Zhao W, Neyt P, Van Lijsebettens M, Shen WH, Berr A (2019b) Interactive and noninteractive roles of histone H2B monoubiquitination and H3K36 methylation in the regulation of active gene transcription and control of plant growth and development. New Phytol 221:1101–1116

    PubMed  CAS  Google Scholar 

  • Zheng B, Chen X (2011) Dynamics of histone H3 lysine 27 trimethylation in plant development. Curr Opin Plant Biol 14:123–129

    PubMed  PubMed Central  CAS  Google Scholar 

  • Zheng X, Chen L, Xia H, Wei H, Lou Q, Li M, Li T, Luo L (2017) Transgenerational epimutations induced by multi-generation drought imposition mediate rice plant's adaptation to drought condition. Sci Rep 7:39843

    PubMed  PubMed Central  CAS  Google Scholar 

  • Zheng D, Wang L, Chen L, Pan X, Lin K, Fang Y, Wang XE, Zhang W (2019) Salt-responsive genes are differentially regulated at the chromatin levels between seedlings and roots in rice. Plant Cell Physiol 60(8):1790–1803

    PubMed  CAS  Google Scholar 

  • Zhong S, Fei Z, Chen YR, Zheng Y, Huang M, Vrebalov J, McQuinn R, Gapper N, Liu B, Xiang J, Shao Y, Giovannoni JJ (2013a) Single-base resolution methylomes of tomato fruit development reveal epigenome modifications associated with ripening. Nat Biotechnol 31:154–159

    PubMed  CAS  Google Scholar 

  • Zhong X, Zhang H, Zhao Y, Sun Q, Hu Y, Peng H, Zhou DX (2013b) The rice NAD(+)-dependent histone deacetylase OsSRT1 targets preferentially to stress- and metabolism-related genes and transposable elements. PLoS ONE 8:e66807

    PubMed  PubMed Central  CAS  Google Scholar 

  • Zhou S, Liu X, Zhou C, Zhou Q, Zhao Y, Li G, Zhou DX (2016) Cooperation between the H3K27me3 chromatin mark and non-CG methylation in epigenetic regulation. Plant Physiol 172:1131–1141

    PubMed  PubMed Central  CAS  Google Scholar 

  • Zhou S, Jiang W, Long F, Cheng S, Yang W, Zhao Y, Zhou DX (2017) Rice homeodomain protein WOX11 recruits a histone acetyltransferase complex to establish programs of cell proliferation of crown root meristem. Plant Cell 29:1088–1104

    PubMed  PubMed Central  CAS  Google Scholar 

  • Zhou C, Wang CS, Liu HB, Zhou QW, Liu Q, Guo Y, Peng T, Song JM, Zhang JW, Chen LL, Zhao Y, Zeng ZX, Zhou DX (2018) Identification and analysis of adenine N-6-methylation sites in the rice genome. Nat Plants 4:554–563

    PubMed  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 JK (2009) Active DNA demethylation mediated by DNA glycosylases. Annu Rev Genet 43:143–166

    PubMed  PubMed Central  CAS  Google Scholar 

  • Zhu B, Zhang W, Zhang T, Liu B, Jiang J (2015) Genome-wide prediction and validation of intergenic enhancers in arabidopsis using open chromatin signatures. Plant Cell 27:2415–2426

    PubMed  PubMed Central  CAS  Google Scholar 

  • Zilberman D, Coleman-Derr D, Ballinger T, Henikoff S (2008) Histone H2A.Z and DNA methylation are mutually antagonistic chromatin marks. Nature 456:125–129

    PubMed  PubMed Central  CAS  Google Scholar 

  • Zong W, Zhong X, You J, Xiong L (2013) Genome-wide profiling of histone H3K4-tri-methylation and gene expression in rice under drought stress. Plant Mol Biol 81:175–188

    PubMed  CAS  Google Scholar 

Download references

Acknowledgements

The work was supported by National Key Research and Development Program of China (No. 2016YFD0100903-3), National Natural Science Foundation of China (No. 31671516, 31730049 and 31970806), and Postdoctoral Science Foundation of China (No. 2019M650182).

Author information

Authors and Affiliations

  1. National Key Laboratory of Crop Genetic Improvement, Huazhong Agricultural University, Wuhan, 430070, China

    Yue Lu, Dao-Xiu Zhou & Yu Zhao

  2. Institute of Plant Science of Paris-Saclay (IPS2), CNRS, INRA, University Paris-Sud, University Paris-Saclay, 91405, Orsay, France

    Dao-Xiu Zhou

Authors
  1. Yue Lu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Dao-Xiu Zhou
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yu Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Yu Zhao conceived the idea. Yue Lu collected all the materials. Yu Zhao and Yue Lu wrote the paper, and Yu Zhao and Dao-Xiu Zhou revised the manuscript.

Corresponding author

Correspondence to Yu Zhao.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Communicated by Qifa Zhang.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lu, Y., Zhou, DX. & Zhao, Y. Understanding epigenomics based on the rice model. Theor Appl Genet 133, 1345–1363 (2020). https://doi.org/10.1007/s00122-019-03518-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00122-019-03518-7

Search

Navigation