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Volume 47 Issue 8
Aug.  2020
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Article Contents

Decoding the plant genome: From epigenome to 3D organization

doi: 10.1016/j.jgg.2020.06.007
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  • The linear genome of eukaryotes is partitioned into diverse chromatin states and packaged into a three-dimensional (3D) structure, which has functional implications in DNA replication, DNA repair, and transcriptional regulation. Over the past decades, research on plant functional genomics and epigenomics has made great progress, with thousands of genes cloned and molecular mechanisms of diverse biological processes elucidated. Recently, 3D genome research has gradually attracted great attention of many plant researchers. Herein, we briefly review the progress in genomic and epigenomic research in plants, with a focus on Arabidopsis and rice, and summarize the currently used technologies and advances in plant 3D genome organization studies. We also discuss the relationships between one-dimensional linear genome sequences, epigenomic states, and the 3D chromatin architecture. This review provides basis for future research on plant 3D genomics.
  • These authors contributed equally.
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  • [1]
    Acemel, R.D., Maeso, I., Gomez-Skarmeta, J.L., 2017. Topologically associated domains: a successful scaffold for the evolution of gene regulation in animals. Wiley Interdiscip. Rev. Dev. Biol. 6.
    [2]
    Avni, R., Nave, M., Barad, O., Baruch, K., Twardziok, S.O., Gundlach, H., Hale, I., Mascher, M., Spannagl, M., Wiebe, K., Jordan, K.W., Golan, G., Deek, J., Ben-Zvi, B., Ben-Zvi, G., Himmelbach, A., Maclachlan, R.P., Sharpe, A.G., Fritz, A., Ben-David, R., Budak, H., Fahima, T., Korol, A., Faris, J.D., Hernandez, A., Mikel, M.A., Levy, A.A., Steffenson, B., Maccaferri, M., Tuberosa R., Cattivelli, L., Faccioli, P., Ceriotti, A., Kashkush, K., Pourkheirandish, M., Komatsuda, T., Eilam, T., Sela, H., Sharon, A., Ohad, N., Chamovitz, D.A., Mayer, K.F.X., Stein, N., Ronen, G., Peleg, Z., Pozniak, C.J., Akhunov, E.D., Distelfeld, A., 2017. Wild emmer genome architecture and diversity elucidate wheat evolution and domestication. Science 357, 93-97.
    [3]
    Baerenfaller, K., Shu, H., Hirsch-hoffmann, M., Futterer, J., Opitz, L., Rehrauer, H., Hennig, L., 2016. Diurnal changes in the histone H3 signature H3K9ac | H3K27ac | H3S28p are associated with diurnal gene expression in Arabidopsis. Plant Cell Environ. 39, 2557-2569.
    [4]
    Beagrie, R.A., Scialdone, A., Schueler, M., Kraemer, D.C.A., Chotalia, M., Xie, S.Q., Barbieri, M., De Santiago, I., Lavitas, L.M., Branco, M.R., Fraser, J., Dostie, J., Game, L., Dillon, N., Edwards, P.A.W., Nicodemi, M., Pombo, A., 2017. Complex multi-enhancer contacts captured by genome architecture mapping. Nature 543, 519-524.
    [5]
    Bell, J.C., Jukam, D., Teran, N.A., Risca, V.I., Smith, O.K., Johnson, W.L., Skotheim, J.M., Greenleaf, W.J., Straight, A.F., 2018. Chromatin-associated RNA sequencing (ChAR-seq) maps genome-wide RNA-to-DNA contacts. Elife 7, e27024.
    [6]
    Bolzer, A., Kreth, G., Solovei, I., Koehler, D., Saracoglu, K., Fauth, C., Muller, S., Eils, R., Cremer, C., Speicher, M.R., Cremer, T., 2005. Three-dimensional maps of all chromosomes in human male fibroblast nuclei and prometaphase rosettes. PLoS Biol. 3, 0826-0842.
    [7]
    Borevitz, J.O., Ecker, J.R., 2004. Plant Genomics: The Third Wave. Annu. Rev. Genomics Hum. Genet. 5, 443-477.
    [8]
    Boyle, A.P., Davis, S., Shulha, H.P., Meltzer, P., Margulies, E.H., Weng, Z., Furey, T.S., Crawford, G.E., 2008. High-resolution mapping and characterization of open chromatin across the genome. Cell 132, 311-322.
    [9]
    Buenrostro, J.D., Giresi, P.G., Zaba, L.C., Chang, H.Y., Greenleaf, W.J., 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.
    [10]
    Byrd, K., Corces, V.G., 2003. Visualization of chromatin domains created by the gypsy insulator of Drosophila. J. Cell Biol. 162, 565-574.
    [11]
    Chalhoub, B., Denoeud, F., Liu, S., Parkin, I.A.P., Tang, H., Wang, Xiyin, Chiquet, J., Belcram, H., Tong, C., Samans, B., Correa, M., Da Silva, C., Just, J., Falentin, C., Koh, C.S., Le Clainche, I., Bernard, M., Bento, P., Noel, B., Labadie, K., Alberti, A., Charles, M., Arnaud, D., Guo, H., Daviaud, C., Alamery, S., Jabbari, K., Zhao, M., Edger, P.P., Chelaifa, H., Tack, D., Lassalle, G., Mestiri, I., Schnel, N., Le Paslier, M.C., Fan, G., Renault, V., Bayer, P.E., Golicz, A.A., Manoli, S., Lee, T.H., Thi, V.H.D., Chalabi, S., Hu Q., Fan, C., Tollenaere, R., Lu, Y., Battail, C., Shen, J., Sidebottom, C.H.D., Wang, Xinfa, Canaguier, A., Chauveau, A., Berard, A., Deniot, G., Guan, M., Liu, Z., Sun, F., Lim, Y.P., Lyons, E., Town, C.D., Bancroft, I., Wang, Xiaowu, Meng, J., Ma, J., Pires, J.C., King, G.J., Brunel, D., Delourme, R., Renard, M., Aury, J.M., Adams, K.L., Batley, J., Snowdon, R.J., Tost, J., Edwards, D., Zhou, Y., Hua, W., Sharpe, A.G., Paterson, A.H., Guan, C., Wincker, P., 2014. Early allopolyploid evolution in the post-neolithic Brassica napus oilseed genome. Science 345, 950-953.
    [12]
    Cokus, Shawn J, Feng, S., Zhang, X., Chen, Z., Merriman, B., Haudenschild, C.D., Pradhan, S., Nelson, S.F., Pellegrini, M., Jacobsen, S.E., 2008. Shotgun bisulphite sequencing of the Arabidopsis genome reveals DNA methylation patterning. Nature 452, 215-219.
    [13]
    Crevillen, P., Sonmez, C., Wu, Z., Dean, C., 2013. A gene loop containing the floral repressor FLC is disrupted in the early phase of vernalization. EMBO J. 32, 140-148.
    [14]
    Dekker, J., Belmont, A.S., Guttman, M., Leshyk, V.O., Lis, J.T., Lomvardas, S., Mirny, L.A., O’Shea, C.C., Park, P.J., Ren, B., Ritland Politz, J.C., Shendure, J., Zhong, S., 2017. The 4D nucleome project. Nature 549, 219-226.
    [15]
    Dekker, J., Rippe, K., Dekker, M., Kleckner, N., 2002. Capturing chromosome conformation. Science 295, 1306-1311.
    [16]
    Deng, P., Liu, S., Nie, X., Weining, S., Wu, L., 2018a. Conservation analysis of long non-coding RNAs in plants. Sci. China Life Sci. 61, 190-198.
    [17]
    Deng, X., Qiu, Q., He, K., Cao, X., 2018b. The seekers: how epigenetic modifying enzymes find their hidden genomic targets in Arabidopsis. Curr. Opin. Plant Biol. 45, 75-81.
    [18]
    Deng, X., Song, X., Wei, L., Liu, C., Cao, X., 2016. Epigenetic regulation and epigenomic landscape in rice. Natl. Sci. Rev. 3, 309-327.
    [19]
    Ding, J., Lu, Q., Ouyang, Y., Mao, H., Zhang, P., Yao, J., Xu, C., Li, X., Xiao, J., Zhang, Q., 2012. A long noncoding RNA regulates photoperiod-sensitive male sterility,an essential component of hybrid rice. Proc. Natl. Acad. Sci. U. S. A. 109, 2654-2659.
    [20]
    Dixon, J.R., Selvaraj, S., Yue, F., Kim, A., Li, Y., Shen, Y., Hu, M., Liu, J.S., Ren, B., 2012. Topological domains in mammalian genomes identified by analysis of chromatin interactions. Nature 485, 376-380.
    [21]
    Dogan, E.S., Liu, C., 2018. Three-dimensional chromatin packing and positioning of plant genomes. Nat. Plants 4, 521-529.
    [22]
    Dong, F., Jiang, J., 1998. Non-Rabl patterns of centromere and telomere distribution in the interphase nuclei of plant cells. Chromosome Res. 6, 551-558.
    [23]
    Dong, P., Tu, X., Chu, P.Y., Lu, P., Zhu, N., Grierson, D., Du, B., Li, P., Zhong, S., 2017. 3D Chromatin architecture of large plant genomes determined by local A/B compartments. Mol. Plant 10, 1497-1509.
    [24]
    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. 62, 201-217.
    [25]
    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.
    [26]
    Dostie, J., Richmond, T.A., Arnaout, R.A., Selzer, R.R., Lee, W.L., Honan, T.A., Rubio, E.D., Krumm, A., Lamb, J., Nusbaum, C., Green, R.D., Dekker, J., 2006. Chromosome conformation capture carbon copy (5C): A massively parallel solution for mapping interactions between genomic elements. Genome Res. 16, 1299-1309.
    [27]
    Du, X., Huang, G., He, S., Yang, Z., Sun, G., Ma, X., Li, N., Zhang, X., Sun, J., Liu, M., Jia, Y., Pan, Z., Gong, W., Liu, Z., Zhu, H., Ma, L., Liu, F., Yang, D., Wang, F., Fan, W., Gong, Q., Peng, Z., Wang, L., Wang, X., Xu, S., Shang, H., Lu, C., Zheng, H., Huang, S., Lin, T., Zhu, Y., Li, F., 2018. Resequencing of 243 diploid cotton accessions based on an updated A genome identifies the genetic basis of key agronomic traits. Nat. Genet. 50, 796-802.
    [28]
    Duan, C.G., Zhu, J.K., Cao, X., 2018. Retrospective and perspective of plant epigenetics in China. J. Genet. Genomics 45, 621-638.
    [29]
    Fan, Y., Yang, J., Mathioni, S.M., Yu, J., Shen, J., Yang, X., Wang, L., Zhang, Q., Cai, Z., Xu, C., Li, X., Xiao, J., Meyers, B.C., Zhang, Q., 2016. PMS1T, producing phased small-interfering RNAs, regulates photoperiod-sensitive male sterility in rice. Proc. Natl. Acad. Sci. U. S. A. 113, 15144-15149.
    [30]
    Fang, R., Yu, M., Li, G., Chee, S., Liu, T., Schmitt, A.D., Ren, B., 2016. Mapping of long-range chromatin interactions by proximity ligation-assisted ChIP-seq. Cell Res. 26, 1345-1348.
    [31]
    Fang, Y., Chen, L., Lin, K., Feng, Y., Zhang, P., Pan, X., Sanders, J., Wu, Y., Wang, X.E., Su, Z., Chen, C., Wei, H., Zhang, W., 2019. Characterization of functional relationships of R-loops with gene transcription and epigenetic modifications in rice. Genome Res. 29, 1287-1297.
    [32]
    Feng, S., Cokus, S.J., Schubert, V., Zhai, J., Pellegrini, M., Jacobsen, S.E., 2014. Genome-wide Hi-C analyses in wild-type and mutants reveal high-resolution chromatin interactions in Arabidopsis. Mol. Cell 55, 694-707.
    [33]
    Feng, S., Cokus, S.J., Zhang, X., Chen, P.Y., Bostick, M., Goll, M.G., Hetzel, J., Jain, J., Strauss, S.H., Halpern, M.E., Ukomadu, C., Sadler, K.C., Pradhan, S., Pellegrini, M., Jacobsen, S.E., 2010. Conservation and divergence of methylation patterning in plants and animals. Proc. Natl. Acad. Sci. U. S. A. 107, 8689-8694.
    [34]
    Feng, S., Jacobsen, S.E., 2011. Epigenetic modifications in plants: an evolutionary perspective. Curr. Opin. Plant Biol. 14, 179-186.
    [35]
    Fransz, P., De Jong, J.H., Lysak, M., Castiglione, M.R., Schubert, I., 2002. Interphase chromosomes in Arabidopsis are organized as well defined chromocenters from which euchromatin loops emanate. Proc. Natl. Acad. Sci. U. S. A. 99, 14584-14589.
    [36]
    Fullwood, M.J., Liu, M.H., Pan, Y.F., Liu, J., Xu, H., Mohamed, Y. Bin, Orlov, Y.L., Velkov, S., Ho, A., Mei, P.H., Chew, E.G.Y., Huang, P.Y.H., Welboren, W.J., Han, Y., Ooi, H.S., Ariyaratne, P.N., Vega, V.B., Luo, Y., Tan, P.Y., Choy, P.Y., Wansa K.D.S.A., Zhao, B., Lim, K.S., Leow, S.C., Yow, J.S., Joseph, R., Li, H., Desai, K. V., Thomsen, J.S., Lee, Y.K., Karuturi, R.K.M., Herve, T., Bourque, G., Stunnenberg, H.G., Ruan, X., Cacheux-Rataboul, V., Sung, W.K., Liu, E.T., Wei, C.L., Cheung, E., Ruan Y., 2009. An oestrogen-receptor-α-bound human chromatin interactome. Nature 462, 58-64.
    [37]
    Giresi, P.G., Kim, J., McDaniell, R.M., Iyer, V.R., Lieb, J.D., 2007. FAIRE (formaldehyde-assisted isolation of regulatory elements) isolates active regulatory elements from human chromatin. Genome Res. 17, 877-885.
    [38]
    Goff, S.A., Ricke, D., Lan, T.H., Presting, G., Wang, R., Dunn, M., Glazebrook, J., Sessions, A., Oeller, P., Varma, H., Hadley, D., Hutchison, D., Martin, C., Katagiri, F., Lange, B.M., Moughamer, T., Xia, Y., Budworth, P., Zhong, J., Miguel, T., Paszkowski, U., Zhang, S., Colbert, M., Sun, W.L., Chen, L., Cooper, B., Park, S., Wood, T.C., Mao, L., Quail, P., Wing, R., Deans, R., Yu, Y., Zharkikh, A., Shen, R., Sahasrabudhe, S., Thomas, A., Cannings, R., Gutin, A., Pruss, D., Reid, J., Tavtigian, S., Mitchell, J., Eldredge, G., Scholl, T., Miller, R.M., Bhatnagar, S., Adey, N., Rubano, T., Tusneem, N., Robinson, R., Feldhaus, J., Macalma, T., Oliphant, A., Briggs, S., 2002. A draft sequence of the rice genome (Oryza sativa L. ssp. japonica). Science 296 (5565), 92–100.
    [39]
    Grob, S., Grossniklaus, U., 2017. Chromosome conformation capture-based studies reveal novel features of plant nuclear architecture. Curr. Opin. Plant Biol. 36, 149-157. https://doi.org/10.1016/j.pbi.2017.03.004
    [40]
    Grob, S., Schmid, M.W., Grossniklaus, U., 2014. Hi-C Analysis in Arabidopsis identifies the KNOT, a structure with similarities to the flamenco locus of Drosophila. Mol. Cell 55, 678-693.
    [41]
    He, Q., Johnston, J., Zeitlinger, J., 2015. ChIP-nexus enables improved detection of in vivo transcription factor binding footprints. Nat. Biotechnol. 33, 395-401.
    [42]
    Heger, P., Marin, B., Bartkuhn, M., Schierenberg, E., Wiehe, T., 2012. The chromatin insulator CTCF and the emergence of metazoan diversity. Proc. Natl. Acad. Sci. U. S. A. 109, 17507-17512.
    [43]
    International Wheat Genome Sequencing Consortium, 2018. Shifting the limits in wheat research and breeding using a fully annotated reference genome. Science 361, eaar7191.
    [44]
    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.
    [45]
    Jiang, Y., Loh, Y.H.E., Rajarajan, P., Hirayama, T., Liao, W., Kassim, B.S., Javidfar, B., Hartley, B.J., Kleofas, L., Park, R.B., Labonte, B., Ho, S.M., Chandrasekaran, S., Do, C., Ramirez, B.R., Peter, C.J., Julia, T.C.W., Safaie, B.M., Morishita, H., Roussos, P., Nestler, E.J., Schaefer, A., Tycko, B., Brennand, K.J., Yagi, T., Shen, L., Akbarian, S., 2017. The methyltransferase SETDB1 regulates a large neuron-specific topological chromatin domain. Nat. Genet. 49, 1239-1250.
    [46]
    Jiao, Y., Wang, Y., Xue, D., Wang, J., Yan, M., Liu, G., Dong, G., Zeng, D., Lu, Z., Zhu, X., Qian, Q., Li, J., 2010. Regulation of OsSPL14 by OsmiR156 defines ideal plant architecture in rice. Nat. Genet. 42, 541-545.
    [47]
    Johnson, D.S., Mortazavi, A., Myers, R.M., Wold, B., 2007. Genome-wide mapping of in vivo protein-DNA interactions. Science 316, 1497-1502.
    [48]
    Kaya-Okur, H.S., Wu, S.J., Codomo, C.A., Pledger, E.S., Bryson, T.D., Henikoff, J.G., Ahmad, K., Henikoff, S., 2019. CUT&Tag for efficient epigenomic profiling of small samples and single cells. Nat. Commun. 10, 1930.
    [49]
    Kim, D.H., Sung, S., 2017. Vernalization-triggered intragenic chromatin loop formation by long noncoding RNAs. Dev. Cell 40, 302-312.e4.
    [50]
    Lai, B., Tang, Q., Jin, W., Hu, G., Wangsa, D., Cui, K., Stanton, B.Z., Ren, G., Ding, Y., Zhao, M., Liu, S., Song, J., Ried, T., Zhao, K., 2018. Trac-looping measures genome structure and chromatin accessibility. Nat. Methods 15, 741-747.
    [51]
    Lane, A.K., Niederhuth, C.E., Ji, L., Schmitz, R.J., 2014. pENCODE: a plant encyclopedia of DNA elements. Annu. Rev. Genet. 48, 49-70.
    [52]
    Li, E., Liu, H., Huang, L., Zhang, X., Dong, X., Song, W., Zhao, H., Lai, J., 2019a. Long-range interactions between proximal and distal regulatory regions in maize. Nat. Commun. 10, 2633.
    [53]
    Li, G., Ruan, X., Auerbach, R.K., Sandhu, K.S., Zheng, M., Wang, P., Poh, H.M., Goh, Y., Lim, J., Zhang, J., Sim, H.S., Peh, S.Q., Mulawadi, F.H., Ong, C.T., Orlov, Y.L., Hong, S., Zhang, Z., Landt, S., Raha, D., Euskirchen, G., Wei, C.L., Ge, W., Wang, H., Davis, C., Fisher-Aylor, K.I., Mortazavi, A., Gerstein, M., Gingeras, T., Wold, B., Sun, Y., Fullwood, M.J., Cheung, E., Liu, E., Sung, W.K., Snyder, M., Ruan, Y., 2012a. Extensive promoter-centered chromatin interactions provide a topological basis for transcription regulation. Cell 148, 84-98.
    [54]
    Li, G., Ruan, Y., Gu, R., Du, S., 2014. Emergence of 3D genomics. Chin. Sci. Bull. 59, 1165-1172.
    [55]
    Li, X., Fu, X.D., 2019b. Chromatin-associated RNAs as facilitators of functional genomic interactions. Nat. Rev. Genet. 20, 503-519.
    [56]
    Li, X., Luo, O.J., Wang, P., Zheng, M., Wang, D., Piecuch, E., Zhu, J.J., Tian, S.Z., 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.
    [57]
    Li, X., Wang, X., He, K., Ma, Y., Su, N., He, H., Stolc, V., Tongprasit, W., Jin, W., Jiang, J., Terzaghi, W., Li, S., Xing, W.D., 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.
    [58]
    Li, X., Zhou, B., Chen, L., Gou, L.T., Li, H., Fu, X.D., 2017b. GRID-seq reveals the global RNA-chromatin interactome. Nat. Biotechnol. 35, 940-950.
    [59]
    Li, X., Zhu, J., Hu, F., Ge, S., Ye, M., Xiang, H., Zhang, G., Zheng, X., Zhang, H., Zhang, S., Li, Q., Luo, R., Yu, C., Yu, J., Sun, J., Zou, X., Cao, X., Xie, X., Wang, J., Wang, W., 2012b. Single-base resolution maps of cultivated and wild rice methylomes and regulatory roles of DNA methylation in plant gene expression. BMC Genomics 13.
    [60]
    Li, Y., Xiao, J., Chen, L., Huang, X., Cheng, Z., Han, B., Zhang, Q., Wu, C., 2018. Rice functional genomics research: past decade and future. Mol. Plant 11, 359-380.
    [61]
    Liang, Z., Shen, L., Cui, X., Bao, S., Geng, Y., Yu, G., Liang, F., Xie, S., Lu, T., Gu, X., Yu, H., 2018. DNA N6-adenine methylation in Arabidopsis thaliana. Dev. Cell 45, 406-416.
    [62]
    Lieberman-Aiden, E., Van Berkum, N.L., Williams, L., Imakaev, M., Ragoczy, T., Telling, A., Amit, I., Lajoie, B.R., Sabo, P.J., Dorschner, M.O., Sandstrom, R., Bernstein, B., Bender, M.A., Groudine, M., Gnirke, A., Stamatoyannopoulos, J., Mirny, L.A., Lander, E.S., Dekker, J., 2009. Comprehensive mapping of long-range interactions reveals folding principles of the human genome. Science 326, 289-293.
    [63]
    Liu, C., Cheng, Y.J., Wang, J.W., Weigel, D., 2017a. Prominent topologically associated domains differentiate global chromatin packing in rice from Arabidopsis. Nat. Plants 3, 742-748.
    [64]
    Liu, C., Wang, C., Wang, G., Becker, C., Zaidem, M., Weigel, D., 2016. Genome-wide analysis of chromatin packing in Arabidopsis thaliana at single-gene resolution. Genome Res. 26, 1057-1068.
    [65]
    Liu, H., Wei, J., Yang, Ting, Mu, W., Song, B., Yang, Tuo, Fu, Y., Wang, X., Hu, G., Li, W., Zhou, H., Chang, Y., Chen, X., Chen, H., Cheng, L., He, X., Cai, H., Cai, X., Wang, M., Li, Y., Sahu, S.K., Yang, J., Wang, Y., Mu, R., Liu, J., Zhao, J., Huang, Z., Xu, X., Liu, X., 2019a. Molecular digitization of a botanical garden: High-depth whole-genome sequencing of 689 vascular plant species from the Ruili Botanical Garden. Gigascience 8, giz007.
    [66]
    Liu, M., Seddon, A.E., Tsai, Z.T., Major, I.T., Floer, M., Howe, G.A., Shiu, S., 2015. Determinants of nucleosome positioning and their influence on plant gene expression. Genome Res. 25, 1182-1195.
    [67]
    Liu, T.T., Zhu, D., Chen, W., Deng, W., He, H., He, G., Bai, B., Qi, Y., Chen, R., Deng, X.W., 2013. A global identification and analysis of small nucleolar RNAs and possible intermediate-sized non-coding RNAs in Oryza sativa. Mol. Plant 6, 830-846.
    [68]
    Liu, X., Zhang, Y., Chen, Y., Li, M., Zhou, F., Li, K., Cao, H., Ni, M., Liu, Y., Gu, Z., Dickerson, K.E., Xie, S., Hon, G.C., Xuan, Z., Zhang, M.Q., Shao, Z., Xu, J., 2017b. In situ capture of chromatin interactions by biotinylated dCas9. Cell 170, 1028-1043.e19.
    [69]
    Liu, Y., Liu, K., Yin, L., Yu, Y., Qi, J., Shen, W.H., Zhu, J., Zhang, Y., 2019b. H3K4me2 functions as a repressive epigenetic mark in plants. Epigenet. Chromatin 12.
    [70]
    Louwers, M., Bader, R., Haring, M., Van Driel, R., De Laat, W., Stam, M., 2009. Tissue- and expression level-specific chromatin looping at maize b1 epialleles. Plant Cell 21, 832-842.
    [71]
    Lu, Y., Xu, Q., Liu, Y., Yu, Y., Cheng, Z.Y., Zhao, Y., Zhou, D.X., 2018. Dynamics and functional interplay of histone lysine butyrylation, crotonylation, and acetylation in rice under starvation and submergence. Genome Biol. 19.
    [72]
    Lu, P., Yu, S., Zhu, N., Chen, Y.R., Zhou, B., Pan, Y., Tzeng, D., Fabi, J.P., Argyris, J., Garcia-Mas, J., Ye, N., Zhang, J., Grierson, D., Xiang, J., Fei, Z., Giovannoni, J., Zhong, S., 2018. Genome encode analyses reveal the basis of convergent evolution of fleshy fruit ripening. Nat. Plants 4, 784-791.
    [73]
    Lu, Z., Hofmeister, B.T., Vollmers, C., DuBois, R.M., Schmitz, R.J., 2017. Combining ATAC-seq with nuclei sorting for discovery of cis-regulatory regions in plant genomes. Nucleic Acids Res. 45, e41.
    [74]
    Lupianez, D.G., Kraft, K., Heinrich, V., Krawitz, P., Brancati, F., Klopocki, E., Horn, D., Kayserili, H., Opitz, J.M., Laxova, R., Santos-Simarro, F., Gilbert-Dussardier, B., Wittler, L., Borschiwer, M., Haas, S.A., Osterwalder, M., Franke, M., Timmermann, B., Hecht, J., Spielmann, M., Visel, A., Mundlos, S., 2015. Disruptions of topological chromatin domains cause pathogenic rewiring of gene-enhancer interactions. Cell 161, 1012-1025.
    [75]
    Maher, K.A., Bajic, M., Kajala, K., Reynoso, M., Pauluzzi, G., West, D.A., Zumstein, K., Woodhouse, M., Bubb, K., Dorrity, M.W., Queitsch, C., Bailey-Serres, J., Sinha, N., Brady, S.M., Deal, R.B., 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.
    [76]
    Malapeira, J., Khaitova, L.C., Mas, P., 2012. Ordered changes in histone modifications at the core of the Arabidopsis circadian clock. Proc. Natl. Acad. Sci. U. S. A. 109, 21540-21545.
    [77]
    Mascher, M., Gundlach, H., Himmelbach, A., Beier, S., Twardziok, S.O., Wicker, T., Radchuk, V., Dockter, C., Hedley, P.E., Russell, J., Bayer, M., Ramsay, L., Liu, H., Haberer, G., Zhang, X.Q., Zhang, Q., Barrero, R.A., Li, L., Taudien, S., Groth, M., Felder, M., Hastie, A., Simkova, H., Stankova, H., Vrana, J., Chan, S., Munoz-Amatriain, M., Ounit, R., Wanamaker, S., Bolser, D., Colmsee, C., Schmutzer, T., Aliyeva-Schnorr, L., Grasso, S., Tanskanen, J., Chailyan, A., Sampath, D., Heavens, D., Clissold, L., Cao, S., Chapman, B., Dai, F., Han, Y., Li, H., Li, X., Lin, C., McCooke, J.K., Tan, C., Wang, P., Wang, S., Yin, S., Zhou, G., Poland, J.A., Bellgard, M.I., Borisjuk, L., Houben, A., Doleael, J., Ayling, S., Lonardi, S., Kersey, P., Langridge, P., Muehlbauer, G.J., Clark, M.D., Caccamo, M., Schulman, A.H., Mayer, K.F.X., Platzer, M., Close, T.J., Scholz, U., Hansson, M., Zhang, G., Braumann, I., Spannagl, M., Li, C., Waugh, R., Stein, N., 2017. A chromosome conformation capture ordered sequence of the barley genome. Nature 544, 427-433.
    [78]
    Miura, K., Ikeda, M., Matsubara, A., Song, X., Ito, M., Asano, K., Matsuoka, M., 2010. OsSPL14 promotes panicle branching and higher grain productivity in rice. Nat. Genet. 42, 545-549.
    [79]
    Mumbach, M.R., Rubin, A.J., Flynn, R.A., Dai, C., Khavari, P.A., Greenleaf, W.J., Chang, H.Y., 2016. HiChIP: Efficient and sensitive analysis of protein-directed genome architecture. Nat. Methods 13, 919-922.
    [80]
    Nora, E.P., Lajoie, B.R., Schulz, E.G., Giorgetti, L., Okamoto, I., Servant, N., Piolot, T., Van Berkum, N.L., Meisig, J., Sedat, J., Gribnau, J., Barillot, E., Bluthgen, N., Dekker, J., Heard, E., 2012. Spatial partitioning of the regulatory landscape of the X-inactivation centre. Nature 485, 381-385.
    [81]
    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.
    [82]
    Prieto, P., Santos, A.P., Moore, G., Shaw, P., 2004. Chromosomes associate premeiotically and in xylem vessel cells via their telomeres and centromeres in diploid rice (Oryza sativa). Chromosoma 112, 300-307.
    [83]
    Quinodoz, S.A., Ollikainen, N., Tabak, B., Palla, A., Schmidt, J.M., Detmar, E., Lai, M.M., Shishkin, A.A., Bhat, P., Takei, Y., Trinh, V., Aznauryan, E., Russell, P., Cheng, C., Jovanovic, M., Chow, A., Cai, L., McDonel, P., Garber, M., Guttman, M., 2018. Higher-order inter-chromosomal hubs shape 3D genome organization in the nucleus. Cell 174, 744-757.e24.
    [84]
    Rao, S.S.P., Huntley, M.H., Durand, N.C., Stamenova, E.K., Bochkov, I.D., Robinson, J.T., Sanborn, A.L., Machol, I., Omer, A.D., Lander, E.S., Aiden, E.L., 2014. A 3D map of the human genome at kilobase resolution reveals principles of chromatin looping. Cell 159, 1665-1680.
    [85]
    Rhee, H.S., Pugh, B.F., 2011. Comprehensive genome-wide protein-DNA interactions detected at single-nucleotide resolution. Cell 147, 1408-1419.
    [86]
    Ricci, W.A., Lu, Z., Ji, L., Marand, A.P., Ethridge, C.L., Murphy, N.G., Noshay, J.M., Galli, M., Mejia-Guerra, M.K., Colome-Tatche, M., Johannes, F., Rowley, M.J., Corces, V.G., Zhai, J., Scanlon, M.J., Buckler, E.S., Gallavotti, A., Springer, N.M., Schmitz, R.J., Zhang, X., 2019. Widespread long-range cis-regulatory elements in the maize genome. Nat. Plants 5,1237-1249.
    [87]
    Risca, V.I., Greenleaf, W.J., 2015. Unraveling the 3D genome: genomics tools for multiscale exploration. Trends Genet. 31, 357-372.
    [88]
    Rodriguez-Granados, N.Y., Ramirez-Prado, J.S., Veluchamy, A., Latrasse, D., Raynaud, C., Crespi, M., Ariel, F., Benhamed, M., 2016. Put your 3D glasses on: Plant chromatin is on show. J. Exp. Bot. 67, 3205-3221.
    [89]
    Rowley, M.J., Nichols, M.H., Lyu, X., Ando-Kuri, M., Rivera, I.S.M., Hermetz, K., Wang, P., Ruan, Y., Corces, V.G., 2017. Evolutionarily conserved principles predict 3D chromatin organization. Mol. Cell 67, 837-852.e7.
    [90]
    Schmidl, C., Rendeiro, A.F., Sheffield, N.C., Bock, C., 2015. ChIPmentation: fast, robust, low-input ChIP-seq for histones and transcription factors. Nat. Methods 12, 963-965.
    [91]
    Schnable, P.S., Ware, D., Fulton, R.S., Stein, J.C., Wei, F., Pasternak, S., Liang, C., Zhang, J., Fulton, L., Graves, T.A., Minx, P., Reily, A.D., Courtney, L., Kruchowski, S.S., Tomlinson, C., Strong, C., Delehaunty, K., Fronick, C., Courtney, B., Rock, S.M., Belter, E., Du, F., Kim, K., Abbott, R.M., Cotton, M., Levy, A., Marchetto, P., Ochoa, K., Jackson, S.M., Gillam, B., Chen, W., Yan, L., Higginbotham, J., Cardenas, M., Waligorski, J., Applebaum, E., Phelps, L., Falcone, J., Kanchi, K., Thane, T., Scimone A., Thane, N., Henke, J., Wang, T., Ruppert, J., Shah, N., Rotter, K., Hodges, J., Ingenthron, E., Cordes, M., Kohlberg, S., Sgro, J., Delgado, B., Mead, K., Chinwalla, A., Leonard, S., Crouse, K., Collura, K., Kudrna, D., Currie, J., He, R., Angelova, A., Rajasekar, S., Mueller, T., Lomeli, R., Scara, G., Ko, A., Delaney, K., Wissotski, M., Lopez, G., Campos, D., Braidotti, M., Ashley, E., Golser W., Kim, H., Lee, S., Lin, J., Dujmic, Z., Kim, W., Talag, J., Zuccolo, A., Fan, C., Sebastian, A., Kramer, M., Spiegel, L., Nascimento, L., Zutavern, T., Miller, B., Ambroise, C., Muller, S., Spooner, W., Narechania, A., Ren, L., Wei, S., Kumari, S., Faga B., Levy, M.J., McMahan, L., Van Buren, P., Vaughn, M.W., Ying, K., Yeh, C.T., Emrich, S.J., Jia, Y., Kalyanaraman, A., Hsia, A.P., Barbazuk, W.B., Baucom, R.S., Brutnell, T.P., Carpita, N.C., Chaparro, C., Chia, J.M., Deragon, J.M., Estill, J.C., Fu, Y., Jeddeloh, J.A., Han, Y., Lee, H., Li, P., Lisch, D.R., Liu, S., Liu, Z., Nagel, D.H., McCann, M.C., Sanmiguel, P., Myers, A.M., Nettleton, D., Nguyen, J., Penning, B.W., Ponnala, L., Schneider, K.L., Schwartz, D.C., Sharma, A., Soderlund, C., Springer, N.M., Sun, Q., Wang, H., Waterman, M., Westerman, R., Wolfgruber, T.K., Yang, L., Yu, Y., Zhang, L., Zhou, S., Zhu, Q., Bennetzen, J.L., Dawe, R.K., Jiang, J., Jiang, N., Presting, G.G., Wessler, S.R., Aluru, S., Martienssen, R.A., Clifton, S.W., McCombie, W.R., Wing, R.A., Wilson, R.K., 2009. The B73 maize genome: complexity, diversity, and dynamics. Science 326, 1112-1115.
    [92]
    Schones, D.E., Cui, K., Cuddapah, S., Roh, T.Y., Barski, A., Wang, Z., Wei, G., Zhao, K., 2008. Dynamic regulation of nucleosome positioning in the human genome. Cell 132, 887-898.
    [93]
    Sexton, T., Yaffe, E., Kenigsberg, E., Bantignies, F., Leblanc, B., Hoichman, M., Parrinello, H., Tanay, A., Cavalli, G., 2012. Three-dimensional folding and functional organization principles of the Drosophila genome. Cell 148, 458-472.
    [94]
    Simonis, M., Klous, P., Splinter, E., Moshkin, Y., Willemsen, R., De Wit, E., Van Steensel, B., De Laat, W., 2006. Nuclear organization of active and inactive chromatin domains uncovered by chromosome conformation capture-on-chip (4C). Nat. Genet. 38, 1348-1354.
    [95]
    Skene, P.J., Henikoff, J.G., Henikoff, S., 2018. Targeted in situ genome-wide profiling with high efficiency for low cell numbers. Nat. Protoc. 13, 1006-1019.
    [96]
    Somerville, C., Somerville, S., 1999. Plant functional genomics. Science 285, 380-383.
    [97]
    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.
    [98]
    Spielmann, M., Lupianez, D.G., Mundlos, S., 2018. Structural variation in the 3D genome. Nat. Rev. Genet. 19, 453-467.
    [99]
    Sridhar, B., Rivas-Astroza, M., Nguyen, T.C., Chen, W., Yan, Z., Cao, X., Hebert, L., Zhong, S., 2017. Systematic mapping of RNA-chromatin interactions in vivo. Curr. Biol. 27, 602-609.
    [100]
    Stam, M., Tark-Dame, M., Fransz, P., 2019. 3D genome organization: a role for phase separation and loop extrusion? Curr. Opin. Plant Biol. 48, 36-46.
    [101]
    Sun, Q., Csorba, T., Skourti-Stathaki, K., Proudfoot, N.J., Dean, C., 2013. R-loop stabilization represses antisense transcription at the Arabidopsis FLC locus. Science 340, 619-621.
    [102]
    Tamim, S., Cai, Z., Mathioni, S.M., Zhai, J., Teng, C., Zhang, Q., Meyers, B.C., 2018. Cis-directed cleavage and nonstoichiometric abundances of 21-nucleotide reproductive phased small interfering RNAs in grasses. New Phytol. 220, 865-877.
    [103]
    Tang, Z., Luo, O.J., Li, X., Zheng, M., Zhu, J.J., Szalaj, P., Trzaskoma, P., Magalska, A., Wlodarczyk, J., Ruszczycki, B., Michalski, P., Piecuch, E., Wang, P., Wang, D., Tian, S.Z., Penrad-Mobayed, M., Sachs, L.M., Ruan, X., Wei, C.L., Liu, E.T., Wilczynski, G.M., Plewczynski, D., Li, G., Ruan, Y., 2015. CTCF-mediated human 3D genome architecture reveals chromatin topology for transcription. Cell 163, 1611-1627.
    [104]
    Tao, J., Zhou, J., Xie, T., Wang, X., Yang, Q., Zhang, H., 2017. Influence of chromatin 3D organization on structural variations of the Arabidopsis thaliana Genome. Mol. Plant 10, 340-344.
    [105]
    The Arabidopsis Genome Initiative, 2000. Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408, 796-815.
    [106]
    The ENCODE Corsortium, 2012. An integrated encyclopedia of DNA elements in the human genome. Nature 489, 57-74.
    [107]
    Travers, A., Muskhelishvili, G., 2015. DNA structure and function. FEBS J. 282, 2279-2295.
    [108]
    Tsompana, M., Buck, M.J., 2014. Chromatin accessibility: a window into the genome. Epigenet. Chromatin 7.
    [109]
    van Dijk, K., Ding, Y., Malkaram, S., Riethoven, J.J.M., Liu, R., Yang, J., Laczko, P., Chen, H., Xia, Y., Ladunga, I., Avramova, Z., Fromm, M., 2010. Dynamic changes in genome-wide histone H3 lysine 4 methylation patterns in response to dehydration stress in Arabidopsis thaliana. BMC Plant Biol. 10, 1-12.
    [110]
    Wang, C., Liu, C., Roqueiro, D., Grimm, D., Schwab, R., Becker, C., Lanz, C., Weigel, D., 2015a. Genome-wide analysis of local chromatin packing in Arabidopsis thaliana. Genome Res. 25, 246-256.
    [111]
    Wang, J., Qi, Y., 2018. Plant non-coding RNAs and epigenetics. Sci. China Life Sci. 61, 135-137.
    [112]
    Wang, J., Yao, W., Zhu, D., Xie, W., Zhang, Q., 2015b. Genetic basis of sRNA quantitative variation analyzed using an experimental population derived from an elite rice hybrid. Elife 4, e04250.
    [113]
    Wang, L., Sun, S., Jin, J., Fu, D., Yang, X., Weng, X., Xu, C., Li, X., Xiao, J., 2015c. Coordinated regulation of vegetative and reproductive branching in rice. Proc. Natl. Acad. Sci. U. S. A. 112, 15504-15509.
    [114]
    Wang, M., Tu, L., Lin, M., Lin, Z., Wang, P., Yang, Q., Ye, Z., Shen, C., Li, J., Zhang, L., Zhou, X., Nie, X., Li, Z., Guo, K., Ma, Y., Huang, C., Jin, S., Zhu, L., Yang, X., Min, L., Yuan, D., Zhang, Q., Lindsey, K., Zhang, X., 2017. Asymmetric subgenome selection and cis-regulatory divergence during cotton domestication. Nat. Genet. 49, 579-587.
    [115]
    Wang, M., Tu, L., Yuan, D., Zhu, D., Shen, C., Li, J., Liu, F., Pei, L., Wang, P., Zhao, G., Ye, Z., Huang, H., Yan, F., Ma, Y., Zhang, L., Liu, M., You, J., Yang, Y., Liu, Z., Huang, F., Li, B., Qiu, P., Zhang, Q., Zhu, L., Jin, S., Yang, X., Min, L., Li, G., Chen, L.L., Zheng, H., Lindsey, K., Lin, Z., Udall, J.A., Zhang, X., 2019a. Reference genome sequences of two cultivated allotetraploid cottons, Gossypium hirsutum and Gossypium barbadense. Nat. Genet. 51, 224-229.
    [116]
    Wang, M., Wang, P., Lin, M., Ye, Z., Li, G., Tu, L., Shen, C., Li, J., Yang, Q., Zhang, X., 2018a. Evolutionary dynamics of 3D genome architecture following polyploidization in cotton. Nat. Plants 4, 90-97.
    [117]
    Wang, Q., Sun, Q., Czajkowsky, D.M., Shao, Z., 2018b. Sub-kb Hi-C in D. melanogaster reveals conserved characteristics of TADs between insect and mammalian cells. Nat. Commun. 9, 188.
    [118]
    Wang, Q., Xiong, H., Ai, S., Yu, X., Liu, Y., Zhang, J., He, A., 2019b. CoBATCH for high-throughput single-cell epigenomic profiling. Mol. Cell 76, 206-216.e7.
    [119]
    Wang, Y., Wang, X., Deng, W., Fan, X., Liu, T.T., He, G., Chen, R., Terzaghi, W., Zhu, D., Wang Deng, X., 2014. Genomic features and regulatory roles of intermediate-sized non-coding RNAs in Arabidopsis. Mol. Plant 7, 514-527.
    [120]
    Wing, R.A., Purugganan, M.D., Zhang, Q., 2018. The rice genome revolution: from an ancient grain to green super rice. Nat. Rev. Genet. 19, 505-517.
    [121]
    Xiao, J., Lee, U.S., Wagner, D., 2016. Tug of war: adding and removing histone lysine methylation in Arabidopsis. Curr. Opin. Plant Biol. 34, 41-53.
    [122]
    Xiao, J., Wu, C., Yuan, M., Wang, N., Fan, Y., Yang, M., Ouyang, Y., Ruan, Y., Zhang, Q., 2015. The progress and perspective of rice functional genomics research in China. Chinese Sci. Bull. 60, 1711-1722.
    [123]
    Xie, T., Zhang, F.G., Zhang, H.Y., Wang, X.T., Hu, J.H., Wu, X.M., 2019. Biased gene retention during diploidization in Brassica linked to three-dimensional genome organization. Nat. Plants 5, 822-832.
    [124]
    Xie, T., Zheng, J.F., Liu, S., Peng, C., Zhou, Y.M., Yang, Q.Y., Zhang, H.Y., 2015. De novo plant genome assembly based on chromatin interactions: A case study of Arabidopsis thaliana. Mol. Plant 8, 489-492.
    [125]
    Xu, W., Xu, H., Li, K., Fan, Y., Liu, Y., Yang, X., Sun, Q., 2017. The R-loop is a common chromatin feature of the Arabidopsis genome. Nat. Plants 3, 704-714.
    [126]
    Yao, W., Li, G., Yu, Y., Ouyang, Y., 2018. funRiceGenes dataset for comprehensive understanding and application of rice functional genes. Gigascience 7, 1-9.
    [127]
    Yu, J., Hu, S., Wang, J., Wong, G.K.S., Li, S., Liu, B., Deng, Y., Dai, L., Zhou, Y., Zhang, X., Cao, M., Liu, J., Sun, J., Tang, J., Chen, Y., Huang, X., Lin, W., Ye, C., Tong, W., Cong, L., Geng, J., Han, Y., Li, L., Li, W., Hu, G., Li, J., Liu, Z., Qi, Q., Li, T., Wang, X., Lu, H., Wu, T., Zhu, M., Ni, P., Han, H., Dong, W., Ren, X., Feng, X., Cui, P., Li, X., Wang, H., Xu, X., Zhai, W., Xu, Z., Zhang, J., He, S., Xu, J., Zhang, K., Zheng, X., Dong, J., Zeng, W., Tao, L., Ye, J., Tan, J., Chen, X., He, J., Liu, D., Tian, W., Tian, C., Xia, H., Bao, Q., Li, G., Gao, H., Cao, T., Zhao, W., Li, P., Chen, W., Zhang, Y., Hu, J., Liu, S., Yang, J., Zhang, G., Xiong, Y., Li, Z., Mao, L., Zhou, C., Zhu, Z., Chen, R., Hao, B., Zheng, W., Chen, S., Guo, W., Tao, M., Zhu, L., Yuan, L., Yang, H., 2002. A draft sequence of the rice genome (Oryza sativa L. ssp. indica). Science 296, 79-92.
    [128]
    Yu, Y., Zhang, Y., Chen, X., Chen, Y., 2019. Plant noncoding RNAs: hidden players in development and stress responses. Annu. Rev. Cell Dev. Biol. 35, 407-431.
    [129]
    Zhang, H., Lang, Z., Zhu, J., 2018. Dynamics and function of DNA methylation in plants. Nat. Rev. Mol. Cell Biol. 19, 489-506.
    [130]
    Zhang, J., Chen, L.L., Xing, F., Kudrna, D.A., Yao, W., Copetti, D., Mu, T., Li, W., Song, J.M., Xie, W., Lee, S., Talag, J., Shao, L., An, Y., Zhang, C.L., Ouyang, Y., Sun, S., Jiao, W.B., Lv, F., Du, B., Luo, M., Maldonado, C.E., Goicoechea, J.L., Xiong, L., Wu, C., Xing, Y., Zhou, D.X., Yu, S., Zhao, Y., Wang, G., Yu, Y., Luo, Y., Zhou, Z.W., Hurtado, B.E.P., Danowitz, A., Wing, R.A., Zhang, Q., 2016. Extensive sequence divergence between the reference genomes of two elite indica rice varieties Zhenshan 97 and Minghui 63. Proc. Natl. Acad. Sci. U. S. A. 113, E5163-E5171.
    [131]
    Zhang, Q., Li, J., Xue, Y., Han, B., Deng, X.W., 2008. Rice 2020: A call for an international coordinated effort in rice functional genomics. Mol. Plant 1, 715-719.
    [132]
    Zhang, Q., Wing, R., 2013. Genome studies and molecular genetics: understanding the functional genome based on the rice model. Curr. Opin. Plant Biol. 16, 129-132.
    [133]
    Zhang, T., Zhang, W., Jiang, J., 2015. Genome-wide nucleosome occupancy and positioning and their impact on gene expression and evolution in plants. Plant Physiol. 168, 1406-1416.
    [134]
    Zhang, W., Wu, Y., Schnable, J.C., Zeng, Z., Freeling, M., Crawford, G.E., Jiang, J., 2012a. High-resolution mapping of open chromatin in the rice genome. Genome Res. 22, 151-162.
    [135]
    Zhang, W., Zhang, T., Wu, Y., Jiang, J., 2012b. Genome-wide identification of regulatory DNA elements and protein-binding footprints using signatures of open chromatin in Arabidopsis. Plant Cell 24, 2719-2731.
    [136]
    Zhang, X., Bernatavichute, Y. V., Cokus, S., Pellegrini, M., Jacobsen, S.E., 2009. Genome-wide analysis of mono-, di- and trimethylation of histone H3 lysine 4 in Arabidopsis thaliana. Genome Biol. 10, 1-14.
    [137]
    Zhao, L., Wang, S., Cao, Z., Ouyang, W., Zhang, Qing, Xie, L., Zheng, R., Guo, M., Ma, M., Hu, Z., Sung, W.K., Zhang, Q., Li, G., Li, X., 2019. Chromatin loops associated with active genes and heterochromatin shape rice genome architecture for transcriptional regulation. Nat. Commun. 10, 3640.
    [138]
    Zhao, Y., Zhou, D.X., 2012. Epigenomic modification and epigenetic regulation in rice. J. Genet. Genomics. 39, 307-315.
    [139]
    Zhao, Z., Tavoosidana, G., Sjolinder, M., Gondor, A., Mariano, P., Wang, S., Kanduri, C., Lezcano, M., Sandhu, K.S., Singh, U., Pant, V., Tiwari, V., Kurukuti, S., Ohlsson, R., 2006. Circular chromosome conformation capture (4C) uncovers extensive networks of epigenetically regulated intra- and interchromosomal interactions. Nat. Genet. 38, 1341-1347.
    [140]
    Zheng, M., Tian, S.Z., Capurso, D., Kim, M., Maurya, R., Lee, B., Piecuch, E., Gong, L., Zhu, J.J., Li, Z., Wong, C.H., Ngan, C.Y., Wang, P., Ruan, X., Wei, C.L., Ruan, Y., 2019. Multiplex chromatin interactions with single-molecule precision. Nature 566, 558-562.
    [141]
    Zhou, C., Wang, C., Liu, H., Zhou, Q., Liu, Q., Guo, Y., Peng, T., Song, J., Zhang, J., Chen, L., Zhao, Y., Zeng, Z., Zhou, D.X., 2018. Identification and analysis of adenine N6-methylation sites in the rice genome. Nat. Plants. 4, 554-563.
    [142]
    Zhou, H., Liu, Q., Li, J., Jiang, D., Zhou, L., Wu, P., Lu, S., Li, F., Zhu, L., Liu, Z., Chen, L., Liu, Y.G., Zhuang, C., 2012. Photoperiod- and thermo-sensitive genic male sterility in rice are caused by a point mutation in a novel noncoding RNA that produces a small RNA. Cell Res. 22, 649-660.
    [143]
    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.
    [144]
    Zhu, Y., Chen, Z., Zhang, K., Wang, M., Medovoy, D., Whitaker, J.W., Ding, B., Li, N., Zheng, L., Wang, W., 2016. Constructing 3D interaction maps from 1D epigenomes. Nat. Commun. 7, 10812.
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