Plant Epigenetics: Mechanisms and Applications

Document Type : Original Article

Authors

1 PhD Student in Biotechnology and Molecular Genetics of Horticulture Plants, Agriculture Sciences and Natural Resources Faculty, Mohaghegh Aradabili University, Ardabil, Iran

2 Associate Professor, Biotechnology Department, Faculty of Life Science and Biotechnology, Shahid Beheshti University, Iran.

3 Assistant Professor, Agriculture Department, Engineering and Technical Faculty, Velayat University, Iranshahr, Iran.

Abstract

Plant epigenetic has become one of the key research topics not only as the subject of basic research, but also as a new source of useful traits for plant breeding. Epigenetic regulation is necessary for the production of differentiated cells throughout plant development, as well as maintaining the stability and integrity of the gene expression profiles. Although epigenetic processes are essential for natural growth, they can become misdirected led to abnormal phenotypes and diseases. Epigenetics is the study of heritable phenotype changes that do not involve alterations in the DNA sequence. The microstructure (not code) of DNA itself or the associated chromatin proteins may be modified, causing activation or silencing. This mechanism enables differentiated cells in a multicellular organism to express only the genes which are necessary for their own activity. In this review, our goal is to introduce epigenetics and its different applications in plants, especially in production of transgenic plants, plants tolerate to biotic and abiotic stresses and understanding the mechanisms of gene silencing. Also, in this review, we have referred to the role of transposons in epigenetic, epigenetic engineering methods, epigenetic fingerprinting and ultimately methods for epigenetic data analysis and related databases.

Keywords

References

Abobatta, W. F. (2018). Epigenetics in the Agricultural Sector. Annals of Reviews Research, 2(5):1-4.
Aceituno, F. F., Nick, M., Seung, Y. R., & Rodrigo, A. G. (2008). The rules of gene expression in plants: organ identity and gene body methylation are key factors for regulation of gene expression in Arabidopsis thaliana. BMC Genomics, 9:438–451.
Al-Lawati, A. Al-Bahry, S., Victor, R., Al-Lawati, AH., Yaish, MW. (2016) Salt stress alters DNA methylation levels in alfalfa (Medicago spp). Genetics and Molecular Research: GMR, 15:15018299.
Allis, C. D., Caparros, M.L., Jenuwein, T. & Reinberg, D. (2014). Epigenetic Regulation in Plant Responses to the Environment. Cold Spring Harbor Perspectives in Biology, 6:a019471.
Alonso, C., Perez, R., Bazaga, P., Medrano, M., & Herrera, C. M. (2014). Individual variation in size and fecundity is correlated with differences in global DNA cytosine methylation in the perennial herb Helleborusfoetidus (Ranunculaceae). American Journal of Botany, 101, 1309–1313.
Álvarez-Venegas, R., & De-la-Peña, C. (2016) Editorial: Recent Advances of Epigenetics in Crop Biotechnology. Frontiers in Plant Science, 7:413.
Angarica, V.E., & Del Sol, A. (2017). Bioinformatics Tools for Genome-Wide Epigenetic Research. Springer International Publishing, 489-512.
Barraza-Villarreal, A., Sunyer, J., Hernandez-Cadena, L., Escamilla-Nuñez, M.C., Sienra-Monge, J.J., Ramírez-Aguilar, M., Cortez-Lugo, M., Holguin, F., Diaz-Sánchez, D., Carin Olin, A., & Romieu, I. (2008). Air Pollution, Airway Inflammation, and Lung Function in a Cohort Study of Mexico City Schoolchildren. Environmental Health Perspectives, 116(6):832.838.
Barski, A., Cuddapah, S., Cui, K., Roh, TY., Schones, DE., Wang, Z., Wei, G., Chepelev, I., & Zhao, K. (2007). High-resolution profiling of histone methylations in the human genome, Cell, 129(4):823–37.
Bartke, T., Borgel, J., & DiMaggio, PA. (2013). Proteomics in epigenetics: new perspectives for cancer research. Brief Funct Genomics, 12(3):205–18.
Bernstein, B. E., Stamatoyannopoulos, J. A., Costello, J. F., Ren, B., Milosavljevic, A., Meissner, A., Kellis, M., Marra, M. A., Beaudet, A. L., Ecker, J. R., Farnham, P. J., Hirst, M., Lander, ES., Mikkelsen, T. S., & Thomson, J. A. (2010). The NIH Roadmap Epigenomics Mapping Consortium. Nature Biotechnology, 28(10):1045–8.
Bibikova, M., Barnes, B., Tsan, C., Ho, V., Klotzle, B., Le, J. M., Delano, D., Zhang, L., Schroth, G. P., Gunderson, K. L., Fan, J. B., & Shen, R. (2011). High density DNA methylation array with single CpG site resolution. Genomics, 98(4):288–95.
Bocchini, M., Bartucca, M. L., Ciancaleoni, S., Mimmo, T., Cesco, S., Pii, Y., Albertini, E., & Del Buono, D. (2015). Iron deficiency in barley plants: Phytosiderophore release, iron translocation, and DNA methylation. Frontiers in Plant Science, 6:514.
Booth, MJ., Branco, M. R., Ficz, G., Oxley, D., Krueger, F., Reik, W., & Balasubramanian, S. (2012). Quantitative sequencing of 5-methylcytosine and 5-hydroxymethylcytosine at single-base resolution. Science. 336(6083):934–7.
Boyko, A., & Kovalchuk, I. (2011). Genetic and epigenetic effects of plant–pathogen interactions: an evolutionary perspective. Molecular Plant, 4:1014–1023.
Brautigam, K., Vining, K. J., Lafon-Placette, C., Fossdal, C. G., Mirouze, M., Marcos, J. G., Fluch, S., Fraga, MF., Guevara, M. A., Abarca, D., Johnsen, O., Maury, S., Strauss, S. H., Campbell, M. M., Rohde, A., Dıaz-Sala, C., & Cervera, MT. (2013) Epigenetic regulation of adaptive responses of forest tree species to the environment. Ecology and Evolution, 3(2):399–415.
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. Nature Methods, 10(12):1213–8.
Cech, T. R. & Steitz, J. A. (2014). The noncoding RNA revolution trashing old rules to forge new ones. Cell, 157:77–94.
Consortium, E. P. (2012). An integrated encyclopedia of DNA elements in the human genome. Nature. 489(7414):57–74.
Cortijo, S., Wardenaar, R., Colomé-Tatché, M., Gilly, A., Etcheverry, M., Labadie, K., Caillieux, E., Hospital, F., Aury, JM., Wincker, P., Roudier, F., Jansen, R. C., Colot, V., & Johannes, F. (2014). Mapping the epigenetic basis of complex traits. Science, 343:1145–1148.
Dai, L. F., Chen, Y. L., Luo, X. D., Wen, X. F., Cui, F. L., Zhang, F. T., Zhou, Y., & Xie, J. K. (2015) Level and pattern of DNA methylation changes in rice cold tolerance introgression lines derived from Oryza rufipogon Griff. Euphytica, 205:73–83.
Day, J. J. (2014). New approaches to manipulating the epigenome. Dialogues in Clinical Neuroscience, 16(3):345-357.
De-la-Pena, C., Nic-Can, G., Ojeda, G., Herrera-Herrera, J., Lopez-Torres, A., Wrobel, K., & Robert-Diaz, M. (2012) KNOX1 is expressed and epigenetically regulated during in vitro conditions in Agave spp. BMC Plant Biology, 12(1):203.
De-La-Peña, C., Rangel-Cano, A., & Alvarez-Venegas, R. (2012). Regulation of disease-responsive genes mediated by epigenetic factors: interaction of Arabidopsis-Pseudomonas. Molecular Plant Pathology, 13(4):388-98.
Ding, B., & Wang, G. L. (2015). Chromatin versus pathogens: the function of epigenetics in plant immunity. Frontiers in Plant Science, 6: 675.
Doerfler, W. (1995). Uptake of foreign DNA by mammalian cells via the gastrointestinal tract in mice: methylation of foreign DNA- A cellular defense mechanism. In: Meyer P, ed. Gene silencing in higher plants and related phenomena in other eukaryotes. Springer-Verlag, 209-224.
Doolittle, W. F., & Sapienza, C. (1980). Selfish genes, the phenotype paradigm and genome evolution. Nature, 284, 601–603.
Dowen, R. H.,, Pelizzola, M., Schmitz, R. J., Lister, R., Dowen, J. M., Nery, J. R., Dixon, J. E., & Ecker, J. R. (2012) Wide spread dynamic DNA methylation in response to biotic stress. Proceedings of the National Academy of Sciences USA, 109, E2183–E2191.
Down, T. A., Rakyan, V. K., Turner, D. J., Flicek, P., Li, H., Kulesha, E., Gräf, S., Johnson, N., Herrero, J., Tomazou, E. M., Thorne, N. P., Bäckdahl, L., Herberth, M., Howe, K. L., Jackson, D. K., Miretti, M. M., Marioni, J. C., Birney, E., Hubbard, T. J., Durbin, R., Tavaré, S., & Beck, S. (2008). A Bayesian deconvolution strategy for immunoprecipitation-based DNA methylome analysis. Nature Biotechnology. 26(7):779–85.
English, J. J., Mueller, E., & Baulcombe, D. C. (1996). Suppression of virus accumulation in transgenic plants exhibiting silencing of nuclear genes. Plant Cell, 8: 179-188.
Fedoroff, N.V. (2012). Transposable Elements, Epigenetics, and Genome Evolution. SCIENCE, 338: 758-767.
Fortes, A., & Gallusci, P. (2017). Plant stress responses and phenotypic plasticity in the Epigenomics era: Perspectives on the grapevine scenario, a model for perennial crop plants. Frontiers in Plant Science, 8: 82.
Fujimoto, R., Sasaki, T., Ishikawa, R., Osabe, K., Kawanabe, T. & Dennis, E.S. (2012). Molecular Mechanisms of Epigenetic Variation in Plants. International Journal of Molecular Sciences, 13:9900-9922.
Furey, TS. (2012). ChIP-seq and beyond: new and improved methodologies to detect and characterize protein-DNA interactions. Nature Reviews Genetics, 13(12):840–52.
Galindo Gonzalez, Leonardo & Sarmiento, Felipe & Quimbaya, Mauricio. (2018). Shaping Plant Adaptability, Genome Structure and Gene Expression through Transposable Element Epigenetic Control: Focus on Methylation. Agronomy. 8: 180.
Girard, L., & Freeling, M. (1999). Regulatory changes as a consequence of transposon insertion. Developmental Genetics, 25, 291–296.
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 Research, 17(6):877–85.
González, R. M. Ricardi, M. M., & Iusem, N. D. (2013) Epigenetic marks in an adaptive water stress-responsive gene in tomato roots under normal and drought conditions. Epigenetics, 8:864–872.
Gourcilleau, D., Bogeat-Triboulot, M. B., Le Thiec, D., Lafon-Placette, C., Delaunay, A., El-Soud, W. A., Brignolas, F., & Maury, S. (2010). DNA methylation and histone acetylation: genotypic variations in hybrid poplars, impact of water deficit and relationships with productivity. Annals of Forest Science, 67: 208–217.
Gregory, D. J., Mikhaylova, L., & Fedulov, A. V. (2012). Selective DNA demethylation by fusion of TDG with a sequence-specific DNA-binding domain. Epigenetics, 7:344-349.
Gutierrez-Marcos, J. F., & Dickinson, H. G. (2012). Epigenetic reprogramming in plant reproductive lineages. Plant and Cell Physiology, 53: 817–823.
Hauben, M., Haesendonckx, B., Standaert, E., Van Der Kelen, K., Azmi, A., Akpo, H., Van Breusegem, F., Guisez, Y., Bots, M., Lambert, B., Laga, B., & De Block, M. (2009). Energy use efficiency is characterized by an epigenetic component that can be directed through artificial selection to increase yield. Proceedings of the National Academy of Sciences of the United States of America, 106:20109–20114.
Henry, R. J. (1998). Molecular and biochemical characterization of somaclonal variation, in Somaclonal Variation and Induced Mutations in Crop Improvement. Somaclonal Variation and Induced Mutations in Crop Improvement, 485–499.
Hickey, D. A. (1982). Selfish DNA: a sexually-transmitted nuclear parasite. Genetics 101:519–531.
Hirsch, S., Baumberger, R., & Grossniklaus, U. (2013). Epigenetic variation, inheritance, and selection in plant populations. Cold Spring Harbor Symposia on Quantitative Biology, 77:97–104.
Holoch, D. & Moazed, D. (2015). RNA-mediated epigenetic regulation of gene expression. Nature Reviews Genetics, 16(2): 71–84.
Jiang, N., Bao, Z., Zhang, X. Eddy, SR., & Wessler, SR. (2004) Pack-MULE transposable elements mediate gene evolution in plants. Nature 431:569–573.
Jordan, I. K., Rogozin, I. B., Glazko, G. V., & Koonin, E. V. (2003). Origin of a substantial fraction of human regulatory sequences from transposable elements. Trends Genet, 19:68–72.
Jurkowska RZ, Jeltsch A (2010) Silencing of gene expression by targeted DNA methylation: concepts and approaches. Methods Mol Biol 649:149–161.
Jurkowski, T.P., Ravichandran, M., & Stepper, P. (2015). Synthetic epigenetics—towards intelligent control of epigenetic states and cell identity. Clinical Epigenetics, 7(1): 18.
Kertbundit, S., Degreve, H., Deboeck, F., Van Montagu, M., & Hernalsteens, J. P. (1991). In vivo random beta-glucuronidase gene fusions in Arabidopsis thaliana. Proceedings of the National Academy of Sciences of the United States of America, 88: 5212-5216.
Kitimu, SR., Taylor, J., March, TJ., Tairo, F., Wilkinson, MJ. & Rodríguez López, CM. (2015) Meristem micropropagation of cassava (Manihot esculenta) evokes genome-wide changes in DNA methylation. Frontiers in Plant Science, 6:590.
Konermann, S., Brigham, MD., Trevino, AE., Hsu, P.D., Heidenreich, M., Cong, L., Platt, R.J., Scott, D.A., Church, G.M. & Zhang, F. (2013). Optical control of mammalian endogenous transcription and epigenetic states. Nature. 500:472-476.
Laayoun, A., & Smith, SS. (1995). Methylation of slipped duplexes, snapbacks and cruciforms by human DNA (cytosine-5) methyltransferase. Nucleic Acids Research, 23: 1584-1589.
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. (2012). Single-base resolution maps of cultivated and wild rice methylomes and regulatory roles of DNA methylation in plant gene expression. BMC Genomics, 13(1):300.
Lim, DHK., & Maher, ER. (2010). DNA methylation: a form ofepigenetic control of gene expression. The Obstetrician & Gynaecologist, 12:37–42.
Lisch, D. (2009). Epigenetic Regulation of Transposable Elements in Plants. Annual Review of Plant Biology, 60:43–66.
Lister, R., Pelizzola, M., Dowen, RH., Hawkins, R. D., Hon, G., Tonti-Filippini, J., Nery, J.R., Lee, L., Ye, Z., Ngo, Q.M., Edsall, L., Antosiewicz-Bourget, J., Stewart, R., Ruotti, V., Millar, A.H., Thomson, J.A., Ren, B. & Ecker, J.R. (2009). Human DNA methylomes at base resolution show widespread epigenomic differences. Nature. 462(7271):315-22.
Liu, J., Feng, L., Li, J., & He, Z. (2015). Genetic and epigenetic control of plant heat responses. Frontiers in Plant Science, 6:267.
Loza-Muller, L., Rodríguez-Corona, U., Sobol, M., Rodríguez-Zapata, L.C., Hozak, P. & Castano, E. (2015). Fibrillarin methylates H2A in RNA polymerase I trans-active promoters in Brassica oleracea. Frontiers in Plant Science, 6: 976.
Lu, X., Wang, W., Ren, W., Chai, Z., Guo, W., Chen, R., Wang, L., Zhao, J., Lang, Z., Fan, Y., Zhao, J., & Zhang, C. (2015). Genome-wide epigenetic regulation of gene transcription in maize seeds. PloS One, 10(10):e0139582.
Madlung, A., & Comai, L. (2004). The effect of stress on genome regulation and structure. Annals of Botany. 94, 481–495.
Maeder, ML., Angstman, JF., Richardson, ME., Linder, SJ., Cascio, VM., Tsai, SQ., Ho, QH., Sander, JD., Reyon, D., Bernstein, BE., Costello, JF., Wilkinson, MF., & Joung, JK. (2013). Targeted DNA demethylation and activation of endogenous genes using programmable TALE-TET1 fusion proteins. Nature Biotechnology, 31:1137-1142.
Magnani, L. (2014). Epigenetic engineering and the art of epigenetic manipulation. Magnani Genome Biology, 15:306.
Matthes, M., Singh, R., Cheah, S. C., & Karp, A. (2001). Variation in oil palm (Elaeis guineensis Jacq.) tissue culture-derived regenerants revealed by AFLPs with methylation-sensitive enzymes. Theoretical and Applied Genetics, 102, 971–979.
Matzke, AJM., Neuhuber, F., Park, YD., Ambros, PF., & Matzke, MA. (1994). Homology-dependent gene silencing in transgenic plants: epistatic silencing loci contain multiple copies of methylated transgenes. Molecular & General Genetics, 244: 219-229.
Mendenhall, EM., Williamson, KE., Reyon, D., Zou, JY., Ram, O., Joung, JK., & Bernstein, BE. (2013). Locus-specific editing of histone modifications at endogenous enhancers. Nature Biotechnology, 31:1133-1136.
Migicovsky, Z., Yao, Y., & Kovalchuk, I. (2014). Transgenerational phenotypic and epigenetic changes in response to heat stress in Arabidopsis thaliana. Plant Signaling & Behavior, 9(2), e27971.
Mirouze, M., & Paszkowski, J. (2011). Epigenetic contribution to stress adaptation in plants. Current Opinion in Plant Biology, 14(3), 267–274.
Munshi, A., Ahuja, Y.R. & Bahadur, B. (2015). Epigenetic Mechanisms in Plants: An Overview. Plant Biology and Biotechnology, 265-278.
Otto, C., Stadler, PF., & Hoffmann, S. (2012). Fast and sensitive mapping of bisulfite-treated sequencing data. Bioinformatics, 28(13):1698–704.
Park, Y-D., Papp, I., Moscone, EA., Iglesias, VA., Vaucheret, H., Matzke, AJM., & Matzke, MA. (1996). Gene silencing mediated by promoter homology occurs at the level of transcription and results in meiotically heritable alterations in methylation and gene activity. Plant Journal, 9: 183–194.
Paul, B., Barnes, S., Demark-Wahnefried, W., Morrow, C., Salvador, C., Skibola, C., & Tollefsbol, TO. (2015). Influences of diet and the gut microbiome on epigenetic modulation in cancer and other diseases. Clinical Epigenetics,16(7):112.
Pikaard, C., & Mittelsten Scheid, O. (2014). Epigenetic regulation in plants. Cold Spring Harbor Perspectives in Biology, 1;6(12):a019315.
Posner, J.L., Baldock, J.O., & Hedtcke, J. L. (2008). Organic and conventional production systems in the wisconsin integrated cropping systems trials: I. Productivity 1990–2002. Agronomy Journal, 100:253–260.
Prols, F., & Meyer, P. (1992). The methylation patterns of chromosomal integration regions influence gene activity of transferred DNA in Petunia hybrida. Plant Journal, 2: 465-475.
Ragupathy, R., Ravichandran, S., Mahdi, SR., Huang, D., Reimer, E., Domaratzki, M., & Cloutier, S. (2016). Deep sequencing of wheat sRNA transcriptome reveals distinct temporal expression pattern of miRNAs in response to heat, light and UV. Scientific Reports, 6:39373.
Reid, L.M., O’Donell, C.P., & Downell, G. (2006). Recent technological advances for the determination of food authenticity. Trends in Food Science & Technology, 17, 344–353.
Reinhart, B. J., & Bartel, D. P., (2002). Small RNAs correspond to centromere heterochromatic repeats. Science. 297(5588):1831.
Rivenbark, A. G., Stolzenburg, S., Beltran, A. S., Yuan, X., Rots, M.G., Strahl, B. D. & Blancafort, P. (2012). Epigenetic reprogramming of cancer cells via targeted DNA methylation. Epigenetics, 7:350-360.
Rodríguez López, C.M., & Wilkinson, M.J. (2015). Epi-fingerprinting and epi-interventions for improved crop production and food quality. Frontiers in Plant Science, 5(6):397.
Saraswat, S., Kumar Yadav, A., Sirohi, P. & Singh, N.K. (2017). Role of Epigenetics in Crop Improvement: Water and Heat Stress. Journal of Plant Biology, 60:231-240.
Schmitt, F., Oakeley, E. J., & Jost, J. P. (1997). Antibiotics induce genome-wide hypermethylation in cultured NicotianaTabacum plants. The Journal of Biological Chemistry, 272:1534–1540.
Schmitz, R.J., He, Y., Valdés-López, O., Khan, S.M., Joshi, T., Urich, M.A., Nery, JR., Diers, B., Xu, D., Stacey, G., & Ecker, JR. (2013). Epigenome-wide inheritance of cytosine methylation variants in a recombinant inbred population. Genome Research, 23:1663–1674.
Sha, A.H., Lin, X.H., Huang, J.B., & Zhang, D.P. (2005). Analysis of DNA methylation related to rice adult plant resistance to bacterial blight based on methylation-sensitive AFLP (MSAP) analysis. Molecular Genetics and Genomics, 273: 484–490.
Shrestha, A., Khan, A. & Dey, N. (2018). Cis-Trans Engineering: Advances and Perspectives on Customized Transcriptional Regulation in Plants. Molecular Plant, 11: 886-898.
Slotkin, R.K., & Martienssen, R. (2007). Transposable elements and the epigenetic regulation of the genome. Nature Reviews Genetics, 8:272-285.
Smith, AD., Chung, WY., Hodges, E., Kendall, J., Hannon, G., Hicks, J., Xuan, Z., & Zhang, M.Q. (2009). Updates to the RMAP short-read mapping software. Bioinformatics, 25(21):2841–2.
Song, L., & Crawford, GE., (2010). DNase-seq: a high-resolution technique for mapping active gene regulatory elements across the genome from mammalian cells. Cold Spring Harbor protocols. 2010(2):pdb prot5384.
Song, Q., Zhang, T., Stelly, DM. & Chen, ZJ. (2017). Epigenomic and functional analyses reveal roles of epialleles in the loss of photoperiod sensitivity during domestication of allotetraploid cottons. Genome Biol, 18:99.
Song, Q., Decato, B., Hong, E. E., Zhou, M., Fang, F., Q. U. J., Garvin, T., Kessler, M., Zhou, J., & Smith., A. D. (2013). A reference methylome database and analysis pipeline to facilitate integrative and comparative epigenomics. PLOS One, 8(12):e81148.
Springer, N. M. (2013). Epigenetics and crop improvement. Trends in Genetics, 29(4):241–247.
Srancikova, A., Horvathova, E., & Kozics, K. (2013). Biological effects of four frequently used medicinal plants of Lamiaceae. Neoplasma, 60:585–597.
Stam, M., Mol, J.N.M. & Kooter, J.M. (1997). Review Article: The Silence of Genes in Transgenic Plants. Annals of Botany, 79(1):3-12.
Su, L.C., Liu, X., Chen, Y.P., & Li, L. (2012). Isolation of AhDHNs from Arachis hypogaea L. and evaluation of AhDHNs expression under exogenous abscisic acid (ABA) and water stress. African Journal of Biotechnology, 11:11221–11229.
Szyf, M. (2009). Epigenetics, DNA methylation, and chromatin modifying drugs. Annual Review of Pharmacology and Toxicology, 49:243-263.
Temel, A., Janack, B. & Humbeck, K. (2015). Epigenetic Regulation in Plants. eLS. John Wiley & Sons, Ltd: Chichester.
Thakore, PI., D’Ippolito, AM., Song, L., Safi, A., Shivakumar, NK., Kabadi, AM., & Gersbach, CA. (2015). Highly Specific Epigenome Editing by CRISPR/Cas9 Repressors for Silencing of Distal Regulatory Elements. Nature methods, 12(12):1143.
Tricker, P., Rodríguez López, C. M., Hadley, P., Wagstaff, C., & Wilkinson, M. J. (2013b). Pre-conditioning the epigenetic response to high vapour pressure deficit increases the drought tolerance in Arabidopsis thaliana. Plant Signaling & Behavior, 8:e25974.
Tricker, P. J., Lo´pez, C. M. R., Gibbings, G., Hadley, P., & Wilkinson, M. J. (2013). Transgenerational, dynamic methylation of stomata genes in response to low relative humidity. International Journal of Molecular Sciences, 14(4), 6674–6689.
Us-Camas, R., Rivera-Solı´s, G., Duarte-Ake, F. & De-la-Pena, C. (2014). In vitro culture: an epigenetic challenge for plants. Plant Cell, Tissue and Organ Culture (PCTOC), 118: 187.
Vanstraelen, M., & Benková, E. (2012). Hormonal interactions in the regulation of plant development. Annual Review of Cell and Developmental Biology, 28(1):463–487.
Vaucheret, H. (1993). Identifcation of a general silencer for 19S and 35S promoters in a transgenic tobacco plant: 90 bp of homology in the promoter sequence are sufficient for trans-inactivation. Comptes Rendus de L'Academie Des Sciences Serie III-Sciences de La Vie-Life Sciences, 316: 1471-1483.
Wang, Q., & Dooner, H. K. (2006). Eukaryotic transposable elements and genome evolution special feature: remarkable variation in maize genome structure inferred from haplotype diversity at the bz locus. Proceedings of the National Academy of Sciences USA, 103:17644–17649.
Wibowo, A., Becker, C., Marconi, G., Durr, J., Price, J., Hagmann, J., Papareddy, R., Putra, H., Kageyama, J., Becker, J., Weigel, D., & Gutierrez-Marcos, J. (2016). Hyperosmotic stress memory in Arabidopsis is mediated by distinct epigenetically labile sites in the genome and is restricted in the male germline by DNA glycosylase activity. eLife, 5:e13546.
Wollmann, H., & Berger, F., (2012). Epigenetic reprogramming during pant reproduction and seed development. Current Opinion in Plant Biology, 15, 63–69.
Wu, TD., & Nacu, S. (2010). Fast and SNP-tolerant detection of complex variants and splicing in short reads. Bioinformatics. 26(7):873–81.
Xi, Y., Bock, C., Muller, F., Sun, D., Meissner, A., & Li, W. (2012). RRBSMAP: a fast, accurate and user-friendly alignment tool for reduced representation bisulfite sequencing. Bioinformatics. 28(3):430–2.
Yakovlev, I. A., Asante, D. K. A., Fossdal, C. G., Junttila, O., & Johnsen, O, (2011) Differential gene expression related to an epigenetic memory affecting climatic adaptation in Norway spruce. Plant Science, 180(1):132–139.
Yong-Villalobos, L. (2015) Methylome analysis reveals an important role for epigenetic changes in the regulation of the Arabidopsis response to phosphate starvation. Proceedings of the National Academy of Sciences USA,112:E7293–E7302.
Zhang, L., Cheng, Z., Qin, R., Qiu, Y., Wang, J.L., Cui, X., Gu, L., Zhang, X., Guo, X., Wang, D., Jiang, L., Wu, C.Y., Wang, H., Cao, X., & Wan, J. (2012). Identification and characterization of an Epi-Allele of FIE1 reveals a regulatory linkage between two epigenetic marks in rice. Plant Cell, 24, 4407–4421.
Zhou, DX. (2009) Regulatory mechanism of histone epigenetic modifications in plants. Epigenetics, 4(1):15–18.
Journal of Epigenetics
Volume 1, Issue 1
February 2019
Pages 24-34

Files

History

  • Receive Date: 10 November 2018
  • Revise Date: 20 January 2019
  • Accept Date: 11 March 2019

Share

How to cite

Statistics