Exploring the crop epigenome: a comparison of DNA methylation profiling techniques

. 2023 ; 14 () : 1181039. [epub] 20230530

Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic-ecollection

Typ dokumentu časopisecké články, přehledy

Perzistentní odkaz   https://www.medvik.cz/link/pmid37389288

Epigenetic modifications play a vital role in the preservation of genome integrity and in the regulation of gene expression. DNA methylation, one of the key mechanisms of epigenetic control, impacts growth, development, stress response and adaptability of all organisms, including plants. The detection of DNA methylation marks is crucial for understanding the mechanisms underlying these processes and for developing strategies to improve productivity and stress resistance of crop plants. There are different methods for detecting plant DNA methylation, such as bisulfite sequencing, methylation-sensitive amplified polymorphism, genome-wide DNA methylation analysis, methylated DNA immunoprecipitation sequencing, reduced representation bisulfite sequencing, MS and immuno-based techniques. These profiling approaches vary in many aspects, including DNA input, resolution, genomic region coverage, and bioinformatics analysis. Selecting an appropriate methylation screening approach requires an understanding of all these techniques. This review provides an overview of DNA methylation profiling methods in crop plants, along with comparisons of the efficacy of these techniques between model and crop plants. The strengths and limitations of each methodological approach are outlined, and the importance of considering both technical and biological factors are highlighted. Additionally, methods for modulating DNA methylation in model and crop species are presented. Overall, this review will assist scientists in making informed decisions when selecting an appropriate DNA methylation profiling method.

BioISI BioSystems and Integrative Sciences Institute Faculdade de Ciências Universidade de Lisboa Lisbon Portugal

Biology Department Ġ F Abela Junior College Msida Malta

Center for Biological Research Madrid Spain

Centre for Agricultural Genomics and Biotechnology Faculty of Agricultural and Food Sciences and Environmental Management University of Debrecen Nyíregyháza Hungary

Centre of Molecular Medicine and Biobanking University of Malta Msida Malta

Centre of Plant Structural and Functional Genomics Institute of Experimental Botany of the Czech Academy of Sciences Olomouc Czechia

Centro de Biotecnología y Genómica de Plantas Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria Madrid Spain

Department of Biology University of Florence Sesto Fiorentino Italy

Department of Chemistry and Biology 'A Zambelli' University of Salerno Fisciano Italy

Department of Clinical Biochemistry Faculty of Pharmacy Collegium Medicum in Bydgoszcz Nicolaus Copernicus University in Toruń Bydgoszcz Poland

Department of Molecular Biology and Genetics Institute of Plant Physiology and Genetics Bulgarian Academy of Sciences Sofia Bulgaria

Department of Vegetables and Field Crops Agricultural Research Organization Volcani Center Institute of Plant Sciences Rishon LeZion Israel

Department of Vitis Institute of Olive Tree Subtropical Crops and Viticulture Athens Greece

Faculty of Agriculture University of Novi Sad Novi Sad Serbia

Faculty of Science University of Sarajevo Sarajevo Bosnia and Herzegovina

Genomic Research Department Thünen Institute of Forest Genetics Grosshansdorf Germany

Institute of Field and Vegetable Crops National Institute of Republic of Serbia Novi Sad Serbia

Laboratoire de Biologie des Ligneux et des Grandes Cultures EA1207 USC1328 INRAE Université d'Orléans Orléans France

Laboratory of Forest Genetics and Biotechnology Institute of Mediterranean Forest Ecosystems Hellenic Agricultural Organization DIMITRA Athens Greece

Laboratory of Plant Breeding and Biometry Department of Crop Science Agricultural University of Athens Athens Greece

Linking Landscape Environment Agriculture and Food Institute of Agronomy University of Lisbon Lisbon Portugal

Mendeleum Insitute of Genetics Faculty of Horticulture Mendel University in Brno Lednice Czechia

Plant Epigenomics Technical University of Munich Freising Germany

Plant Physiology Department of Organisms and Systems Biology and University Institute of Biotechnology of Asturias University of Oviedo Oviedo Spain

Zobrazit více v PubMed

Abid G., Mingeot D., Muhovski Y., Mergeai G., Aouida M., Abdelkarim S., et al. . (2017). Analysis of DNA methylation patterns associated with drought stress response in faba bean (Vicia faba l.) using methylation-sensitive amplification polymorphism (MSAP). Environ. Exp. Bot. 142, 34–44. doi: 10.1016/j.envexpbot.2017.08.004 DOI

Agius F., Kapoor A., Zhu J. K. (2006). Role of the arabidopsis DNA glycosylase/lyase ROS1 in active DNA demethylation. Proc. Natl. Acad. Sci. U.S.A. 103, 11796–11801. doi: 10.1073/pnas.0603563103 PubMed DOI PMC

Aliche E. B., Talsma W., Munnik T., Bouwmeester H. (2021). Characterization of maize root microbiome in two different soils by minimizing plant DNA contamination in metabarcoding analysis. Biol. Fertil. Soils 57, 731–737. doi: 10.1007/s00374-021-01555-3 DOI

Allendorf F. W. (2017). Genetics and the conservation of natural populations: allozymes to genomes. Mol. Ecol. 26, 420–430. doi: 10.1111/mec.13948 PubMed DOI

Andorf C. M., Cannon E. K., Portwood J. L., Gardiner J. M., Harper L. C., Schaeffer M. L., et al. . (2016). MaizeGDB update: new tools, data and interface for the maize model organism database. Nucleic Acids Res. 44 (D1), D1195–D1201. doi: 10.1093/nar/gkv1007 PubMed DOI PMC

Andrews S. (2013). Reduced representation bisulfite-seq - a brief guide to RRBS. Babraham Bioinf., 1–12.

Ashapkin V. V., Kutueva L. I., Aleksandrushkina N. I., Vanyushin B. F. (2020). Epigenetic mechanisms of plant adaptation to biotic and abiotic stresses. Int. J. Mol. Sci. 21, 7457. doi: 10.3390/ijms21207457 PubMed DOI PMC

Ashikawa I. (2001). Gene-associated CpG islands in plants as revealed by analyses of genomic sequences. Plant J. 26, 617–625. doi: 10.1046/j.1365-313x.2001.01062.x PubMed DOI

Atsumi G., Matsuo K., Fukuzawa N., Matsumura T. (2021). Virus-mediated targeted DNA methylation illuminates the dynamics of methylation in an endogenous plant gene. Int. J. Mol. Sci. 22, 4125. doi: 10.3390/ijms22084125 PubMed DOI PMC

Avramidou E., Ganopoulos I. V., Doulis A. G., Tsaftaris A. S., Aravanopoulos F. A. (2015). Beyond population genetics: natural epigenetic variation in wild cherry (Prunus avium). Tree Genet. Genomes 11, 1–9. doi: 10.1007/s11295-015-0921-7 DOI

Avramidou E., Kapazoglou A., Aravanopoulos F. A., Xanthopoulou A., Ganopoulos I., Tsaballa A., et al. . (2014). Global DNA methylation changes in Cucurbitaceae inter-species grafting. Crop Breed. Appl. Biotechnol. 15, 112–116. doi: 10.1590/1984-70332015v15n2n20 DOI

Avramidou E., Moysiadis T., Ganopoulos I., Michailidis M., Kissoudis C., Valasiadis D., et al. . (2021). Phenotypic, genetic, and epigenetic variation among diverse sweet cherry gene pools. Agronomy 11, 680. doi: 10.3390/agronomy11040680 DOI

Baránek M., Čechová J., Kovacs T., Eichmeier A., Wang S., Raddová J., et al. . (2016). Use of combined MSAP and NGS techniques to identify differentially methylated regions in somaclones: a case study of two stable somatic wheat mutants. PloS One 11, e0165749. doi: 10.1371/journal.pone.0165749 PubMed DOI PMC

Baránek M., Kováčová V., Gazdík F., Špetík M., Eichmeier A., Puławska J., et al. . (2021). Epigenetic modulating chemicals significantly affect the virulence and genetic characteristics of the bacterial plant pathogen Xanthomonas campestris pv. campestris. Genes 12, 804. doi: 10.3390/genes12060804 PubMed DOI PMC

Baránková K., Nebish A., Tříska J., Raddová J., Baránek M. (2021). Comparison of DNA methylation landscape between Czech and Armenian vineyards show their unique character and increased diversity. Czech J. Genet. Plant Breed 57, 67–75. doi: 10.17221/90/2020-CJGPB DOI

Bartlett A., O'Malley R. C., Huang S. S. C., Galli M., Nery J. R., Gallavotti A., et al. . (2017). Mapping genome-wide transcription-factor binding sites using DAP-seq. Nat. Protoc. 12, 1659–1672. doi: 10.1038/nprot.2017.055 PubMed DOI PMC

Baubec T., Dinh H. Q., Pečinka A., Rakic B., Rozhon W., Wohlrab B., et al. . (2010). Cooperation of multiple chromatin modifications can generate unanticipated stability of epigenetic states in Arabidopsis . Plant Cell 22, 34–47. doi: 10.1105/tpc.109.072819 PubMed DOI PMC

Baubec T., Finke A., Mittelsten Scheid O., Pečinka A. (2014). Meristem-specific expression of epigenetic regulators safeguards transposon silencing in Arabidopsis . EMBO Rep. 15, 446–452. doi: 10.1002/embr.201337915 PubMed DOI PMC

Beck D., Ben Maamar M., Skinner M. K. (2022). Genome-wide CpG density and DNA methylation analysis method (MeDIP, RRBS, and WGBS) comparisons. Epigenetics 17, 518–530. doi: 10.1080/15592294.2021.1924970 PubMed DOI PMC

Bednarek P. T., Orłowska R., Niedziela A. (2017). A relative quantitative methylation-sensitive amplified polymorphism (MSAP) method for the analysis of abiotic stress. BMC Plant Biol. 17, 1–13. doi: 10.1186/s12870-017-1028-0 PubMed DOI PMC

Berenguer E., Bárány I., Solís M. T., Pérez-Pérez Y., Risueño M. C., Testillano P. S. (2017). Inhibition of histone H3K9 methylation by BIX-01294 promotes stress-induced microspore totipotency and enhances embryogenesis initiation. Front. Plant Sci. 8. doi: 10.3389/fpls.2017.01161 PubMed DOI PMC

Bewick A. J., Schmitz R. J. (2017). Gene body DNA methylation in plants. Curr. Opin. Plant Biol. 36, 103–110. doi: 10.1016/j.pbi.2016.12.007 PubMed DOI PMC

Bond D. M., Baulcombe D. C. (2015). Epigenetic transitions leading to heritable, RNA-mediated de novo silencing in Arabidopsis thaliana . Proc. Natl. Acad. Sci. U. S. A. 112, 917–922. doi: 10.1073/pnas.1413053112 PubMed DOI PMC

Boquete M. T., Muyle A., Alonso C. (2021). Plant epigenetics: phenotypic and functional diversity beyond the DNA sequence. Am. J. Bot. 108, 553–558. doi: 10.1002/ajb2.1645 PubMed DOI

Bull H., Casao M. C., Zwirek M., Flavell A. J., Thomas W. T., Guo W., et al. . (2017). Barley SIX-ROWED SPIKE3 encodes a putative jumonji c-type H3K9me2/me3 demethylase that represses lateral spikelet fertility. Nat. Commun. 8, 936. doi: 10.1038/s41467-017-00940-7 PubMed DOI PMC

Calhoun C. S., Crist D. K., Knee E. M., Price C. G., Lindsey B. E., Castrejon D. M., et al. . (2019). “The genetic resources of arabidopsis thaliana: the arabidopsis biological resource center,” in The biological resources of model organisms (CRC Press; ), 13–34. doi: 10.1201/9781315100999 DOI

Cao X., Jacobsen S. E. (2002). Role of the Arabidopsis DRM methyltransferases in de novo DNA methylation and gene silencing. Curr. Biol. 12, 1138–1144. doi: 10.1016/s0960-9822(02)00925-9 PubMed DOI

Chen X., Ge X., Wang J., Tan C., King G. J., Liu K. (2015). Genome-wide DNA methylation profiling by modified reduced representation bisulfite sequencing in Brassica rapa suggests that epigenetic modifications play a key role in polyploid genome evolution. Front. Plant Sci. 6. doi: 10.3389/fpls.2015.00836 PubMed DOI PMC

Chen G., Li Y., Wei Z., Gan L., Liu J., Wang Z. (2022). Dynamic profiles of DNA methylation and the interaction with histone acetylation during fiber cell initiation of Gossypium hirsutum . J. Cotton Res. 5, 1–14. doi: 10.1186/s42397-022-00115-w DOI

Chen K., Wang Y., Zhang R., Zhang H., Gao C. (2019). CRISPR/Cas genome editing and precision plant breeding in agriculture. Annu. Rev. Plant Biol. 70, 667–697. doi: 10.1146/annurev-arplant-050718-100049 PubMed DOI

Cheng J., Niu Q., Zhang B., Chen K., Yang R., Zhu J. K., et al. . (2018). Downregulation of RdDM during strawberry fruit ripening. Genome Biol. 19, 1–14. doi: 10.1186/s13059-018-1587-x PubMed DOI PMC

Chwialkowska K., Korotko U., Kosinska J., Szarejko I., Kwasniewski M. (2017). Methylation sensitive amplification polymorphism sequencing (MSAP-seq) - a method for high-throughput analysis of differentially methylated CCGG sites in plants with large genomes. Front. Plant Sci. 8. doi: 10.3389/fpls.2017.02056 PubMed DOI PMC

Chwialkowska K., Korotko U., Kwasniewski M. (2019). “DNA Methylation analysis in barley and other species with large genomes,” in Barley. methods in molecular biology, vol. 1900 . Ed. Harwood W. (New York, NY: Humana Press; ), 253–268. doi: 10.1007/978-1-4939-8944-7_16 PubMed DOI

Chwialkowska K., Nowakowska U., Mroziewicz A., Szarejko I., Kwasniewski M. (2016). Water-deficiency conditions differently modulate the methylome of roots and leaves in barley (Hordeum vulgare l.). J. Exp. Bot. 67, 1109–1121. doi: 10.1093/jxb/erv552 PubMed DOI PMC

Cicatelli A., Todeschini V., Lingua G., Biondi S., Torrigiani P., Castiglione S. (2014). Epigenetic control of heavy metal stress response in mycorrhizal versus non-mycorrhizal poplar plants. Environ. Sci. pollut. Res. 21, 1723–1737. doi: 10.1007/s11356-013-2072-4 PubMed DOI

Clark S. J., Harrison J., Paul C. L., Frommer M. (1994). High sensitivity mapping of methylated cytosines. Nucleic Acids Res. 22, 2990–2997. doi: 10.1093/nar/22.15.2990 PubMed DOI PMC

Cokus S. J., Feng S., Zhang X., Chen Z., Merriman B., Haudenschild C. D., et al. . (2008). Shotgun bisulphite sequencing of the Arabidopsis genome reveals DNA methylation patterning. Nature 452, 215–219. doi: 10.1038/nature06745 PubMed DOI PMC

Conde D., González-Melendi P., Allona I. (2013). Poplar stems show opposite epigenetic patterns during winter dormancy and vegetative growth. Trees 27, 311–320. doi: 10.1007/s00468-012-0800-x DOI

Conde D., Moreno-Cortés A., Dervinis C., Ramos-Sánchez J. M., Kirst M., Perales M., et al. . (2017). Overexpression of DEMETER, a DNA demethylase, promotes early apical bud maturation in poplar. Plant Cell Environ. 40, 2806–2819. doi: 10.1111/pce.13056 PubMed DOI

Cornet L., Baurain D. (2022). Contamination detection in genomic data: more is not enough. Genome Biol. 23, 60. doi: 10.1186/s13059-022-02619-9 PubMed DOI PMC

Cortijo S., Wardenaar R., Colome-Tatche M., Gilly A., Etcheverry M., Labadie K., et al. . (2014). Mapping the epigenetic basis of complex traits. Science 343, 1145–1148. doi: 10.1126/science.1248127 PubMed DOI

Crisp P. A., Marand A. P., Noshay J. M., Zhou P., Lu Z., Schmitz R. J., et al. . (2020). Stable unmethylated DNA demarcates expressed genes and their cis-regulatory space in plant genomes. Proc. Natl. Acad. Sci. U.S.A. 117, 23991–24000. doi: 10.1073/pnas.2010250117 PubMed DOI PMC

Davis B. M., Chao M. C., Waldor M. K. (2013). Entering the era of bacterial epigenomics with single molecule real time DNA sequencing. Curr. Opin. Microbiol. 16, 192–198. doi: 10.1016/j.mib.2013.01.011 PubMed DOI PMC

Deamer D., Akesone M., Branton D. (2016). Three decades of nanopore sequencing. Nat. Biotechnol. 34, 518–524. doi: 10.1038/nbt.3423 PubMed DOI PMC

Deans C., Maggert K. A. (2015). What do you mean, “epigenetic”? Genetics 199, 887–896. doi: 10.1534/genetics.114.173492 PubMed DOI PMC

Dobosy J. R., Selker E. U. (2001). Emerging connections between DNA methylation and histone acetylation. CMLS 58, 721–727. doi: 10.1007/pl00000895 PubMed DOI PMC

Eid J., Fehr A., Gray J., Luong K., Lyle J., Otto G., et al. . (2009). Real-time DNA sequencing from single polymerase molecules. Science 323, 133–138. doi: 10.1126/science.1162986 PubMed DOI

El-Tantawy A. A., Solís M. T., Risueño M. C., Testillano P. S. (2014). Changes in DNA methylation levels and nuclear distribution patterns after microspore reprogramming to embryogenesis in barley. Cytogenet. Genome Res. 143, 200–208. doi: 10.1159/000365232 PubMed DOI

Erdmann R. M., Picard C. L. (2020). RNA-Directed DNA methylation. PloS Genet. 16, e1009034. doi: 10.1371/journal.pgen.1009034 PubMed DOI PMC

Erdmann R. M., Souza A. L., Clish C. B., Gehring M. (2015). 5-hydroxymethylcytosine is not present in appreciable quantities in Arabidopsis DNA. G3-Genes Genomes Genet. 5, 1–8. doi: 10.1534/g3.114.014670 PubMed DOI PMC

Esposito-Polesi N. P., de Abreu-Tarazi M. F., de Almeida C. V., Tsai S. M., de Almeida M. (2017). Investigation of endophytic bacterial community in supposedly axenic cultures of pineapple and orchids with evidence on abundant intracellular bacteria. Curr. Microbiol. 74, 103–113. doi: 10.1007/s00284-016-1163-0 PubMed DOI

Feng S., Zhong Z., Wang M., Jacobsen S. E. (2020). Efficient and accurate determination of genome-wide DNA methylation patterns in Arabidopsis thaliana with enzymatic methyl sequencing. Epigenet. Chromatin 13, 42. doi: 10.1186/s13072-020-00361-9 PubMed DOI PMC

Finnegan E. J., Dennis E. S. (1993). Isolation and identification by sequence homology of a putative cytosine methyltransferase from Arabidopsis thaliana . Nucleic Acid Res. 21, 2383–2388. doi: 10.1093/nar/21.10.2383 PubMed DOI PMC

Flusberg B. A., Webster D. R., Lee J. H., Travers K. J., Olivares E. C., Clark T. A., et al. . (2010). Direct detection of DNA methylation during single-molecule, real-time sequencing. Nat. Methods 7, 461–465. doi: 10.1038/nmeth.1459 PubMed DOI PMC

Foerster A. M., Scheid O. M. (2010). “Analysis of DNA methylation in plants by bisulfite sequencing,” in Plant epigenetics. methods in molecular biology, vol. 631 . Eds. Kovalchuk I., Zemp F. (Humana Press; ), 1–11. doi: 10.1007/978-1-60761-646-7_1 PubMed DOI

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. doi: 10.1073/pnas.212325299 PubMed DOI PMC

Frommer M., McDonald L. E., Millar D. S., Collis C. M., Watt F., Grigg G. W., et al. . (1992). A genomic sequencing protocol that yields a positive display of 5-methylcytosine residues in individual DNA strands. Proc. Natl. Acad. Sci. U. S. A. 89, 1827–1831. doi: 10.1073/pnas.89.5.1827 PubMed DOI PMC

Fu Y., He C. (2012). Nucleic acid modifications with epigenetic significance. Curr. Opin. Chem. Biol. 16, 516–524. doi: 10.1016/j.cbpa.2012.10.002 PubMed DOI PMC

Fulneček J., Kovařík A. (2014). How to interpret methylation sensitive amplified polymorphism (MSAP) profiles? BMC Genet. 15, 1–9. doi: 10.1186/1471-2156-15-2 PubMed DOI PMC

Fulneček J., Matyášek R., Votruba I., Holý A., Křížová K., Kovařík A. (2011). Inhibition of SAH-hydrolase activity during seed germination leads to deregulation of flowering genes and altered flower morphology in tobacco. Mol. Genet. Genomics 285, 225–236. doi: 10.1007/s00438-011-0601-8 PubMed DOI

Gallego-Bartolomé J., Gardiner J., Liu W., Papikian A., Ghoshal B., Kuo H. Y., et al. . (2018). Targeted DNA demethylation of the Arabidopsis genome using the human TET1 catalytic domain. Proc. Natl. Acad. Sci. U. S. A. 115, E2125–E2134. doi: 10.1073/pnas.171694511 PubMed DOI PMC

Gallego-Bartolomé J., Liu W., Kuo P. H., Feng S., Ghoshal B., Gardiner J., et al. . (2019). Co-Targeting RNA polymerases IV and V promotes efficient de novo DNA methylation in Arabidopsis . Cell 176, 1068–1082. doi: 10.1016/j.cell.2019.01.029 PubMed DOI PMC

Ganesan A., Arimondo P. B., Rots M. G., Jeronimo C., Berdasco M. (2019). The timeline of epigenetic drug discovery: from reality to dreams. Clin. Epigenet. 11, 1–17. doi: 10.1186/s13148-019-0776-0 PubMed DOI PMC

Gao Y., Wang H., Zhang H., Wang Y., Chen J., Gu L. (2017). PRAPI: post-transcriptional regulation analysis pipeline for iso-seq. Bioinformatics 34, 1580–1582. doi: 10.1093/bioinformatics/btx830 PubMed DOI

Gáspár B., Bossdorf O., Durka W. (2019). Structure, stability and ecological significance of natural epigenetic variation: a large-scale survey in Plantago lanceolata . New Phytol. 221, 1585–1596. doi: 10.1111/nph.15487 PubMed DOI

Gent J. I., Ellis N. A., Guo L., Harkess A. E., Yao Y., Zhang X., et al. . (2013). CHH islands: de novo DNA methylation in near-gene chromatin regulation in maize. Genome Res. 23, 628–637. doi: 10.1101/gr.146985.112 PubMed DOI PMC

Ghoshal B., Picard C. L., Vong B., Feng S., Jacobsen S. E. (2021). CRISPR-based targeting of DNA methylation in Arabidopsis thaliana by a bacterial CG-specific DNA methyltransferase. Proc. Natl. Acad. Sci. U. S. A. 118, e2125016118. doi: 10.1073/pnas.212501611 PubMed DOI PMC

Gomez-Cabellos S., Toorop P. E., Cañal M. J., Iannetta P. P. M., Fernández-Pascual E., Pritchard H. W., et al. . (2022). Global DNA methylation and cellular 5-methylcytosine and H4 acetylated patterns in primary and secondary dormant seeds of Capsella bursa-pastoris (L.) medik. (shepherd’s purse). Protoplasma 259, 595–614. doi: 10.1007/s00709-021-01678-2 PubMed DOI PMC

Gong Z., Morales-Ruiz T., Ariza R. R., Roldán-Arjona T., David L., Zhu J. K. (2002). ROS1, a repressor of transcriptional gene silencing in Arabidopsis, encodes a DNA glycosylase/lyase. Cell 111, 803–814. doi: 10.1016/S0092-8674(02)01133-9 PubMed DOI

Gong W., Pan X., Xu D., Ji G., Wang Y., Tian Y., et al. . (2022). Benchmarking DNA methylation analysis of 14 alignment algorithms for whole genome bisulfite sequencing in mammals. Comput. Struct. Biotechnol. J. 20, 4704–4716. doi: 10.1016/j.csbj.2022.08.051 PubMed DOI PMC

González-Benito M. E., Ibáñez M.Á., Pirredda M., Mira S., Martín C. (2020). Application of the MSAP technique to evaluate epigenetic changes in plant conservation. Int. J. Mol. Sci. 21, 7459. doi: 10.3390/ijms21207459 PubMed DOI PMC

Gouil Q., Keniry A. (2019). Latest techniques to study DNA methylation. Essays Biochem. 63, 639–648. doi: 10.1042/EBC20190027 PubMed DOI PMC

Grehl C., Kuhlmann M., Becker C., Glaser B., Grosse I. (2018). How to design a whole-genome bisulfite sequencing experiment. Epigenomes 2, 21. doi: 10.3390/epigenomes2040021 DOI

Griffin P. T., Niederhuth C. E., Schmitz R. J. (2016). A comparative analysis of 5-azacytidine- and zebularine-induced DNA demethylation. G3 (Bethesda) 6, 2773–2780. doi: 10.1534/g3.116.030262 PubMed DOI PMC

Groot M. P., Wagemaker N., Ouborg N. J., Verhoeven K. J., Vergeer P. (2018). Epigenetic population differentiation in field-and common garden-grown Scabiosa columbaria plants. Ecol. Evol. 8, 3505–3517. doi: 10.1002/ece3.3931 PubMed DOI PMC

Grunau C., Clark S. J., Rosenthal A. (2001). Bisulfite genomic sequencing: systematic investigation of critical experimental parameters. Nucleic Acids Res. 29, e65–e65. doi: 10.1093/nar/29.13.e65 PubMed DOI PMC

Gruntman E., Qi Y., Slotkin R. K., Roeder T., Martienssen R. A., Sachidanandam R. (2008). Kismeth: analyzer of plant methylation states through bisulfite sequencing. BMC Bioinf. 9, 371. doi: 10.1186/1471-2105-9-371 PubMed DOI PMC

Gu H., Smith Z. D., Bock C., Boyle P., Gnirke A., Meissner A. (2011). Preparation of reduced representation bisulfite sequencing libraries for genome-scale DNA methylation profiling. Nat. Protoc. 6, 468–481. doi: 10.1038/nprot.2010.190 PubMed DOI

Guarino F., Heinze B., Castiglione S., Cicatelli A. (2020). Epigenetic analysis through MSAP-NGS coupled technology: the case study of white poplar monoclonal populations/stands. Int. J. Mol. Sci. 21, 7393. doi: 10.3390/ijms21197393 PubMed DOI PMC

Gugger P. F., Fitz-Gibbon S., PellEgrini M., Sork V. L. (2016). Species-wide patterns of DNA methylation variation in Quercus lobata and their association with climate gradients. Mol. Ecol. 25, 1665–1680. doi: 10.1111/mec.13563 PubMed DOI

Guo W., Fiziev P., Yan W., Cokus S., Sun X., Zhang M. Q., et al. . (2013). BS-Seeker2: a versatile aligning pipeline for bisulfite sequencing data. BMC Genom. 14, 1–8. doi: 10.1186/1471-2164-14-774 PubMed DOI PMC

Han Y., Zheleznyakova G. Y., Marincevic-Zuniga Y., Kakhki M. P., Raine A., Needhamsen M., et al. . (2021). Comparison of EM-seq and PBAT methylome library methods for low-input DNA. Epigenetics, 17, 1195-1204. doi: 10.1080/15592294.2021.1997406 PubMed DOI PMC

Harrison A., Parle-McDermott A. (2011). DNA Methylation: a timeline of methods and applications. Front. Genet. 2. doi: 10.3389/fgene.2011.00074 PubMed DOI PMC

He X. J., Ma Z. Y., Liu Z. W. (2014). Non-coding RNA transcription RNA-directed DNA methylation Arabidopsis. Mol. Plant 7, 1406–1414. doi: 10.1093/mp/ssu075 PubMed DOI

He L., Zhao C., Zhang Q., Zinta G., Wang D., Lozano-Durán R., et al. . (2021). Pathway conversion enables a double-lock mechanism to maintain DNA methylation and genome stability. Proc. Natl. Acad. Sci. U. S. A. 118, e2107320118. doi: 10.1073/pnas.2107320118 PubMed DOI PMC

Head S. R., Komori H. K., LaMere S. A., Whisenant T., Van Nieuwerburgh F., Salomon D. R., et al. . (2014). Library construction for next-generation sequencing: overviews and challenges. Biotechniques 56, 61–77. doi: 10.2144/000114133 PubMed DOI PMC

Hébrard C., Peterson D. G., Willems G., Delaunay A., Jesson B., Lefèbvre M., et al. . (2016). Epigenomics and bolting tolerance in sugar beet genotypes. J. Exp. Bot. 67, 207–225. doi: 10.1093/jxb/erv449 PubMed DOI PMC

Heer K., Ullrich K. K., Hiss M., Liepelt S., Schulze Brüning R., Zhou J., et al. . (2018). Detection of somatic epigenetic variation in Norway spruce via targeted bisulfite sequencing. Ecol. Evol. 8, 9672–9682. doi: 10.1002/ece3.4374 PubMed DOI PMC

Henderson I. R., Chan S. R., Cao X., Johnson L., Jacobsen S. E. (2010). Accurate sodium bisulfite sequencing in plants. Epigenetics 5, 47–49. doi: 10.4161/epi.5.1.10560 PubMed DOI PMC

Hetzl J., Foerster A. M., Raidl G., Scheid O. M. (2007). CyMATE: a new tool for methylation analysis of plant genomic DNA after bisulphite sequencing. Plant J. 51, 526–536. doi: 10.1111/j.1365-313X.2007.03152.x PubMed DOI

Holmes E. E., Jung M., Meller S., Leisse A., Sailer V., Zech J., et al. . (2014). Performance evaluation of kits for bisulfite-conversion of DNA from tissues, cell lines, FFPE tissues, aspirates, lavages, effusions, plasma, serum, and urine. PloS One 9, e93933. doi: 10.1371/journal.pone.0093933 PubMed DOI PMC

Hoppers A., Williams L., Ponnaluri V. C., Sexton B., Saleh L., Campbell M., et al. . (2020). Enzymatic methyl-seq: next generation methylomes. J. Biomol. Tech. 31 (Suppl.), S15.

Hsu F. M., Wang C. J. R., Chen P. Y. (2018). Reduced representation bisulfite sequencing in maize. Bio-Protocol 8, e2778. doi: 10.21769/BioProtoc.2778 PubMed DOI PMC

Hsu F. M., Yen M. R., Wang C. T., Lin C. Y., Wang C. J. R., Chen P. Y. (2017). Optimized reduced representation bisulfite sequencing reveals tissue-specific mCHH islands in maize. Epigenet. Chromatin 10, 1–16. doi: 10.1186/s13072-017-0148-y PubMed DOI PMC

Ibáñez M. A., Alvarez-Mari A., Rodríguez-Sanz H., Kremer C., González-Benito M. E., Martín C. (2019). Genetic and epigenetic stability of recovered mint apices after several steps of a cryopreservation protocol by encapsulation-dehydration. a new approach for epigenetic analysis. Plant Physiol. Biochem. 143, 299–307. doi: 10.1016/j.plaphy.2019.08.026 PubMed DOI

Inácio V., Barros P. M., Costa A., Roussado C., Gonçalves E., Costa R., et al. . (2017). Differential DNA methylation patterns are related to phellogen origin and quality of Quercus suber cork. PloS One 12, e0169018. doi: 10.1371/journal.pone.0169018 PubMed DOI PMC

Inácio V., Martins M. T., Graça J., Morais-Cecílio L. (2018). Cork oak young and traumatic periderms show PCD typical chromatin patterns but different chromatin-modifying genes expression. Front. Plant Sci. 9. doi: 10.3389/fpls.2018.01194 PubMed DOI PMC

Irvine R. A., Lin I. G., Hsieh C. L. (2002). DNA Methylation has a local effect on transcription and histone acetylation. Mol. Cell. Biol. 22, 6689–6696. doi: 10.1128/MCB.22.19.6689-6696.2002 PubMed DOI PMC

Ito S., Shen L., Dai Q., Wu S. C., Collins L. B., Swenberg J. A., et al. . (2011). Tet proteins can convert 5-methylcytosine to 5-formylcytosine and 5-carboxylcytosine. Science 333, 1300–1303. doi: 10.1126/science.1210597 PubMed DOI PMC

Iwasaki M., Paszkowski J. (2014). Epigenetic memory in plants. EMBO J. 33, 1987–1998. doi: 10.15252/embj.201488883 PubMed DOI PMC

Jain M., Olsen H. E., Paten B., Akeson M. (2016). The Oxford nanopore MinION: delivery of nanopore sequencing to the genomics community. Genome Biol. 17, 1–11. doi: 10.1186/s13059-016-1103-0 PubMed DOI PMC

Jang H., Shin H., Eichman B. F., Huh J. H. (2014). Excision of 5-hydroxymethylcytosine by DEMETER family DNA glycosylases. Biochem. Biophys. Res. Commun. 446, 1067–1072. doi: 10.1016/j.bbrc.2014.03.060 PubMed DOI PMC

Johnson L. M., Du J., Hale C. J., Bischof S., Feng S., Chodavarapu R. K., et al. . (2014). SRA- and SET-domain-containing proteins link RNA polymerase V occupancy to DNA methylation. Nature 507, 124–128. doi: 10.1038/nature12931 PubMed DOI PMC

Kacmarczyk T. J., Fall M. P., Zhang X., Xin Y., Li Y., Alonso A., et al. . (2018). “Same difference”: comprehensive evaluation of four DNA methylation measurement platforms. Epigenet. Chromatin 11, 21. doi: 10.1186/s13072-018-0190-4 PubMed DOI PMC

Kalinka A., Achrem M. (2020). The distribution pattern of 5-methylcytosine in rye (Secale l.) chromosomes. PloS One 15, e0240869. doi: 10.1371/journal.pone.0240869 PubMed DOI PMC

Kankel M. W., Ramsey D. E., Stokes T. L., Flowers S. K., Haag J. R., Jeddeloh J. A., et al. . (2003). Arabidopsis MET1 cytosine methyltransferase mutants. Genetics 163, 1109–1122. doi: 10.1093/genetics/163.3.1109 PubMed DOI PMC

Kint S., De Spiegelaere W., De Kesel J., Vandekerckhove L., Van Criekinge W. (2018). Evaluation of bisulfite kits for DNA methylation profiling in terms of DNA fragmentation and DNA recovery using digital PCR. PloS One 13 (6), e0199091. doi: 10.1371/journal.pone.0199091 PubMed DOI PMC

Komivi D., Marie A. M., Rong Z., Qi Z., Mei Y., Ndiaga C., et al. . (2018). The contrasting response to drought and waterlogging is underpinned by divergent DNA methylation programs associated with transcript accumulation in sesame. Plant Sci. 277, 207–217. doi: 10.1016/j.plantsci.2018.09.012 PubMed DOI

Kooke R., Johannes F., Wardenaar R., Becker F., Etcheverry M., Colot V., et al. . (2015). Epigenetic basis of morphological variation and phenotypic plasticity in Arabidopsis thaliana . Plant Cell 27, 337–348. doi: 10.1105/tpc.114.133025 PubMed DOI PMC

Kosciuk T., Wang M., Hong J. Y., Lin H. (2019). Updates on the epigenetic roles of sirtuins. Curr. Opin. Chem. Biol. 51, 18–29. doi: 10.1016/j.cbpa.2019.01.023 PubMed DOI PMC

Kovacova V., Janousek B. (2012). Bisprimer - a program for the design of primers for bisulfite-based genomic sequencing of both plant and mammalian DNA samples. J. Hered. 103, 308–312. doi: 10.1093/jhered/esr137 PubMed DOI

Kovařík A., Koukalova B., Holý A., Bezdk M. (1994). Sequence-specific hypomethylation of the tobacco genome induced with dihydroxypropyladenine, ethionine and 5-azacytidine. FEBS Lett. 353, 309–311. doi: 10.1016/0014-5793(94)01048-x PubMed DOI

Kozarewa I., Armisen J., Gardner A. F., Slatko B. E., Hendrickson C. L. (2015). Overview of target enrichment strategies. Curr. Protoc. Mol. Biol. 112, 7–21. doi: 10.1002/0471142727.mb0721s112 PubMed DOI

Kumar S., Mohapatra T. (2021). Dynamics of DNA methylation and its functions in plant growth and development. Front. Plant Sci. 12. doi: 10.3389/fpls.2021.596236 PubMed DOI PMC

Kumar G., Rattan U. K., Singh A. K. (2016). Chilling-mediated DNA methylation changes during dormancy and its release reveal the importance of epigenetic regulation during winter dormancy in apple (Malus x domestica borkh.). PloS One 11, e0149934. doi: 10.1371/journal.pone.0149934 PubMed DOI PMC

Kuo K. C., Mccune R. A., Gehrke C. W., Midgett R., Ehrlich M. (1980). Quantitative reversed-phase high performance liquid chromatographic determination of major and modified deoxyribonucleosides in DNA. Nucleic Acids Res. 8, 4763–4776. doi: 10.1093/nar/8.20.4763 PubMed DOI PMC

Kurata N., Yamazaki Y. (2006). Oryzabase. an integrated biological and genome information database for rice. Plant Physiol. 140, 12–17. doi: 10.1104/pp.105.063008 PubMed DOI PMC

Kurowska M., Daszkowska-Golec A., Gruszka D., Marzec M., Szurman M., Szarejko I., et al. . (2011). TILLING: a shortcut in functional genomics. J. Appl. Genet. 52, 371–390. doi: 10.1007/s13353-011-0061-1 PubMed DOI PMC

Lacks S., Greenberg B. (1975). A deoxyribonuclease of Diplococcus pneumoniae specific for methylated DNA. J. Biol. Chem. 250, 4060–4066. doi: 10.1016/S0021-9258(19)41386-0 PubMed DOI

Lafon-Placette C., Faivre-Rampant P., Delaunay A., Street N., Brignolas F., Maury S. (2013). Methylome of DNase I sensitive chromatin in Populus trichocarpa shoot apical meristematic cells: a simplified approach revealing characteristics of gene-body DNA methylation in open chromatin state. New Phytol. 197, 416–430. doi: 10.1111/nph.12026 PubMed DOI

Lafon-Placette C., Le Gac A. L., Chauveau D., Segura V., Delaunay A., Lesage-Descauses M. C., et al. . (2018). Changes in the epigenome and transcriptome of the poplar shoot apical meristem in response to water availability affect preferentially hormone pathways. J. Exp. Bot. 69, 537–551. doi: 10.1093/jxb/erx409 PubMed DOI

Laird C. D., Pleasant N. D., Clark A. D., Sneeden J. L., Hassan K. M., Manley N. C., et al. . (2004). Hairpin-bisulfite PCR: assessing epigenetic methylation patterns on complementary strands of individual DNA molecules. Proc. Natl. Acad. Sci. U. S. A. 101, 204–209. doi: 10.1073/pnas.2536758100 PubMed DOI PMC

Latzel V., Rendina González A. P., Rosenthal J. (2016). Epigenetic memory as a basis for intelligent behavior in clonal plants. Front. Plant Sci. 7. doi: 10.3389/fpls.2016.01354 PubMed DOI PMC

Law J. A., Jacobsen S. E. (2010). Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nat. Rev. Genet. 11, 204–220. doi: 10.1038/nrg2719 PubMed DOI PMC

Lee S. C., Ernst E., Berube B., Borges F., Parent J. S., Ledon P., et al. . (2020). Arabidopsis retrotransposon virus-like particles and their regulation by epigenetically activated small RNA. Genome Res. 30, 576–588. doi: 10.1101/gr.259044.119 PubMed DOI PMC

Lee E. J., Pei L., Srivastava G., Joshi T., Kushwaha G., Choi J. H., et al. . (2011). Targeted bisulfite sequencing by solution hybrid selection and massively parallel sequencing. Nucleic Acids Res. 39, e127–e127. doi: 10.1093/nar/gkr598 PubMed DOI PMC

Lele L., Ning D., Cuiping P., Xiao G., Weihua G. (2018). Genetic and epigenetic variations associated with adaptation to heterogeneous habitat conditions in a deciduous shrub. Ecol. Evol. 8, 2594–2606. doi: 10.1002/ece3.3868 PubMed DOI PMC

Lephatsi M., Nephali L., Meyer V., Piater L. A., Buthelezi N., Dubery I. A., et al. . (2022). Molecular mechanisms associated with microbial biostimulant-mediated growth enhancement, priming and drought stress tolerance in maize plants. Sci. Rep. 12, 10450. doi: 10.1038/s41598-022-14570-7 PubMed DOI PMC

Levene M. J., Korlach J., Turner S. W., Foquet M., Craighead H. G., Webb W. W. (2003). Zero-mode waveguides for single-molecule analysis at high concentrations. Science 299, 682–686. doi: 10.1126/science.1079700 PubMed DOI

Li B., Cai H., Liu K., An B., Wang R., Yang F., et al. . (2022). DNA Methylation alterations and their association with high temperature tolerance in rice anthesis. J. Plant Growth Regul., 42, 780-794. doi: 10.1007/s00344-022-10586-5 DOI

Li Q., Eichten S. R., Hermanson P. J., Zaunbrecher V. M., Song J., Wendt J., et al. . (2014). Genetic perturbation of the maize methylome. Plant Cell 26, 4602–4616. doi: 10.1105/tpc.114.133140 PubMed DOI PMC

Li R., Hu F., Li B., Zhang Y., Chen M., Fan T., et al. . (2020). Whole genome bisulfite sequencing methylome analysis of mulberry (Morus alba) reveals epigenome modifications in response to drought stress. Sci. Rep. 10, 1–17. doi: 10.1038/s41598-020-64975-5 PubMed DOI PMC

Li Z., Liu Z., Chen R., Li X., Tai P., Gong Z., et al. . (2015. b). DNA Damage and genetic methylation changes caused by cd in arabidopsis thaliana seedlings. Environ. Toxicol. Chem. 34, 2095–2103. doi: 10.1002/etc.3033 PubMed DOI

Li Q., Suzuki M., Wendt J., Patterson N., Eichten S. R., Hermanson P. J., et al. . (2015. a). Post-conversion targeted capture of modified cytosines in mammalian and plant genomes. Nucleic Acids Res. 43, e81–e81. doi: 10.1093/nar/gkv244 PubMed DOI PMC

Li H., Tahir ul Qamar M., Yang L., Liang J., You J., Wang L. (2023). Current progress, applications and challenges of multi-omics approaches in sesame genetic improvement. Int. J. Mol. Sci. 24, 3105. doi: 10.3390/ijms24043105 PubMed DOI PMC

Li S., Xia Q., Wang F., Yu X., Ma J., Kou H., et al. . (2017). Laser irradiation-induced DNA methylation changes are heritable and accompanied with transpositional activation of mPing in rice. Front. Plant Sci. 8. doi: 10.3389/fpls.2017.00363 PubMed DOI PMC

Liang Z., Shen L., Cui X., Bao S., Geng Y., Yu G., et al. . (2018). DNA N6-adenine methylation in Arabidopsis thaliana. dev. Cell 45, 406–416. doi: 10.1016/j.devcel.2018.03.012 PubMed DOI

Liang D., Zhang Z., Wu H., Huang C., Shuai P., Ye C. Y., et al. . (2014). Single-base-resolution methylomes of Populus trichocarpa reveal the association between DNA methylation and drought stress. BMC Genet. 15, 1–11. doi: 10.1186/1471-2156-15-S1-S9 PubMed DOI PMC

Lira-Medeiros C. F., Parisod C., Fernandes R. A., Mata C. S., Cardoso M. A., Ferreira P. C. G. (2010). Epigenetic variation in mangrove plants occurring in contrasting natural environment. PloS One 5, e10326. doi: 10.1371/journal.pone.0010326 PubMed DOI PMC

Lister R., O’Malley R. C., Tonti-Filippini J., Gregory B. D., Berry C. C., Millar A. H., et al. . (2008). Highly integrated single-base resolution maps of the epigenome in Arabidopsis . Cell 133, 523–536. doi: 10.1016/j.cell.2008.03.029 PubMed DOI PMC

Liu S., Dunwell T. L., Pfeifer G. P., Dunwell J. M., Ullah I., Wang Y. (2013). Detection of oxidation products of 5-methyl-2’-deoxycytidine in Arabidopsis DNA. PloS One 8, e84620. doi: 10.1371/journal.pone.0084620 PubMed DOI PMC

Liu Q., Fang L., Yu G., Wang D., Xiao C. L., Wang K. (2019). Detection of DNA base modifications by deep recurrent neural network on Oxford nanopore sequencing data. Nat. Commun. 10, 2449. doi: 10.1038/s41467-019-10168-2 PubMed DOI PMC

Liu C. H., Finke A., Díaz M., Rozhon W., Poppenberger B., Baubec T., et al. . (2015). Repair of DNA damage induced by the cytidine analog zebularine requires ATR and ATM in Arabidopsis . Plant Cell 27, 1788–1800. doi: 10.1105/tpc.114.135467 PubMed DOI PMC

Liu W., Gallego-Bartolomé J., Zhou Y., Zhong Z., Wang M., Wongpalee S. P., et al. . (2021). Ectopic targeting of CG DNA methylation in Arabidopsis with the bacterial SssI methyltransferase. Nat. Commun. 12, 3130. doi: 10.1038/s41467-021-23346-y PubMed DOI PMC

Liu T., Li Y., Duan W., Huang F., Hou X. (2017). Cold acclimation alters DNA methylation patterns and confers tolerance to heat and increases growth rate in brassica rapa. J. Exp. Bot. 68, 1213–1224. doi: 10.1093/jxb/erw496 PubMed DOI PMC

Liu Y., Rosikiewicz W., Pan Z., Jillette N., Wang P., Taghbalout A., et al. . (2021). DNA Methylation-calling tools for Oxford nanopore sequencing: a survey and human epigenome-wide evaluation. Genome Biol. 22, 295. doi: 10.1186/s13059-021-02510-z PubMed DOI PMC

Liu G., Xia Y., Liu T., Dai S., Hou X. (2018). The DNA methylome and association of differentially methylated regions with differential gene expression during heat stress in Brassica rapa . Int. J. Mol. Sci. 19, 1414. doi: 10.3390/ijms19051414 PubMed DOI PMC

Lu X., Liu J., Ren W., Yang Q., Chai Z., Chen R., et al. . (2018). Gene-indexed mutations in maize. Mol. Plant 11, 496–504. doi: 10.1016/j.molp.2017.11.013 PubMed DOI

Lucibelli F., Valoroso M. C., Aceto S. (2022). Plant DNA methylation: an epigenetic mark in development, environmental interactions, and evolution. Int. J. Mol. Sci. 23, 8299. doi: 10.3390/ijms23158299 PubMed DOI PMC

Lupo V., Van Vlierberghe M., Vanderschuren H., Kerff F., Baurain D., Cornet L. (2021). Contamination in reference sequence databases: time for divide-and-rule tactics. Front. Microbiol. 12. doi: 10.3389/fmicb.2021.755101 PubMed DOI PMC

Ma K., Sun L., Cheng T., Pan H., Wang J., Zhang Q. (2018). Epigenetic variance, performing cooperative structure with genetics, is associated with leaf shape traits in widely distributed populations of ornamental tree Prunus mume . Front. Plant Sci. 9. doi: 10.3389/fpls.2018.00041 PubMed DOI PMC

Madlung A., Tyagi A. P., Watson B., Jiang H., Kagochi T., Doerge R., et al. . (2005). Genomic changes in synthetic Arabidopsis polyploids. Plant J. 41, 221–230. doi: 10.1111/j.1365-313X.2004.02297.x PubMed DOI

Mahmood A. M., Dunwell J. M. (2019). Evidence for novel epigenetic marks within plants. AIMS Genet. 6, 70–87. doi: 10.3934/genet.2019.4.70 PubMed DOI PMC

Malinowska M., Nagy I., Wagemaker C. A., Ruud A. K., Svane S. F., Thorup-Kristensen K., et al. . (2020). The cytosine methylation landscape of spring barley revealed by a new reduced representation bisulfite sequencing pipeline, WellMeth. Plant Genome 13 (3), 1–18,article e20049. doi: 10.1002/tpg2.20049 PubMed DOI

Marconi G., Pace R., Traini A., Raggi L., Lutts S., Chiusano M., et al. . (2013). Use of MSAP markers to analyse the effects of salt stress on DNA methylation in rapeseed (Brassica napus var. oleifera). PloS One 8, e75597. doi: 10.1371/journal.pone.0075597 PubMed DOI PMC

Marfil C., Ibañez V., Alonso R., Varela A., Bottini R., Masuelli R., et al. . (2019). Changes in grapevine DNA methylation and polyphenols content induced by solar ultraviolet-b radiation, water deficit and abscisic acid spray treatments. Plant Physiol. Biochem. 135, 287–294. doi: 10.1016/j.plaphy.2018.12.021 PubMed DOI

McInroy G. R., Beraldi D., Raiber E. A., Modrzynska K., van Delft P., Billker O., et al. . (2016). Enhanced methylation analysis by recovery of unsequenceable fragments. PloS One 11, e0152322. doi: 10.1371/journal.pone.0152322 PubMed DOI PMC

Meijón M., Valledor L., Santamaría E., Testillano P. S., Risueño M. C., Rodríguez R., et al. . (2009). Epigenetic characterization of the vegetative and floral stages of azalea buds: dynamics of DNA methylation and histone H4 acetylation. J. Plant Physiol. 166, 1624–1636. doi: 10.1016/j.jplph.2009.04.014 PubMed DOI

Meissner A., Gnirke A., Bell G. W., Ramsahoye B., Lander E. S., Jaenisch R. (2005). Reduced representation bisulfite sequencing for comparative high-resolution DNA methylation analysis. Nucleic Acids Res. 33, 5868–5877. doi: 10.1093/nar/gki901 PubMed DOI PMC

Miga K. H., Koren S., Rhie A., Vollger M. R., Gershman A., Bzikadze A., et al. . (2020). Telomere-to-telomere assembly of a complete human X chromosome. Nature 585, 79–84. doi: 10.1038/s41586-020-2547-7 PubMed DOI PMC

Miryeganeh M., Marlétaz F., Gavriouchkina D., Saze H. (2022). De novo genome assembly and in natura epigenomics reveal salinity-induced DNA methylation in the mangrove tree Bruguiera gymnorhiza . New Phytol. 233, 2094–2110. doi: 10.1111/nph.17738 PubMed DOI PMC

Miryeganeh M., Saze H. (2020). Epigenetic inheritance and plant evolution. Popul. Ecol. 62, 17–27. doi: 10.1002/1438-390X.12018 DOI

Moricová P., Ondřej V., Navrátilová B., Luhová L. (2013). Changes of DNA methylation and hydroxymethylation in plant protoplast cultures. Acta Biochim. Pol. 60, 33–36. doi: 10.18388/abp.2013_1947 PubMed DOI

Morselli M., Farrell C., Rubbi L., Fehling H. L., Henkhaus R., Pellegrini M. (2021). Targeted bisulfite sequencing for biomarker discovery. Methods 187, 13–27. doi: 10.1016/j.ymeth.2020.07.006 PubMed DOI PMC

Mounger J., Ainouche M. L., Bossdorf O., Cavé-Radet A., Li B., Parepa M., et al. . (2021). Epigenetics and the success of invasive plants. Philos. Trans. R. Soc B 376, 20200117. doi: 10.1098/rstb.2020.0117 PubMed DOI PMC

Muyle A. M., Seymour D. K., Lv Y., Huettel B., Gaut B. S. (2022). Gene body methylation in plants: mechanisms, functions, and important implications for understanding evolutionary processes. Genome Biol. Evol. 14, evac038. doi: 10.1093/gbe/evac038 PubMed DOI PMC

Ni P., Huang N., Nie F., Zhang J., Zhang Z., Wu B., et al. . (2021). Genome-wide detection of cytosine methylations in plant from nanopore data using deep learning. Nat. Commun. 12, 5976. doi: 10.1038/s41467-021-26278-9 PubMed DOI PMC

Ni P., Huang N., Zhang Z., Wang D. P., Liang F., Miao Y., et al. . (2019). DeepSignal: detecting DNA methylation state from nanopore sequencing reads using deep-learning. Bioinformatics 35, 4586–4595. doi: 10.1093/bioinformatics/btz276 PubMed DOI

Ni P., Xu J., Zhong Z., Zhang J., Huang N., Nie F., et al. . (2022). DNA 5-methylcytosine detection and methylation phasing using PacBio circular consensus sequencing. bioRxiv, 482074. doi: 10.1101/2022.02.26.482074 PubMed DOI PMC

Niederhuth C. E., Bewick A. J., Ji L., Alabady M. S., Kim K. D., Li Q., et al. . (2016). Widespread natural variation of DNA methylation within angiosperms. Genome Biol. 17, 1–19. doi: 10.1186/s13059-016-1059-0 PubMed DOI PMC

Ning Y. Q., Liu N., Lan K. K., Su Y. N., Li L., Chen S., et al. . (2020). DREAM complex suppresses DNA methylation maintenance genes and precludes DNA hypermethylation. Nat. Plants 6, 942–956. doi: 10.1038/s41477-020-0710-7 PubMed DOI

Nowicka A., Tokarz B., Zwyrtková J., Dvořák Tomaštíková E., Procházková K., Ercan U., et al. . (2020). Comparative analysis of epigenetic inhibitors reveals different degrees of interference with transcriptional gene silencing and induction of DNA damage. Plant J. 102, 68–84. doi: 10.1111/tpj.14612 PubMed DOI

Olova N., Krueger F., Andrews S., Oxley D., Berrens R. V., Branco M. R., et al. . (2018). Comparison of whole-genome bisulfite sequencing library preparation strategies identifies sources of biases affecting DNA methylation data. Genome Biol. 19, 1–19. doi: 10.1186/s13059-018-1408-2 PubMed DOI PMC

Ortega-Galisteo A. P., Morales-Ruiz T., Ariza R. R., Roldán-Arjona T. (2008). Arabidopsis DEMETER-LIKE proteins DML2 and DML3 are required for appropriate distribution of DNA methylation marks. Plant Mol. Biol. 67, 671–681. doi: 10.1007/s11103-008-9346-0 PubMed DOI

Papikian A., Liu W., Gallego-Bartolomé J., Jacobsen S. E. (2019). Site-specific manipulation of Arabidopsis loci using CRISPR-Cas9 SunTag systems. Nat. Commun. 10, 1–11. doi: 10.1038/s41467-019-08736-7 PubMed DOI PMC

Paun O., Verhoeven K. J. F., Richards C. L. (2019). Opportunities and limitations of reduced representation bisulfite sequencing in plant ecological epigenomics. New Phytol. 221, 738–742. doi: 10.1111/nph.15388 PubMed DOI PMC

Pečinka A., Liu C. H. (2014). Drugs for plant chromosome and chromatin research. Cytogenet. Genome Res. 143, 51–59. doi: 10.1159/000360774 PubMed DOI

Penterman J., Zilberman D., Huh J. H., Ballinger T., Henikoff S., Fischer R. L. (2007). DNA Demethylation in the Arabidopsis genome. Proc. Natl. Acad. Sci. U.S.A. 104, 6752–6757. doi: 10.1073/pnas.0701861104 PubMed DOI PMC

Pérez M., Viejo M., LaCuesta M., Toorop P., Cañal M. J. (2015). Epigenetic and hormonal profile during maturation of Quercus suber l. somatic embryos. J. Plant Physiol. 173, 51–61. doi: 10.1016/j.jplph.2014.07.028 PubMed DOI

Pfaffeneder T., Hackner B., Truß M., Münzel M., Müller M., Deiml C. A., et al. . (2011). The discovery of 5-formylcytosine in embryonic stem cell DNA. Angew. Chem. Int. Ed. 50, 7008–7012. doi: 10.1002/anie.201103899 PubMed DOI

Pikaard C. S., Scheid O. M. (2014). Epigenetic regulation in plants. Cold Spring Harb. Perspect. Biol. 6, a019315. doi: 10.1101/cshperspect.a019315 PubMed DOI PMC

Podevin N., Davies H. V., Hartung F., Nogué F., Casacuberta J. M. (2013). Site-directed nucleases: a paradigm shift in predictable, knowledge-based plant breeding. Trends Biotechnol. 31, 375–383. doi: 10.1016/j.tibtech.2013.03.004 PubMed DOI

Přibylová A., Čermák V., Tyč D., Fischer L. (2019). Detailed insight into the dynamics of the initial phases of de novo RNA-directed DNA methylation in plant cells. Epigenet. Chromatin 12, 1–14. doi: 10.1186/s13072-019-0299-0 PubMed DOI PMC

Prochazkova K., Finke A., Tomaštíková E. D., Filo J., Bente H., Dvořák P., et al. . (2022). Zebularine induces enzymatic DNA-protein crosslinks in 45S rDNA heterochromatin of Arabidopsis nuclei. Nucleic Acids Res. 50, 244–258. doi: 10.1093/nar/gkab1218 PubMed DOI PMC

Raiber E. A., Hardisty R., van Delft P., Balasubramanian S. (2017). Mapping and elucidating the function of modified bases in DNA. Nat. Rev. Chem. 1, 69. doi: 10.1038/s41570-017-0069 DOI

Ramos M., Rocheta M., Carvalho L., Inácio V., Graça J., Morais-Cecilio L. (2013). Expression of DNA methyltransferases is involved in Quercus suber cork quality. Tree Genet. Genomes 9, 1481–1492. doi: 10.1007/s11295-013-0652-6 DOI

Regulski M., Lu Z., Kendall J., Donoghue M. T., Reinders J., Llaca V., et al. . (2013). The maize methylome influences mRNA splice sites and reveals widespread paramutation-like switches guided by small RNA. Genome Res. 23, 1651–1662. doi: 10.1101/gr.153510.112 PubMed DOI PMC

Reyna-López G. E., Simpson J., Ruiz-Herrera J. (1997). Differences in DNA methylation patterns are detectable during the dimorphic transition of fungi by amplification of restriction polymorphisms. Mol. Gen. Genet. 253, 703–710. doi: 10.1007/s004380050374 PubMed DOI

Rhoads A., Au K. F. (2015). PacBio sequencing and its applications. GPB 13, 278–289. doi: 10.1016/j.gpb.2015.08.002 PubMed DOI PMC

Ribeiro T., Viegas W., Morais-Cecílio L. (2009). Epigenetic marks in the mature pollen of Quercus suber l. (Fagaceae). Sex Plant Reprod. 22, 1–7. doi: 10.1007/s00497-008-0083-y PubMed DOI

Rodríguez J. L., Valledor L., Hasbún R., Sánchez P., Rodríguez R., Cañal M. J. (2016). The effects of hormone treatment on epigenetic marks during organogenesis in Pinus radiata d. don embryos. J. Plant Growth Regul. 35, 97–108. doi: 10.1007/s00344-015-9510-0 DOI

Rodríguez-Sanz H., Manzanera J. A., Solís M. T., Gómez-Garay A., Pintos B., Risueño M. C., et al. . (2014. a). Early markers are present in both embryogenesis pathways from microspores and immature zygotic embryos in cork oak, Quercus suber l. BMC Plant Biol. 14, 1–18. doi: 10.1186/s12870-014-0224-4 PubMed DOI PMC

Rodríguez-Sanz H., Moreno-Romero J., Solís M. T., Köhler C., Risueño M. C., Testillano P. S. (2014. b). Changes in histone methylation and acetylation during microspore reprogramming to embryogenesis occur concomitantly with BnHKMT and BnHAT expression and are associated with cell totipotency, proliferation, and differentiation in Brassica napus . Cytogenet. Genome Res. 143, 209–218. doi: 10.1159/000365261 PubMed DOI

Roje S. (2006). S-Adenosyl-L-methionine: beyond the universal methyl group donor. Phytochemistry 67, 1686–1698. doi: 10.1016/j.phytochem.2006.04.019 PubMed DOI

Rosenberg E., Zilber-Rosenberg I. (2018). The hologenome concept of evolution after 10 years. Microbiome 6, 78. doi: 10.1186/s40168-018-0457-9 PubMed DOI PMC

Saez-Laguna E., Guevara M. A., Diaz L. M., Sanchez-Gomez D., Collada C., Aranda I., et al. . (2014). Epigenetic variability in the genetically uniform forest tree species Pinus pinea l. PloS One 9, e103145. doi: 10.1371/journal.pone.0103145 PubMed DOI PMC

Saito T., Ariizumi T., Okabe Y., Asamizu E., Hiwasa-Tanase K., Fukuda N., et al. . (2011). TOMATOMA: a novel tomato mutant database distributing micro-tom mutant collections. Plant Cell Physiol. 52, 283–296. doi: 10.1093/pcp/pcr004 PubMed DOI PMC

Santamaría M., Hasbún R., Valera M., Meijón M., Valledor L., Rodríguez J. L., et al. . (2009). Acetylated H4 histone and genomic DNA methylation patterns during bud set and bud burst in Castanea sativa . J. Plant Physiol. 166, 1360–1369. doi: 10.1016/j.jplph.2009.02.014 PubMed DOI

Saze H., Kitayama J., Takashima K., Miura S., Harukawa Y., Ito T., et al. . (2013). Mechanism for full-length RNA processing of Arabidopsis genes containing intragenic heterochromatin. Nat. Commun. 4, 2301. doi: 10.1038/ncomms3301 PubMed DOI

Schmidt M., Van Bel M., Woloszynska M., Slabbinck B., Martens C., De Block M., et al. . (2017). Plant-RRBS, a bisulfite and next-generation sequencing-based methylome profiling method enriching for coverage of cytosine positions. BMC Plant Biol. 17, 115. doi: 10.1186/s12870-017-1070-y PubMed DOI PMC

Schmitz R. J., Lewis Z. A., Goll M. G. (2019). DNA Methylation: shared and divergent features across eukaryotes. Trends Genet. 35, 818–827. doi: 10.1016/j.tig.2019.07.007 PubMed DOI PMC

Schulz B., Eckstein R. L., Durka W. (2013). Scoring and analysis of methylation-sensitive amplification polymorphisms for epigenetic population studies. Mol. Ecol. Resour. 13, 642–653. doi: 10.1111/1755-0998.12100 PubMed DOI

Selberg S., Blokhina D., Aatonen M., Koivisto P., Siltanen A., Mervaala E., et al. . (2019). Discovery of small molecules that activate RNA methylation through cooperative binding to the METTL3-14-WTAP complex active site. Cell Rep. 26, 3762–3771. doi: 10.1016/j.celrep.2019.02.100 PubMed DOI

She W., Baroux C., Grossniklaus U. (2018). “Cell-type specific chromatin analysis in whole-mount plant tissues by immunostaining,” in Plant chromatin dynamics: methods and protocols, vol. 1675 . Eds. Bemer M., Baroux C. (New York, NY: Humana Press; ), 443–454. doi: 10.1007/978-1-4939-7318-7_25 PubMed DOI

Silva A. C., Ruiz-Ferrer V., Müller S. Y., Pellegrin C., Abril-Urías P., Martínez-Gómez Á., et al. . (2022). The DNA methylation landscape of the root-knot nematode-induced pseudo-organ, the gall, in Arabidopsis, is dynamic, contrasting over time, and critically important for successful parasitism. New Phytol. 236, 1888–1907. doi: 10.1111/nph.18395 PubMed DOI PMC

Simpson J. T., Workman R. E., Zuzarte P. C., David M., Dursi L. J., Timp W. (2017). Detecting DNA cytosine methylation using nanopore sequencing. Nat. Methods 14, 407–410. doi: 10.1038/nmeth.4184 PubMed DOI

Singh R. R. (2022). Target enrichment approaches for next-generation sequencing applications in oncology. Diagnostics 12, 1539. doi: 10.3390/diagnostics12071539 PubMed DOI PMC

Slotkin R. K., Martienssen R. (2007). Transposable elements and the epigenetic regulation of the genome. Nat. Rev. Genet. 8, 272–285. doi: 10.1038/nrg2072 PubMed DOI

Solís M. T., Chakrabarti N., Corredor E., Cortés-Eslava J., Rodríguez-Serrano M., Biggiogera M., et al. . (2014). Epigenetic changes accompany developmental programmed cell death in tapetum cells. Plant Cell Physiol. 55, 16–29. doi: 10.1093/pcp/pct152 PubMed DOI

Solís M. T., El-Tantawy A. A., Cano V., Risueño M. C., Testillano P. S. (2015). 5-azacytidine promotes microspore embryogenesis initiation by decreasing global DNA methylation, but prevents subsequent embryo development in rapeseed and barley. Front. Plant Sci. 6. doi: 10.3389/fpls.2015.00472 PubMed DOI PMC

Solís M. T., Rodríguez-Serrano M., Meijón M., Cañal M. J., Cifuentes A., Risueño M. C., et al. . (2012). DNA Methylation dynamics and MET1a-like gene expression changes during stress-induced pollen reprogramming to embryogenesis. J. Exp. Bot. 63, 6431–6444. doi: 10.1093/jxb/ers298 PubMed DOI PMC

Sood A. J., Viner C., Hoffman M. M. (2019). DNAmod: the DNA modification database. J. Cheminform. 11, 30. doi: 10.1186/s13321-019-0349-4 PubMed DOI PMC

Starczak M., Abakir A., Ruzov A., Gackowski D. (2022). “Detection and quantification of RNA modifications on RNA-DNA hybrids using SID-UPLC-MS/MS, in r-loops,” in Methods in molecular biology, vol. 2528 . Eds. Aguilera A., Ruzov A. (New York, NY: Humana Press; ), 127–143. doi: 10.1007/978-1-0716-2477-7_9 PubMed DOI

Stocks J. J., Metheringham C. L., Plumb W. J., Lee S. J., Kelly L. J., Nichols R. A., et al. . (2019). Genomic basis of European ash tree resistance to ash dieback fungus. Nat. Ecol. Evol. 3, 1686–1696. doi: 10.1038/s41559-019-1036-6 PubMed DOI PMC

Stoiber M., Quick J., Egan R., Lee J. E., Celniker S., Neely R. K., et al. . (2017). De novo identification of DNA modifications enabled by genome-guided nanopore signal processing. bioRxiv, 094672. doi: 10.1101/094672 DOI

Stroud H., Greenberg M. V., Feng S., Bernatavichute Y. V., Jacobsen S. E. (2013). Comprehensive analysis of silencing mutants reveals complex regulation of the Arabidopsis methylome. Cell 152, 352–364. doi: 10.1016/j.cell.2012.10.054 PubMed DOI PMC

Su Y., Bai X., Yang W., Wang W., Chen Z., Ma J., et al. . (2018). Single-base-resolution methylomes of Populus euphratica reveal the association between DNA methylation and salt stress. Tree Genet. Genomes 14, 1–11. doi: 10.1007/s11295-018-1298-1 DOI

Tadege M., Wen J., He J., Tu H., Kwak Y., Eschstruth A., et al. . (2008). Large Scale insertional mutagenesis using Tnt1 retrotransposon in the model legume Medicago truncatula . Plant J. 54, 335–347. doi: 10.1111/j.1365-313X.2008.03418.x PubMed DOI

Tadele Z. (2016). Mutagenesis and TILLING to dissect gene function in plants. Curr. Genomics 17, 499–508. doi: 10.2174/1389202917666160520104158 PubMed DOI PMC

Tahiliani M., Koh K. P., Shen Y., Pastor W. A., Bandukwala H., Brudno Y., et al. . (2009). Conversion of 5-methylcytosine to 5-hydroxymethylcytosine in mammalian DNA by MLL partner TET1. Science 324, 930–935. doi: 10.1126/science.1170116 PubMed DOI PMC

Takahashi S., Osabe K., Fukushima N., Takuno S., Miyaji N., Shimizu M., et al. . (2018). Genome-wide characterization of DNA methylation, small RNA expression, and histone H3 lysine nine di-methylation in Brassica rapa l. DNA Res. 25, 511–520. doi: 10.1093/dnares/dsy021 PubMed DOI PMC

Takuno S., Ran J. H., Gaut B. S. (2016). Evolutionary patterns of genic DNA methylation vary across land plants. Nat. Plants 2, 15222. doi: 10.1038/nplants.2015.222 PubMed DOI

Tanenbaum M. E., Gilbert L. A., Qi L. S., Weissman J. S., Vale R. D. (2014). A protein-tagging system for signal amplification in gene expression and fluorescence imaging. Cell 159, 635–646. doi: 10.1016/j.cell.2014.09.039 PubMed DOI PMC

Tang X. M., Tao X., Wang Y., Ma D. W., Li D., Yang H., et al. . (2014. a). Analysis of DNA methylation of perennial ryegrass under drought using the methylation-sensitive amplification polymorphism (MSAP) technique. Mol. Genet. Genomics 289, 1075–1084. doi: 10.1007/s00438-014-0869-6 PubMed DOI

Tang Y., Xiong J., Jiang H. P., Zheng S. J., Feng Y. Q., Yuan B. F. (2014. b). Determination of oxidation products of 5-methylcytosine in plants by chemical derivatization coupled with liquid chromatography/tandem mass spectrometry analysis. Anal. Chem. 86, 7764–7772. doi: 10.1021/ac5016886 PubMed DOI

Taudt A., Colomé-Tatché M., Johannes F. (2016). Genetic sources of population epigenomic variation. Nat. Rev. Genet. 17, 319–332. doi: 10.1038/nrg.2016.45 PubMed DOI

Terragni J., Bitinaite J., Zheng Y., Pradhan S. (2012). Biochemical characterization of recombinant β-glucosyltransferase and analysis of global 5-hydroxymethylcytosine in unique genomes. Biochemistry 51, 1009–1019. doi: 10.1021/bi2014739 PubMed DOI PMC

Tessadori F., Chupeau M. C., Chupeau Y., Knip M., Germann S., van Driel R., et al. . (2007). Large-Scale dissociation and sequential reassembly of pericentric heterochromatin in dedifferentiated Arabidopsis cells. J. Cell Sci. 120, 1200–1208. doi: 10.1242/jcs.000026 PubMed DOI

Testillano P. S., Risueño M. C. (2016). “Detection of epigenetic modifications during microspore embryogenesis: analysis of DNA methylation patterns dynamics,” in In vitro embryogenesis in higher plants. methods in molecular biology, vol. 1359 . Eds. Germana M., Lambardi M. (New York, NY: Humana Press; ), 491–502. doi: 10.1007/978-1-4939-3061-6_28 PubMed DOI

Testillano P. S., Solís M., Risueño M. C. (2013). The 5-methyl-deoxy-cytidine (5mdC) localization to reveal in situ the dynamics of DNA methylation chromatin pattern in a variety of plant organ and tissue cells during development. Physiol. Plant 149, 104–113. doi: 10.1111/ppl.12015 PubMed DOI

Tsaballa A., Sperdouli I., Avramidou E. V., Ganopoulos I., Koukounaras A., Ntinas G. K. (2022). Epigenetic and physiological responses to varying root-zone temperatures in greenhouse rocket. Genes 13, 364. doi: 10.3390/genes13020364 PubMed DOI PMC

Tse O. Y. O., Jiang P., Cheng S. H., Peng W., Shang H., Wong J., et al. . (2021). Genome-wide detection of cytosine methylation by single molecule real-time sequencing. Proc. Natl. Acad. Sci. U. S. A. 118, e2019768118. doi: 10.1073/pnas.2019768118 PubMed DOI PMC

Turcotte H., Hooker J., Samanfar B., Parent J. S. (2022). Can epigenetics guide the production of better adapted cultivars? Agronomy 12, 838. doi: 10.3390/agronomy12040838 DOI

Underwood C. J., Henderson I. R., Martienssen R. A. (2017). Genetic and epigenetic variation of transposable elements in Arabidopsis . Curr. Opin. Plant Biol. 36, 135–141. doi: 10.1016/j.pbi.2017.03.002 PubMed DOI PMC

Usai G., Mascagni F., Giordani T., Vangelisti A., Bosi E., Zuccolo A., et al. . (2020). Epigenetic patterns within the haplotype phased fig (Ficus carica l.) genome. Plant J. 102, 600–614. doi: 10.1111/tpj.14635 PubMed DOI

Uthup T. K., Karumamkandathil R., Ravindran M., Saha T. (2018). Heterografting induced DNA methylation polymorphisms in Hevea brasiliensis . Planta 248, 579–589. doi: 10.1007/s00425-018-2918-6 PubMed DOI

Vaisvila R., Ponnaluri V. C., Sun Z., Langhorst B. W., Saleh L., Guan S., et al. . (2021). Enzymatic methyl sequencing detects DNA methylation at single-base resolution from picograms of DNA. Genome Res. 31, 1280–1289. doi: 10.1101/gr.266551.120 PubMed DOI PMC

van der Graaf A., Wardenaar R., Neumann D. A., Taudt A., Shaw R. G., Jansen R. C., et al. . (2015). Rate, spectrum, and evolutionary dynamics of spontaneous epimutations. Proc. Natl. Acad. Sci. U. S. A. 112, 6676–6681. doi: 10.1073/pnas.1424254112 PubMed DOI PMC

van Esse G. W., Walla A., Finke A., Koornneef M., Pečinka A., Von Korff M. (2017). Six-rowed Spike3 (VRS3) is a histone demethylase that controls lateral spikelet development in barley. Plant Physiol. 174, 2397–2408. doi: 10.1104/pp.17.00108 PubMed DOI PMC

Vannier N., Mony C., Bittebière A. K., Vandenkoornhuyse P. (2015). Epigenetic mechanisms and microbiota as a toolbox for plant phenotypic adjustment to environment. Front. Plant Sci. 23. doi: 10.3389/fpls.2015.01159 PubMed DOI PMC

Varela A., Ibañez V. N., Alonso R., Zavallo D., Asurmendi S., Gomez Talquenca S., et al. . (2021). Vineyard environments influence Malbec grapevine phenotypic traits and DNA methylation patterns in a clone-dependent way. Plant Cell Rep. 40, 111–125. doi: 10.1007/s00299-020-02617-w PubMed DOI

Veley K. M., Okwuonu I., Jensen G., Yoder M., Taylor N. J., Meyers B. C., et al. . (2021). Gene tagging via CRISPR-mediated homology-directed repair in cassava. G3 11, jkab028. doi: 10.1093/g3journal/jkab028 PubMed DOI PMC

Ventouris Y. E., Tani E., Avramidou E. V., Abraham E. M., Chorianopoulou S. N., Vlachostergios D. N., et al. . (2020). Recurrent water deficit and epigenetic memory in Medicago sativa l. varieties. Appl. Sci. 10, 3110. doi: 10.3390/app10093110 DOI

Vial-Pradel S., Hasegawa Y., Nakagawa A., Miyaki S., Machida Y., Kojima S., et al. . (2019). SIMON: simple methods for analyzing DNA methylation by targeted bisulfite next-generation sequencing. Plant Biotechnol. (Tokyo) 36, 213–222. doi: 10.5511/plantbiotechnology.19.0822a PubMed DOI PMC

Vidalis A., Živković D., Wardenaar R., Roquis D., Tellier A., Johannes F., et al. . (2016). Methylome evolution in plants. Genome Biol. 17, 264–278. doi: 10.1186/s13059-016-1127-5 PubMed PMC

Vos P., Hogers R., Bleeker M., Reijans M., Lee T. V. D., Hornes M., et al. . (1995). AFLP: a new technique for DNA fingerprinting. Nucleic Acids Res. 23, 4407–4414. doi: 10.1093/nar/23.21.4407 PubMed DOI PMC

Waddington C. H. (1942). Canalization of development and the inheritance of acquired characters. Nature 150, 563–565. doi: 10.1038/150563a0 PubMed DOI

Wang X., Guo T., Wang S., Chen X., Chen Y., Yuan J., et al. . (2017). Determination of 5-hydroxymethyl-2′-deoxycytidine in rice by high-performance liquid chromatography-tandem mass spectrometry with isotope dilution. Anal. Lett. 50, 2351–2358. doi: 10.1080/00032719.2017.1286668 DOI

Wang Z., He Y. (2009). Effect of cryopreservation on the development and DNA methylation patterns of Arabidopsis thaliana . Life Sci. J. 6, 55–60. doi: 10.7537/marslsj060109.11 DOI

Wang W., Huang F., Qin Q., Zhao X., Li Z., Fu B. (2015. a). Comparative analysis of DNA methylation changes in two rice genotypes under salt stress and subsequent recovery. Biochem. Biophys. Res. Commun. 465, 790–796. doi: 10.1016/j.bbrc.2015.08.089 PubMed DOI

Wang M., Li H., Tang M., Yu F. (2022). DNA Methylation correlates with responses of experimental Hydrocotyle vulgaris populations to different flood regimes. Front. Plant Sci. 13. doi: 10.3389/fpls.2022.831175 PubMed DOI PMC

Wang N., Long T., Yao W., Xiong L., Zhang Q., Wu C. (2013). Mutant resources for the functional analysis of the rice genome. Mol. Plant 6, 596–604. doi: 10.1093/mp/sss142 PubMed DOI

Wang W. S., Pan Y. J., Zhao X. Q., Dwivedi D., Zhu L. H., Ali J., et al. . (2011). Drought-induced site-specific DNA methylation and its association with drought tolerance in rice (Oryza sativa l.). J. Exp. Bot. 62, 1951–1960. doi: 10.1093/jxb/erq391 PubMed DOI PMC

Wang X. L., Song S. H., Wu Y. S., Li Y. L., Chen T. T., Huang Z. Y., et al. . (2015. b). Genome-wide mapping of 5-hydroxymethylcytosine in three rice cultivars reveals its preferential localization in transcriptionally silent transposable element genes. J. Exp. Bot. 66, 6651–6663. doi: 10.1093/jxb/erv372 PubMed DOI PMC

Wang B., Zhang M., Fu R., Qian X., Rong P., Zhang Y., et al. . (2016). Epigenetic mechanisms of salt tolerance and heterosis in upland cotton (Gossypium hirsutum l.) revealed by methylation-sensitive amplified polymorphism analysis. Euphytica 208, 477–491. doi: 10.1007/s10681-015-1586-x DOI

Wardenaar R., Liu H., Colot V., Colomé-Tatché M., Johannes F. (2013). “Evaluation of MeDIP-chip in the context of whole-genome bisulfite sequencing (WGBS-seq) in arabidopsis,” in Tiling arrays. methods in molecular biology, vol. 1067 . Eds. Lee T. L., Shui Luk A. C. (Totowa, NJ: Humana Press; ), 203–224. doi: 10.1007/978-1-62703-607-8_13 PubMed DOI

Wendt J., Rosenbaum H., Richmond T. A., Jeddeloh J. A., Burgess D. L. (2018). “Targeted bisulfite sequencing using the SeqCap epi enrichment system,” in DNA Methylation protocols. methods in molecular biology, vol. 1708 . Ed. Tost J. (New York, NY: Humana Press; ), 383–405. doi: 10.1007/978-1-4939-7481-8_20 PubMed DOI

Wenger A. M., Peluso P., Rowell W. J., Chang P. C., Hall R. J., Concepcion G. T. (2019). “Accurate circular consensus long-read sequencing improves variant detection and assembly of a human genome.,” Nat. Biotechnol., 37, 1155-1162. doi: 10.1038/s41587-019-0217-9 PubMed PMC

White L. K., Hesselberth J. R. (2022). Modification mapping by nanopore sequencing. Front. Genet. 13. doi: 10.3389/fgene.2022.1037134 PubMed DOI PMC

Wu R., Wang X., Lin Y., Ma Y., Liu G., Yu X., et al. . (2013). Inter-species grafting caused extensive and heritable alterations of DNA methylation in Solanaceae plants. PloS One 8, e61995. doi: 10.1371/journal.pone.0061995 PubMed DOI PMC

Wu S. C., Zhang Y. (2010). Active DNA demethylation: many roads lead to Rome. Nat. Rev. Mol. Cell Biol. 11, 607–620. doi: 10.1038/nrm2950 PubMed DOI PMC

Xanthopoulou A., Tsaballa A., Ganopoulos I., Kapazoglou A., Avramidou E., Aravanopoulos F. A., et al. . (2019). Intra-species grafting induces epigenetic and metabolic changes accompanied by alterations in fruit size and shape of Cucurbita pepo l. Plant Growth Regul. 87, 93–108. doi: 10.1007/s10725-018-0456-7 DOI

Xie H., Konate M., Sai N., Tesfamicael K. G., Cavagnaro T., Gilliham M., et al. . (2017). Global DNA methylation patterns can play a role in defining terroir in grapevine (Vitis vinifera cv. Shiraz). Front. Plant Sci. 8. doi: 10.3389/fpls.2017.01860 PubMed DOI PMC

Xiong L. Z., Xu C. G., Maroof M. A. S., Zhang Q. (1999). Patterns of cytosine methylation in an elite rice hybrid and its parental lines, detected by a methylation-sensitive amplification polymorphism technique. Mol. Gen. Genet. 261, 439–446. doi: 10.1007/s004380050986 PubMed DOI

Xiong J., Ye T. T., Ma C. J., Cheng Q. Y., Yuan B. F., Feng Y. Q. (2019). N6 -hydroxymethyladenine: a hydroxylation derivative of N6 -methyladenine in genomic DNA of mammals. Nucleic Acids Res. 47, 1268–1277. doi: 10.1093/nar/gky1218 PubMed DOI PMC

Xu J., Chen G., Hermanson P. J., Xu Q., Sun C., Chen W., et al. . (2019). Population-level analysis reveals the widespread occurrence and phenotypic consequence of DNA methylation variation not tagged by genetic variation in maize. Genome Biol. 20, 1–16. doi: 10.1186/s13059-019-1859-0 PubMed DOI PMC

Yakovlev I. A., Gackowski D., Abakir A., Viejo M., Ruzov A., Olinski R., et al. . (2019). Mass spectrometry reveals the presence of specific set of epigenetic DNA modifications in the Norway spruce genome. Sci. Rep. 9, 19314. doi: 10.1038/s41598-019-55826-z PubMed DOI PMC

Yang F., Zhang L., Li J., Huang J., Wen R., Ma L., et al. . (2010). Trichostatin a and 5-azacytidine both cause an increase in global histone H4 acetylation and a decrease in global DNA and H3K9 methylation during mitosis in maize. BMC Plant Biol. 10, 1–11. doi: 10.1186/1471-2229-10-178 PubMed DOI PMC

Yao Q., Song C. X., He C., Kumaran D., Dunn J. J. (2012). Heterologous expression and purification of Arabidopsis thaliana VIM1 protein: In vitro evidence for its inability to recognize hydroxymethylcytosine, a rare base in Arabidopsis DNA. Protein Expr. Purif. 83, 104–111. doi: 10.1016/j.pep.2012.03.003 PubMed DOI

Ye G., Zhang H., Chen B., Nie S., Liu H., Gao W., et al. . (2019). De novo genome assembly of the stress tolerant forest species Casuarina equisetifolia provides insight into secondary growth. Plant J. 97, 779–794. doi: 10.1111/tpj.14159 PubMed DOI

Yi H., Li L. (2013). DNA Methylation changes in response to sulfur dioxide stress in Arabidopsis plants. Proc. Environ. Sci. 18, 37–42. doi: 10.1016/j.proenv.2013.04.006 DOI

Yuen Z. W. S., Srivastava A., Daniel R., McNevin D., Jack C., Eyras E. (2021). Systematic benchmarking of tools for CpG methylation detection from nanopore sequencing. Nat. Commun. 12, 3438. doi: 10.1038/s41467-021-23778-6 PubMed DOI PMC

Zemach A., Kim M. Y., Hsieh P. H., Coleman-Derr D., Eshed-Williams L., Thao K., et al. . (2013). The Arabidopsis nucleosome remodeler DDM1 allows DNA methyltransferases to access H1-containing heterochromatin. Cell 153, 193–205. doi: 10.1016/j.cell.2013.02.033 PubMed DOI PMC

Zenda T., Liu S., Yao D., Duan H. (2018). Analysis of sulphur and chlorine induced DNA cytosine methylation alterations in fresh corn (Zea mays l. saccharata and rugosa) leaf tissues by methylation sensitive amplification polymorphism (MSAP) approach. Genes Genom. 40, 913–925. doi: 10.1007/s13258-018-0685-1 PubMed DOI

Zhang H., Deng X., Miki D., Cutler S., La H., Hou Y. J., et al. . (2012). Sulfamethazine suppresses epigenetic silencing in Arabidopsis by impairing folate synthesis. Plant Cell 24, 1230–1241. doi: 10.1105/tpc.112.096149 PubMed DOI PMC

Zhang H., Lang Z., Zhu J. K. (2018. a). Dynamics and function of DNA methylation in plants. Nat. Rev. Mol. Cell Biol. 19, 489–506. doi: 10.1038/s41580-018-0016-z PubMed DOI

Zhang Q., Liang Z., Cui X., Ji C., Li Y., Zhang P., et al. . (2018. b). N6-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. doi: 10.1016/j.molp.2018.11.005 PubMed DOI

Zhang H., Wang B., Duan C. G., Zhu J. K. (2013). Chemical probes in plant epigenetics studies. Plant Signal. Behav. 8, e25364. doi: 10.4161/psb.25364 PubMed DOI PMC

Zhong S., Fei Z., Chen Y. R., Zheng Y., Huang M., Vrebalov J., et al. . (2013). Single-base resolution methylomes of tomato fruit development reveal epigenome modifications associated with ripening. Nat. Biotechnol. 31, 154–159. doi: 10.1038/nbt.2462 PubMed DOI

Zhou L., Ng H. K., Drautz-Moses D. I., Schuster S. C., Beck S., Kim C., et al. . (2019). Systematic evaluation of library preparation methods and sequencing platforms for high-throughput whole genome bisulfite sequencing. Sci. Rep. 9, 1–16. doi: 10.1038/s41598-019-46875-5 PubMed DOI PMC

Zhu J. K. (2009). Active DNA demethylation mediated by DNA glycosylases. Annu. Rev. Genet. 43, 143–166. doi: 10.1146/annurev-genet-102108-134205 PubMed DOI PMC

Zhu J., Kapoor A., Sridhar V. V., Agius F., Zhu J. K. (2007). The DNA glycosylase/lyase ROS1 functions in pruning DNA methylation patterns in Arabidopsis . Curr. Biol. 17, 54–59. doi: 10.1016/j.cub.2006.10.059 PubMed DOI

Zicola J., Liu L., Tänzler P., Turck F. (2019). Targeted DNA methylation represses two enhancers of FLOWERING LOCUS t in Arabidopsis thaliana . Nat. Plants 5, 300–307. doi: 10.1038/s41477-019-0375-2 PubMed DOI

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...