Exploring the crop epigenome: a comparison of DNA methylation profiling techniques
Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic-ecollection
Typ dokumentu časopisecké články, přehledy
PubMed
37389288
PubMed Central
PMC10306282
DOI
10.3389/fpls.2023.1181039
Knihovny.cz E-zdroje
- Klíčová slova
- DNA methylation modulation, DNA methylation profiling, bisulfite sequencing, crop epigenome, immunological techniques, mass spectrometry, next-generation sequencing,
- Publikační typ
- časopisecké články MeSH
- přehledy MeSH
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.
Biology Department Ġ F Abela Junior College Msida Malta
Center for Biological Research Madrid Spain
Centre of Molecular Medicine and Biobanking University of Malta Msida Malta
Department of Biology University of Florence Sesto Fiorentino Italy
Department of Chemistry and Biology 'A Zambelli' University of Salerno Fisciano Italy
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
Mendeleum Insitute of Genetics Faculty of Horticulture Mendel University in Brno Lednice Czechia
Plant Epigenomics Technical University of Munich Freising Germany
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