Beyond the Primary Structure of Nucleic Acids: Potential Roles of Epigenetics and Noncanonical Structures in the Regulations of Plant Growth and Stress Responses

Jazyk angličtina Země Spojené státy americké Médium print

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid36944887

Epigenetics deals with changes in gene expression that are not caused by modifications in the primary sequence of nucleic acids. These changes beyond primary structures of nucleic acids not only include DNA/RNA methylation, but also other reversible conversions, together with histone modifications or RNA interference. In addition, under particular conditions (such as specific ion concentrations or protein-induced stabilization), the right-handed double-stranded DNA helix (B-DNA) can form noncanonical structures commonly described as "non-B DNA" structures. These structures comprise, for example, cruciforms, i-motifs, triplexes, and G-quadruplexes. Their formation often leads to significant differences in replication and transcription rates. Noncanonical RNA structures have also been documented to play important roles in translation regulation and the biology of noncoding RNAs. In human and animal studies, the frequency and dynamics of noncanonical DNA and RNA structures are intensively investigated, especially in the field of cancer research and neurodegenerative diseases. In contrast, noncanonical DNA and RNA structures in plants have been on the fringes of interest for a long time and only a few studies deal with their formation, regulation, and physiological importance for plant stress responses. Herein, we present a review focused on the main fields of epigenetics in plants and their possible roles in stress responses and signaling, with special attention dedicated to noncanonical DNA and RNA structures.

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Waddington CH (2008) The basic ideas of biology. Biol Theory 3:238–253. https://doi.org/10.1162/biot.2008.3.3.238 DOI

Dupont C, Armant DR, Brenner CA (2009) Epigenetics: definition, mechanisms and clinical perspective. Semin Reprod Med 27:351–357. https://doi.org/10.1055/s-0029-1237423 PubMed DOI PMC

Wu CT, Morris JR (2001) Genes, genetics, and epigenetics: a correspondence. Science 293:1103–1105. https://doi.org/10.1126/science.293.5532.1103 DOI

Shrestha A, Thapa B (2020) Epigenetic mechanisms and its role in plant growth and development. J Plant Biochem Physiol 8:255

Wang E, Thombre R, Shah Y et al (2021) G-Quadruplexes as pathogenic drivers in neurodegenerative disorders. Nucleic Acids Res 49:4816–4830. https://doi.org/10.1093/nar/gkab164 PubMed DOI PMC

Pan F, Zhang Y, Xu P et al (2021) Molecular conformations and dynamics of nucleotide repeats associated with neurodegenerative diseases: double helices and CAG hairpin loops. Comput Struct Biotechnol J 19:2819–2832. https://doi.org/10.1016/j.csbj.2021.04.037 PubMed DOI PMC

Kosiol N, Juranek S, Brossart P et al (2021) G-quadruplexes: a promising target for cancer therapy. Mol Cancer 20:40. https://doi.org/10.1186/s12943-021-01328-4 PubMed DOI PMC

Čutová M, Manta J, Porubiaková O et al (2020) Divergent distributions of inverted repeats and G-quadruplex forming sequences in Saccharomyces cerevisiae. Genomics 112:1897–1901. https://doi.org/10.1016/j.ygeno.2019.11.002 PubMed DOI

Bartas M, Čutová M, Brázda V et al (2019) The presence and localization of G-quadruplex forming sequences in the domain of bacteria. Molecules 24:1711. https://doi.org/10.3390/molecules24091711 PubMed DOI PMC

Brázda V, Luo Y, Bartas M et al (2020) G-quadruplexes in the archaea domain. Biomolecules 10:1349. https://doi.org/10.3390/biom10091349 PubMed DOI PMC

Cagirici HB, Budak H, Sen TZ (2021) Genome-wide discovery of G-quadruplexes in barley. Sci Rep 11:7876. https://doi.org/10.1038/s41598-021-86838-3 PubMed DOI PMC

Yang X, Cheema J, Zhang Y et al (2020) RNA G-quadruplex structures exist and function in vivo in plants. Genome Biol 21:226. https://doi.org/10.1186/s13059-020-02142-9 PubMed DOI PMC

Yadav V, Hemansi KN et al (2017) G quadruplex in plants: a ubiquitous regulatory element and its biological relevance. Front Plant Sci 8:1163. https://doi.org/10.3389/fpls.2017.01163 PubMed DOI PMC

Kim N (2019) The interplay between G-quadruplex and transcription. Curr Med Chem 26:2898–2917. https://doi.org/10.2174/0929867325666171229132619 PubMed DOI PMC

Cho H, Cho HS, Nam H et al (2018) Translational control of phloem development by RNA G-quadruplex–JULGI determines plant sink strength. Nat Plants 4:376–390. https://doi.org/10.1038/s41477-018-0157-2 PubMed DOI

Zhao J, Bacolla A, Wang G, Vasquez KM (2010) Non-B DNA structure-induced genetic instability and evolution. Cell Mol Life Sci 67:43–62. https://doi.org/10.1007/s00018-009-0131-2 PubMed DOI

Piazza A, Adrian M, Samazan F et al (2015) Short loop length and high thermal stability determine genomic instability induced by G-quadruplex-forming minisatellites. EMBO J 34:1718–1734. https://doi.org/10.15252/embj.201490702 PubMed DOI PMC

Goswami P, Bartas M, Lexa M et al (2021) SARS-CoV-2 hot-spot mutations are significantly enriched within inverted repeats and CpG island loci. Brief Bioinform 22:1338–1345. https://doi.org/10.1093/bib/bbaa385 PubMed DOI

Laanen P, Saenen E, Mysara M et al (2021) Changes in DNA methylation in Arabidopsis thaliana plants exposed over multiple generations to gamma radiation. Front Plant Sci 12:611783. https://doi.org/10.3389/fpls.2021.611783 PubMed DOI PMC

Zhang K, Sridhar VV, Zhu J et al (2007) Distinctive core histone post-translational modification patterns in Arabidopsis thaliana. PLoS One 2:e1210. https://doi.org/10.1371/journal.pone.0001210 PubMed DOI PMC

Liu X, Yang S, Yu CW et al (2016) Chapter six – histone acetylation and plant development. In: Lin C, Luan S (eds) Developmental signaling in plants. Academic Press, Cambridge, MA. https://doi.org/10.1016/bs.enz.2016.08.001 DOI

Liu C, Lu F, Cui X, Cao X (2010) Histone methylation in higher plants. Annu Rev Plant Biol 61:395–420. https://doi.org/10.1146/annurev.arplant.043008.091939 PubMed DOI

Jambhekar A, Dhall A, Shi Y (2019) Roles and regulation of histone methylation in animal development. Nat Rev Mol Cell Biol 20:625–641. https://doi.org/10.1038/s41580-019-0151-1 PubMed DOI PMC

Song X, Cao X (2017) Context and complexity: analyzing methylation in trinucleotide sequences. Trends Plant Sci 22:351–353. https://doi.org/10.1016/j.tplants.2017.03.013 PubMed DOI

Kenchanmane Raju SG, Ritter EJ, Niederhuth CE (2019) Establishment, maintenance, and biological roles of non-CG methylation in plants. Essays Biochem 63:743–755. https://doi.org/10.1042/EBC20190032 PubMed DOI PMC

Gouil Q, Baulcombe DC (2016) DNA methylation signatures of the plant chromomethyltransferases. PLoS Genet 12:e1006526. https://doi.org/10.1371/journal.pgen.1006526 PubMed DOI PMC

Finnegan EJ, Kovac KA (2000) Plant DNA methyltransferases. Plant Mol Biol 43:189–201. https://doi.org/10.1023/a:1006427226972 PubMed DOI

He XJ, Chen T, Zhu JK (2011) Regulation and function of DNA methylation in plants and animals. Cell Res 21:442–465. https://doi.org/10.1038/cr.2011.23 PubMed DOI PMC

Lee SI, Kim NS (2014) Transposable elements and genome size variations in plants. Genomics Inform 12:87–97. https://doi.org/10.5808/GI.2014.12.3.87 PubMed DOI PMC

Schnable PS, Ware D, Fulton RS et al (2009) The B73 maize genome: complexity, diversity, and dynamics. Science 326:1112–1115. https://doi.org/10.1126/science.1178534 PubMed DOI

Zhang X, Yazaki J, Sundaresan A et al (2006) Genome-wide high-resolution mapping and functional analysis of DNA methylation in Arabidopsis. Cell 126:1189–1201. https://doi.org/10.1016/j.cell.2006.08.003 PubMed DOI

Kumar S, Chinnusamy V, Mohapatra T (2018) Epigenetics of modified DNA bases: 5-methylcytosine and beyond. Front Genet 9:640. https://doi.org/10.3389/fgene.2018.00640 PubMed DOI PMC

Yu L, Sun Y, Zhang X et al (2022) ROS1 promotes low temperature-induced anthocyanin accumulation in apple by demethylating the promoter of anthocyanin-associated genes. Hortic Res 9:uhac007. https://doi.org/10.1093/hr/uhac007 PubMed DOI PMC

Yue H, Nie X, Yan Z, Weining S (2019) N6-methyladenosine regulatory machinery in plants: composition, function and evolution. Plant Biotechnol J 17:1194–1208. https://doi.org/10.1111/pbi.13149 PubMed DOI PMC

Gardiner-Garden M, Frommer M (1987) CpG Islands in vertebrate genomes. J Mol Biol 196:261–282. https://doi.org/10.1016/0022-2836(87)90689-9 PubMed DOI

Anreiter I, Mir Q, Simpson JT et al (2021) New twists in detecting mRNA modification dynamics. Trends Biotechnol 39:72–89. https://doi.org/10.1016/j.tibtech.2020.06.002 PubMed DOI

Manduzio S, Kang H (2021) RNA methylation in chloroplasts or mitochondria in plants. RNA Biol 18:2127–2135. https://doi.org/10.1080/15476286.2021.1909321 PubMed DOI PMC

Manavski N, Vicente A, Chi W, Meurer J (2021) The chloroplast epitranscriptome: factors, sites, regulation, and detection methods. Genes (Basel) 12:1121. https://doi.org/10.3390/genes12081121 PubMed DOI

Machnicka MA, Milanowska K, Osman Oglou O et al (2013) MODOMICS: a database of RNA modification pathways—2013 update. Nucleic Acids Res 41:D262–D267. https://doi.org/10.1093/nar/gks1007 PubMed DOI

Boccaletto P, Machnicka MA, Purta E et al (2018) MODOMICS: a database of RNA modification pathways. 2017 update. Nucleic Acids Res 46:D303–D307. https://doi.org/10.1093/nar/gkx1030 PubMed DOI

Jackman JE, Alfonzo JD (2013) Transfer RNA modifications: nature’s combinatorial chemistry playground. Wiley Interdiscip Rev RNA 4:35–48. https://doi.org/10.1002/wrna.1144 PubMed DOI

Chmielowska-Bąk J, Arasimowicz-Jelonek M, Deckert J (2019) In search of the mRNA modification landscape in plants. BMC Plant Biol 19:421. https://doi.org/10.1186/s12870-019-2033-2 PubMed DOI PMC

Arasimowicz-Jelonek M, Floryszak-Wieczorek J (2019) A physiological perspective on targets of nitration in NO-based signaling networks in plants. J Exp Bot 70:4379–4389. https://doi.org/10.1093/jxb/erz300 PubMed DOI

Waititu JK, Zhang C, Liu J, Wang H (2020) Plant non-coding RNAs: origin, biogenesis, mode of action and their roles in abiotic stress. Int J Mol Sci 21:8401. https://doi.org/10.3390/ijms21218401 PubMed DOI PMC

Yu Y, Zhang Y, Chen X et al (2019) Plant noncoding RNAs: hidden players in development and stress responses. Annu Rev Cell Dev Biol 35:407–431. https://doi.org/10.1146/annurev-cellbio-100818-125218 PubMed DOI PMC

Sunkar R, Li YF, Jagadeeswaran G (2012) Functions of microRNAs in plant stress responses. Trends Plant Sci 17:196–203. https://doi.org/10.1016/j.tplants.2012.01.010 PubMed DOI

Xu C, Tian J, Mo B (2013) siRNA-mediated DNA methylation and H3K9 dimethylation in plants. Protein Cell 4:656–663. https://doi.org/10.1007/s13238-013-3052-7 PubMed DOI PMC

Jia X, Yan J, Tang G (2011) MicroRNA-mediated DNA methylation in plants. Front Biol 6:133–139. https://doi.org/10.1007/s11515-011-1136-4 DOI

Zhang P, Li S, Chen M (2020) Characterization and function of circular RNAs in plants. Front Mol Biosci 7:91. https://doi.org/10.3389/fmolb.2020.00091 PubMed DOI PMC

Kawaji H, Hayashizaki Y (2008) Exploration of small RNAs. PLoS Genet 4:e22. https://doi.org/10.1371/journal.pgen.0040022 PubMed DOI PMC

Morais P, Adachi H, Yu YT (2021) Spliceosomal snRNA epitranscriptomics. Front Genet 12:652129. https://doi.org/10.3389/fgene.2021.652129 PubMed DOI PMC

Watson JD, Crick FHC (1953) Molecular structure of nucleic acids: a structure for deoxyribose nucleic acid. Nature 171:737–738. https://doi.org/10.1038/171737a0 PubMed DOI

Arnott S, Hukins DWL (1973) Refinement of the structure of B-DNA and implications for the analysis of X-ray diffraction data from fibers of biopolymers. J Mol Biol 81:93–105. https://doi.org/10.1016/0022-2836(73)90182-4 PubMed DOI

Shing P, Carter M (2011) DNA structure: alphabet soup for the cellular soul. In: Seligmann H (ed) DNA replication-current advances. IntechOpen, London

Ghosh A, Bansal M (2003) A glossary of DNA structures from A to Z. Acta Crystallogr D Biol Crystallogr 59:620–626. https://doi.org/10.1107/S0907444903003251 PubMed DOI

Franklin RE, Gosling RG (1953) The structure of sodium thymonucleate fibres. I. The influence of water content. Acta Crystallogr 6:673–677. https://doi.org/10.1107/S0365110X53001939 DOI

Wang AHJ, Quigley GJ, Kolpak FJ et al (1979) Molecular structure of a left-handed double helical DNA fragment at atomic resolution. Nature 282:680–686. https://doi.org/10.1038/282680a0 PubMed DOI

Wang G (2007) Z-DNA, an active element in the genome. Front Biosci 12:4424. https://doi.org/10.2741/2399 PubMed DOI

Kresge N, Simoni RD, Hill RL (2009) The discovery of Z-DNA: the work of Alexander Rich. J Biol Chem 284:e23–e25. https://doi.org/10.1016/S0021-9258(20)37564-5 DOI PMC

Pohl FM, Jovin TM (1972) Salt-induced co-operative conformational change of a synthetic DNA: equilibrium and kinetic studies with poly (dG-dC). J Mol Biol 67:375–396. https://doi.org/10.1016/0022-2836(72)90457-3 PubMed DOI

Zhou C, Zhou F, Xu Y (2009) Comparative analyses of distributions and functions of Z-DNA in Arabidopsis and rice. Genomics 93:383–391. https://doi.org/10.1016/j.ygeno.2008.11.012 PubMed DOI

Ferl RJ, Paul AL (1992) Chemical detection of Z-DNA within the maize Adh1 promoter. Plant Mol Biol 18:1181–1184. https://doi.org/10.1007/BF00047722 PubMed DOI

Marincs F, White DWR (1996) Regulation of gene expression at a distance: the hypothetical role of regulatory protein-mediated topological changes of DNA. FEBS Lett 382:1–5. https://doi.org/10.1016/0014-5793(96)00139-1 PubMed DOI

Gangappa SN, Srivastava AK, Maurya JP et al (2013) Z-box binding transcription factors (ZBFs): a new class of transcription factors in Arabidopsis seedling development. Mol Plant 6:1758–1768. https://doi.org/10.1093/mp/sst140 PubMed DOI

Krzyzaniak A, Siatecka M, Szyk A et al (2000) Specific induction of Z-DNA conformation by a nuclear localization signal peptide of lupin glutaminyl tRNA synthetase. Mol Biol Rep 27:51–54. https://doi.org/10.1023/A:1007146516710 PubMed DOI

Gellert M, Lipsett MN, Davies DR (1962) Helix formation by guanylic acid. Proc Natl Acad Sci 48:2013–2018 PubMed DOI PMC

Henderson E, Hardin CC, Walk SK et al (1987) Telomeric DNA oligonucleotides form novel intramolecular structures containing guanine·guanine base pairs. Cell 51:899–908. https://doi.org/10.1016/0092-8674(87)90577-0 PubMed DOI

Li X, Sánchez-Ferrer A, Bagnani M et al (2020) Metal ions confinement defines the architecture of G-quartet, G-quadruplex fibrils and their assembly into nematic tactoids. Proc Natl Acad Sci 117:9832–9839. https://doi.org/10.1073/pnas.1919777117 PubMed DOI PMC

Bartas M, Brázda V, Karlický V (2018) Bioinformatics analyses and in vitro evidence for five and six stacked G-quadruplex forming sequences. Biochimie 150:70–75. https://doi.org/10.1016/j.biochi.2018.05.002 PubMed DOI

Wu F, Niu K, Cui Y et al (2021) Genome-wide analysis of DNA G-quadruplex motifs across 37 species provides insights into G4 evolution. Commun Biol 4:1–11. https://doi.org/10.1038/s42003-020-01643-4 DOI

Griffin BD, Bass HW (2018) Review: plant G-quadruplex (G4) motifs in DNA and RNA; abundant, intriguing sequences of unknown function. Plant Sci 269:143–147. https://doi.org/10.1016/j.plantsci.2018.01.011 PubMed DOI

Dobrovolná M, Bohálová N, Peška V et al (2022) The newly sequenced genome of Pisum sativum is replete with potential G-quadruplex-forming sequences—implications for evolution and biological regulation. Int J Mol Sci 23:8482. https://doi.org/10.3390/ijms23158482 PubMed DOI PMC

Feng Y, Tao S, Zhang P et al (2022) Epigenomic features of DNA G-quadruplexes and their roles in regulating rice gene transcription. Plant Physiol 188:1632–1648. https://doi.org/10.1093/plphys/kiab566 PubMed DOI

Cagirici HB, Sen TZ (2020) Genome-wide discovery of G-quadruplexes in wheat: distribution and putative functional roles. G3 (Bethesda) 10:2021–2032. https://doi.org/10.1534/g3.120.401288 PubMed DOI

Garg R, Aggarwal J, Thakkar B (2016) Genome-wide discovery of G-quadruplex forming sequences and their functional relevance in plants. Sci Rep 6:28211. https://doi.org/10.1038/srep28211 PubMed DOI PMC

Volná A, Bartas M, Karlický V et al (2021) G-quadruplex in gene encoding large subunit of plant RNA polymerase II: a billion-year-old story. Int J Mol Sci 22:7381. https://doi.org/10.3390/ijms22147381 PubMed DOI PMC

Lexa M, Kejnovský E, Steflová P et al (2014) Quadruplex-forming sequences occupy discrete regions inside plant LTR retrotransposons. Nucleic Acids Res 42:968–978. https://doi.org/10.1093/nar/gkt893 PubMed DOI

Mullen MA, Olson KJ, Dallaire P et al (2010) RNA G-Quadruplexes in the model plant species Arabidopsis thaliana: prevalence and possible functional roles. Nucleic Acids Res 38:8149–8163. https://doi.org/10.1093/nar/gkq804 PubMed DOI PMC

Havlová K, Fajkus J (2020) G4 structures in control of replication and transcription of rRNA genes. Front Plant Sci 11:593692. https://doi.org/10.3389/fpls.2020.593692 PubMed DOI PMC

Kwok CK, Ding Y, Shahid S et al (2015) A stable RNA G-quadruplex within the 5′-UTR of Arabidopsis thaliana ATR mRNA inhibits translation. Biochem J 467:91–102. https://doi.org/10.1042/BJ20141063 PubMed DOI

Wu WQ, Zhang ML, Song CP (2020) A comprehensive evaluation of a typical plant telomeric G-quadruplex (G4) DNA reveals the dynamics of G4 formation, rearrangement, and unfolding. J Biol Chem 295:5461–5469. https://doi.org/10.1074/jbc.RA119.012383 PubMed DOI PMC

Andorf CM, Kopylov M, Dobbs D et al (2014) G-quadruplex (G4) motifs in the maize (Zea mays L.) genome are enriched at specific locations in thousands of genes coupled to energy status, hypoxia, low sugar, and nutrient deprivation. J Genet Genomics 41:627–647. https://doi.org/10.1016/j.jgg.2014.10.004 PubMed DOI

Ding D, Wei C, Dong K et al (2020) LOTUS domain is a novel class of G-rich and G-quadruplex RNA binding domain. Nucleic Acids Res 48:9262–9272. https://doi.org/10.1093/nar/gkaa652 PubMed DOI PMC

Sjakste T, Leonova E, Petrovs R et al (2020) Tight DNA-protein complexes isolated from barley seedlings are rich in potential guanine quadruplex sequences. PeerJ 8:e8569. https://doi.org/10.7717/peerj.8569 PubMed DOI PMC

Volná A, Bartas M, Nezval J et al (2021) Searching for G-quadruplex-binding proteins in plants: new insight into possible G-quadruplex regulation. Biotech 10:20. https://doi.org/10.3390/biotech10040020 PubMed DOI PMC

Kopylov M, Bass HW, Stroupe ME (2015) The maize (Zea mays L.) nucleoside diphosphate kinase1 (ZmNDPK1) gene encodes a human NM23-H2 homologue that binds and stabilizes G-quadruplex DNA. Biochemistry 54:1743–1757. https://doi.org/10.1021/bi501284g PubMed DOI

Thomas M, White RL, Davis RW (1976) Hybridization of RNA to double-stranded DNA: formation of R-loops. Proc Natl Acad Sci 73:2294–2298 PubMed DOI PMC

Xu W, Xu H, Li K et al (2017) The R-loop is a common chromatin feature of the Arabidopsis genome. Nat Plants 3:704–714. https://doi.org/10.1038/s41477-017-0004-x PubMed DOI

Liu Y, Liu Q, Su H et al (2021) Genome-wide mapping reveals R-loops associated with centromeric repeats in maize. Genome Res 31:1409–1418. https://doi.org/10.1101/gr.275270.121 PubMed DOI PMC

Liu X, Gao Y, Liao J et al (2021) Genome-wide profiling of circular RNAs, alternative splicing, and R-loops in stem-differentiating xylem of Populus trichocarpa. J Integr Plant Biol 63:1294–1308. https://doi.org/10.1111/jipb.13081 PubMed DOI

Skourti-Stathaki K, Proudfoot NJ (2014) A double-edged sword: R loops as threats to genome integrity and powerful regulators of gene expression. Genes Dev 28:1384–1396. https://doi.org/10.1101/gad.242990.114 PubMed DOI PMC

Kenchanmane Raju SK (2020) The R-loop: an additional chromatin feature for gene regulation in Arabidopsis. Plant Cell 32:785–786. https://doi.org/10.1105/tpc.20.00157 PubMed DOI PMC

Xu W, Li K, Li S et al (2020) The R-loop atlas of Arabidopsis development and responses to environmental stimuli. Plant Cell 32:888–903. https://doi.org/10.1105/tpc.19.00802 PubMed DOI PMC

Yuan W, Zhou J, Tong J et al (2019) ALBA protein complex reads genic R-loops to maintain genome stability in Arabidopsis. Sci Adv 5:eaav9040. https://doi.org/10.1126/sciadv.aav9040 PubMed DOI PMC

Yang Z, Hou Q, Cheng L et al (2017) RNase H1 cooperates with DNA gyrases to restrict R-loops and maintain genome integrity in Arabidopsis chloroplasts. Plant Cell 29:2478–2497. https://doi.org/10.1105/tpc.17.00305 PubMed DOI PMC

Yang Z, Li M, Sun Q (2020) RHON1 co-transcriptionally resolves R-loops for Arabidopsis chloroplast genome maintenance. Cell Rep 30:243–256. https://doi.org/10.1016/j.celrep.2019.12.007 PubMed DOI

Zhang P, Gao J, Li X et al (2021) Interplay of DNA and RNA N6-methyladenine with R-loops in regulating gene transcription in Arabidopsis. Physiol Mol Biol Plants 27:1163–1171. https://doi.org/10.1007/s12298-021-01010-5 PubMed DOI PMC

Lee CY, McNerney C, Ma K et al (2020) R-loop induced G-quadruplex in non-template promotes transcription by successive R-loop formation. Nat Commun 11:3392. https://doi.org/10.1038/s41467-020-17176-7 PubMed DOI PMC

Shafiq S, Chen C, Yang J et al (2017) DNA topoisomerase 1 prevents R-loop accumulation to modulate auxin-regulated root development in rice. Mol Plant 10:821–833. https://doi.org/10.1016/j.molp.2017.04.001 PubMed DOI

Gierer A (1966) Model for DNA and protein interactions and the function of the operator. Nature 212:1480–1481. https://doi.org/10.1038/2121480a0 PubMed DOI

Brázda V, Lýsek J, Bartas M et al (2018) Complex analyses of short inverted repeats in all sequenced chloroplast DNAs. Biomed Res Int 2018:e1097018. https://doi.org/10.1155/2018/1097018 DOI

Čechová J, Lýsek J, Bartas M et al (2018) Complex analyses of inverted repeats in mitochondrial genomes revealed their importance and variability. Bioinformatics 34:1081–1085. https://doi.org/10.1093/bioinformatics/btx729 PubMed DOI

Chen J, Hu Q, Zhang Y et al (2014) P-MITE: a database for plant miniature inverted-repeat transposable elements. Nucleic Acids Res 42:D1176–D1181. https://doi.org/10.1093/nar/gkt1000 PubMed DOI

Kim JM, Sasaki T, Ueda M et al (2015) Chromatin changes in response to drought, salinity, heat, and cold stresses in plants. Front Plant Sci 6:114. https://www.frontiersin.org/article/10.3389/fpls.2015.00114 PubMed DOI PMC

Stassen JHM, López A, Jain R et al (2018) The relationship between transgenerational acquired resistance and global DNA methylation in Arabidopsis. Sci Rep 8:14761. https://doi.org/10.1038/s41598-018-32448-5 PubMed DOI PMC

Kou HP, Li Y, Song XX et al (2011) Heritable alteration in DNA methylation induced by nitrogen-deficiency stress accompanies enhanced tolerance by progenies to the stress in rice (Oryza sativa L.). J Plant Physiol 168:1685–1693. https://doi.org/10.1016/j.jplph.2011.03.017 PubMed DOI

Zhi P, Chang C (2021) Exploiting epigenetic variations for crop disease resistance improvement. Front Plant Sci 12:692328. https://www.frontiersin.org/article/10.3389/fpls.2021.692328 PubMed DOI PMC

Zhang K, Zhuang X, Dong Z et al (2021) The dynamics of N6-methyladenine RNA modification in interactions between rice and plant viruses. Genome Biol 22:189. https://doi.org/10.1186/s13059-021-02410-2 PubMed DOI PMC

Zhang TY, Wang ZQ, Hu HC et al (2021) Transcriptome-wide N6-methyladenosine (m6A) profiling of susceptible and resistant wheat varieties reveals the involvement of variety-specific m6A modification involved in virus-host interaction pathways. Front Microbiol 12:656302. https://doi.org/10.3389/fmicb.2021.656302 PubMed DOI PMC

Du Q, Fang Y, Jiang J et al (2022) Characterization of histone deacetylases and their roles in response to abiotic and PAMPs stresses in Sorghum bicolor. BMC Genomics 23:28. https://doi.org/10.1186/s12864-021-08229-2 PubMed DOI PMC

Shuai P, Liang D, Tang S et al (2014) Genome-wide identification and functional prediction of novel and drought-responsive lincRNAs in Populus trichocarpa. J Exp Bot 65:4975–4983. https://doi.org/10.1093/jxb/eru256 PubMed DOI PMC

Zhang C, Tang G, Peng X et al (2018) Long non-coding RNAs of switchgrass (Panicum virgatum L.) in multiple dehydration stresses. BMC Plant Biol 18:79. https://doi.org/10.1186/s12870-018-1288-3 PubMed DOI PMC

Zhang W, Han Z, Guo Q et al (2014) Identification of maize long non-coding RNAs responsive to drought stress. PLoS One 9:e98958. https://doi.org/10.1371/journal.pone.0098958 PubMed DOI PMC

Chung PJ, Jung H, Jeong DH et al (2016) Transcriptome profiling of drought responsive noncoding RNAs and their target genes in rice. BMC Genomics 17:563. https://doi.org/10.1186/s12864-016-2997-3 PubMed DOI PMC

Ben Amor B, Wirth S, Merchan F et al (2009) Novel long non-protein coding RNAs involved in Arabidopsis differentiation and stress responses. Genome Res 19:57–69. https://doi.org/10.1101/gr.080275.108 PubMed DOI PMC

Li S, Yu X, Lei N et al (2017) Genome-wide identification and functional prediction of cold and/or drought-responsive lncRNAs in cassava. Sci Rep 7:45981. https://doi.org/10.1038/srep45981 PubMed DOI PMC

Qi X, Xie S, Liu Y et al (2013) Genome-wide annotation of genes and noncoding RNAs of foxtail millet in response to simulated drought stress by deep sequencing. Plant Mol Biol 83:459–473. https://doi.org/10.1007/s11103-013-0104-6 PubMed DOI

Zhao J, He Q, Chen G et al (2016) Regulation of non-coding RNAs in heat stress responses of plants. Front Plant Sci 7:1213. https://www.frontiersin.org/article/10.3389/fpls.2016.01213 PubMed DOI PMC

Huo C, Zhang B, Wang R (2022) Research progress on plant noncoding RNAs in response to low-temperature stress. Plant Signal Behav 17:2004035. https://doi.org/10.1080/15592324.2021.2004035 PubMed DOI

Yang B, Tang J, Yu Z et al (2019) Light stress responses and prospects for engineering light stress tolerance in crop plants. J Plant Growth Regul 38:1489–1506. https://doi.org/10.1007/s00344-019-09951-8 DOI

Subburaj S, Ha HJ, Jin Y-T et al (2017) Identification of γ-radiation-responsive microRNAs and their target genes in Tradescantia (BNL clone 4430). J Plant Biol 60:116–128. https://doi.org/10.1007/s12374-016-0433-5 DOI

Sunkar R, Zhu JK (2004) Novel and stress-regulated microRNAs and other small RNAs from Arabidopsis. Plant Cell 16:2001–2019. https://doi.org/10.1105/tpc.104.022830 PubMed DOI PMC

Boycheva I, Vassileva V, Iantcheva A (2014) Histone acetyltransferases in plant development and plasticity. Curr Genomics 15:28–37. https://doi.org/10.2174/138920291501140306112742 PubMed DOI PMC

Latrasse D, Benhamed M, Henry Y et al (2008) The MYST histone acetyltransferases are essential for gametophyte development in Arabidopsis. BMC Plant Biol 8:121. https://doi.org/10.1186/1471-2229-8-121 PubMed DOI PMC

Berr A, Shafiq S, Shen WH (2011) Histone modifications in transcriptional activation during plant development. Biochim Biophys Acta – Gene Regul Mech 1809:567–576. https://doi.org/10.1016/j.bbagrm.2011.07.001 DOI

Casati P, Campi M, Chu F et al (2008) Histone acetylation and chromatin remodeling are required for UV-B–dependent transcriptional activation of regulated genes in maize. Plant Cell 20:827–842. https://doi.org/10.1105/tpc.107.056457 PubMed DOI PMC

Graindorge S, Cognat V, To Berens PJ et al (2019) Photodamage repair pathways contribute to the accurate maintenance of the DNA methylome landscape upon UV exposure. PLoS Genet 15:e1008476. https://doi.org/10.1371/journal.pgen.1008476 PubMed DOI PMC

Friedrich T, Faivre L, Bäurle I et al (2019) Chromatin-based mechanisms of temperature memory in plants. Plant Cell Environ 42:762–770. https://doi.org/10.1111/pce.13373 PubMed DOI

Jaskiewicz M, Conrath U, Peterhänsel C (2011) Chromatin modification acts as a memory for systemic acquired resistance in the plant stress response. EMBO Rep 12:50–55. https://doi.org/10.1038/embor.2010.186 PubMed DOI

Bräutigam K, Soolanayakanahally R, Champigny M et al (2017) Sexual epigenetics: gender-specific methylation of a gene in the sex determining region of Populus balsamifera. Sci Rep 7:45388. https://doi.org/10.1038/srep45388 PubMed DOI PMC

Yang L, Perrera V, Saplaoura E et al (2019) m5C methylation guides systemic transport of messenger RNA over graft junctions in plants. Curr Biol 29:2465–2476.e5. https://doi.org/10.1016/j.cub.2019.06.042 PubMed DOI

Song Y, Ma K, Ci D et al (2013) Sexual dimorphic floral development in dioecious plants revealed by transcriptome, phytohormone, and DNA methylation analysis in Populus tomentosa. Plant Mol Biol 83:559–576. https://doi.org/10.1007/s11103-013-0108-2 PubMed DOI

Chang YN, Zhu C, Jiang J et al (2020) Epigenetic regulation in plant abiotic stress responses. J Integr Plant Biol 62:563–580. https://doi.org/10.1111/jipb.12901 PubMed DOI

Ou X, Zhang Y, Xu C et al (2012) Transgenerational inheritance of modified DNA methylation patterns and enhanced tolerance induced by heavy metal stress in rice (Oryza sativa L.). PLoS One 7:e41143. https://doi.org/10.1371/journal.pone.0041143 PubMed DOI PMC

Yamaguchi A, Abe M (2012) Regulation of reproductive development by non-coding RNA in Arabidopsis: to flower or not to flower. J Plant Res 125:693–704. https://doi.org/10.1007/s10265-012-0513-7 PubMed DOI PMC

Wang CY, Liu SR, Zhang XY et al (2017) Genome-wide screening and characterization of long non-coding RNAs involved in flowering development of trifoliate orange (Poncirus trifoliata L. Raf.). Sci Rep 7:43226. https://doi.org/10.1038/srep43226 PubMed DOI PMC

Lu D, Zhai J, Xi M (2022) Regulation of DNA methylation during plant endosperm development. Front Genet 13:760690. https://doi.org/10.3389/fgene.2022.760690 PubMed DOI PMC

Gorelick R (2003) Evolution of dioecy and sex chromosomes via methylation driving Muller’s ratchet. Biol J Linn Soc 80:353–368. https://doi.org/10.1046/j.1095-8312.2003.00244.x DOI

Tian L, Fong MP, Wang JJ et al (2005) Reversible histone acetylation and deacetylation mediate genome-wide, promoter-dependent and locus-specific changes in gene expression during plant development. Genetics 169:337–345. https://doi.org/10.1534/genetics.104.033142 PubMed DOI PMC

Minshull TC, Dickman MJ (2014) Mass spectrometry analysis of histone post translational modifications. Drug Discov Today Dis Models 12:41–48. https://doi.org/10.1016/j.ddmod.2015.03.002 DOI

Hayashi-Takanaka Y, Kina Y, Nakamura F et al (2020) Histone modification dynamics as revealed by multicolor immunofluorescence-based single-cell analysis. J Cell Sci 133:jcs243444. https://doi.org/10.1242/jcs.243444 PubMed DOI PMC

European Molecular Biology Open Software Suite (EMBOSS) (1999) newcpgseek. https://galaxy-iuc.github.io/emboss-5.0-docs/newcpgseek.html . Accessed 29 Aug 2022

European Molecular Biology Open Software Suite (EMBOSS): (1999) cpgplot. https://galaxy-iuc.github.io/emboss-5.0-docs/cpgplot.html . Accessed 29 Aug 2022

Afgan E, Baker D, Batut B et al (2018) The Galaxy platform for accessible, reproducible and collaborative biomedical analyses: 2018 update. Nucleic Acids Res 46:W537–W544. https://doi.org/10.1093/nar/gky379 PubMed DOI PMC

Li Y, Tollefsbol TO (2011) DNA methylation detection: bisulfite genomic sequencing analysis. Methods Mol Biol 791:11–21. https://doi.org/10.1007/978-1-61779-316-5_2 PubMed DOI PMC

Rand AC, Jain M, Eizenga JM et al (2017) Mapping DNA methylation with high throughput nanopore sequencing. Nat Methods 14:411–413. https://doi.org/10.1038/nmeth.4189 PubMed DOI PMC

Kurdyukov S, Bullock M (2016) DNA methylation analysis: choosing the right method. Biology (Basel) 5:3. https://doi.org/10.3390/biology5010003 PubMed DOI

Petell CJ, Loiseau G, Gandy R et al (2017) A refined DNA methylation detection method using MspJI coupled quantitative PCR. Anal Biochem 533:1–9. https://doi.org/10.1016/j.ab.2017.06.006 PubMed DOI PMC

Yi X, Zhang Z, Ling Y et al (2015) PNRD: a plant non-coding RNA database. Nucleic Acids Res 43:D982–D989. https://doi.org/10.1093/nar/gku1162 PubMed DOI

Jin J, Lu P, Xu Y et al (2021) PLncDB V2.0: a comprehensive encyclopedia of plant long noncoding RNAs. Nucleic Acids Res 49:D1489–D1495. https://doi.org/10.1093/nar/gkaa910 PubMed DOI

Guo Z, Kuang Z, Wang Y et al (2020) PmiREN: a comprehensive encyclopedia of plant miRNAs. Nucleic Acids Res 48:D1114–D1121. https://doi.org/10.1093/nar/gkz894 PubMed DOI

Zhang Z, Yu J, Li D et al (2010) PMRD: plant microRNA database. Nucleic Acids Res 38:D806–D813. https://doi.org/10.1093/nar/gkp818 PubMed DOI

Liao P, Li S, Cui X et al (2018) A comprehensive review of web-based resources of non-coding RNAs for plant science research. Int J Biol Sci 14:819–832. https://doi.org/10.7150/ijbs.24593 PubMed DOI PMC

Benesova S, Kubista M, Valihrach L (2021) Small RNA-sequencing: approaches and considerations for miRNA analysis. Diagnostics (Basel) 11:964. https://doi.org/10.3390/diagnostics11060964 PubMed DOI

Hüttenhofer A, Vogel J (2006) Experimental approaches to identify non-coding RNAs. Nucleic Acids Res 34:635–646. https://doi.org/10.1093/nar/gkj469 PubMed DOI PMC

Koh HR, Myong S (2018) Single-cell imaging approaches for studying small-RNA-induced gene regulation. Biophys J 115:203–208. https://doi.org/10.1016/j.bpj.2018.05.040 PubMed DOI PMC

Quadruplex forming G-Rich Sequences (QGRS) (2006) QGRS Mapper. https://bioinformatics.ramapo.edu/QGRS/index.php . Accessed 25 Feb 2022

non-B DNA Motif Search Tool (nBMST) (2022) Advanced Biomedical Computing Center (ABCC). https://nonb-abcc.ncifcrf.gov/apps/nBMST/default/ . Accessed 25 Feb 2022

Panda D, Saha P, Chaudhuri R et al (2019) A competitive pull-down assay using G-quadruplex DNA linked magnetic nanoparticles to determine specificity of G-quadruplex ligands. Anal Chem 12:7705–7711. https://doi.org/10.1021/acs.analchem.9b00889 DOI

Busto N, Calvo P, Santolaya J et al (2018) Fishing for G-quadruplexes in solution with a perylene diimide derivative labeled with biotins. Chem Eur J 24:11292–11296. https://doi.org/10.1002/chem.201802365 PubMed DOI

Jamroskovic J, Obi I, Movahedi A et al (2019) Identification of putative G-quadruplex DNA structures in S. pombe genome by quantitative PCR stop assay. DNA Repair 82:102678. https://doi.org/10.1016/j.dnarep.2019.102678 PubMed DOI

Takahashi H, Nakagawa A, Kojima S et al (2012) Discovery of novel rules for G-quadruplex-forming sequences in plants by using bioinformatics methods. J Biosci Bioeng 114:570–575. https://doi.org/10.1016/j.jbiosc.2012.05.017 PubMed DOI

Brázda V, Kolomazník J, Lýsek J et al (2019) G4Hunter web application: a web server for G-quadruplex prediction. Bioinformatics 35:3493–3495. https://doi.org/10.1093/bioinformatics/btz087 PubMed DOI PMC

Yang C, Hu R, Li Q et al (2018) Visualization of parallel G-quadruplexes in cells with a series of new developed bis(4-aminobenzylidene)acetone derivatives. ACS Omega 3:10487–10492. https://doi.org/10.1021/acsomega.8b01190 PubMed DOI PMC

Zheng K, Zhang J, He YD et al (2020) Detection of genomic G-quadruplexes in living cells using a small artificial protein. Nucleic Acids Res 48:11706–11720. https://doi.org/10.1093/nar/gkaa841 PubMed DOI PMC

Krafcikova M, Hänsel-Hertsch R, Trantirek L et al (2019) In cell NMR spectroscopy: investigation of G-quadruplex structures inside living Xenopus laevis oocytes. Methods Mol Biol 2035:397–405. https://doi.org/10.1007/978-1-4939-9666-7_25 PubMed DOI

Murat P, Bonnet R, Van der Heyden A et al (2010) Template-assembled synthetic G-quadruplex (TASQ): a useful system for investigating the interactions of ligands with constrained quadruplex topologies. Chemistry 16:6106–6114. https://doi.org/10.1002/chem.200903456 PubMed DOI

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