Epigenetic Mechanisms of Plant Adaptation: Comparison
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Please note this is a comparison between Version 2 by Vasily Ashapkin and Version 6 by Bruce Ren.

Unlike animals, plants are immobile and could not actively escape the effects of aggressive environmental factors, such as pathogenic microorganisms, insect pests, parasitic plants, extreme temperatures, drought, and many others. To counteract these unfavorable encounters, plants have evolved very high phenotypic plasticity. In a rapidly changing environment, adaptive phenotypic changes often occur in time frames that are too short for the natural selection of adaptive mutations. Probably, some kind of epigenetic variability underlines environmental adaptation in these cases. Indeed, isogenic plants often have quite variable phenotypes in different habitats. There are examples of successful “invasions” of relatively small and genetically homogenous plant populations into entirely new habitats. The unique capability of quick environmental adaptation appears to be due to a high tendency to transmit epigenetic changes between plant generations. Multiple studies show that epigenetic memory serves as a mechanism of plant adaptation to a rapidly changing environment and, in particular, to aggressive biotic and abiotic stresses. In wild nature, this mechanism underlies, to a very significant extent, plant capability to live in different habitats and endure drastic environmental changes. In agriculture, a deep understanding of this mechanism could serve to elaborate more effective and safe approaches to plant protection.

  • plant epigenetics
  • epigenetic variability
  • abiotic stress
  • biotic stress
  • environmental adaptation
  • gene expression
  • DNA methylation
  • chromatin
  • siRNA
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References

  1. Feng, S.; Jacobsen, S.E. Epigenetic modifications in plants: an evolutionary perspective. Curr. Opin. Plant Biol. 2011, 14, 179–186, doi:10.1016/j.pbi.2010.12.002.
  2. Vanyushin, B.F.; Ashapkin, V.V. DNA methylation in higher plants: Past, present and future. Biochim. Biophys. Acta BBA - Gene Regul. Mech. 2011, 1809, 360–368, doi:10.1016/j.bbagrm.2011.04.006.
  3. Woo, H.R.; Dittmer, T.A.; Richards, E.J. Three SRA-Domain Methylcytosine-Binding Proteins Cooperate to Maintain Global CpG Methylation and Epigenetic Silencing in Arabidopsis. PLoS Genet. 2008, 4, e1000156, doi:10.1371/journal.pgen.1000156.
  4. Du, J.; Zhong, X.; Bernatavichute, Y.V.; Stroud, H.; Feng, S.; Caro, E.; Vashisht, A.A.; Terragni, J.; Chin, H.G.; Tu, A.; et al. Dual Binding of Chromomethylase Domains to H3K9me2-Containing Nucleosomes Directs DNA Methylation in Plants. Cell 2012, 151, 167–180, doi:10.1016/j.cell.2012.07.034.
  5. Cao, X.; Jacobsen, S.E. Role of the Arabidopsis DRM Methyltransferases in De Novo DNA Methylation and Gene Silencing. Curr. Biol. 2002, 12, 1138–1144, doi:10.1016/S0960-9822(02)00925-9.
  6. Stroud, H.; Do, T.; Du, J.; Zhong, X.; Feng, S.; Johnson, L.; Patel, D.J.; Jacobsen, S.E. Non-CG methylation patterns shape the epigenetic landscape in Arabidopsis. Nat. Struct. Mol. Biol. 2014, 21, 64–72, doi:10.1038/nsmb.2735.
  7. Zemach, A.; Kim, M.Y.; Hsieh, P.-H.; Coleman-Derr, D.; Eshed-Williams, L.; Thao, K.; Harmer, S.L.; Zilberman, D. The Arabidopsis Nucleosome Remodeler DDM1 Allows DNA Methyltransferases to Access H1-Containing Heterochromatin. Cell 2013, 153, 193–205, doi:10.1016/j.cell.2013.02.033.
  8. Matzke, M.A.; Kanno, T.; Matzke, A.J.M. RNA-Directed DNA Methylation: The Evolution of a Complex Epigenetic Pathway in Flowering Plants. Annu. Rev. Plant Biol. 2015, 66, 243–267, doi:10.1146/annurev-arplant-043014-114633.
  9. Wendte, J.M.; Pikaard, C.S. The RNAs of RNA-directed DNA methylation. Biochim. Biophys. Acta BBA - Gene Regul. Mech. 2017, 1860, 140–148, doi:10.1016/j.bbagrm.2016.08.004.
  10. Gehring, M.; Reik, W.; Henikoff, S. DNA demethylation by DNA repair. Trends Genet. 2009, 25, 82–90, doi:10.1016/j.tig.2008.12.001.
  11. Tang, K.; Lang, Z.; Zhang, H.; Zhu, J.-K. The DNA demethylase ROS1 targets genomic regions with distinct chromatin modifications. Nat. Plants 2016, 2, 16169, doi:10.1038/nplants.2016.169.
  12. Berr, A.; Shafiq, S.; Shen, W.-H. Histone modifications in transcriptional activation during plant development. Biochim. Biophys. Acta BBA - Gene Regul. Mech. 2011, 1809, 567–576, doi:10.1016/j.bbagrm.2011.07.001.
  13. Zhang, X.; Bernatavichute, Y.V.; Cokus, S.; Pellegrini, M.; Jacobsen, S.E. Genome-wide analysis of mono-, di- and trimethylation of histone H3 lysine 4 in Arabidopsis thaliana. Genome Biol. 2009, 10, R62, doi:10.1186/gb-2009-10-6-r62.
  14. Zhang, X.; Clarenz, O.; Cokus, S.; Bernatavichute, Y.V.; Pellegrini, M.; Goodrich, J.; Jacobsen, S.E. Whole-Genome Analysis of Histone H3 Lysine 27 Trimethylation in Arabidopsis. PLoS Biol. 2007, 5, e129, doi:10.1371/journal.pbio.0050129.
  15. Zhang, X.; Germann, S.; Blus, B.J.; Khorasanizadeh, S.; Gaudin, V.; Jacobsen, S.E. The Arabidopsis LHP1 protein colocalizes with histone H3 Lys27 trimethylation. Nat. Struct. Mol. Biol. 2007, 14, 869–871, doi:10.1038/nsmb1283.
  16. Bernatavichute, Y.V.; Zhang, X.; Cokus, S.; Pellegrini, M.; Jacobsen, S.E. Genome-Wide Association of Histone H3 Lysine Nine Methylation with CHG DNA Methylation in Arabidopsis thaliana. PLoS ONE 2008, 3, e3156, doi:10.1371/journal.pone.0003156.
  17. Lee, C.H.; Carroll, B.J. Evolution and Diversification of Small RNA Pathways in Flowering Plants. Plant Cell Physiol. 2018, doi:10.1093/pcp/pcy167.
  18. Verhoeven, K.J.F.; Jansen, J.J.; van Dijk, P.J.; Biere, A. Stress-induced DNA methylation changes and their heritability in asexual dandelions. New Phytol. 2010, 185, 1108–1118, doi:10.1111/j.1469-8137.2009.03121.x.
  19. Zhu, J.-K. Abiotic Stress Signaling and Responses in Plants. Cell 2016, 167, 313–324, doi:10.1016/j.cell.2016.08.029.
  20. Yang, R.; Hong, Y.; Ren, Z.; Tang, K.; Zhang, H.; Zhu, J.-K.; Zhao, C. A Role for PICKLE in the Regulation of Cold and Salt Stress Tolerance in Arabidopsis. Front. Plant Sci. 2019, 10, 900, doi:10.3389/fpls.2019.00900.
  21. Yang, R.; Zheng, Z.; Chen, Q.; Yang, L.; Huang, H.; Miki, D.; Wu, W.; Zeng, L.; Liu, J.; Zhou, J.-X.; et al. The developmental regulator PKL is required to maintain correct DNA methylation patterns at RNA-directed DNA methylation loci. Genome Biol. 2017, 18, 103, doi:10.1186/s13059-017-1226-y.
  22. Carter, B.; Bishop, B.; Ho, K.K.; Huang, R.; Jia, W.; Zhang, H.; Pascuzzi, P.E.; Deal, R.B.; Ogas, J. The Chromatin Remodelers PKL and PIE1 Act in an Epigenetic Pathway That Determines H3K27me3 Homeostasis in Arabidopsis. Plant Cell 2018, 30, 1337–1352, doi:10.1105/tpc.17.00867.
  23. Park, J.; Lim, C.J.; Shen, M.; Park, H.J.; Cha, J.-Y.; Iniesto, E.; Rubio, V.; Mengiste, T.; Zhu, J.-K.; Bressan, R.A.; et al. Epigenetic switch from repressive to permissive chromatin in response to cold stress. Proc. Natl. Acad. Sci. 2018, 115, E5400–E5409, doi:10.1073/pnas.1721241115.
  24. Ohama, N.; Sato, H.; Shinozaki, K.; Yamaguchi-Shinozaki, K. Transcriptional Regulatory Network of Plant Heat Stress Response. Trends Plant Sci. 2017, 22, 53–65, doi:10.1016/j.tplants.2016.08.015.
  25. Popova, O.V.; Dinh, H.Q.; Aufsatz, W.; Jonak, C. The RdDM Pathway Is Required for Basal Heat Tolerance in Arabidopsis. Mol. Plant 2013, 6, 396–410, doi:10.1093/mp/sst023.
  26. Lämke, J.; Brzezinka, K.; Altmann, S.; Bäurle, I. A hit‐and‐run heat shock factor governs sustained histone methylation and transcriptional stress memory. EMBO J. 2016, 35, 162–175, doi:10.15252/embj.201592593.
  27. Ferreira, L.J.; Azevedo, V.; Maroco, J.; Oliveira, M.M.; Santos, A.P. Salt Tolerant and Sensitive Rice Varieties Display Differential Methylome Flexibility under Salt Stress. PLOS ONE 2015, 10, e0124060, doi:10.1371/journal.pone.0124060.
  28. Wang, W.; Huang, F.; Qin, Q.; Zhao, X.; Li, Z.; Fu, B. Comparative analysis of DNA methylation changes in two rice genotypes under salt stress and subsequent recovery. Biochem. Biophys. Res. Commun. 2015, 465, 790–796, doi:10.1016/j.bbrc.2015.08.089.
  29. Baek, D.; Jiang, J.; Chung, J.-S.; Wang, B.; Chen, J.; Xin, Z.; Shi, H. Regulated AtHKT1 Gene Expression by a Distal Enhancer Element and DNA Methylation in the Promoter Plays an Important Role in Salt Tolerance. Plant Cell Physiol. 2011, 52, 149–161, doi:10.1093/pcp/pcq182.
  30. Kim, J.-M.; Sasaki, T.; Ueda, M.; Sako, K.; Seki, M. Chromatin changes in response to drought, salinity, heat, and cold stresses in plants. Front. Plant Sci. 2015, 6, doi:10.3389/fpls.2015.00114.
  31. Sani, E.; Herzyk, P.; Perrella, G.; Colot, V.; Amtmann, A. Hyperosmotic priming of Arabidopsis seedlings establishes a long-term somatic memory accompanied by specific changes of the epigenome. Genome Biol. 2013, 14, R59, doi:10.1186/gb-2013-14-6-r59.
  32. Xu, R.; Wang, Y.; Zheng, H.; Lu, W.; Wu, C.; Huang, J.; Yan, K.; Yang, G.; Zheng, C. Salt-induced transcription factor MYB74 is regulated by the RNA-directed DNA methylation pathway in Arabidopsis. J. Exp. Bot. 2015, 66, 5997–6008, doi:10.1093/jxb/erv312.
  33. Avramova, Z. Transcriptional ‘memory’ of a stress: transient chromatin and memory (epigenetic) marks at stress-response genes. Plant J. 2015, 83, 149–159, doi:10.1111/tpj.12832.
  34. Avramova, Z. Defence-related priming and responses to recurring drought: Two manifestations of plant transcriptional memory mediated by the ABA and JA signalling pathways: dehydration stress memory and jasmonic acid priming. Plant Cell Environ. 2019, 42, 983–997, doi:10.1111/pce.13458.
  35. Ding, Y.; Avramova, Z.; Fromm, M. The Arabidopsis trithorax-like factor ATX1 functions in dehydration stress responses via ABA-dependent and ABA-independent pathways: ATX1 functions in dehydration stress responses. Plant J. 2011, 66, 735–744, doi:10.1111/j.1365-313X.2011.04534.x.
  36. Ding, Y.; Fromm, M.; Avramova, Z. Multiple exposures to drought “train” transcriptional responses in Arabidopsis. Nat. Commun. 2012, 3, 740, doi:10.1038/ncomms1732.
  37. Ding, Y.; Liu, N.; Virlouvet, L.; Riethoven, J.-J.; Fromm, M.; Avramova, Z. Four distinct types of dehydration stress memory genes in Arabidopsis thaliana. BMC Plant Biol. 2013, 13, 229, doi:10.1186/1471-2229-13-229.
  38. Virlouvet, L.; Fromm, M. Physiological and transcriptional memory in guard cells during repetitive dehydration stress. New Phytol. 2015, 205, 596–607, doi:10.1111/nph.13080.
  39. Gupta, A.; Rico-Medina, A.; Caño-Delgado, A.I. The physiology of plant responses to drought. Science 2020, 368, 266–269, doi:10.1126/science.aaz7614.
  40. Ramirez-Prado, J.S.; Abulfaraj, A.A.; Rayapuram, N.; Benhamed, M.; Hirt, H. Plant Immunity: From Signaling to Epigenetic Control of Defense. Trends Plant Sci. 2018, 23, 833–844, doi:10.1016/j.tplants.2018.06.004.
  41. Zheng, X.; Chen, L.; Li, M.; Lou, Q.; Xia, H.; Wang, P.; Li, T.; Liu, H.; Luo, L. Transgenerational Variations in DNA Methylation Induced by Drought Stress in Two Rice Varieties with Distinguished Difference to Drought Resistance. PLoS ONE 2013, 8, e80253, doi:10.1371/journal.pone.0080253.
  42. Secco, D.; Whelan, J.; Rouached, H.; Lister, R. Nutrient stress-induced chromatin changes in plants. Curr. Opin. Plant Biol. 2017, 39, 1–7, doi:10.1016/j.pbi.2017.04.001.Liang, D.; Zhang, Z.; Wu, H.; Huang, C.; Shuai, P.; Ye, C.-Y.; Tang, S.; Wang, Y.; Yang, L.; Wang, J.; et al. Single-base-resolution methylomes of populus trichocarpa reveal the association between DNA methylation and drought stress. BMC Genet. 2014, 15, S9, doi:10.1186/1471-2156-15-S1-S9.
  43. Widiez, T.; El Kafafi, E.S.; Girin, T.; Berr, A.; Ruffel, S.; Krouk, G.; Vayssières, A.; Shen, W.-H.; Coruzzi, G.M.; Gojon, A.; et al. HIGH NITROGEN INSENSITIVE 9 (HNI9)-mediated systemic repression of root NO 3 − uptake is associated with changes in histone methylation. Proc. Natl. Acad. Sci. 2011, 108, 13329–13334, doi:10.1073/pnas.1017863108.Song, Y.; Ci, D.; Tian, M.; Zhang, D. Stable methylation of a non-coding RNA gene regulates gene expression in response to abiotic stress in Populus simonii. J. Exp. Bot. 2016, 67, 1477–1492, doi:10.1093/jxb/erv543.
  44. Fan, H.; Zhang, Z.; Wang, N.; Cui, Y.; Sun, H.; Liu, Y.; Wu, H.; Zheng, S.; Bao, S.; Ling, H.-Q. SKB1/PRMT5-mediated histone H4R3 dimethylation of Ib subgroup bHLH genes negatively regulates iron homeostasis in Arabidopsis thaliana. Plant J. 2014, 77, 209–221, doi:10.1111/tpj.12380.Goll, M.G.; Kirpekar, F.; Maggert, K.A.; Yoder, J.A.; Hsieh, C.-L.; Zhang, X.; Golic, K.G.; Jacobsen, S.E.; Bestor, T.H. Methylation of tRNA Asp by the DNA methyltransferase homolog Dnmt2. Science 2006, 311, 395–398, doi:10.1126/science.1120976.
  45. Xing, J.; Wang, T.; Liu, Z.; Xu, J.; Yao, Y.; Hu, Z.; Peng, H.; Xin, M.; Yu, F.; Zhou, D.; et al. GENERAL CONTROL NONREPRESSED PROTEIN5-Mediated Histone Acetylation of FERRIC REDUCTASE DEFECTIVE3 Contributes to Iron Homeostasis in Arabidopsis. Plant Physiol. 2015, 168, 1309–1320, doi:10.1104/pp.15.00397.Secco, D.; Whelan, J.; Rouached, H.; Lister, R. Nutrient stress-induced chromatin changes in plants. Curr. Opin. Plant Biol. 2017, 39, 1–7, doi:10.1016/j.pbi.2017.04.001.
  46. Chandrika, N.N.P.; Sundaravelpandian, K.; Yu, S.-M.; Schmidt, W. ALFIN-LIKE 6 is involved in root hair elongation during phosphate deficiency in Arabidopsis. New Phytol. 2013, 198, 709–720, doi:10.1111/nph.12194.Widiez, T.; El Kafafi, E.S.; Girin, T.; Berr, A.; Ruffel, S.; Krouk, G.; Vayssières, A.; Shen, W.-H.; Coruzzi, G.M.; Gojon, A.; et al. HIGH NITROGEN INSENSITIVE 9 (HNI9)-mediated systemic repression of root NO 3 − uptake is associated with changes in histone methylation. Proc. Natl. Acad. Sci. 2011, 108, 13329–13334, doi:10.1073/pnas.1017863108.
  47. Secco, D.; Wang, C.; Shou, H.; Schultz, M.D.; Chiarenza, S.; Nussaume, L.; Ecker, J.R.; Whelan, J.; Lister, R. Stress induced gene expression drives transient DNA methylation changes at adjacent repetitive elements. eLife 2015, 4, e09343, doi:10.7554/eLife.09343.Fan, H.; Zhang, Z.; Wang, N.; Cui, Y.; Sun, H.; Liu, Y.; Wu, H.; Zheng, S.; Bao, S.; Ling, H.-Q. SKB1/PRMT5-mediated histone H4R3 dimethylation of Ib subgroup bHLH genes negatively regulates iron homeostasis in Arabidopsis thaliana. Plant J. 2014, 77, 209–221, doi:10.1111/tpj.12380.
  48. Yong-Villalobos, L.; González-Morales, S.I.; Wrobel, K.; Gutiérrez-Alanis, D.; Cervantes-Peréz, S.A.; Hayano-Kanashiro, C.; Oropeza-Aburto, A.; Cruz-Ramírez, A.; Martínez, O.; Herrera-Estrella, L. Methylome analysis reveals an important role for epigenetic changes in the regulation of the Arabidopsis response to phosphate starvation. Proc. Natl. Acad. Sci. 2015, 112, E7293–E7302, doi:10.1073/pnas.1522301112.Xing, J.; Wang, T.; Liu, Z.; Xu, J.; Yao, Y.; Hu, Z.; Peng, H.; Xin, M.; Yu, F.; Zhou, D.; et al. GENERAL CONTROL NONREPRESSED PROTEIN5-Mediated Histone Acetylation of FERRIC REDUCTASE DEFECTIVE3 Contributes to Iron Homeostasis in Arabidopsis. Plant Physiol. 2015, 168, 1309–1320, doi:10.1104/pp.15.00397.
  49. Martínez-Pérez, M.; Aparicio, F.; López-Gresa, M.P.; Bellés, J.M.; Sánchez-Navarro, J.A.; Pallás, V. Arabidopsis m 6 A demethylase activity modulates viral infection of a plant virus and the m 6 A abundance in its genomic RNAs. Proc. Natl. Acad. Sci. 2017, 114, 10755–10760, doi:10.1073/pnas.1703139114.Chandrika, N.N.P.; Sundaravelpandian, K.; Yu, S.-M.; Schmidt, W. ALFIN-LIKE 6 is involved in root hair elongation during phosphate deficiency in Arabidopsis. New Phytol. 2013, 198, 709–720, doi:10.1111/nph.12194.
  50. Deleris, A.; Halter, T.; Navarro, L. DNA Methylation and Demethylation in Plant Immunity. Annu. Rev. Phytopathol. 2016, 54, 579–603, doi:10.1146/annurev-phyto-080615-100308.Secco, D.; Wang, C.; Shou, H.; Schultz, M.D.; Chiarenza, S.; Nussaume, L.; Ecker, J.R.; Whelan, J.; Lister, R. Stress induced gene expression drives transient DNA methylation changes at adjacent repetitive elements. eLife 2015, 4, e09343, doi:10.7554/eLife.09343.
  51. Yu, A.; Lepere, G.; Jay, F.; Wang, J.; Bapaume, L.; Wang, Y.; Abraham, A.-L.; Penterman, J.; Fischer, R.L.; Voinnet, O.; et al. Dynamics and biological relevance of DNA demethylation in Arabidopsis antibacterial defense. Proc. Natl. Acad. Sci. 2013, 110, 2389–2394, doi:10.1073/pnas.1211757110.Yong-Villalobos, L.; González-Morales, S.I.; Wrobel, K.; Gutiérrez-Alanis, D.; Cervantes-Peréz, S.A.; Hayano-Kanashiro, C.; Oropeza-Aburto, A.; Cruz-Ramírez, A.; Martínez, O.; Herrera-Estrella, L. Methylome analysis reveals an important role for epigenetic changes in the regulation of the Arabidopsis response to phosphate starvation. Proc. Natl. Acad. Sci. 2015, 112, E7293–E7302, doi:10.1073/pnas.1522301112.
  52. López Sánchez, A.; Stassen, J.H.M.; Furci, L.; Smith, L.M.; Ton, J. The role of DNA (de)methylation in immune responsiveness of Arabidopsis. Plant J. 2016, 88, 361–374, doi:10.1111/tpj.13252.Chen, X.; Sch�nberger, B.; Menz, J.; Ludewig, U. Plasticity of DNA methylation and gene expression under zinc deficiency in Arabidopsis roots. Plant Cell Physiol. 2018, 59, 1790–1802, doi:10.1093/pcp/pcy100.
  53. Meller, B.; Kuźnicki, D.; Arasimowicz-Jelonek, M.; Deckert, J.; Floryszak-Wieczorek, J. BABA-Primed Histone Modifications in Potato for Intergenerational Resistance to Phytophthora infestans. Front. Plant Sci. 2018, 9, 1228, doi:10.3389/fpls.2018.01228.Mager, S.; Schönberger, B.; Ludewig, U. The transcriptome of zinc deficient maize roots and its relationship to DNA methylation loss. BMC Plant Biol. 2018, 18, 372, doi:10.1186/s12870-018-1603-z.
  54. Rambani, A.; Rice, J.H.; Liu, J.; Lane, T.; Ranjan, P.; Mazarei, M.; Pantalone, V.; Stewart, C.N.; Staton, M.; Hewezi, T. The Methylome of Soybean Roots during the Compatible Interaction with the Soybean Cyst Nematode. Plant Physiol. 2015, 168, 1364–1377, doi:10.1104/pp.15.00826.Martínez-Pérez, M.; Aparicio, F.; López-Gresa, M.P.; Bellés, J.M.; Sánchez-Navarro, J.A.; Pallás, V. Arabidopsis m 6 A demethylase activity modulates viral infection of a plant virus and the m 6 A abundance in its genomic RNAs. Proc. Natl. Acad. Sci. 2017, 114, 10755–10760, doi:10.1073/pnas.1703139114.
  55. Rambani, A.; Pantalone, V.; Yang, S.; Rice, J.H.; Song, Q.; Mazarei, M.; Arelli, P.R.; Meksem, K.; Stewart, C.N.; Hewezi, T. Identification of introduced and stably inherited DNA methylation variants in soybean associated with soybean cyst nematode parasitism. New Phytol. 2020, 227, 168–184, doi:10.1111/nph.16511.Deleris, A.; Halter, T.; Navarro, L. DNA Methylation and Demethylation in Plant Immunity. Annu. Rev. Phytopathol. 2016, 54, 579–603, doi:10.1146/annurev-phyto-080615-100308.
  56. Gaut, B.S.; Miller, A.J.; Seymour, D.K. Living with Two Genomes: Grafting and Its Implications for Plant Genome-to-Genome Interactions, Phenotypic Variation, and Evolution. Annu. Rev. Genet. 2019, 53, 195–215, doi:10.1146/annurev-genet-112618-043545.Dowen, R.H.; Pelizzola, M.; Schmitz, R.J.; Lister, R.; Dowen, J.M.; Nery, J.R.; Dixon, J.E.; Ecker, J.R. Widespread dynamic DNA methylation in response to biotic stress. Proc. Natl. Acad. Sci. 2012, 109, E2183–E2191, doi:10.1073/pnas.1209329109.
  57. Kim, G.; LeBlanc, M.L.; Wafula, E.K.; dePamphilis, C.W.; Westwood, J.H. Genomic-scale exchange of mRNA between a parasitic plant and its hosts. Science 2014, 345, 808–811, doi:10.1126/science.1253122.Yu, A.; Lepere, G.; Jay, F.; Wang, J.; Bapaume, L.; Wang, Y.; Abraham, A.-L.; Penterman, J.; Fischer, R.L.; Voinnet, O.; et al. Dynamics and biological relevance of DNA demethylation in Arabidopsis antibacterial defense. Proc. Natl. Acad. Sci. 2013, 110, 2389–2394, doi:10.1073/pnas.1211757110.
  58. Kaiser, B.; Vogg, G.; Fürst, U.B.; Albert, M. Parasitic plants of the genus Cuscuta and their interaction with susceptible and resistant host plants. Front. Plant Sci. 2015, 6, doi:10.3389/fpls.2015.00045.López Sánchez, A.; Stassen, J.H.M.; Furci, L.; Smith, L.M.; Ton, J. The role of DNA (de)methylation in immune responsiveness of Arabidopsis. Plant J. 2016, 88, 361–374, doi:10.1111/tpj.13252.
  59. LeBlanc, M.; Kim, G.; Patel, B.; Stromberg, V.; Westwood, J. Quantification of tomato and Arabidopsis mobile RNAs trafficking into the parasitic plant Cuscuta pentagona. New Phytol. 2013, 200, 1225–1233, doi:10.1111/nph.12439.Furci, L.; Jain, R.; Stassen, J.; Berkowitz, O.; Whelan, J.; Roquis, D.; Baillet, V.; Colot, V.; Johannes, F.; Ton, J. Identification and characterisation of hypomethylated DNA loci controlling quantitative resistance in Arabidopsis. eLife 2019, 8, e40655, doi:10.7554/eLife.40655.
  60. Alakonya, A.; Kumar, R.; Koenig, D.; Kimura, S.; Townsley, B.; Runo, S.; Garces, H.M.; Kang, J.; Yanez, A.; David-Schwartz, R.; et al. Interspecific RNA Interference of SHOOT MERISTEMLESS-Like Disrupts Cuscuta pentagona Plant Parasitism. Plant Cell 2012, 24, 3153–3166, doi:10.1105/tpc.112.099994.Liégard, B.; Baillet, V.; Etcheverry, M.; Joseph, E.; Lariagon, C.; Lemoine, J.; Evrard, A.; Colot, V.; Gravot, A.; Manzanares‐Dauleux, M.J.; et al. Quantitative resistance to clubroot infection mediated by transgenerational epigenetic variation in Arabidopsis. New Phytol. 2019, 222, 468–479, doi:10.1111/nph.15579.
  61. Shahid, S.; Kim, G.; Johnson, N.R.; Wafula, E.; Wang, F.; Coruh, C.; Bernal-Galeano, V.; Phifer, T.; dePamphilis, C.W.; Westwood, J.H.; et al. MicroRNAs from the parasitic plant Cuscuta campestris target host messenger RNAs. Nature 2018, 553, 82–85, doi:10.1038/nature25027.Meller, B.; Kuźnicki, D.; Arasimowicz-Jelonek, M.; Deckert, J.; Floryszak-Wieczorek, J. BABA-Primed Histone Modifications in Potato for Intergenerational Resistance to Phytophthora infestans. Front. Plant Sci. 2018, 9, 1228, doi:10.3389/fpls.2018.01228.
  62. Sanchez, D.H.; Paszkowski, J. Heat-Induced Release of Epigenetic Silencing Reveals the Concealed Role of an Imprinted Plant Gene. PLoS Genet. 2014, 10, e1004806, doi:10.1371/journal.pgen.1004806.Kuźnicki, D.; Meller, B.; Arasimowicz-Jelonek, M.; Braszewska-Zalewska, A.; Drozda, A.; Floryszak-Wieczorek, J. BABA-Induced DNA Methylome Adjustment to Intergenerational Defense Priming in Potato to Phytophthora infestans. Front. Plant Sci. 2019, 10, 650, doi:10.3389/fpls.2019.00650.
  63. Lämke, J.; Bäurle, I. Epigenetic and chromatin-based mechanisms in environmental stress adaptation and stress memory in plants. Genome Biol. 2017, 18, 124, doi:10.1186/s13059-017-1263-6.Lee, S.; Fu, F.; Xu, S.; Lee, S.Y.; Yun, D.-J.; Mengiste, T. Global regulation of plant immunity by histone lysine methyl transferases. Plant Cell 2016, tpc.00012.2016, doi:10.1105/tpc.16.00012.
  64. Ashapkin, V.V.; Kutueva, L.I.; Vanyushin, B.F. Epigenetic variability in plants: Heritability, adaptability, evolutionary significance. Russ. J. Plant Physiol. 2016, 63, 181–192, doi:10.1134/S1021443716020059.Crespo-Salvador, Ó.; Sánchez-Giménez, L.; López-Galiano, M.; Fernández-Crespo, E.; Scalschi, L.; García-Robles, I.; Rausell, C.; Real, M.; González-Bosch, C. The Histone Marks Signature in Exonic and Intronic Regions Is Relevant in Early Response of Tomato Genes to Botrytis cinerea and in miRNA Regulation. Plants 2020, 9, 300, doi:10.3390/plants9030300.
  65. Cong, W.; Miao, Y.; Xu, L.; Zhang, Y.; Yuan, C.; Wang, J.; Zhuang, T.; Lin, X.; Jiang, L.; Wang, N.; et al. Transgenerational memory of gene expression changes induced by heavy metal stress in rice (Oryza sativa L.). BMC Plant Biol. 2019, 19, 282, doi:10.1186/s12870-019-1887-7.Rambani, A.; Rice, J.H.; Liu, J.; Lane, T.; Ranjan, P.; Mazarei, M.; Pantalone, V.; Stewart, C.N.; Staton, M.; Hewezi, T. The Methylome of Soybean Roots during the Compatible Interaction with the Soybean Cyst Nematode. Plant Physiol. 2015, 168, 1364–1377, doi:10.1104/pp.15.00826.
  66. Zheng, X.; Chen, L.; Xia, H.; Wei, H.; Lou, Q.; Li, M.; Li, T.; Luo, L. Transgenerational epimutations induced by multi-generation drought imposition mediate rice plant’s adaptation to drought condition. Sci. Rep. 2017, 7, 39843, doi:10.1038/srep39843.Rambani, A.; Pantalone, V.; Yang, S.; Rice, J.H.; Song, Q.; Mazarei, M.; Arelli, P.R.; Meksem, K.; Stewart, C.N.; Hewezi, T. Identification of introduced and stably inherited DNA methylation variants in soybean associated with soybean cyst nematode parasitism. New Phytol. 2020, 227, 168–184, doi:10.1111/nph.16511.
  67. Law, J.A.; Jacobsen, S.E. Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nat. Rev. Genet. 2010, 11, 204–220, doi:10.1038/nrg2719.Gaut, B.S.; Miller, A.J.; Seymour, D.K. Living with Two Genomes: Grafting and Its Implications for Plant Genome-to-Genome Interactions, Phenotypic Variation, and Evolution. Annu. Rev. Genet. 2019, 53, 195–215, doi:10.1146/annurev-genet-112618-043545.
  68. Ito, H.; Gaubert, H.; Bucher, E.; Mirouze, M.; Vaillant, I.; Paszkowski, J. An siRNA pathway prevents transgenerational retrotransposition in plants subjected to stress. Nature 2011, 472, 115–119, doi:10.1038/nature09861.Kim, G.; LeBlanc, M.L.; Wafula, E.K.; dePamphilis, C.W.; Westwood, J.H. Genomic-scale exchange of mRNA between a parasitic plant and its hosts. Science 2014, 345, 808–811, doi:10.1126/science.1253122.
  69. Eichten, S.R.; Schmitz, R.J.; Springer, N.M. Epigenetics: Beyond Chromatin Modifications and Complex Genetic Regulation. Plant Physiol. 2014, 165, 933–947, doi:10.1104/pp.113.234211.Kaiser, B.; Vogg, G.; Fürst, U.B.; Albert, M. Parasitic plants of the genus Cuscuta and their interaction with susceptible and resistant host plants. Front. Plant Sci. 2015, 6, doi:10.3389/fpls.2015.00045.
  70. Schmitz, R.J.; Ecker, J.R. Epigenetic and epigenomic variation in Arabidopsis thaliana. Trends Plant Sci. 2012, 17, 149–154, doi:10.1016/j.tplants.2012.01.001.LeBlanc, M.; Kim, G.; Patel, B.; Stromberg, V.; Westwood, J. Quantification of tomato and Arabidopsis mobile RNAs trafficking into the parasitic plant Cuscuta pentagona. New Phytol. 2013, 200, 1225–1233, doi:10.1111/nph.12439.
  71. Alakonya, A.; Kumar, R.; Koenig, D.; Kimura, S.; Townsley, B.; Runo, S.; Garces, H.M.; Kang, J.; Yanez, A.; David-Schwartz, R.; et al. Interspecific RNA Interference of SHOOT MERISTEMLESS-Like Disrupts Cuscuta pentagona Plant Parasitism. Plant Cell 2012, 24, 3153–3166, doi:10.1105/tpc.112.099994.
  72. Shahid, S.; Kim, G.; Johnson, N.R.; Wafula, E.; Wang, F.; Coruh, C.; Bernal-Galeano, V.; Phifer, T.; dePamphilis, C.W.; Westwood, J.H.; et al. MicroRNAs from the parasitic plant Cuscuta campestris target host messenger RNAs. Nature 2018, 553, 82–85, doi:10.1038/nature25027.
  73. Sanchez, D.H.; Paszkowski, J. Heat-Induced Release of Epigenetic Silencing Reveals the Concealed Role of an Imprinted Plant Gene. PLoS Genet. 2014, 10, e1004806, doi:10.1371/journal.pgen.1004806.
  74. Lämke, J.; Bäurle, I. Epigenetic and chromatin-based mechanisms in environmental stress adaptation and stress memory in plants. Genome Biol. 2017, 18, 124, doi:10.1186/s13059-017-1263-6.
  75. Liu, N.; Ding, Y.; Fromm, M.; Avramova, Z. Different gene-specific mechanisms determine the ‘revised-response’ memory transcription patterns of a subset of A. thaliana dehydration stress responding genes. Nucleic Acids Res. 2014, 42, 5556–5566, doi:10.1093/nar/gku220.
  76. Liu, N.; Fromm, M.; Avramova, Z. H3K27me3 and H3K4me3 Chromatin Environment at Super-Induced Dehydration Stress Memory Genes of Arabidopsis thaliana. Mol. Plant 2014, 7, 502–513, doi:10.1093/mp/ssu001.
  77. Ashapkin, V.V.; Kutueva, L.I.; Vanyushin, B.F. Epigenetic variability in plants: Heritability, adaptability, evolutionary significance. Russ. J. Plant Physiol. 2016, 63, 181–192, doi:10.1134/S1021443716020059.
  78. Cong, W.; Miao, Y.; Xu, L.; Zhang, Y.; Yuan, C.; Wang, J.; Zhuang, T.; Lin, X.; Jiang, L.; Wang, N.; et al. Transgenerational memory of gene expression changes induced by heavy metal stress in rice (Oryza sativa L.). BMC Plant Biol. 2019, 19, 282, doi:10.1186/s12870-019-1887-7.
  79. Zheng, X.; Chen, L.; Xia, H.; Wei, H.; Lou, Q.; Li, M.; Li, T.; Luo, L. Transgenerational epimutations induced by multi-generation drought imposition mediate rice plant’s adaptation to drought condition. Sci. Rep. 2017, 7, 39843, doi:10.1038/srep39843.
  80. Law, J.A.; Jacobsen, S.E. Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nat. Rev. Genet. 2010, 11, 204–220, doi:10.1038/nrg2719.
  81. Ito, H.; Gaubert, H.; Bucher, E.; Mirouze, M.; Vaillant, I.; Paszkowski, J. An siRNA pathway prevents transgenerational retrotransposition in plants subjected to stress. Nature 2011, 472, 115–119, doi:10.1038/nature09861.
  82. Matsunaga, W.; Kobayashi, A.; Kato, A.; Ito, H. The effects of heat induction and the siRNA biogenesis pathway on the transgenerational transposition of ONSEN, a copia-like retrotransposon in Arabidopsis thaliana. Plant Cell Physiol. 2012, 53, 824–833, doi:10.1093/pcp/pcr179.
  83. Matsunaga, W.; Ohama, N.; Tanabe, N.; Masuta, Y.; Masuda, S.; Mitani, N.; Yamaguchi-Shinozaki, K.; Ma, J.F.; Kato, A.; Ito, H. A small RNA mediated regulation of a stress-activated retrotransposon and the tissue specific transposition during the reproductive period in Arabidopsis. Front. Plant Sci. 2015, 6, doi:10.3389/fpls.2015.00048.
  84. Cavrak, V.V.; Lettner, N.; Jamge, S.; Kosarewicz, A.; Bayer, L.M.; Mittelsten Scheid, O. How a Retrotransposon Exploits the Plant’s Heat Stress Response for Its Activation. PLoS Genet. 2014, 10, e1004115, doi:10.1371/journal.pgen.1004115.
  85. Saze, H. Epigenetic regulation of intragenic transposable elements: a two-edged sword. J. Biochem. (Tokyo) 2018, 164, 323–328, doi:10.1093/jb/mvy060.
  86. Ito, H.; Kim, J.-M.; Matsunaga, W.; Saze, H.; Matsui, A.; Endo, T.A.; Harukawa, Y.; Takagi, H.; Yaegashi, H.; Masuta, Y.; et al. A Stress-Activated Transposon in Arabidopsis Induces Transgenerational Abscisic Acid Insensitivity. Sci. Rep. 2016, 6, 23181, doi:10.1038/srep23181.
  87. Rasmann, S.; De Vos, M.; Casteel, C.L.; Tian, D.; Halitschke, R.; Sun, J.Y.; Agrawal, A.A.; Felton, G.W.; Jander, G. Herbivory in the Previous Generation Primes Plants for Enhanced Insect Resistance. Plant Physiol. 2012, 158, 854–863, doi:10.1104/pp.111.187831.
  88. Ou, X.; Zhang, Y.; Xu, C.; Lin, X.; Zang, Q.; Zhuang, T.; Jiang, L.; von Wettstein, D.; Liu, B. Transgenerational Inheritance of Modified DNA Methylation Patterns and Enhanced Tolerance Induced by Heavy Metal Stress in Rice (Oryza sativa L.). PLoS ONE 2012, 7, e41143, doi:10.1371/journal.pone.0041143.
  89. Lira-Medeiros, C.F.; Parisod, C.; Fernandes, R.A.; Mata, C.S.; Cardoso, M.A.; Ferreira, P.C.G. Epigenetic Variation in Mangrove Plants Occurring in Contrasting Natural Environment. PLoS ONE 2010, 5, e10326, doi:10.1371/journal.pone.0010326.
  90. Richards, C.L.; Schrey, A.W.; Pigliucci, M. Invasion of diverse habitats by few Japanese knotweed genotypes is correlated with epigenetic differentiation. Ecol. Lett. 2012, 15, 1016–1025, doi:10.1111/j.1461-0248.2012.01824.x.
  91. Preite, V.; Snoek, L.B.; Oplaat, C.; Biere, A.; van der Putten, W.H.; Verhoeven, K.J.F. The epigenetic footprint of poleward range-expanding plants in apomictic dandelions. Mol. Ecol. 2015, 24, 4406–4418, doi:10.1111/mec.13329.
  92. Wilschut, R.A.; Oplaat, C.; Snoek, L.B.; Kirschner, J.; Verhoeven, K.J.F. Natural epigenetic variation contributes to heritable flowering divergence in a widespread asexual dandelion lineage. Mol. Ecol. 2016, 25, 1759–1768, doi:10.1111/mec.13502.
  93. Preite, V.; Oplaat, C.; Biere, A.; Kirschner, J.; van der Putten, W.H.; Verhoeven, K.J.F. Increased transgenerational epigenetic variation, but not predictable epigenetic variants, after environmental exposure in two apomictic dandelion lineages. Ecol. Evol. 2018, 8, 3047–3059, doi:10.1002/ece3.3871.
  94. Foust, C.M.; Preite, V.; Schrey, A.W.; Alvarez, M.; Robertson, M.H.; Verhoeven, K.J.F.; Richards, C.L. Genetic and epigenetic differences associated with environmental gradients in replicate populations of two salt marsh perennials. Mol. Ecol. 2016, 25, 1639–1652, doi:10.1111/mec.13522.
  95. Schmitz, R.J.; Schultz, M.D.; Urich, M.A.; Nery, J.R.; Pelizzola, M.; Libiger, O.; Alix, A.; McCosh, R.B.; Chen, H.; Schork, N.J.; et al. Patterns of population epigenomic diversity. Nature 2013, 495, 193–198, doi:10.1038/nature11968.
  96. Dubin, M.J.; Zhang, P.; Meng, D.; Remigereau, M.-S.; Osborne, E.J.; Paolo Casale, F.; Drewe, P.; Kahles, A.; Jean, G.; Vilhjálmsson, B.; et al. DNA methylation in Arabidopsis has a genetic basis and shows evidence of local adaptation. eLife 2015, 4, e05255, doi:10.7554/eLife.05255.
  97. Keller, T.E.; Lasky, J.R.; Yi, S.V. The multivariate association between genomewide DNA methylation and climate across the range of Arabidopsis thaliana. Mol. Ecol. 2016, 25, 1823–1837, doi:10.1111/mec.13573.
  98. Herrera, C.M.; Medrano, M.; Bazaga, P. Comparative spatial genetics and epigenetics of plant populations: heuristic value and a proof of concept. Mol. Ecol. 2016, 25, 1653–1664, doi:10.1111/mec.13576.
  99. Zoldoš, V.; Biruš, I.; Muratović, E.; Šatović, Z.; Vojta, A.; Robin, O.; Pustahija, F.; Bogunić, F.; Vičić Bočkor, V.; Siljak-Yakovlev, S. Epigenetic Differentiation of Natural Populations of Lilium bosniacum Associated with Contrasting Habitat Conditions. Genome Biol. Evol. 2018, 10, 291–303, doi:10.1093/gbe/evy010.
  100. Vanden Broeck, A.; Cox, K.; Brys, R.; Castiglione, S.; Cicatelli, A.; Guarino, F.; Heinze, B.; Steenackers, M.; Vander Mijnsbrugge, K. Variability in DNA Methylation and Generational Plasticity in the Lombardy Poplar, a Single Genotype Worldwide Distributed Since the Eighteenth Century. Front. Plant Sci. 2018, 9, 1635, doi:10.3389/fpls.2018.01635.
  101. Alakärppä, E.; Salo, H.M.; Valledor, L.; Cañal, M.J.; Häggman, H.; Vuosku, J. Natural variation of DNA methylation and gene expression may determine local adaptations of Scots pine populations. J. Exp. Bot. 2018, 69, 5293–5305, doi:10.1093/jxb/ery292.
  102. Eichten, S.R.; Srivastava, A.; Reddiex, A.J.; Ganguly, D.R.; Heussler, A.; Streich, J.C.; Wilson, P.B.; Borevitz, J.O. Extending the Genotype in Brachypodium by Including DNA Methylation Reveals a Joint Contribution with Genetics on Adaptive Traits. G3amp58 GenesGenomesGenetics 2020, 10, 1629–1637, doi:10.1534/g3.120.401189.
  103. Eichten, S.R.; Schmitz, R.J.; Springer, N.M. Epigenetics: Beyond Chromatin Modifications and Complex Genetic Regulation. Plant Physiol. 2014, 165, 933–947, doi:10.1104/pp.113.234211.
  104. Schmitz, R.J.; Ecker, J.R. Epigenetic and epigenomic variation in Arabidopsis thaliana. Trends Plant Sci. 2012, 17, 149–154, doi:10.1016/j.tplants.2012.01.001.
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