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Plant Epigenetic Stress Memory Induced by Drought: A Physiological and Molecular Perspective

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Plant Epigenetics and Epigenomics

Part of the book series: Methods in Molecular Biology ((MIMB,volume 2093))

Abstract

Drought stress is one of the most common stresses encountered by crops and other plants and leads to significant productivity losses. It commonly happens that drought stress occurs more than once during the plant’s life cycle. Plants suffering from drought stress can adapt their life strategies to acclimate and survive in many different ways. Interestingly, some plants have evolved a stress response strategy referred to as stress memory which leads to an enhanced response the next time the stress is encountered. The acquisition of stress memory leads to a reprogrammed transcriptional response during subsequent stress and subsequent changes both at the physiological and molecular level. Recent advances in understanding chromatin dynamics have demonstrated the involvement of chromatin modifications, especially histone marks, associated with drought stress-responsive memory genes and subsequent enhanced transcriptional responses to repeated drought stress. In this chapter, we describe recent progress in this area and summarize techniques for the study of plant epigenetic responses to stress, including the roles of ABA and transcription factors in superinduced transcriptional activation during recurrent drought stress. We also review the possible use of seed priming to induce stress memory later in the plant life cycle. Finally, we discuss the potential implications of understanding the epigenetic mechanisms involved in plant stress memory for future applications in crop improvement and drought resistance.

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References

  1. Ciais P, Reichstein M, Viovy N et al (2005) Europe-wide reduction in primary productivity caused by the heat and drought in 2003. Nature 437:529–533. https://doi.org/10.1038/nature03972

    Article  CAS  PubMed  Google Scholar 

  2. Lobell DB, Schlenker W, Costa-Roberts J (2011) Climate trends and global crop production since 1980. Science 333(80):616–620. https://doi.org/10.1126/science.1204531

    Article  CAS  PubMed  Google Scholar 

  3. Tack J, Barkley A, Nalley LL (2015) Effect of warming temperatures on US wheat yields. Proc Natl Acad Sci U S A 112:6931–6936. https://doi.org/10.1073/pnas.1415181112

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Daryanto S, Wang L, Jacinthe P-A (2016) Global synthesis of drought effects on maize and wheat production. PLoS One 11:e0156362. https://doi.org/10.1371/journal.pone.0156362

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Jakab G, Ton J, Flors V et al (2005) Enhancing Arabidopsis salt and drought stress tolerance by chemical priming for its abscisic acid responses. Plant Physiol 139:267 LP–267274. https://doi.org/10.1104/pp.105.065698

    Article  CAS  Google Scholar 

  6. Maseda PH, Fernández RJ (2006) Stay wet or else: three ways in which plants can adjust hydraulically to their environment. J Exp Bot 57:3963–3977. https://doi.org/10.1093/jxb/erl127

    Article  CAS  PubMed  Google Scholar 

  7. Ding Y, Fromm M, Avramova Z (2012) Multiple exposures to drought “train” transcriptional responses in Arabidopsis. Nat Commun 3:740–749. https://doi.org/10.1038/ncomms1732

    Article  CAS  PubMed  Google Scholar 

  8. Ding Y, Virlouvet L, Liu N et al (2014) Dehydration stress memory genes of Zea mays; comparison with Arabidopsis thaliana. BMC Plant Biol 14:141. https://doi.org/10.1186/1471-2229-14-141

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Ramírez DA, Rolando JL, Yactayo W et al (2015) Improving potato drought tolerance through the induction of long-term water stress memory. Plant Sci 238:26–32. https://doi.org/10.1016/j.plantsci.2015.05.016

    Article  CAS  PubMed  Google Scholar 

  10. Walter J, Nagy L, Hein R et al (2011) Do plants remember drought? Hints towards a drought-memory in grasses. Environ Exp Bot 71:34–40. https://doi.org/10.1016/j.envexpbot.2010.10.020

    Article  Google Scholar 

  11. D’Urso A, Brickner JH (2014) Mechanisms of epigenetic memory. Trends Genet 30:230–236. https://doi.org/10.1016/j.tig.2014.04.004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Crisp PA, Ganguly D, Eichten SR et al (2016) Reconsidering plant memory: intersections between stress recovery, RNA turnover, and epigenetics. Sci Adv 2:e1501340–e1501340. https://doi.org/10.1126/sciadv.1501340

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Skirycz A, Inzé D (2010) More from less: plant growth under limited water. Curr Opin Biotechnol 21:197–203. https://doi.org/10.1016/j.copbio.2010.03.002

    Article  CAS  PubMed  Google Scholar 

  14. Ton J, Jakab G, Toquin V et al (2005) Dissecting the β-aminobutyric acid–induced priming phenomenon in Arabidopsis. Plant Cell 17:987 LP–987999. https://doi.org/10.1105/tpc.104.029728

    Article  CAS  Google Scholar 

  15. Zimmerli L, Hou B-H, Tsai C-H et al (2008) The xenobiotic β-aminobutyric acid enhances Arabidopsis thermotolerance. Plant J 53:144–156. https://doi.org/10.1111/j.1365-313X.2007.03343.x

    Article  CAS  PubMed  Google Scholar 

  16. van Hulten M, Pelser M, van Loon LC et al (2006) Costs and benefits of priming for defense in Arabidopsis. Proc Natl Acad Sci U S A 103:5602–5607. https://doi.org/10.1073/pnas.0510213103

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Kinoshita T, Seki M (2014) Epigenetic memory for stress response and adaptation in plants. Plant Cell Physiol 55:1859–1863. https://doi.org/10.1093/pcp/pcu125

    Article  CAS  PubMed  Google Scholar 

  18. Avramova Z (2015) Transcriptional “memory” of a stress: transient chromatin and memory (epigenetic) marks at stress-response genes. Plant J 83:149–159. https://doi.org/10.1111/tpj.12832

    Article  CAS  PubMed  Google Scholar 

  19. Lämke J, Bäurle I (2017) Epigenetic and chromatin-based mechanisms in environmental stress adaptation and stress memory in plants. Genome Biol 18:1–11. https://doi.org/10.1186/s13059-017-1263-6

    Article  CAS  Google Scholar 

  20. Hilker M, Schwachtje J, Baier M et al (2016) Priming and memory of stress responses in organisms lacking a nervous system. Biol Rev 91:1118–1133. https://doi.org/10.1111/brv.12215

    Article  PubMed  Google Scholar 

  21. Weinhold A (2018) Transgenerational stress-adaption: an opportunity for ecological epigenetics. Plant Cell Rep 37:3–9. https://doi.org/10.1007/s00299-017-2216-y

    Article  CAS  PubMed  Google Scholar 

  22. Iglesias FM, Cerdán PD (2016) Maintaining epigenetic inheritance during DNA replication in plants. Front Plant Sci 7:38

    Article  PubMed  PubMed Central  Google Scholar 

  23. Hauser M-T, Aufsatz W, Jonak C, Luschnig C (2011) Transgenerational epigenetic inheritance in plants. Biochim Biophys Acta 1809:459–468. https://doi.org/10.1016/j.bbagrm.2011.03.007

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Amtmann A, Sani E, Herzyk P et al (2013) Hyperosmotic priming of Arabidopsis seedlings establishes a long-term somatic memory accompanied by specific changes of the epigenome. Genome Biol 14:R59

    Article  PubMed  PubMed Central  Google Scholar 

  25. Wibowo A, Becker C, Marconi G et al (2016) Hyperosmotic stress memory in Arabidopsis is mediated by distinct epigenetically labile sites in the genome and is restricted in the male germline by DNA glycosylase activity. Elife 5:e13546. https://doi.org/10.7554/eLife.13546

    Article  PubMed  PubMed Central  Google Scholar 

  26. Pecinka A, Mittelsten Scheid O (2012) Stress-induced chromatin changes: a critical view on their heritability. Plant Cell Physiol 53:801–808. https://doi.org/10.1093/pcp/pcs044

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Bruce TJA, Matthes MC, Napier JA, Pickett JA (2007) Stressful “memories” of plants: evidence and possible mechanisms. Plant Sci 173:603–608. https://doi.org/10.1016/j.plantsci.2007.09.002

    Article  CAS  Google Scholar 

  28. Conrath U, Beckers GJM, Langenbach CJG, Jaskiewicz MR (2015) Priming for enhanced defense. Annu Rev Phytopathol 53:97–119. https://doi.org/10.1146/annurev-phyto-080614-120132

    Article  CAS  PubMed  Google Scholar 

  29. Kim J-M, Sasaki T, Ueda M et al (2015) Chromatin changes in response to drought, salinity, heat, and cold stresses in plants. Front Plant Sci 6:1–12. https://doi.org/10.3389/fpls.2015.00114

    Article  Google Scholar 

  30. Zentner GE, Henikoff S (2013) Regulation of nucleosome dynamics by histone modifications. Nat Struct Mol Biol 20:259

    Article  CAS  PubMed  Google Scholar 

  31. Luger K, Mäder AW, Richmond RK et al (1997) Crystal structure of the nucleosome core particle at 2.8 Å resolution. Nature 389:251–260. https://doi.org/10.1038/38444

    Article  CAS  PubMed  Google Scholar 

  32. Hergeth SP, Schneider R (2015) The H1 linker histones: multifunctional proteins beyond the nucleosomal core particle. EMBO Rep 16:1439–1453. https://doi.org/10.15252/embr.201540749

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Yuan L, Liu X, Luo M et al (2013) Involvement of histone modifications in plant abiotic stress responses. J Integr Plant Biol 55:892–901. https://doi.org/10.1111/jipb.12060

    Article  CAS  PubMed  Google Scholar 

  34. Campos EI, Reinberg D (2009) Histones: annotating chromatin. Annu Rev Genet 43:559–599. https://doi.org/10.1146/annurev.genet.032608.103928

    Article  CAS  PubMed  Google Scholar 

  35. Bártová E, Krejcí J, Harnicarová A et al (2008) Histone modifications and nuclear architecture: a review. J Histochem Cytochem 56:711–721. https://doi.org/10.1369/jhc.2008.951251

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Farooq M, Hussain M, Wahid A, Siddique KHM (2012) Drought stress in plants: an overview. In: Aroca R (ed) Plant responses to drought stress: from morphological to molecular features. Springer, Berlin, Heidelberg, pp 1–33

    Google Scholar 

  37. Kim JM, To TK, Ishida J et al (2012) Transition of chromatin status during the process of recovery from drought stress in arabidopsis thaliana. Plant Cell Physiol 53:847–856. https://doi.org/10.1093/pcp/pcs053

    Article  CAS  PubMed  Google Scholar 

  38. Bäurle I (2018) Can’t remember to forget you: chromatin-based priming of somatic stress responses. Semin Cell Dev Biol 83:133–139. https://doi.org/10.1016/j.semcdb.2017.09.032

    Article  CAS  PubMed  Google Scholar 

  39. Tuteja N (2007) Abscisic acid and abiotic stress signaling. Plant Signal Behav 2:135–138

    Article  PubMed  PubMed Central  Google Scholar 

  40. Verslues PE, Agarwal M, Katiyar-Agarwal S et al (2006) Methods and concepts in quantifying resistance to drought, salt and freezing, abiotic stresses that affect plant water status. Plant J 45:523–539. https://doi.org/10.1111/j.1365-313X.2005.02593.x

    Article  CAS  PubMed  Google Scholar 

  41. Fleta-Soriano E, Pintó-Marijuan M, Munné-Bosch S (2015) Evidence of drought stress memory in the facultative CAM, Aptenia cordifolia: possible role of phytohormones. PLoS One 10:1–12. https://doi.org/10.1371/journal.pone.0135391

    Article  CAS  Google Scholar 

  42. Ding Y, Liu N, Virlouvet L et al (2013) Four distinct types of dehydration stress memory genes in Arabidopsis thaliana. BMC Plant Biol 13:229. https://doi.org/10.1186/1471-2229-13-229

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Virlouvet L, Fromm M (2015) Physiological and transcriptional memory in guard cells during repetitive dehydration stress. New Phytol 205:596–607. https://doi.org/10.1111/nph.13080

    Article  CAS  PubMed  Google Scholar 

  44. Li P, Yang H, Wang L et al (2019) Physiological and transcriptome analyses reveal short-term responses and formation of memory under drought stress in rice. Front Genet 10:1–16. https://doi.org/10.3389/fgene.2019.00055

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Selote DS, Khanna-Chopra R (2010) Antioxidant response of wheat roots to drought acclimation. Protoplasma 245:153–163. https://doi.org/10.1007/s00709-010-0169-x

    Article  CAS  PubMed  Google Scholar 

  46. Selote DS, Khanna-Chopra R (2006) Drought acclimation confers oxidative stress tolerance by inducing co-ordinated antioxidant defense at cellular and subcellular level in leaves of wheat seedlings. Physiol Plant 127:494–506. https://doi.org/10.1111/j.1399-3054.2006.00678.x

    Article  CAS  Google Scholar 

  47. Wang X, Vignjevic M, Jiang D et al (2014) Improved tolerance to drought stress after anthesis due to priming before anthesis in wheat (Triticum aestivum L.) var. Vinjett. J Exp Bot 65:6441–6456. https://doi.org/10.1093/jxb/eru362

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Sgherri CLM, Navari-lzzo F, Menconi M, Pinzino C (1995) Activated oxygen production and detoxification in wheat plants subjected to a water deficit programme. J Exp Bot 46:1123–1130. https://doi.org/10.1093/jxb/46.9.1123

    Article  Google Scholar 

  49. Li X, Zhang L, Li Y (2011) Preconditioning alters antioxidative enzyme responses in rice seedlings to water stress. Procedia Environ Sci 11:1346–1351. https://doi.org/10.1016/j.proenv.2011.12.202

    Article  CAS  Google Scholar 

  50. Wang X, Liu F-L, Jiang D (2017) Priming: a promising strategy for crop production in response to future climate. J Integr Agric 16(12):2709–2716. https://doi.org/10.1016/S2095-3119(17)61786-6

    Article  Google Scholar 

  51. Wang X, Vignjevic M, Liu F et al (2015) Drought priming at vegetative growth stages improves tolerance to drought and heat stresses occurring during grain filling in spring wheat. Plant Growth Regul 75:677–687. https://doi.org/10.1007/s10725-014-9969-x

    Article  CAS  Google Scholar 

  52. Zhang X, Xu Y, Huang B (2019) Lipidomic reprogramming associated with drought stress priming-enhanced heat tolerance in tall fescue (Festuca arundinacea). Plant Cell Environ 42:947–958. https://doi.org/10.1111/pce.13405

    Article  CAS  PubMed  Google Scholar 

  53. Ashoub A, Baeumlisberger M, Neupaertl M et al (2015) Characterization of common and distinctive adjustments of wild barley leaf proteome under drought acclimation, heat stress and their combination. Plant Mol Biol 87:459–471. https://doi.org/10.1007/s11103-015-0291-4

    Article  CAS  PubMed  Google Scholar 

  54. Chen K, Arora R (2013) Priming memory invokes seed stress-tolerance. Environ Exp Bot 94:33–45. https://doi.org/10.1016/j.envexpbot.2012.03.005

    Article  CAS  Google Scholar 

  55. Buitink J, Leger JJ, Guisle I et al (2006) Transcriptome profiling uncovers metabolic and regulatory processes occurring during the transition from desiccation-sensitive to desiccation-tolerant stages in Medicago truncatula seeds. Plant J 47:735–750

    Article  CAS  PubMed  Google Scholar 

  56. Daws MI, Bolton S, Burslem DFRP et al (2007) Loss of desiccation tolerance during germination in neo-tropical pioneer seeds: implications for seed mortality and germination characteristics. Seed Sci Res 17:273–281. https://doi.org/10.1017/S0960258507837755

    Article  Google Scholar 

  57. Maia J, Dekkers BJW, Provart NJ et al (2011) The re-establishment of desiccation tolerance in germinated arabidopsis thaliana seeds and its associated transcriptome. PLoS One 6:e29123. https://doi.org/10.1371/journal.pone.0029123

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Bruggink T, Van P (1995) Induction of desiccation tolerance in germinated seeds. Seed Sci Res 5:1–4. https://doi.org/10.1017/S096025850000252X

    Article  Google Scholar 

  59. Buitink J, Ly Vu B, Satour P, Leprince O (2003) The re-establishment of desiccation tolerance in germinated radicles of Medicago truncatula Gaertn. seeds. Seed Sci Res 13:273–286. https://doi.org/10.1079/SSR2003145

    Article  CAS  Google Scholar 

  60. Vieira CV, Amaral da Silva EA, de Alvarenga AA et al (2010) Stress-associated factors increase after desiccation of germinated seeds of Tabebuia impetiginosa Mart. Plant Growth Regul 62:257–263. https://doi.org/10.1007/s10725-010-9496-3

    Article  CAS  Google Scholar 

  61. Gallardo K (2001) Proteomic analysis of Arabidopsis seed germination and priming. Plant Physiol 126:835–848. https://doi.org/10.1104/pp.126.2.835

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Catusse J, Meinhard J, Job C et al (2011) Proteomics reveals potential biomarkers of seed vigor in sugarbeet. Proteomics 11:1569–1580. https://doi.org/10.1002/pmic.201000586

    Article  CAS  PubMed  Google Scholar 

  63. Hayat S, Hayat Q, Alyemeni MN et al (2012) Role of proline under changing environments: a review. Plant Signal Behav 7:1456–1466. https://doi.org/10.4161/psb.21949

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Leufen G, Noga G, Hunsche M (2016) Drought stress memory in sugar beet: mismatch between biochemical and physiological parameters. J Plant Growth Regul 35:680–689. https://doi.org/10.1007/s00344-016-9571-8

    Article  CAS  Google Scholar 

  65. Feng XJ, Li JR, Qi SL et al (2016) Light affects salt stress-induced transcriptional memory of P5CS1 in Arabidopsis. Proc Natl Acad Sci U S A 113:E8335–E8343. https://doi.org/10.1073/pnas.1610670114

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Lämke J, Brzezinka K, Altmann S, Bäurle I (2016) A hit-and-run heat shock factor governs sustained histone methylation and transcriptional stress memory. EMBO J 35:162 LP–162175. https://doi.org/10.15252/embj.201592593

    Article  CAS  Google Scholar 

  67. Chen L-Q, Luo J-H, Cui Z-H et al (2017) Encode putative H3K4 methyltransferases and are critical for plant development. Plant Physiol 174:1795–1806. https://doi.org/10.1104/pp.16.01944

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Ding Y, Avramova Z, Fromm M (2011) The Arabidopsis trithorax-like factor ATX1 functions in dehydration stress responses via ABA-dependent and ABA-independent pathways. Plant J 66:735–744. https://doi.org/10.1111/j.1365-313X.2011.04534.x

    Article  CAS  PubMed  Google Scholar 

  69. Schubert D, Primavesi L, Bishopp A et al (2006) Silencing by plant Polycomb-group genes requires dispersed trimethylation of histone H3 at lysine 27. EMBO J 25:4638–4649. https://doi.org/10.1038/sj.emboj.7601311

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Liu N, Fromm M, Avramova Z (2014) H3K27me3 and H3K4me3 chromatin environment at super-induced dehydration stress memory genes of arabidopsis thaliana. Mol Plant 7:502–513. https://doi.org/10.1093/mp/ssu001

    Article  CAS  PubMed  Google Scholar 

  71. Liu N, Ding Y, Fromm M, Avramova Z (2014) Different gene-specific mechanisms determine the “revised-response” memory transcription patterns of a subset of A. thaliana dehydration stress responding genes. Nucleic Acids Res 42:5556–5566. https://doi.org/10.1093/nar/gku220

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Köhler C, Villar CBR (2008) Programming of gene expression by Polycomb group proteins. Trends Cell Biol 18:236–243. https://doi.org/10.1016/J.TCB.2008.02.005

    Article  PubMed  Google Scholar 

  73. Roudier F, Ahmed I, Bérard C et al (2011) Integrative epigenomic mapping defines four main chromatin states in Arabidopsis. EMBO J 30:1928–1938. https://doi.org/10.1038/emboj.2011.103

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Schmitges FW, Prusty AB, Faty M et al (2011) Histone methylation by PRC2 Is inhibited by active chromatin marks. Mol Cell 42:330–341. https://doi.org/10.1016/j.molcel.2011.03.025

    Article  CAS  PubMed  Google Scholar 

  75. Saleh A, Al-Abdallat A, Ndamukong I et al (2007) The Arabidopsis homologs of trithorax (ATX1) and enhancer of zeste (CLF) establish “bivalent chromatin marks” at the silent AGAMOUS locus. Nucleic Acids Res 35:6290–6296. https://doi.org/10.1093/nar/gkm464

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Bernstein BE, Mikkelsen TS, Xie X et al (2006) A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell 125:315–326. https://doi.org/10.1016/j.cell.2006.02.041

    Article  CAS  PubMed  Google Scholar 

  77. Fujita Y, Fujita M, Shinozaki K, Yamaguchi-Shinozaki K (2011) ABA-mediated transcriptional regulation in response to osmotic stress in plants. J Plant Res 124:509–525. https://doi.org/10.1007/s10265-011-0412-3

    Article  CAS  PubMed  Google Scholar 

  78. Yamaguchi-Shinozaki K, Shinozaki K (2005) Organization of cis-acting regulatory elements in osmotic- and cold-stress-responsive promoters. Trends Plant Sci 10:88–94. https://doi.org/10.1016/j.tplants.2004.12.012

    Article  CAS  PubMed  Google Scholar 

  79. Klingler JP, Batelli G, Zhu J-K (2010) ABA receptors: the START of a new paradigm in phytohormone signalling. J Exp Bot 61:3199–3210. https://doi.org/10.1093/jxb/erq151

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Nakashima K, Yamaguchi-Shinozaki K (2013) ABA signaling in stress-response and seed development. Plant Cell Rep 32:959–970. https://doi.org/10.1007/s00299-013-1418-1

    Article  CAS  PubMed  Google Scholar 

  81. Virlouvet L, Ding Y, Fujii H et al (2014) ABA signaling is necessary but not sufficient for RD29B transcriptional memory during successive dehydration stresses in Arabidopsis thaliana. Plant J 79:150–161. https://doi.org/10.1111/tpj.12548

    Article  CAS  PubMed  Google Scholar 

  82. Kim JM, To TK, Ishida J et al (2008) Alterations of lysine modifications on the histone H3 N-tail under drought stress conditions in Arabidopsis thaliana. Plant Cell Physiol 49:1580–1588. https://doi.org/10.1093/pcp/pcn133

    Article  CAS  PubMed  Google Scholar 

  83. Vongs A, Kakutani T, Martienssen RA, Richards EJ (1993) Arabidopsis thaliana DNA methylation mutants. Science 260:1926–1928

    Article  CAS  PubMed  Google Scholar 

  84. Jeddeloh JA, Stokes TL, Richards EJ (1999) Maintenance of genomic methylation requires a SWI2/SNF2-like protein. Nat Genet 22:94

    Article  CAS  PubMed  Google Scholar 

  85. Lippman Z, Gendrel A-V, Black M et al (2004) Role of transposable elements in heterochromatin and epigenetic control. Nature 430:471

    Article  CAS  PubMed  Google Scholar 

  86. Saze H (2008) Epigenetic memory transmission through mitosis and meiosis in plants. Semin Cell Dev Biol 19:527–536. https://doi.org/10.1016/j.semcdb.2008.07.017

    Article  PubMed  Google Scholar 

  87. Simpson VJ, Johnson TE, Hammen RF (1986) Caenorhabditis elegans DNA does not contain 5-methylcytosine at any time during development or aging. Nucleic Acids Res 14:6711–6719

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Patel CV, Gopinathan KP (1987) Determination of trace amounts of 5-methylcytosine in DNA by reverse-phase high-performance liquid chromatography. Anal Biochem 164:164–169

    Article  CAS  PubMed  Google Scholar 

  89. Tamaru H, Selker EU (2001) A histone H3 methyltransferase controls DNA methylation in Neurospora crassa. Nature 414:277

    Article  CAS  PubMed  Google Scholar 

  90. Papikian A, Liu W, Gallego-Bartolomé J, Jacobsen SE (2019) Site-specific manipulation of Arabidopsis loci using CRISPR-Cas9 SunTag systems. Nat Commun 10:729. https://doi.org/10.1038/s41467-019-08736-7

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Gallego-Bartolomé J, Gardiner J, Liu W 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. https://doi.org/10.1073/pnas.1716945115

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. van Dijk K, Ding Y, Malkaram S et al (2010) Dynamic changes in genome-wide histone H3 lysine 4 methylation patterns in response to dehydration stress in Arabidopsis thaliana. BMC Plant Biol 10:238. https://doi.org/10.1186/1471-2229-10-238

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Godwin, J., Farrona, S. (2020). Plant Epigenetic Stress Memory Induced by Drought: A Physiological and Molecular Perspective. In: Spillane, C., McKeown, P. (eds) Plant Epigenetics and Epigenomics . Methods in Molecular Biology, vol 2093. Humana, New York, NY. https://doi.org/10.1007/978-1-0716-0179-2_17

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