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Origin of Epigenetic Variation in Plants: Relationship with Genetic Variation and Potential Contribution to Plant Memory

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Memory and Learning in Plants

Part of the book series: Signaling and Communication in Plants ((SIGCOMM))

Abstract

Plants are sessile organisms that must cope with various environmental cues. Mechanisms allowing learning and memory are, therefore, essential for the plant life cycle. Various studies suggest that epigenetic-related mechanisms could play a key role in plant learning and memory. The importance of epigenetics in these processes mainly relies on its correlation with environment and the possibility to more easily revert the resulting phenotypic changes compared to those associated with the direct DNA sequence alteration. Nevertheless, an obvious cross talk between genetic and epigenetic variation occurs. This review discusses about the nature and origin of epigenetic variation, thus allowing to better understand the contribution of epigenetic variation to plant memory.

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References

  • Baubec T, Ivánek R, Lienert F, Schübeler D (2013) Methylation-dependent and -independent genomic targeting principles of the MBD protein family. Cell 153:480–492

    Article  CAS  Google Scholar 

  • Becker C, Hagmann J, Müller J, Koenig D, Stegle O, Borgwardt K, Weigel D (2011) Spontaneous epigenetic variation in the Arabidopsis thaliana methylome. Nature 480:245–249

    Article  CAS  Google Scholar 

  • Bewick AJ, Ji L, Niederhuth CE, Willing EM, Hofmeister BT, Shi X, Wang L, Lu Z, Rohr NA, Hartwig B, Kiefer C, Deal RB, Schmutz J, Grimwood J, Stroud H, Jacobsen SE, Schneeberger K, Zhang X, Schmitz RJ (2016) On the origin and evolutionary consequences of gene body DNA methylation. Proc Natl Acad Sci USA 113:9111–9116

    Article  CAS  Google Scholar 

  • Bossdorf O, Arcuri D, Richards CL, Pigliucci M (2010) Experimental alteration of DNA methylation affects the phenotypic plasticity of ecologically relevant traits in Arabidopsis thaliana. Evol Ecol 24:541–553

    Article  Google Scholar 

  • Cao X, Jacobsen SE (2002a) Locus-specific control of asymmetric and CpNpG methylation by the DRM and CMT3 methyltransferase genes. Proc Natl Acad Sci USA 4:16491–16498

    Article  Google Scholar 

  • Cao X, Jacobsen SE (2002b) Role of the Arabidopsis DRM methyltransferases in de novo DNA methylation and gene silencing. Curr Biol 12:1138–1144

    Article  CAS  Google Scholar 

  • Chandler V, Alleman M (2008) Paramutation: epigenetic instructions passed across generations. Genetics 178:1839–1844

    CAS  PubMed  PubMed Central  Google Scholar 

  • Choi Y, Gehring M, Johnson L, Hannon M, Harada JJ, Goldberg RB, Jacobsen SE, Fischer RL (2002) DEMETER, a DNA glycosylase domain protein, is required for endosperm gene imprinting and seed viability in Arabidopsis. Cell 110:33–42

    Article  CAS  Google Scholar 

  • Coe EH (1959) A regular and continuing conversion-type phenomenon at the b locus in maize. Proc Natl Acad Sci USA 45:828–832

    Article  CAS  Google Scholar 

  • Cokus SJ, Feng S, Zhang X, Chen Z, Merriman B, Haudenschild CD, Pradhan S, Nelson SF, Pellegrini M, Jacobsen SE (2008) Shotgun bisulphite sequencing of the Arabidopsis genome reveals DNA methylation patterning. Nature 452:215–219

    Article  CAS  Google Scholar 

  • Corley RHV (1986) Oil palm. In: Monselise SP (ed) CRC handbook of fruit set and development. CRC Press, Boca Raton, pp 253–259

    Google Scholar 

  • Corley RHV, Law IH (1997) The future for oil palm clones. In: Pushparajah E (ed) Plantation management for the 21st century. Incorp Soc Planters, Kuala Lumpur, pp 279–289

    Google Scholar 

  • Cortijo S, Wardenaar R, Colomé-Tatché M, Gilly A, Etcheverry M, Labadie K, Caillieux E, Hospital F, Aury JM, Wincker P, Roudier F, Jansen RC, Colot V, Johannes F (2014) Mapping the epigenetic basis of complex traits. Science 343:1145–1148

    Article  CAS  Google Scholar 

  • Crisp PA, Ganguly D, Eichten SR, Borevitz JO, Pogson BJ (2016) Reconsidering plant memory: intersections between stress recovery, RNA turnover, and epigenetics. Sci Adv 2:e1501340

    Article  Google Scholar 

  • Cubas P, Vincent C, Coen E (1999) An epigenetic mutation responsible for natural variation in floral symmetry. Nature 401:157–161

    Article  CAS  Google Scholar 

  • Dubin MJ, Zhang P, Meng D, Remigereau MS, Osborne EJ, Paolo Casale F, Drewe P, Kahles A, Jean G, Vilhjálmsson B, Jagoda J, Irez S, Voronin V, Song Q, Long Q, Rätsch G, Stegle O, Clark RM, Nordborg M (2015) DNA methylation in Arabidopsis has a genetic basis and shows evidence of local adaptation. eLife 4:e05255

    Article  Google Scholar 

  • Eichten SR, Springer NM (2015) Minimal evidence for consistent changes in maize DNA methylation patterns following environmental stress. Front Plant Sci 6:308

    Article  Google Scholar 

  • Eichten SR, Ellis NA, Makarevitch I, Yeh CT, Gent JI, Guo L, McGinnis KM, Zhang X, Schnable PS, Vaughn MW, Dawe RK, Springer NM (2012) Spreading of heterochromatin is limited to specific families of maize retrotransposons. PLoS Genet 8:e1003127

    Article  CAS  Google Scholar 

  • Eichten SR, Schmitz RJ, Springer NM (2014) Epigenetics: beyond chromatin modifications and complex genetic regulation. Plant Physiol 165:933–947

    Article  CAS  Google Scholar 

  • Feng S, Cokus SJ, Schubert V, Zhai J, Pellegrini M, Jacobsen SE (2014) Genome-wide Hi-C analyses in wild-type and mutants reveal high-resolution chromatin interactions in Arabidopsis. Mol Cell 55:694–707

    Article  CAS  Google Scholar 

  • Finnegan EJ, Genger RK, Peacock WJ, Dennis ES (1998) DNA methylation in plants. Annu Rev Plant Physiol Plant Mol Biol 49:223–247

    Article  CAS  Google Scholar 

  • Fujimoto R, Kinoshita Y, Kawabe A, Kinoshita T, Takashima K, Nordborg M, Nasrallah ME, Shimizu KK, Kudoh H, Kakutani T (2008) Evolution and control of imprinted FWA genes in the genus Arabidopsis. PLoS Genet 4:e1000048

    Article  Google Scholar 

  • Goff SA, Cone KC, Chandler VL (1992) Functional analysis of the transcriptional activator encoded by the maize B gene: evidence for a direct functional interaction between two classes of regulatory proteins. Genes Dev 6:864–875

    Article  CAS  Google Scholar 

  • Gouil Q, Baulcombe DC (2016) DNA methylation signatures of the plant chromomethyltransferases. PLoS Genet 12:e1006526

    Article  Google Scholar 

  • Grob S, Schmid MW, Grossniklaus U (2014) Hi-C analysis in Arabidopsis identifies the KNOT, a structure with similarities to the flamenco locus of Drosophila. Mol Cell 55:678–693

    Article  CAS  Google Scholar 

  • Guan JS, Xie H, Ding X (2015) The role of epigenetic regulation in learning and memory. Exp Neurol 268:30–36

    Article  CAS  Google Scholar 

  • Hagmann J, Becker C, Müller J, Stegle O, Meyer RC, Wang G, Schneeberger K, Fitz J, Altmann T, Bergelson J, Borgwardt K, Weigel D (2015) Century-scale methylome stability in a recently diverged Arabidopsis thaliana lineage. PLoS Genet 11:e13546

    Article  Google Scholar 

  • Hauben M, Haesendonckx B, Standaert E, Van Der Kelen K, Azmi A, Akpo H, Van Breusegem F, Guisez Y, Bots M, Lambert B, Laga B, De Block M (2009) Energy use efficiency is characterized by an epigenetic component that can be directed through artificial selection to increase yield. Proc Natl Acad Sci USA 106:20109–920114

    Article  CAS  Google Scholar 

  • Hollick JB (2010) Paramutation and development. Annu Rev Cell Dev Biol 26:557–579

    Article  CAS  Google Scholar 

  • Holliday R (1987) The inheritance of epigenetic defects. Science 238:163–170

    Article  CAS  Google Scholar 

  • Hu L, Li N, Xu C, Zhong S, Lin X, Yang J, Zhou T, Yuliang A, Wu Y, Chen YR, Cao X, Zemach A, Rustgi S, von Wettstein D, Liu B (2014) Mutation of a major CG methylase in rice causes genome-wide hypomethylation, dysregulated genome expression, and seedling lethality. Natl Acad Sci USA 111:10642–10647

    Article  CAS  Google Scholar 

  • Jaligot E, Rival A, Beule T, Dussert S, Verdeil JL (2000) Somaclonal variation in oil palm (Elaeis guineensis Jacq): the DNA methylation hypothesis. Plant Cell Rep 19:684–690

    Article  CAS  Google Scholar 

  • Johannes F, Porcher E, Teixeira FK, Saliba-Colombani V, Simon M, Agier N, Bulski A, Albuisson J, Heredia F, Audigier P, Bouchez D, Dillmann C, Guerche P, Hospital F, Colot V (2009) Assessing the impact of transgenerational epigenetic variation on complex traits. PLoS Genet 5:e1000530

    Article  Google Scholar 

  • Kawakatsu T, Huang SS, Jupe F, Sasaki E, Schmitz RJ, Urich MA, Castanon R, Nery JR, Barragan C, He Y, Chen H, Dubin M, Lee CR, Wang C, Bemm F, Becker C, O’Neil R, O’Malley RC, Quarless DX, 1001 Genomes Consortium, Schork NJ, Weigel D, Nordborg M, Ecker JR (2016) Epigenomic diversity in a global collection of Arabidopsis thaliana accessions. Cell 166:492–505

    Article  CAS  Google Scholar 

  • Kinoshita T, Seki M (2014) Epigenetic memory for stress response and adaptation in plants. Plant Cell Physiol 55:1859–1863

    Article  CAS  Google Scholar 

  • Kinoshita Y, Saze H, Kinoshita T, Miura A, Soppe WJ, Koornneef M, Kakutani T (2007) Control of FWA gene silencing in Arabidopsis thaliana by SINE-related direct repeats. Plant J 49:38–45

    Article  CAS  Google Scholar 

  • Kooke R, Johannes F, Wardenaar R, Becker F, Etcheverry M, Colot V, Vreugdenhil D, Keurentjes JJ (2015) Epigenetic basis of morphological variation and phenotypic plasticity in Arabidopsis thaliana. Plant Cell 27:337–348

    Article  CAS  Google Scholar 

  • Lamke J, Baurle I (2017) Epigenetic and chromatin-based mechanisms in environmental stress adaption and stress memory in plant. Genome Biol 18:124

    Article  Google Scholar 

  • Law JA, Jacobsen SE (2010) Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nat Rev Genet 11:204–220

    Article  CAS  Google Scholar 

  • Levenson JM, Sweatt JD (2005) Epigenetic mechanisms in memory formation. Nat Rev Neurosci 6:108–118

    Article  CAS  Google Scholar 

  • Li Q, Eichten SR, Hermanson PJ, Zaunbrecher VM, Song J, Wendt J, Rosenbaum H, Madzima TF, Sloan AE, Huang J, Burgess DL, Richmond TA, McGinnis KM, Meeley RB, Danilevskaya ON, Vaughn MW, Kaeppler SM, Jeddeloh JA, Springer NM (2014) Genetic perturbation of the maize methylome. Plant Cell 26:4602–4616

    Article  Google Scholar 

  • Li Q, Song J, West PT, Zynda G, Eichten SR, Vaughn MW, Springer NM (2015) Examining the causes and consequences of context-specific differential DNA methylation in maize. Plant Physiol 168:1262–1274

    Article  CAS  Google Scholar 

  • Lindroth AM, Cao X, Jackson JP, Zilberman D, McCallum CM, Henikoff S, Jacobsen SE (2001) Requirement of CHROMOMETHYLASE3 for maintenance of CpXpG methylation. Science 292:2077–2080

    Article  CAS  Google Scholar 

  • Lisch D (2012) Regulation of transposable elements in maize. Curr Opin Plant Biol 15:511–516

    Article  CAS  Google Scholar 

  • Lisch D, Bennetzen JL (2011) Transposable element origins of epigenetic gene regulation. Curr Opin Plant Biol 14:156–161

    Article  CAS  Google Scholar 

  • Lister R, O’Malley RC, Tonti-Filippini J, Gregory BD, Berry CC, Millar AH, Ecker JR (2008) Highly integrated single-base resolution maps of the epigenome in Arabidopsis. Cell 133:523–536

    Article  CAS  Google Scholar 

  • Martinez G, Köhler C (2017) Role of small RNAs in epigenetic reprogramming during plant sexual reproduction. Curr Opin Plant Biol 36:22–28

    Article  CAS  Google Scholar 

  • Matzke MA, Kanno T, Matzke AJ (2015) RNA-directed DNA methylation: the evolution of a complex epigenetic pathway in flowering plants. Annu Rev Plant Biol 66:243–267

    Article  CAS  Google Scholar 

  • Meagher RB (2010) The evolution of epitype. Plant Cell 22:1658–1666

    Article  CAS  Google Scholar 

  • Mirouze M, Reinders J, Bucher E, Nishimura T, Schneeberger K, Ossowski S, Cao J, Weigel D, Paszkowski J, Mathieu O (2009) Selective epigenetic control of retrotransposition in Arabidopsis. Nature 461:427–430

    Article  CAS  Google Scholar 

  • Niederhuth CE, Bewick AJ, Ji L, Alabady MS, Kim KD, Li Q, Rohr NA, Rambani A, Burke JM, Udall JA, Egesi C, Schmutz J, Grimwood J, Jackson SA, Springer NM, Schmitz RJ (2016) Widespread natural variation of DNA methylation within angiosperms. Genome Biol 17:194

    Article  Google Scholar 

  • Ong-Abdullah M, Ordway JM, Jiang N, Ooi SE, Kok SY, Sarpan N, Azimi N, Hashim AT, Ishak Z, Rosli SK, Malike FA, Bakar NA, Marjuni M, Abdullah N, Yaakub Z, Amiruddin MD, Nookiah R, Singh R, Low ET, Chan KL, Azizi N, Smith SW, Bacher B, Budiman MA, Van Brunt A, Wischmeyer C, Beil M, Hogan M, Lakey N, Lim CC, Arulandoo X, Wong CK, Choo CN, Wong WC, Kwan YY, Alwee SS, Sambanthamurthi R, Martienssen RA (2015) Loss of Karma transposon methylation underlies the mantled somaclonal variant of oil palm. Nature 252:533–537

    Article  Google Scholar 

  • Ossowski S, Schneeberger K, Lucas-Lledó JI, Warthmann N, Clark RM, Shaw RG, Weigel D, Lynch M (2010) The rate and molecular spectrum of spontaneous mutations in Arabidopsis thaliana. Science 327:92–94

    Article  CAS  Google Scholar 

  • Patterson GI, Thorpe CJ, Chandler VL (1993) Paramutation, an allelic interaction, is associated with a stable and heritable reduction of transcription of the maize b regulatory gene. Genetics 135:881–894

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pecinka A, Abdelsamad A, Vu GT (2013) Hidden genetic nature of epigenetic natural variation in plants. Trends Plant Sci 18:625–632

    Article  CAS  Google Scholar 

  • Pikaard CS, Mittelsten Scheid O (2014) Epigenetic regulation in plants. Cold Spring Harb Perspect Biol 6:a019315

    Article  Google Scholar 

  • Quadrana L, Colot V (2016) Plant transgenerational epigenetics. Annu Rev Genet 50:467–491

    Article  CAS  Google Scholar 

  • Reinders J, Wulff BB, Mirouze M, Marí-Ordóñez A, Dapp M, Rozhon W, Bucher E, Theiler G, Paszkowski J (2009) Compromised stability of DNA methylation and transposon immobilization in mosaic Arabidopsis epigenomes. Genes Dev 23:839–850

    Article  Google Scholar 

  • Richards EJ (2006) Inherited epigenetic variation – revisiting soft inheritance. Nat Rev Genet 7:395–401

    Article  CAS  Google Scholar 

  • Richardson SR, Morell S, Faulkner GJ (2014) L1 retrotransposons and somatic mosaicism in the brain. Annu Rev Genet 48:1–27

    Article  CAS  Google Scholar 

  • Roux F, Colomé-Tatché M, Edelist C, Wardenaar R, Guerche P, Hospital F, Colot V, Jansen RC, Johannes F (2011) Genome-wide epigenetic perturbation jump-starts patterns of heritable variation found in nature. Genetics 188:1015–1017

    Article  CAS  Google Scholar 

  • Schmitz RJ, Schultz MD, Lewsey MG, O’Malley RC, Urich MA, Libiger O, Schork NJ, Ecker JR (2011) Transgenerational epigenetic instability is a source of novel methylation variants. Science 334:369–373

    Article  CAS  Google Scholar 

  • Secco D, Wang C, Shou H, Schultz MD, Chiarenza S, Nussaume L, Ecker JR, Whelan J, Lister R (2015) Stress induced gene expression drives transient DNA methylation changes at adjacent repetitive elements. Elife 4:e09343. https://doi.org/10.7554/eLife.09343

    Article  PubMed Central  Google Scholar 

  • Seymour DK, Becker C (2017) The causes and consequences of DNA methylome variation in plants. Curr Opin Plant Biol 36:56–63

    Article  CAS  Google Scholar 

  • Seymour DK, Koenig D, Hagmann J, Becker C, Weigel D (2014) Evolution of DNA methylation patterns in the Brassicaceae is driven by differences in genome organization. PLoS Genet 10:e13546

    Article  Google Scholar 

  • Shen X, De Jonge J, Forsberg SK, Pettersson ME, Sheng Z, Hennig L, Carlborg Ö (2014) Natural CMT2 variation is associated with genome-wide methylation changes and temperature seasonality. PLoS Genet 10:e1004842

    Article  Google Scholar 

  • Soppe WJ, Jacobsen SE, Alonso-Blanco C, Jackson JP, Kakutani T, Koornneef M, Peeters AJ (2000) The late flowering phenotype of fwa mutants is caused by gain-of-function epigenetic alleles of a homeodomain gene. Mol Cell 6:791–802

    Article  CAS  Google Scholar 

  • Stam M, Belele C, Dorweiler JE, Chandler VL (2002a) Differential chromatin structure within a tandem array 100 kb upstream of the maize b1 locus is associated with paramutation. Genes Dev 16:1906–1918

    Article  CAS  Google Scholar 

  • Stam M, Belele C, Ramakrishna W, Dorweiler JE, Bennetzen JL, Chandler VL (2002b) The regulatory regions required for B’ paramutation and expression are located far upstream of the maize b1 transcribed sequences. Genetics 162:917–930

    CAS  PubMed  PubMed Central  Google Scholar 

  • Stelpflug SC, Eichten SR, Hermanson PJ, Springer NM, Kaeppler SM (2014) Consistent and heritable alterations of DNA methylation are induced by tissue culture in maize. Genetics 198:209–218

    Article  CAS  Google Scholar 

  • Stroud H, Ding B, Simon SA, Feng S, Bellizzi M, Pellegrini M, Wang GL, Meyers BC, Jacobsen SE (2013) Plants regenerated from tissue culture contain stable epigenome changes in rice. Elife 2:e00354

    Article  Google Scholar 

  • Stroud H, Do T, Du J, Zhong X, Feng S, Johnson L, Patel DJ, Jacobsen SE (2014) Non-CG methylation patterns shape the epigenetic landscape in Arabidopsis. Nat Struct Mol Biol 21:64–72

    Article  CAS  Google Scholar 

  • Takuno S, Gaut BS (2012) Body-methylated genes in Arabidopsis thaliana are functionally important and evolve slowly. Mol Biol Evol 29:219–227

    Article  CAS  Google Scholar 

  • Tanurdzic M, Vaughn MW, Jiang H, Lee TJ, Slotkin RK, Sosinski B, Thompson WF, Doerge RW, Martienssen RA (2008) Epigenomic consequences of immortalized plant cell suspension culture. PLoS Biol 6:2880–2895

    Article  CAS  Google Scholar 

  • Verhoeven KJ, Van Dijk PJ, Biere A (2010) Changes in genomic methylation patterns during the formation of triploid asexual dandelion lineages. Mol Ecol 19:315–324

    Article  CAS  Google Scholar 

  • Verhoeven KJF, Macel M, Wolfe LM, Biere A (2011) Population admixture, biological invasions and the balance between local adaptation and inbreeding depression. Proc Biol Sci 278:2–8

    Article  Google Scholar 

  • Wang C, Liu C, Roqueiro D, Grimm D, Schwab R, Becker C, Lanz C, Weigel D (2015) Genome-wide analysis of local chromatin packing in Arabidopsis thaliana. Genome Res 25:246–256

    Article  Google Scholar 

  • Wibowo A, Becker C, Marconi G, Durr J, Price J, Hagmann J, Papareddy R, Putra H, Kageyama J, Becker J, Weigel D, Gutierrez-Marcos J (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

    Article  Google Scholar 

  • Woo HR, Pontes O, Pikaard CS, Richards EJ (2007) VIM1, a methylcytosine-binding protein required for centromeric heterochromatinization. Genes Dev 12:267–277

    Article  Google Scholar 

  • Xu J, Tanino KK, Horner KN, Robinson SJ (2016) Quantitative trait variation is revealed in a novel hypomethylated population of woodland strawberry (Fragaria vesca). BMC Plant Biol 16:240

    Article  Google Scholar 

  • Zemach A, Kim MY, Hsieh PH, Coleman-Derr D, Eshed-Williams L, Thao K, Harmer SL, Zilberman D (2013) The Arabidopsis nucleosome remodeler DDM1 allows DNA methyltransferases to access H1-containing heterochromatin. Cell 153:193–205

    Article  CAS  Google Scholar 

  • Zhang X, Yazaki J, Sundaresan A, Cokus S, Chan SW, Chen H, Henderson IR, Shinn P, Pellegrini M, Jacobsen SE, Ecker JR (2006) Genome-wide high-resolution mapping and functional analysis of DNA methylation in Arabidopsis. Cell 126:189–201

    Google Scholar 

  • Zilberman D (2017) An evolutionary case for functional gene body methylation in plants and animals. Genome Biol 18:87

    Article  Google Scholar 

  • Zilberman D, Gehring M, Tran RK, Ballinger T, Henikoff S (2006) Genome-wide analysis of Arabidopsis thaliana DNA methylation uncovers an interdependence between methylation and transcription. Nature Genet 39:61–69

    Article  Google Scholar 

  • Zovkic IB, Guzman-Karlsson MC, Sweatt JD (2013) Epigenetic regulation of memory formation and maintenance. Learn Mem 20:61–74

    Article  CAS  Google Scholar 

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Acknowledgments

We thank Steve Eichten for critical reading of the manuscript and useful suggestions. The work regarding epigenetic studies in Massimiliano Lauria and Vincenzo Rossi laboratories is principally supported by special grants from the Italian Ministry of Education, University and Research (MIUR) and the National Research Council of Italy (CNR) for the Epigenomics Flagship Project (EPIGEN).

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Lauria, M., Rossi, V. (2018). Origin of Epigenetic Variation in Plants: Relationship with Genetic Variation and Potential Contribution to Plant Memory. In: Baluska, F., Gagliano, M., Witzany, G. (eds) Memory and Learning in Plants. Signaling and Communication in Plants. Springer, Cham. https://doi.org/10.1007/978-3-319-75596-0_6

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